Environmental Science and Pollution Research

, Volume 22, Issue 12, pp 8989–9041

Spatial and temporal trends of the Stockholm Convention POPs in mothers’ milk — a global review

  • Johan Fång
  • Elisabeth Nyberg
  • Ulrika Winnberg
  • Anders Bignert
  • Åke Bergman
Open Access
Review Article

DOI: 10.1007/s11356-015-4080-z

Cite this article as:
Fång, J., Nyberg, E., Winnberg, U. et al. Environ Sci Pollut Res (2015) 22: 8989. doi:10.1007/s11356-015-4080-z

Abstract

Persistent organic pollutants (POPs) have been of environmental and health concern for more than half a century and have their own intergovernmental regulation through the Stockholm Convention, from 2001. One major concern is the nursing child’s exposure to POPs, a concern that has led to a very large number of scientific studies on POPs in mothers’ milk. The present review is a report on the assessment on worldwide spatial distributions of POPs and of their temporal trends. The data presented herein is a compilation based on scientific publications between 1995 and 2011. It is evident that the concentrations in mothers’ milk depend on the use of pesticides and industrial chemicals defined as POPs. Polychlorinated biphenyls (PCBs) and “dioxins” are higher in the more industrialized areas, Europe and Northern America, whereas pesticides are higher in Africa and Asia and polybrominated diphenyl ethers (PBDEs) are reported in higher concentrations in the USA. POPs are consequently distributed to women in all parts of the world and are thus delivered to the nursing child. The review points out several major problems in the reporting of data, which are crucial to enable high quality comparisons. Even though the data set is large, the comparability is hampered by differences in reporting. In conclusion, much more detailed instructions are needed for reporting POPs in mothers’ milk. Temporal trend data for POPs in mothers’ milk is scarce and is of interest when studying longer time series. The only two countries with long temporal trend studies are Japan and Sweden. In most cases, the trends show decreasing concentrations of POPs in mothers’ milk. However, hexabromocyclododecane is showing increasing temporal concentration trends in both Japan and Sweden.

Keywords

Breast milk Persistent organic pollutants Stockholm Convention DDT Dioxin HCH HCB PBDE HBCDD 

Introduction

Mothers’ milk is a source of nutrients, energy, and protection for the newborn child, and it carries essential elements from the mother to the child (Kramer and Kakuma 2012). Due to the lipophilic properties of a range of anthropogenic organic pollutants, ubiquitously distributed in human food and our environment, many of these chemicals are accumulated in mothers’ milk. Accordingly, the nursing child is targeted by a vast number of undesirable pollutants (IPCS 2007; UNEP and WHO 2013). These pollutants are similar to those entering the fetus via the cord blood after transfer across the placental barrier (CDC 2013; Frederiksen et al. 2010), although there are differences in the presence of pollutants in the blood and in the mothers’ milk. Due to the high chemical and metabolic stability and toxicity of some anthropogenic chemicals as well as their ability to spread globally, and bioaccumulate, 25 chemicals have been adopted under the Stockholm Convention (SCa), known as persistent organic pollutants (POPs). Among these listed POPs, polybrominated diphenyl ethers (PBDEs) are separated into tetra-/pentaBDEs and hexa-/heptaBDEs, which actually make the POPs to 24 different entries. Six other POPs are presently under discussion for inclusion among the legacy POPs (SCb), and among these, short chain chlorinated paraffins (SCCPs) are included in the present review. The POPs reviewed herein are listed in Table 1.
Table 1

Names and abbreviations of all POPs and two suggested POPs are presented, CAS numbers are given, as well as chemical structures or general structures. Some major review documents regarding the POPs are presented under “Review articles” (the column to the far right)

The overarching toxicity of POPs is related to endocrine disruption (UNEP and WHO 2013) and/or listed as carcinogenic, mutagenic, or reprotoxic (CMRs). The toxicities of the POPs are extensively studied and will not be discussed in any detail here; instead, we prefer to refer to some of the most recent reviews on the different POPs listed in Table 1. Toxicological data for many of the POPs are often related to accidental exposures to humans or wildlife and considerable animal testing in toxicological laboratories. Some of the POPs show acute toxicity, like the “drins” (i.e., dieldrin, endrin, and aldrin). On the contrary, chronic effects have been observed for, e.g., DDT, and its transformation product dichlorodiphenyldichloroethylene (DDE), effects which were particularly emphasized in birds. The effects of many of the POPs on reproduction have been shown among wildlife species.

Accordingly, it is of interest to review the present exposure situation to POPs for nursing children worldwide, i.e., spatial exposure data as well as levels of POPs in mothers’ milk over time. The objective of this review is to summarize the concentrations of POPs in mothers’ milk during a delimited time period, 1995–2011. In addition, some recent data have been generated within the Swedish monitoring program and are included herein.

Analysis of some of the first identified POPs in mothers’ milk was published in the 1960s (Norén and Westöö 1968) and then novel POPs were added to the list (Westöö and Norén 1978). Still, as shown herein, there is limited mothers’ milk data for several of the POPs.

Materials and methods

Names, abbreviations, and (general) structures of the POPs applied in the present review are presented in Table 1, together with reviews discussing their toxicities/ecotoxicological effects.

Methods for data retrieval on POPs in mothers’ milk

A literature search was performed using the database Web of Science and the following search terms were used: “Human Milk,” “Breast Milk,” “Mother’s Milk,” and “Mothers Milk,” combined with the name of the substance of interest. All references found were compiled in one database and duplicates were removed.

Methods for inclusion of data

To reduce errors due to comparison of data from different sources and to avoid presenting a historical overview, the following limits were set for inclusion in the study:
  • The study must be a scientific peer-reviewed paper published 1995–2011.

  • Studies must report and quantify any of the POPs listed in Table 1, in at least six subjects (donors). In the case of pooled samples, a pool should contain a minimum of six donors.

  • Information about place and year of sampling are required.

  • Inclusion of a time series requires a minimum of five reported data points and is only included if the report/paper includes the original values of the time series.

Other sources of data

Data from the Swedish Environmental Monitoring Program are included herein (http://www.imm.ki.se/Datavard/aBiologiska_mätdata_-_organiska_ämnen), as well as time series data from Fång et al. (2013).

Substance summary tables

Concentration data are presented in the substance summary tables (Tables 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, and 13) in the following manner:
Table 2

Concentrations (ng/g fat) of 4,4′-DDT and its metabolites/transformation products, 4,4′-DDE, 4,4′-DDD, and ∑DDT, in mothers’ milk, as reported in studies from around the world, 1995–2011. The concentration ratio of 4,4′-DDT/4,4′-DDE has been calculated and is presented in the table

Region

Country

4,4′-DDE

4,4′-DDD

4,4′-DDT

∑DDTs

4,4′-DDT/4,4′-DDE

Reference

Mean

Median

GM

Mean

Median

GM

Mean

Median

GM

Mean

Median

GM

Mean

Median

GM

Africa

Africa

          

980

    

UNEP (2011)

Cambodia

         

1200; 1800

860; 1100

    

Kunisue et al. (2004b)

Egypt

530a

     

73.25a

     

0.14

  

Saleh et al. (1996)

Ghana

45

  

8

  

31

  

78

  

0.70

  

Ntow et al. (2008)

Ghana

490

              

Ntow (2001)

Ghana

         

230

     

UNEP (2009)

Libya

120

  

120

     

420

     

Elafi et al. (2001)

Mozambique

330

190

 

7.5

3.8

 

220

67

 

550

280

 

0.67

0.35

 

Manaca et al. (2011)

Nigeria

         

860

     

UNEP (2009)

Senegal

         

460

     

UNEP (2009)

South Africa

490–3000

  

36–91

  

260–1700

  

800–4800

  

0.53–0.66

  

Bouwman et al. (2006)

South Africa

4600

3600

    

1600

890

 

6300

4900

 

0.35

0.25

 

Darnerud et al. (2011)

South Africa

70,000a

  

44,000a

  

40,000a

  

150,000a

  

0.57

  

Okonkwo et al. (2008)

South Africa

2700; 6100

2400; 4600

 

27; 36

17; 27

 

2500; 4200

2000; 4500

 

5600; 11,000

4700; 10,000

 

0.69; 0.92

0.83; 0.98

 

Sereda et al. (2009)

Swaziland

200

        

1700

     

Okonkwo et al. (1999)

Tunisia

2400

  

280

  

1000

  

3900

  

0.42

  

Ennaceur et al. (2007)

Tunisia

41–3100

  

4–320

  

23–1200

     

0.81–1.7

  

Ennaceur et al. (2008)

Uganda

         

3000

     

Ejobi et al. (1998)

Zimbabwe

1200–14,000

500–9000

    

250–9100

150–5400

 

1600–25,000

810–17,000

 

0.21–0.67

0.077–0.59

 

Chikuni et al. (1997)

Asia, Australia, and the Pacific region

Asia and the Pacific

          

800

    

UNEP (2011)

Australia

150–870

  

0.06–0.45

  

3.6–30

     

0.016–0.045

  

Harden et al. (2007)

Australia

310

280

 

0.18

0.18

 

11

12

    

0.035

0.043

 

Mueller et al. (2008)

Australia

               

Noakes et al. (2006)

Australia

890–1000

     

220–230

     

0.22–0.26

  

Quinsey et al. (1995)

China

  

1300

  

11

  

65

  

1300

  

0.051

Fujii et al. (2011)

China

1200

  

5.7

  

38

  

1300

  

0.030

  

Haraguchi et al. (2009)

China

830; 2000

  

1.6; 6.0

  

40; 130

  

870; 2100

  

0.048; 0.065

  

Kunisue et al. (2004a)

China

 

560; 720

  

2.2; 4.9

  

21; 38

  

580; 770

  

0.038; 0.050

 

Leng et al. (2009)

China

1900

1800

 

83

94

 

120

140

 

2500

2100

 

0.062

0.079

 

Qu et al. (2010)

China

 

2100; 3100

1900; 3300

            

Sun et al. (2005)

China

140; 170

110; 120

 

3.5; 4.8

2.6; 2.7

 

4.5; 5.0

3.5; 3.9

 

150; 180

120; 130

 

0.029; 0.033

0.030; 0.035

 

Tao et al. (2008b)

China

2800

     

320

  

3100

  

0.12

  

Tsang et al. (2011)

China

  

150a

        

210a

   

Wang et al. (2008)

China

2500; 2800

     

390; 700

     

0.16; 0.24

  

Wong et al. (2002)

China

420

  

140

  

84

  

720

  

0.20

  

Yao et al. (2005)

China

 

1300; 1500

1100; 1500

            

Zhao et al. (2007)

Hong Kong

         

3300

     

Poon et al. (2005)

India

380–1200

  

7.3–24

  

68–210

  

450–1500

  

0.18–0.22

  

Devanathan et al. (2009)

India

56–56

  

60–66

     

170–180

     

Kumar et al. (2006)

India

980; 1000

     

1200; 1400

  

2900; 3200

  

1.2; 1.3

  

Mishra and Sharma (2011)

India

               

Sanghi et al. (2003)

India

9500a

  

75a

  

2750a

  

14,000a

  

0.29

  

Siddiqui et al. (2002)

India

16,800a

  

5200a

  

3950a

  

32000a

  

0.24

  

Nair et al. (1996)

Indonesia

400

     

90

     

0.23

  

Burke et al. (2003)

Indonesia

600–1100

140–860

 

1.2–2.8

0.44–1.2

 

32–180

8.4–17

 

640–1300

160–910

 

0.029–0.16

0.01–0.071

 

Sudaryanto et al. (2006)

Indonesia

940

670

 

1.3

0.47

 

39

14

 

990

670

 

0.041

0.021

 

Sudaryanto et al. (2008a)

Iran

1300–2900

490–1100

 

2.0–34

  

170–480

6.0–270

 

1600–3600

700–1400

 

0.13–0.32

0.0070–0.33

 

Behrooz et al. (2009)

Iran

1700

     

300

  

2200

  

0.18

  

Cok et al. (1999)

Japan

  

110

  

3.2

  

6.7

  

120

  

0.062

Fujii et al. (2011)

Japan

92–250

  

1.1–1.7

  

4.0–6.9

  

97–260

  

0.028–0.43

  

Haraguchi et al. (2009)

Japan

270

     

17.8

     

0.066

  

Konishi et al. (2001)

Japan

260

  

0.78

  

11

  

280

  

0.042

  

Kunisue et al. (2006)

Japan

 

72

             

Miyake et al. (2011)

Japan

      

92a

        

Nagayama et al. (2007a)

Japan

          

290

    

Nagayama et al. (2007b)

Jordan

260

     

80

     

0.30

  

Alawi et al. (2006)

Jordan

2000-9400

  

1960

  

4400

  

9700

  

2.3

  

Nasir et al. (1998)

Kazakhstan

2000

1500

             

Lutter et al. (1998)

Kazakhstan

1800–3300

     

220–460

     

0.12–0.31

  

Hooper et al. (1997)

Korea

  

120

  

4.2

  

140

  

140

  

1.2

Fujii et al. (2011)

Korea

170

  

2

  

10

  

180

  

0.059

  

Haraguchi et al. (2009)

Korea

         

160

     

UNEP (2009)

Kuwait

830

  

4.2

  

12

  

850

  

0.015

  

Saeed et al. (2000)

Malaysia

1600

  

3

  

46

  

1600

  

0.029

  

Sudaryanto et al. (2005)

Philippines

56–160

30–65

 

0.57–1.2

0.33–0.44

 

5.0–7.1

3.6–5.1

 

60–170

38–70

 

0.045–0.089

0.075–0.12

 

Malarvannan et al. (2009)

Russia

530; 600

  

2.2; 3.6

  

50; 52

  

580; 660

  

0.083; 0.098

  

Tsydenova et al. (2007)

Saudi Arabia

490; 540

  

6.0; 23

  

71; 110

  

570; 680

  

0.14; 0.20

  

Al-Saleh et al. (2002)

Saudi Arabia

240–1800

200; 260

 

2.0–360

  

37–1200

62; 88

 

280–3300

260; 400

 

0.10–0.67

0.32; 0.34

 

Al-Saleh et al. (2003)

Taiwan

310

     

23

  

330

  

0.074

  

Chao et al. (2006)

Thailand

7200a

4200a

 

200a

170a

 

2300a

1700a

 

9800a

5200a

 

0.32

0.41

 

Stuetz et al. (2001)

Turkey

1900; 2000

     

72; 140

  

2200; 2700

  

0.036; 0.076

  

Cok et al. (1997)

Turkey

2100

     

110

  

2600

  

0.053

  

Cok et al. (2005)

Turkey

1000

     

260

  

1400

  

0.24

  

Cok et al. (2011)

Turkey

 

1500

 

1.8

1.5

  

65

  

1600

  

0.043

 

Erdogrul et al. (2004)

Turkey

6.8

3.6

 

10

5.6

 

20

11

 

37

20

 

3.0

3.1

 

Ozcan et al. (2011)

Uzbekistan

 

870

     

70

     

0.080

 

Ataniyazova et al. (2001)

Vietnam

1200

  

9.4

  

56

  

1200

  

0.047

  

Haraguchi et al. (2009)

Vietnam

1900

  

7.0; 11

  

170; 260

  

2100; 2300

  

0.089; 0.13

  

Minh et al. (2004)

Vietnam

 

220; 720

  

1.8; 2.1

  

14; 20

  

240; 750

  

0.028; 0.064

 

Nguyen et al. (2010)

Europe

Belgium

120

              

Colles et al. (2008)

Central and Eastern Europe

          

380

    

UNEP (2011)

Croatia

27

22

 

8.8

4.7

 

7.1

2.1

    

0.26

0.10

 

Frkovic et al. (1996)

Croatia

 

230; 260

  

2; 5

  

14; 19

     

0.060; 0.075

 

Kozul and Romanic (2010)

Croatia

250–490

              

Krauthacker et al. (1998)

Croatia

 

100–380

     

13; 170

     

0.12; 0.60

 

Krauthacker et al. (2009)

Czech Republic

920; 1000

820; 860

    

81; 86

60; 74

    

0.080; 0.093

0.073; 0.086

 

Cajka and Hajslova (2003)

Czech Republic

260–840

170–680

    

24–98

14–90

 

280–920

240–730

 

0.044–0.14

0.042–0.14

 

Cerna et al. (2010)

Czech Republic

         

830-1300

     

(Schoula et al. 1996)

Denmark

 

59; 130

  

0.31; 0.36

  

3.4; 5.7

  

63; 140

  

0.042; 0.058

 

Shen et al. (2008)

Denmark and Finland

 

90

  

8.7

  

4.3

  

130

  

0.048

 

Damgaard et al. (2006)

England

               

Thomas et al. (2006)

Finland

77; 140

  

0.41; 0.48

  

4.4; 7.1

  

82; 140

  

0.052; 0.056

  

Shen et al. (2007)

France

 

80

             

Brucker-Davis et al. (2010)

Germany

160

87

     

4

 

180

100

  

0.046

 

Raab et al. (2008)

Germany

      

240

200

       

Schade and Heinzow (1998)

Germany

         

360; 380

     

Schlaud et al. (1995)

Germany

550

              

Skopp et al. (2002)

Germany

      

130–170

81–110

       

Zietz et al. (2008)

Greece

720

  

15

  

66

  

800

  

0.091

  

Schinas et al. (2000)

Italy

210–510

     

9.4–44

     

0.045–0.10

  

Abballe et al. (2008)

Latvia

150–240

     

13–22

     

0.069–0.12

  

Bake et al. (2007)

Norway

93–110

93–110

 

0.2–0.3

0.2–0.3

 

7.2–10

7.5

 

100–120

100–120

 

0.064–0.11

0.63–0.10

 

Polder et al. (2008b)

Norway

53; 140

41; 61

             

Polder et al. (2009)

Poland

500–690a

  

12–30a

  

62–140a

     

0.15–0.24

  

Czaja et al. (1997b)

Poland

820

630

    

51

42

 

870

680

 

0.062

0.066

 

Jaraczewska et al. (2006)

Romania

350

  

81

  

34

  

700

  

0.10

  

Cioroiu et al. (2010)

Romania

1700a

1200a

 

44a

29a

 

310a

190a

 

2000a

1400a

 

0.19

0.16

 

Covaci et al. (2001)

Russia

800; 810

680; 710

 

3; 5

3; 3

 

91; 220

78; 160

 

900; 1000

720; 920

 

0.11; 0.27

0.12; 0.22

 

Polder et al. (2008a)

Russia

890; 1300

900; 1200

 

4.1; 8.2

3.4; 6.5

    

1100; 1500

1000; 1200

    

Polder et al. (1998)

Slovak Republic

9.0–1300

1.0–430

    

7.0–180

5.0–110

    

0.024–1.2

0.15–8.0

 

Veningerova et al. (2001)

Slovak Republic

630; 660

540; 540

    

33; 36

26; 27

    

0.052; 0.055

0.048; 0.050

 

Yu et al. (2007)

Spain

220

  

1.2

  

12

  

240

  

0.052

  

Bordajandi et al. (2008)

Spain

390a

  

4.3a

  

12a

     

0.030

  

Pico et al. (1995)

Spain

 

800; 1000

             

Ribas-Fito et al. (2005)

Sweden

100

72

    

5.7

3.7

    

0.056

0.051

 

Aune et al. (2002)

Sweden

58; 160

52

    

4.0; 7.0

3.7

    

0.044; 0.069

0.071

 

Bergman et al. (2010)

Sweden

120

78

    

6.0

5.2

    

0.053

0.067

 

Darnerud (2001)

Sweden

 

110

             

Darnerud et al. (2010)

Sweden

 

46–72

     

65

     

0.98

 

Glynn et al. (2011)

Sweden

70

59

    

4.5

4.2

 

75

  

0.065

0.072

 

Lignell et al. (2003)

Sweden

270

100

    

9.1

6.1

    

0.033

0.060

 

Lignell et al. (2004)

Sweden

230

     

22

     

0.10

  

Lundén and Norén (1998)

Sweden

250

     

32

     

0.13

  

Norén et al. (1996)

Sweden

84–190

82

    

1.7–3.2

1.3

    

0.016–0.022

0.016

 

Athanasiadou and Bergman (2008)

Netherlands

550

      

40

       

Albers et al. (1996)

Ukraine

 

2300; 2800

     

320; 340

     

0.12; 0.14

 

Gladen et al. (1999)

Ukraine

 

2500

     

340

     

0.14

 

Gladen et al. (2003)

UK

430

280

    

40

25

    

0.093

0.088

 

Harris et al. (1999)

UK

 

150

150

 

0.3

0.3

 

6.2

6.2

 

160

160

 

0.041

0.04

Kalantzi et al. (2004)

Western Europe and other States

          

82

    

UNEP (2011)

Yugoslavia

330; 460a

280; 360a

    

12; 360a

290a

    

0.038; 0.79

0.79

 

Vukavic et al. (2003)

The Americas

Antigua and Barbuda

         

190

     

UNEP (2009)

Brazil

1500

  

6

  

180

  

1700

  

0.12

  

Paumgartten et al. (2000)

Brazil

29

  

72

  

360

  

460

  

12

  

Azeredo et al. (2008)

Canada

340

              

Dewailly et al. (1996)

Canada

  

960

            

Dewailly et al. (2000)

Canada

440

320

    

24

21

    

0.055

0.065

 

Newsome and Ryan (1999)

Canada

220

93–150a

    

22

12–18a

    

0.10

0.12–0.14

 

Newsome et al. (1995)

Canada and USA

  

180

            

Fitzgerald et al. (2001)

Chile

         

210

     

UNEP (2009)

GROLACb

          

200

    

UNEP (2011)

Mexico

 

2500–1300

  

140; 250

          

Elvia et al. (2000)

Mexico

5300

  

88

  

2100

  

7800

  

0.40

  

Pardio et al. (1998)

Mexico

3000

     

210

  

3100

  

0.069

  

Rodas-Ortiz et al. (2008)

Mexico

590

     

160

  

900

  

0.27

  

Torres-Arreola et al. (1999)

Mexico

3900

  

70

  

1600

  

5700

  

0.40

  

Waliszewski et al. (1998)

Mexico

4000; 4800

  

2.0; 5.0

  

650; 900

  

4700; 5700

  

0.16; 0.19

  

Waliszewski et al. (1999b)

Nicaragua

2800

     

130

     

0.046

  

Romero et al. (2000)

Uruguay

         

130

     

UNEP (2009)

USA

  

190

            

Fitzgerald et al. (2001)

USA

270

260

             

Greizerstein et al. (1999)

USA

53

35

 

3.1

2.7

 

6.7

  

65

41

 

0.13

  

Johnson-Restrepo et al. (2007)

USA

220

              

Kostyniak et al. (1999)

USA

120

     

5

     

0.041

  

Pan et al. (2010)

USA

110; 440a

79; 87a

    

3.1; 9.4a

2.6; 2.7a

 

120; 460a

83; 91a

 

0.021; 0.027

0.029; 0.033

 

Weldon et al. (2011)

Venezuela

         

280–1000a

     

Brunetto et al. (1996)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

bGroup of Latin America and Caribbean countries

Table 3

Concentrations (ng/g fat) of CB-153, ∑ 6 indicator PCBs, and ∑PCBs, in mothers’ milk, as reported in studies from around the world, 1995–2011

Region

Country

CB-153

∑ 6 indicator PCBsa

∑PCB

Reference

Mean

Median

Mean

Median

Mean

Median

GM

Africa

Africa

   

31

   

UNEP (2011)

Ghana

6.4–22

5.4–19

  

30–82

26–72

 

Asante et al. (2011)

South Africa

2.6

2

  

10

8.4

 

Darnerud et al. (2011)

Tunisia

18–120

 

95–660

 

110–750

  

Ennaceur et al. (2008)

Zimbabwe

    

2.8–60

  

Chikuni et al. (1997)

Asia, Australia, and the Pacific region

Asia and the Pacific

   

15

   

UNEP (2011)

Australia

    

160–480

  

Quinsey et al. (1995)

Cambodia

    

20–29

13–24

 

Kunisue et al. (2004a)

China

    

28–42

  

Kunisue et al. (2004a)

China

    

74

  

Poon et al. (2005)

China

14

   

49

  

Tsang et al. (2011)

China

    

33; 42

  

Wong et al. (2002)

China

    

9.5

  

Xing et al. (2009)

China

0.49–16

 

2.4–29

    

Zhang et al. (2011)

China

 

13.28

   

210

210

Zhao et al. (2007)

India

    

23–40

  

Devanathan et al. (2009)

Indonesia

    

21–33

17–27

 

Sudaryanto et al. (2006)

Iran

200–250

46–150

990–1900

130–1000

   

Behrooz et al. (2009)

Japan

    

120

110

 

Kawashiro et al. (2008)

Japan

    

200

  

Konishi et al. (2001)

Japan

    

120

  

Kunisue et al. (2006)

Japan

    

120

100

 

Nakamura et al. (2008)

Japan

     

110

 

Nagayama et al. (2007a)

Japan

19

18

39

36

73

67

 

Todaka et al. (2011)

Jordan

25

   

42

  

Alawi et al. (2006)

Kazakhstan

  

100–430

 

220–820

  

Hooper et al. (1997)

Kazakhstan

  

100–350

 

410

  

Lutter et al. (1998)

Kazakhstan

65

50

180

130

370

290

 

She et al. (1998)

Malaysia

    

14; 80

  

Sudaryanto et al. (2005)

Russia

    

160–240

  

Tsydenova et al. (2007)

Taiwan

  

55

  

54

 

Wang et al. (2004)

Philippines

    

50–70

40–60

 

Malarvannan et al. (2009)

Turkey

11

 

26

 

27

  

Cok et al. (2011)

Turkey

110

 

190

 

210

  

Cok et al. (2003)

Turkey

3.4–11

 

11–19

 

18–36

  

Cok et al. (2009)

Turkey

8.5b

8.2b

  

27b

28b

 

Erdogrul et al. (2004)

Turkey

12

6.5

100

69

   

Ozcan et al. (2011)

Vietnam

11–43

   

56–150

  

Haraguchi et al. (2009)

Vietnam

    

74; 79

  

Minh et al. (2004)

Vietnam

 

5.7; 8.2

  

33; 46

24; 33

 

Tue et al. (2010)

Vietnam

 

4.7; 8.1

 

14; 22

 

33; 47

 

Nguyen et al. (2010)

Europe

Belgium

43

 

97

 

110

  

Colles et al. (2008)

Central and Eastern Europe

   

47

   

UNEP (2011)

Croatia

 

39; 42

 

110; 110

 

120; 130

 

Kozul and Romanic (2010)

Croatia

     

210

 

Krauthacker et al. (1998)

Croatia

 

29

   

120

 

Krauthacker et al. (2009)

Croatia

 

10

 

110

 

140

 

Zubcic and Krauthacker (2004)

Czech Republic

220; 420

 

530; 1100

 

620; 1200

  

Bencko et al. (1998)

Czech Republic

260; 300

220; 260

  

940; 1100

780; 900

 

Cajka and Hajslova (2003)

Czech Republic

93–900

98–650

300–2000

310–1500

490–4900

480–3400

 

Cerna et al. (2010)

Czech Republic

270–480

   

860–1100

  

Schoula et al. (1996)

Finland

88; 110

   

350; 440

  

Vartiainen et al. (1997)

France

 

59

   

170

 

Brucker-Davis et al. (2010)

Germany

    

550

500

 

Schade and Heinzow (1998)

Germany

    

540; 1300

  

Schlaud et al. (1995)

Germany

140

   

310

  

Skopp et al. (2002)

Germany

90

   

210

  

Wittsiepe et al. (2007)

Germany

    

200

180

 

Zietz et al. (2008)

Italy

54

 

120

 

200

  

Alivernini et al. (2011)

Italy

110

110

  

280

280

 

Riva et al. (2004)

Italy

22–38

 

50–92

 

82–130

  

Ulaszewska et al. (2011)

Latvia

16–24

   

110–170

  

Bake et al. (2007)

Lithuania

130–160

 

290–360

 

400–480

  

Becher et al. (1995)

Netherlands

 

77

 

240

 

270

 

Albers et al. (1996)

Netherlands

120–140

 

300–350

 

360–410

  

van den Berg et al. (1995)

Norway

130–140

 

270; 300

 

330–380

  

Becher et al. (1995)

Norway

     

99

 

Eggesbo et al. (2006)

Norway

44–53

52

100–120

100–120

160–180

160–200

 

Polder et al. (2008b)

Norway

    

110; 120

100; 110

 

Polder et al. (2009)

Poland

    

190–550b

  

Czaja et al. (1997a)

Poland

40

35

  

150

130

 

Jaraczewska et al. (2006)

Poland

    

170–350

  

Pietrzak-Fiecko et al. (2005)

Poland

30; 38

 

56; 77

 

82;97

  

Skrbic et al. (2010)

Romania

58b

37b

  

9.7

6.5

 

Covaci et al. (2001)

Russia

120; 130

110; 120

30–230

20–210

300–350

290; 330

 

Polder et al. (1998)

Russia

50; 90

50; 50

120; 200

100; 180

190; 350

180; 320

 

Polder et al. (2008a)

Serbia

26b

11b

76b

27b

81b

31b

 

Vukavic et al. (2008)

Slovak Republic

230–480

 

540–1200

 

590–1300

  

Petrik et al. (2001)

Slovak Republic

200; 200

180; 180

  

600; 650

500; 540

 

Yu et al. (2007)

Spain

    

280

  

Schuhmacher et al. (2009)

Sweden

42–70

51

87–140

100

120–180

140

 

Athanasiadou and Bergman (2008)

Sweden

100

   

240

  

Atuma et al. (1998)

Sweden

51

48

  

140

130

 

Aune et al. (2002)

Sweden

29; 30

27

  

99; 100

98

 

Bergman et al. (2010)

Sweden

56

55

110

110

148

144

 

Darnerud (2001)

Sweden

 

64

     

Darnerud et al. (2010)

Sweden

74

69

150

136

170

160

 

Glynn et al. (2001)

Sweden

 

31–48

   

80–120

 

Glynn et al. (2011)

Sweden

61

   

190

  

Guvenius et al. (2003)

Sweden

47

43

  

120

110

 

Lignell et al. (2003)

Sweden

62

57

  

150

140

 

Lignell et al. (2004)

Sweden

58

52

  

140

120

 

Lignell et al. (2009b)

Sweden

58

   

110

  

Lignell et al. (2011)

Sweden

96

 

200

 

380

  

Lundén and Norén (1998)

Sweden

96

   

410

  

Norén et al. (1996)

Switzerland

36

28

  

290

240

 

Zehringer and Herrmann (2001)

Ukraine

     

600

 

Gladen et al. (2003)

Ukraine

     

490; 680

 

Gladen et al. (1999)

UK

 

49

   

180

150

Kalantzi et al. (2004)

Western Europe and other States

   

79

   

UNEP (2011)

Former Yugoslavia

    

11; 20

4.9; 8.2

 

Vukavic et al. (2003)

The Americas

Brazil

37

   

150

  

Paumgartten et al. (2000)

Canada

54

   

130

  

Dewailly et al. (1996)

Canada

      

620

Dewailly et al. (2000)

Canada

38

33.4

  

240

210

 

Newsome et al. (1995)

Canada

    

250

240

 

Newsome and Ryan (1999)

Canada and USA

50

   

220

  

Fitzgerald et al. (1998)

GROLACc

   

28

   

UNEP (2011)

Mexico

110

   

1500

  

Rodas-Ortiz et al. (2008)

USA

33

   

120

  

Fitzgerald et al. (1998)

USA

69

65

  

300

280

 

Greizerstein et al. (1999)

USA

  

57d

 

270

  

Kostyniak et al. (1999)

USA

17

    

77

 

Pan et al. (2010)

USA

    

91

  

Park et al. (2011)

USA

1.5; 9.0b

1.1; 6.0b

  

22; 29b

19; 20b

 

Weldon et al. (2011)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aSum of CB-28, CB-52, CB-101, CB-138, CB-153, and CB-180

bRecalculated from fresh weight, assuming 4 % fat content

cGroup of Latin America and Caribbean countries

dReported as the sum of CB-105, CB-132, and CB-153

Table 4

Concentrations (ng/g fat) of hexachlorobenzene (HCB) and the three HCH isomers, α-HCH, β-HCH, and γ-HCH, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented. Also the ∑HCH data are presented, giving data as reported in the studies referred to

Region

Country

HCB

α-HCH

β-HCH

γ-HCH

δ-HCH

∑HCHs

Reference

Mean

Median

Geo. mean

Mean

Median

Geo. mean

Mean

Median

Geo. mean

Mean

Median

Geo. mean

Mean

Median

Geo. mean

Mean

Median

Geo. mean

Africa

Africa

 

2.8

                

UNEP (2011)

Egypt

         

210a

     

210

  

Saleh et al. (1996)

Ghana

4.9

  

190

  

14

        

46

  

Darko and Acquaah (2008)

Ghana

40

                 

Ntow (2001)

Ghana

2.5–14

              

3.5–65

  

UNEP (2009)

Libya

   

140

  

240

  

120

     

500

  

Elafi et al. (2001)

Nigeria

5.0

              

29

  

UNEP (2009)

Senegal

3.7

              

65

  

UNEP (2009)

South Africa

1.9

1.8

             

12

4.3

 

Darnerud et al. (2011)

Swaziland

                  

Okonkwo et al. (1999)

Tunisia

0.38–290

     

16–110

  

3–70

     

26–130

  

Ennaceur et al. (2008)

Tunisia

260

     

50

        

67

  

Ennaceur et al. (2007)

Uganda

                  

Ejobi et al. (1998)

Asia, Australia, and the Pacific region

Asia and the Pacific

 

1.25

                

UNEP (2011)

Australia

6.6–76

14.3

 

0.03–0.18

0.047

 

7.6–660

21

 

0.08–.47

0.22

    

7.7–660

21

 

Harden et al. (2007)

Australia

30

19

 

0.18

0.13

 

24

27

 

0.2

0.2

    

24

27

 

Mueller et al. (2008)

Australia

                  

Noakes et al. (2006)

Australia

370–460

  

61–85

  

200–550

  

100–130

  

100–130

  

500–900

  

Quinsey et al. (1995)

Australia

51

35

    

9.8

        

9.8

  

Khanjani and Sim (2006)

Cambodia

1.6; 1.8

1.4; 1.5

             

4.8; 5.6

3.5; 3.6

 

Kunisue et al. (2004a)

China

56; 81

  

4.7; 5.0

  

550; 1400

  

0.93; 1.3

     

550; 1400

  

Kunisue et al. (2004a)

China

 

19; 48

  

3.7

  

240; 630

  

1.8; 1.8

     

240; 640

 

Leng et al. (2009)

China

   

5.3

3.9

 

55

42

 

4.5

2.9

 

4.3

1.5

 

80

55

 

Qu et al. (2010)

China

 

88; 100

85; 98

    

10; 180

21; 110

         

Sun et al. (2005)

China

      

950; 1100

           

Wong et al. (2002)

China

   

64

  

49.5

  

55.6

     

170

  

Yao et al. (2005)

China

   

0.80; 1.4

 

0.67; 1.0

310; 360

 

210; 280

2.3

 

2.4

0.91

 

0.72

310; 360

 

210; 290

Yu et al. (2009)

China

 

38; 48

33; 47

 

25; 76

18; 53

 

160; 210

200; 210

 

6.0; 17

8.0; 14

    

190; 350

260; 270

Zhao et al. (2007)

China

33

              

230

  

Zhou et al. (2011)

Hong Kong

               

1000

  

Poon et al. (2005)

Hong Kong and China

22

  

0.6

  

940

  

1.8

     

940

  

Hedley et al. (2010)

India

   

1800

  

8800

  

2300

     

13,000

  

Banerjee et al. (1997)

India

1.7–4.4

  

4.6–9.1

  

210–680

  

1.1–82

     

220–670

  

Devanathan et al. (2009)

India

   

32–37

  

39–43

  

51–54

     

120–130

  

Kumar et al. (2006)

India

   

640; 830

  

1000; 1100

  

600; 620

  

77; 170

  

2700; 2300

  

Mishra and Sharma (2011)

India

   

1100a

  

5000a

  

2100a

     

8200a

  

Nair et al. (1996)

India

      

1600a

  

900a

  

100a

  

2600a

  

Sanghi et al. (2003)

India

   

1800a

  

16,000a

  

1300a

  

2300a

  

22,000a

  

Siddiqui et al. (2002)

Indonesia

60

     

90

        

90

  

Burke et al. (2003)

Indonesia

1.8–2.3

1.6–2.3

 

0.02–0.22

0.08; 0.18

 

6.6–31

5.4–9.0

 

0.26–1.2

0.12; 0.22

    

7–30

5.5–8.3

 

Sudaryanto et al. (2006)

Indonesia

2.1

1.8

 

0.18

  

12

6.3

 

0.68

0.08

    

12

6.8

 

Sudaryanto et al. (2008a)

Iran

630–1500

280–820

 

880–1700

420–1300

 

1600–4000

910–15,000

 

126–460

70–240

    

2600–5700

1400–17,000

 

Behrooz et al. (2009)

Iran

61

  

22

  

400

  

180

     

600

  

Cok et al. (1999)

Japan

14

     

210

        

210

  

Konishi et al. (2001)

Japan

13

  

0.48

  

92

        

92

  

Kunisue et al. (2006)

Japan

 

7

     

28

        

28

 

Miyake et al. (2011)

Japan

0.18

              

1.2

  

Nagayama et al. (2007a)

Japan

       

330

        

330

 

Nagayama et al. (2007b)

Japan

34

     

63

        

63

  

Saito et al. (2005)

Jordan

61

  

82

  

390

  

39

     

510

  

Alawi et al. (2006)

Jordan

350

  

180

     

710

     

890

  

Nasir et al. (1998)

Kazakhstan

73–97

71–80

    

1700–2300

1400–1800

          

Lutter et al. (1998)

Kazakhstan

52–180

  

41–97

  

1600–3500

        

1600–3500

  

Hooper et al. (1997)

Korea

7.7

              

20

  

UNEP (2009)

Kuwait

   

0.69

  

3.6

  

1.1

     

5.4

  

Saeed et al. (2000)

Malaysia

11

  

1

  

230

  

1.3

     

230

  

Sudaryanto et al. (2005)

Philippines

1.7–2.5

1.5–1.9

 

0.24–0.29

0.17–0.25

 

3.2–4.9

2.7–4.0

 

0.15–0.34

0.14–0.16

    

3.6–5.5

3.1–4.3

 

Malarvannan et al. (2009)

Taiwan

      

1.9

  

1.5

     

3.4

  

Chao et al. (2006)

Thailand

130a

140a

       

90a

        

Stuetz et al. (2001)

Turkey

44–58

  

50–67

  

360–420

  

16–17

     

440–480

  

Cok et al. (1997)

Turkey

39

  

1

  

150

  

8

     

160

  

Cok et al. (2011)

Turkey

73

  

27

  

280

  

14

     

340

  

Cok et al. (2005)

Turkey

 

20

     

150

  

3

     

150

 

Erdogrul et al. (2004)

Turkey

   

5.9

2.5

 

5.90

14

 

2.8

10

 

8.04

5.01

 

23

32

 

Ozcan et al. (2011)

Uzbekistan

 

28

  

76

  

1100

  

8

     

1200

 

Ataniyazova et al. (2001)

Vietnam

7.4–86

     

49–570

           

Haraguchi et al. (2009)

Vietnam

2.5; 3.9

     

14; 58

           

Minh et al. (2004)

Vietnam

 

1.8; 3.0

  

0.20

  

5.1; 18

  

0.055

     

5.8; 18

 

Nguyen et al. (2010)

Europe

Belgium

16.2

                 

Colles et al. (2008)

Central and Eastern Europe

 

3.1

                

UNEP (2011)

Croatia

4.2

4.0

       

1.1

     

1.1

  

Frkovic et al. (1996)

Croatia

 

7.4–12

  

1.5–2.4

  

19–20

  

15–18

     

36–41

 

Romanic and Krauthacker (2006)

Croatia

 

11–31

     

24–39

        

26–40

 

Krauthacker et al. (1998)

Croatia

 

5–13

  

2

  

12–54

  

7–14

     

24–62

 

Krauthacker et al. (2009)

Czech Republic

320; 420

250; 370

    

56; 64

55; 57

       

56; 64

55; 57

 

Cajka and Hajslova (2003)

Czech Republic

119–748

92–357

    

22–36

20–27

          

Cerna et al. (2010)

Czech Republic

480–640

     

71–80

           

Schoula et al. (1996)

Denmark

12

  

0.51

  

18

  

0.74

  

0.06

  

740

740

 

Shen et al. (2007)

Denmark

 

12

  

0.26

  

17

  

0.65

  

0.04

  

18

 

Shen et al. (2008)

Finland

8.4

  

0.19

  

12

  

0.61

  

0.04

  

860

660

 

Shen et al. (2007)

Finland

 

8.0

  

0.16

  

11

  

0.4

  

0.03

  

12

 

Shen et al. (2007)

Finland and Denmark

 

10

  

0.19

  

13

        

13

 

Damgaard et al. (2006)

France

 

23

                

Brucker-Davis et al. (2010)

Germany

27

21

    

17

8

       

17

8

 

Raab et al. (2008)

Germany

80

70

    

40

40

       

40

40

 

Schade and Heinzow (1998)

Germany

150; 220

     

45; 59

  

12; 16

     

61; 71

  

Schlaud et al. (1995)

Germany

27; 38

23; 31

    

21; 27

12; 17

 

1.7; 3.7

3

    

22–30

12–20

 

Zietz et al. (2008)

Greece

   

6.0

  

15.51

  

7.0

  

6.8

  

59

  

Schinas et al. (2000)

Italy

38–70

                 

Abballe et al. (2008)

Latvia

19–32

  

0.18–0.27

  

42–90

  

0.06–0.34

     

42–90

  

Bake et al. (2007)

Norway

12

12

                

Eggesbo et al. (2009)

Norway

17–19

18–20

 

0.2–0.2

0.2–0.2

 

10–16

9.2–14

 

0.3–0.7

0.3–0.5

    

10–17

9.7–14

 

Polder et al. (2008b)

Norway

11; 15

11; 13

    

5.4; 18

4.7; 8.1

          

Polder et al. (2009)

Poland

33–55a

  

5.0–20a

  

35–100a

  

5–12a

     

45–130a

  

Czaja et al. (1997b)

Poland

32

29

    

13.3

11

 

0.8

     

14

11

 

Jaraczewska et al. (2006)

Romania

20

  

43

  

27.5

  

75

  

45

  

190

  

Cioroiu et al. (2010)

Romania

16a

14a

 

17a

15a

 

480a

440a

 

35a

15a

    

520a

440a

 

Covaci et al. (2001)

Russia

58; 65

55; 58

 

3.0; 3.2

2.0; 3.0

 

180; 230

160; 190

 

0.5; 2.0

0.5; 1.0

    

240

200

 

Polder et al. (2008a)

Russia

110; 130

93;110

 

4.5; 5.6

3.8; 5.7

 

740; 850

620; 660

 

0.4; 0.7

0.3; 0.7

    

750; 860

620; 660

 

Polder et al. (1998)

Russia

100; 130

  

10; 18

  

800; 1000

  

0.45; 0.58

     

810; 1000

  

Tsydenova et al. (2007)

Serbia

   

11; 38a

13; 56a

    

33; 50a

29; 38a

    

110; 190a

100; 130a

 

Vukavic et al. (2003)

Slovak Republic

19–240

5.0–170

    

11–87

10–65

 

2.0–12

1.0–7.0

    

18–95

14–70

 

Veningerova et al. (2001)

Slovak Republic

98; 102

79; 80

    

19; 20

15; 16

       

19; 20

15; 16

 

Yu et al. (2007)

Spain

340a

     

8.3a

           

Pico et al. (1995)

Spain

 

630; 910

                

Ribas-Fito et al. (2005)

Sweden

11.7

11.8

    

15

9.6

       

15

9.6

 

Aune et al. (2002)

Sweden

8.2; 11

7.7

    

6.4; 32

6.3

          

Bergman et al. (2010)

Sweden

15.1

13.7

    

15

10

       

15

9.7

 

Darnerud (2001)

Sweden

9.4

8.8

    

7.9

7.2

       

7.9

7.2

 

Lignell et al. (2003)

Sweden

15

14

    

14

12

       

14

12

 

Lignell et al. (2004)

Sweden

31

                 

Lundén and Norén (1998)

Sweden

                  

Norén et al. (1996)

Sweden

6.3–8.5

     

3.5–6.4

           

Athanasiadou and Bergman (2008)

Netherlands

 

100

     

80

          

Albers et al. (1996)

Ukraine

 

150; 190

     

710; 750

          

Gladen et al. (1999)

Ukraine

 

168

     

730

        

730

 

Gladen et al. (2003)

UK

43

25

    

68

50

       

68

50

 

Harris et al. (1999)

UK

 

18

17

  

0.2

 

17

15

 

0.6

0.8

   

16

18

 

Kalantzi et al. (2004)

Western Europe and other States

 

2.3

                

UNEP (2011)

The Americas

Antigua and Barbuda

5.3

              

5

  

UNEP (2009)

Brazil

12

  

1

  

270

  

5

     

280

  

Paumgartten et al. (2000)

Canada

                  

Dewailly et al. (1996)

Canada

  

107

               

Dewailly et al. (2000)

Canada

43

43

 

4.4

1.6

 

18

21

 

0.76

0.66

    

23

23

 

Newsome and Ryan (1999)

Canada

15

8–12a

 

0.31

  

23

12–16a

 

1.0

     

24

19

 

Newsome et al. (1995)

Canada and USA

  

12

               

Fitzgerald et al. (2001)

Chile

11

              

6.4

  

UNEP (2009)

Mexico

    

60–160

  

160–230

        

280–320

 

Elvia et al. (2000)

Mexico

                  

Pardio et al. (1998)

Mexico

92

  

310

  

610

  

380

  

240

  

750

  

Rodas-Ortiz et al. (2008)

Mexico

53

  

19

  

430

  

84

     

530

  

Waliszewski et al. (1998)

Mexico

25; 41

 

20; 35

1.0; 4.0

  

61; 90

 

44; 66

2; 4

     

63; 99

 

48; 74

Waliszewski et al. (1999a)

Mexico

30

 

20

   

60

 

40

      

60

 

50

Sun et al. (2010)

Nicaragua

      

6.0

  

1

     

7

  

Romero et al. (2000)

Uruguay

14.

              

30

  

UNEP (2009)

USA

15.

 

15

               

Greizerstein et al. (1999)

USA

2.3

 

1.6

1.7

1.4

 

7.7

4.4

 

7.6

5.1

 

1.9

  

19

13

 

Johnson-Restrepo et al. (2007)

USA

  

14

               

Fitzgerald et al. (2001)

USA

9.6

                 

Kostyniak et al. (1999)

USA

5.8; 6.6a

4.8; 5.6a

    

7.8; 14a

5.5; 11a

          

Weldon et al. (2011)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

Table 5

Concentrations (ng/g fat) of oxychlordane, α-chlordane, γ-chlordane, and ∑chlordanes, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

Oxychlordane

α-Chlordane

γ-Chlordane

∑Chlordanes

Reference

Mean

Median

Mean

Median

Mean

Median

Mean

Median

Africa

Africa

       

4.1

UNEP (2011)

Ghana

      

1.2

 

UNEP (2009)

Nigeria

      

2.4

 

UNEP (2009)

Senegal

      

11.7

 

UNEP (2009)

Asia and the Pacific region

Asia and the Pacific

       

3.6

UNEP (2011)

Australia

7.6

7

      

Khanjani and Sim (2006)

Australia

2.8–18

       

Harden et al. (2007)

Australia

5.1

5.1

  

5.5

5.4

  

Mueller et al. (2008)

Australia

140; 150

       

Quinsey et al. (1995)

Australia

 

7

      

Sim et al. (1998)

China

0.49

       

Haraguchi et al. (2009)

China

2.9; 8

       

Kunisue et al. (2004a)

China

 

1.0; 1.0

 

1.2

    

Leng et al. (2009)

Hong Kong and China

6.1

     

6.1

 

Hedley et al. (2010)

India

      

2.6–3.4

 

Devanathan et al. (2009)

Indonesia

0.49–2.4

0.49–0.73

    

7.0–30

5.5–8.3

Sudaryanto et al. (2006)

Japan

3–4.8

       

Haraguchi et al. (2009)

Japan

      

85

 

Konishi et al. (2001)

Japan

14

     

58

 

Kunisue et al. (2006)

Japan

      

0.76

 

Nagayama et al. (2007a)

Jordan

  

460

 

590

   

Nasir et al. (1998)

Korea

5.1

       

Haraguchi et al. (2009)

Korea

      

3.7

 

UNEP (2009)

Malaysia

7.1

       

Sudaryanto et al. (2005)

Taiwan

  

10

     

Chao et al. (2006)

Philippines

1.7–3.0

1.6–2.5

0.59–1.4

0.52–0.60

    

Malarvannan et al. (2009)

Turkey

7a

5a

      

Erdogrul et al. (2004)

Vietnam

0.047

       

Haraguchi et al. (2009)

Vietnam

0.9; 2.4

 

0.8; 1.1

 

1.5; 3.7

 

2; 6.9

 

Minh et al. (2004)

Vietnam

 

0.26; 0.51

     

0.4; 0.96

Nguyen et al. (2010)

Europe

Central and Eastern Europe

       

1.85

UNEP (2011)

Denmark

5.1

 

0.03

 

0.05

   

Shen et al. (2007)

Denmark

 

4.7

 

0.03

 

0.05

  

Shen et al. (2008)

Finland

4.0

 

0.02

 

0.04

   

Shen et al. (2007)

Finland

 

3.6

 

0.02

 

0.03

  

Shen et al. (2008)

Finland and Denmark

 

4.3

   

0.050

  

Damgaard et al. (2006)

Germany

5

4

      

Raab et al. (2008)

Germany

8.8

       

Skopp et al. (2002)

Norway

3.6–4.9

3.9–5.0

1.6–2.3

1.4–2.5

    

Polder et al. (2008b)

Norway

3.0; 4.4

2.8; 3.2

      

Polder et al. (2009)

Poland

3.3

2.8

      

Jaraczewska et al. (2006)

Russia

5; 6

5; 5

1; 3

1; 2

  

21; 22

16; 20

Polder et al. (2008a)

Russia

3.9; 5.6

     

10; 19

 

Tsydenova et al. (2007)

Russia

7.9; 8.1

 

3.3; 6.9

3; 5.4

  

33; 59

21; 52

Polder et al. (1998)

Sweden

2.5–3.5

2.4; 3.4

      

Athanasiadou and Bergman (2008)

Sweden

4.4

3.6

      

Darnerud (2001)

Sweden

3.3

3.1

      

Lignell et al. (2003)

Sweden

4.4

3.8

      

Lignell et al. (2004)

Ukraine

 

16; 22

      

Gladen et al. (1999)

Ukraine

 

18

      

Gladen et al. (2003)

UK

   

0.3

    

Kalantzi et al. (2004)

Western Europe and other States

       

3.6

UNEP (2011)

The Americas

Antigua and Barbuda

      

4.4

 

UNEP (2009)

Canada

59

43

1.3

     

Newsome and Ryan (1999)

Canada

13

7.8–13a

0.21

 

0.16

   

Newsome et al. (1995)

Chile

      

2

 

UNEP (2009)

GROLACb

       

4.4

UNEP (2011)

Mexico

 

30–40

      

Elvia et al. (2000)

Mexico

  

260

 

930

 

970

 

Rodas-Ortiz et al. (2008)

Uruguay

      

4.4

 

UNEP (2009)

USA

17

3.8

2.7

1.2

1.1

   

Johnson-Restrepo et al. (2007)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

bGroup of Latin America and Caribbean countries

Table 6

Concentrations (pg TEQs/g fat) PCDDs/PCDFs and DL-PCBs, in mothers’ milk, as reported in studies from around the world, 1995 – 2011 are presenteda. Also the ∑TEQs levels are presented, giving data as reported in the studies referred to

Region

Country

∑PCDD/F

∑DL-PCB

Total-TEQ

mean

median

mean

mean

mean

median

(TEQ1998)

(TEQ2005)

(TEQ1998)

(TEQ2005)

(TEQ1998)

(TEQ2005)

(TEQ1998)

(TEQ2005)

(TEQ1998)

Reference

Africa

           

Africa

   

3.6

     

(UNEP 2011)

Ghana

        

3.2

(UNEP 2009)

Nigeria

        

3.1

(UNEP 2009)

Senegal

        

7.2

(UNEP 2009)

Asia and the Pacific region

           

Asia & the Pacific

   

4.5

     

(UNEP 2011)

China

15

9.0

       

(Chan et al. 2007)

China

      

2.9-16

2.4-13

 

(Li et al. 2009)

China

4.9

3.9

  

3.3

2.3

8.2

6.2

 

(Sun et al. 2011)

China

4.4-6.2

1.9-3.9

     

6.2-7.5

 

(Sun et al. 2010)

China

0.12

0.29

       

(Zheng et al. 2003)

China

  

17; 17

     

23

(Sun et al. 2005)

Hong Kong

8.2

7.2

    

13

  

(Hedley et al. 2006)

Japan

13

11

    

21

  

(Kunisue et al. 2006)

Japan

      

0.28

  

(Nagayama et al. 2007a)

Japan

11

9.7

    

19

  

(Nakamura et al. 2008)

Japan

19

10

  

6

7

25

18

 

(Saito et al. 2005)

Japan

17

15

  

6.8

5.5

24

21

 

(Suzuki et al. 2005)

Japan

15

13

  

11

 

26

13

 

(Tajimi et al. 2005)

Japan

6.9

1.1

  

4.6

3.4

11

8.6

 

(Todaka et al. 2011)

Japan

        

23

(Nagayama et al. 2007b)

Kazakhstan

23; 46

21; 45

       

(Hooper et al. 1998)

Korea

       

4.0

 

(UNEP 2009)

Korea

10; 23

8.9; 21

  

4.8; 6.1

3.5; 4.8

15; 29

12; 25

 

(Yang et al. 2002)

Taiwan

7.4; 12

0.73; 6.6

    

12

  

(Chao et al. 2005)

Taiwan

15

13

       

(Hsu et al. 2007)

Taiwan

7.6

     

13

  

(Wang et al. 2004)

Turkey

4.9-12

3.9-10

    

6.8-16

  

(Cok et al. 2009)

Uzbekistan

  

22

      

(Ataniyazova et al. 2001)

Vietnam

   

2.7; 6.6

     

(Nhu et al. 2011)

Vietnam

0.086; 0.13

0.073-0.12

       

(Tawara et al. 2011)

Europe

           

Belgium

29

16

32

   

41

 

42

(Focant et al. 2002)

Central &

          

Eastern Europe

   

5.9

     

(UNEP 2011)

Czech Rep.

13; 20

9.8; 15

  

6.0-9.8

4.7-8.6

19-30

15-23

 

(Bencko et al. 1998)

Faroe Islands

36

31

  

14

14

50

46

 

(Grandjean et al. 1995)

Finland

  

8.6; 12

     

14; 19

(Alaluusua et al. 2002)

Finland

21; 26

19; 23

  

22; 29

13; 19

43; 55

32; 42

 

(Vartiainen et al. 1997)

Germany

9.8

4.9

    

20

14

 

(Raab et al. 2008)

Germany

14

11

    

27

11

 

(Wittsiepe et al. 2007)

Italy

9.4-15

7.8-12

    

20-34

  

(Abballe et al. 2008)

Italy

4.6-6.1

3.8-4.9

  

6.2-6.9

4.8-5.7

11-13

8.6-11

 

(Ulaszewska et al. 2011)

Latvia

7.1-12

5.8-9.2

  

170; 190

 

170; 200

  

(Bake et al. 2007)

Lithuania

14-18

12-15

  

30-30

16-17

44-48

28-31

 

(Becher et al. 1995)

Norway

9.7-13

8.2-11

  

18-30

9.3-20

29-40

18-29

 

(Becher et al. 1995)

Russia

16; 28

7.2; 9.5

    

27; 28

  

(Schecter et al. 2002)

Slovak Rep.

5.7-12

4.5-9.0

    

14-24

  

(Chovancova et al. 2011)

Spain

      

10.9

  

(Bordajandi et al. 2008)

Spain

   

7.6

 

9

 

16.6

 

(Schuhmacher et al. 2009)

Sweden

13

11

  

13

12

26

24

 

(Atuma et al. 1998)

Sweden

  

9

     

13

(Darnerud et al. 2010)

Sweden

8.8

7.6

    

19

  

(Glynn et al. 2001)

Sweden

8.1

6.9

7.4

6.4

8.1

5.6

16

13

15

(Glynn et al. 2007)

Sweden

8.2

7.0

    

16

13

 

(Lignell et al. 2009a)

Sweden

21

15

  

20

13

40

28

 

(Lundén and Norén 1998)

Sweden

3.5

2.9

  

3.6

2.2

7.0

5.0

 

(Fång et al. 2013)

Western Europe & other States

   

6.0

     

(UNEP 2011)

The Americas

           

Antigua & Barbuda

       

4.3

 

(UNEP 2009)

Brazil

10

10

  

4.4

0.60

14

11

 

(Paumgartten et al. 2000)

Canada

4.9-14

3.3-8.3

    

6.5-18

  

(Newsome & Ryan 1999)

Chile

       

9.7

 

(UNEP 2009)

GROLACa

   

5.6

     

(UNEP 2011)

Uruguay

       

6.9

 

(UNEP 2009)

 

Country

∑PCDD/F

∑PCDD/F

∑PCDD/F

∑PCDD/F

Total-TEQ

Total-TEQ

  

(mean,TEQ1998)

(mean,TEQ2005)

(mean, I-TEQ)

(CALUX-TEQ)

(CALUX-TEQ)

(EROD-TEQ)

 

Brazilb

10

 

8.1

   

(Paumgartten et al. 2000)

China

  

9.4; 13

14; 15

  

(Leng et al. 2009)

Chinab

0.12

0.29

1.0

   

(Zheng et al. 2003)

Hong Kong

     

18

(Tsang et al. 2009)

Germany

  

20; 23

   

(Schlaud et al. 1995)

Kazakhstanb

23; 46

 

20; 40

   

(Hooper et al. 1998)

Spain

12

 

10

   

(Schuhmacher et al. 2004)

aWhen concentrations from more than one sampling site in the same country and study have been reported the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a hyphen “–“ (for more than two concentrations)

bIncluded for comparison with WHO TEQs, not unique samples

cGroup of Latin America and Caribbean Countries

Table 7

Concentrations (ng/g fat) of BDE-47, BDE-209, and ∑PBDE, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

BDE-47

BDE-209

∑PBDE

Reference

Country

Mean

Median

Geo. mean

Mean

Median

Mean

Median

Geo. mean

Africa

Ghana

0.77–2.1

0.49–1.7

 

0.83–1.4

0.39–0.95

2.2–5.8

1.3–4.3

 

Asante et al. (2011)

South Africa

0.29

0.3

   

1.7

1.4

 

Darnerud et al. (2011)

Asia and the Pacific region

China

0.89

    

1.9

  

Haraguchi et al. (2009)

China

0.33; 0.66

0.32; 0.62

 

0.95; 1.3

1.8

4.7; 7.7

2.8; 7.1

 

Sudaryanto et al. (2008b)

China

0.23–0.74

0.22–0.71

 

0.22–0.70

0.22–0.57

3.4–4.2

2.2–4.1

 

Sun et al. (2010)

China

0.21–0.73

    

0.85–3.0

  

Zhang et al. (2011)

Hong Kong and South China

1.9

    

3.4

  

Hedley et al. (2010)

Indonesia

0.22–0.58

  

0.53; 0.54

 

0.91–1.8

  

Sudaryanto et al. (2008a)

Japan

0.37

    

1.4

  

Akutsu et al. (2003)

Japan

19

0.58

   

31

1.5

 

Akutsu and Hori (2004)

Japan

0.57–0.76

    

1.3–1.7

  

Haraguchi et al. (2009)

Japan

2.1a

0.43a

   

4.6

3

 

Kawashiro et al. (2008)

Korea

2

    

3.7

  

Haraguchi et al. (2009)

Korea

1.2

    

2.7

  

Kim et al. (2011b)

Philippines

1.2; 4.9

1.1; 1.2

 

1.8

1.8

2.6; 10

2.7; 4.2

 

Malarvannan et al. (2009)

Taiwan

0.58

0.52

 

0.48

0.36

3.5

3.3

 

Koh et al. (2010)

Turkey

0.15a

0.1a

   

0.2a

0.1a

 

Erdogrul et al. (2004)

Turkey

6.0

3.3

   

67

43

 

Ozcan et al. (2011)

Vietnam

0.19

    

0.42

  

Haraguchi et al. (2009)

Vietnam

 

0.13; 0.40

  

0.57; 2.3

 

1.1; 4.0

 

Tue et al. (2010)

Europe

Czech Republic

0.86

0.61

      

Kazda et al. (2004)

France

    

1.5

 

2.7

 

Antignac et al. (2008)

Germany

0.67

0.48

   

2.0

1.6

 

Raab et al. (2008)

Italy

0.82

    

1.3

  

Alivernini et al. (2011)

Norway

1.7

0.95

 

0.5

0.25

3.3

1.9

 

Eggesbo et al. (2011)

Norway

1.7

1.3

 

0.22

0.13

3.8

3.2

 

Polder et al. (2008b)

Norway

1.7

   

0.32

3.4

2.1

 

Thomsen et al. (2010)

Poland

1.1

0.73

   

2.5

2

 

Jaraczewska et al. (2006)

Russia

0.43; 0.65

0.36; 0.58

 

0.35

0.19

1.1; 1.2

0.96; 1.1

 

Polder et al. (2008a)

Russia

      

0.96

 

Tsydenova et al. (2007)

Spain

     

0.33

  

Bordajandi et al. (2008)

Spain

      

2.5

 

Schuhmacher et al. (2009)

Sweden

1.6; 2

  

0.2; 1.5

 

3.9; 4.8

  

Athanasiadou and Bergman (2008)

Sweden

1.79

1.3

   

3.0

2.4

 

Aune et al. (2002)

Sweden

0.93; 2.4

0.71

 

0.66

 

2.1; 4.3

1.9

 

Bergman et al. (2010)

Sweden

1.9

1.7

   

3.2

3.2

 

Darnerud (2001)

Sweden

0.92

    

2.4

  

Fängström et al. (2008)

Sweden

 

1.2–1.8

    

2.2–3.3

 

Glynn et al. (2011)

Sweden

 

1.2

      

Guvenius et al. (2003)

Sweden

1.8

1.3

   

3.4

2.8

 

Lignell et al. (2003)

Sweden

1.2

0.76

      

Lignell et al. (2009b)

Sweden

1.9

1.5

   

3.5

2.9

 

Lignell et al. (2009a)

Sweden

1.5

1.5

   

2.6

2.5

 

Lind et al. (2003)

Sweden

2.3

    

4.0

  

Meironyté et al. (1999)

UK

 

2.7

3.0

   

6.3

6.6

Kalantzi et al. (2004)

The Americas

USA

 

28

    

51

 

Daniels et al. (2010)

USA

41

7.7

   

75

20

 

Johnson-Restrepo et al. (2007)

USA

73

  

3.7

1.4

130

  

Park et al. (2011)

USA

41

18

 

0.92

 

74

34

 

Schecter et al. (2003)

USA

36

17

 

1.4

0.10

66

30

 

Schecter et al. (2005)

USA

36

24

   

76

40

 

Schecter et al. (2010)

When concentrations from more than one sampling site in the same country and study are reported, the concentrations are given as two values separated by a semicolon (two concentrations) or a dash (for more than two levels)

aRecalculated from fresh weight, assuming 4 % fat content

Table 8

Concentrations (ng/g fat) of cis-HCL-epoxide, HCL-epoxide, and heptachlor, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

cis-HCL-epoxide

HCL-epoxide

Heptachlor

Reference

Mean

Mean

Median

Mean

Median

Africa

Africa

    

2.25

UNEP (2011)

Ghana

   

0.9

 

UNEP (2009)

Nigeria

   

0.9

 

UNEP (2009)

Senegal

   

1.3

 

UNEP (2009)

Asia and the Pacific region

Asia and the Pacific

    

0.55

UNEP (2011)

Australia

 

2.2–17

7.4

  

Harden et al. (2007)

Australia

 

5.9

6

  

Mueller et al. (2008)

Australia

 

53; 78

   

Quinsey et al. (1995)

Australia

  

7

  

Sim et al. (1998)

Australia

 

9.9

7

  

Khanjani and Sim (2006)

China

0.7

    

Hedley et al. (2010)

Iran

 

54

   

Cok et al. (1999)

Japan

 

7.5

   

Konishi et al. (2001)

Japan

 

7.4

   

Saito et al. (2005)

Japan

 

3

   

Nagayama et al. (2007a)

Jordan

 

190

 

500

 

Nasir et al. (1998)

Korea

   

2.2

 

UNEP (2009)

Kuwait

 

1.3

   

Saeed et al. (2000)

Taiwan

 

4.3

 

3

 

Chao et al. (2006)

Thailand

 

160a

110a

110a

110a

Stuetz et al. (2001)

Turkey

 

61

   

Cok et al. (2005)

Turkey

 

38

   

Cok et al. (2011)

Europe

Central and Eastern Europe

    

0.50

UNEP (2011)

Croatia

 

0.7

   

Frkovic et al. (1996)

Denmark

  

2.9

  

Shen et al. (2008)

Denmark

2.8

    

Shen et al. (2007)

Denmark and Finland

  

2.3

  

Damgaard et al. (2006)

Finland

  

2.0

  

Shen et al. (2008)

Finland

2.2

    

Shen et al. (2007)

Germany

 

4

3

  

Raab et al. (2008)

Germany

   

21; 22

 

Schlaud et al. (1995)

Germany

 

0.11

   

Zietz et al. (2008)

Germany

7.3

    

Skopp et al. (2002)

Netherlands

  

30

  

Albers et al. (1996)

Spain

   

9a

 

Pico et al. (1995)

Ukraine

  

22

  

Gladen et al. (1999)

Ukraine

  

16

  

Gladen et al. (2003)

The Americas

Antigua and Barbuda

   

1.4

 

UNEP (2009)

Brazil

8

    

Paumgartten et al. (2000)

Canada

 

0.94

   

Newsome and Ryan (1999)

Canada

 

3.8

0.75–3.2a

  

Newsome et al. (1995)

Chile

   

1.7

 

UNEP (2009)

GROLACb

    

1.4

UNEP (2011)

Mexico

  

40

  

Elvia et al. (2000)

Mexico

 

160

 

580

 

Rodas-Ortiz et al. (2008)

Nicaragua

 

6

 

1

 

Romero et al. (2000)

Uruguay

   

1

 

UNEP (2009)

Western Europe and other States

    

0.8

UNEP (2011)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

bGroup of Latin America and Caribbean countries

Table 9

Concentrations (ng/g fat) of aldrin, dieldrin, endrin, and ∑drins, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

Aldrin

Dieldrin

Endrin

∑drins

Reference

Mean

Median

Mean

Median

Geo. mean

Mean

Median

Mean

Africa

Africa

   

2.8

    

UNEP (2011)

Ghana

  

120

     

Ntow et al. (2008)

Ghana

  

1.3

     

UNEP (2009)

Nigeria

  

4.1

     

UNEP (2009)

Senegal

  

3.1

     

UNEP (2009)

Tunisia

  

25

     

Ennaceur et al. (2008)

Tunisia

  

59

36

    

Ennaceur et al. (2007)

Asia and the Pacific region

Asia and the Pacific

   

1.8

    

UNEP (2011)

Australia

  

51

40

    

Khanjani and Sim (2006)

Australia

0.01–0.68

 

15

     

Harden et al. (2007)

Australia

0.19

0.05

16

14

    

Mueller et al. (2008)

Australia

   

25a

    

Noakes et al. (2006)

Australia

  

150; 160

     

Quinsey et al. (1995)

Australia

   

39

    

Sim et al. (1998)

China

  

9300–10,000a

     

Wang et al. (2008)

China

       

7.9

Zhou et al. (2011)

China and Hong Kong

  

1.1

     

Hedley et al. (2010)

India

250a

       

Siddiqui et al. (2002)

Japan

  

28

     

Konishi et al. (2001)

Japan

   

3

    

Nagayama et al. (2007a)

Jordan

860

 

1400

   

3300

 

Nasir et al. (1998)

Korea

  

1.3

     

UNEP (2009)

Kuwait

5.2

 

4.2

  

4.0

  

Saeed et al. (2000)

Europe

Central and Eastern Europe

   

1.6

    

UNEP (2011)

Croatia

1.3

 

1.0

  

2.0

0.7

 

Frkovic et al. (1996)

Denmark

    

5.1

   

Shen et al. (2007)

Denmark

   

4.9

    

Shen et al. (2008)

Finland

    

2.8

   

Shen et al. (2007)

Finland

   

2.4

    

Shen et al. (2008)

Finland and Denmark

   

3.6

    

Damgaard et al. (2006)

Germany

  

14

     

Schlaud et al. (1995)

Germany

  

0.018–3.8

4

    

Zietz et al. (2008)

Germany

  

4

2

    

Raab et al. (2008)

Great Britain

  

48

25

    

Harris et al. (1999)

Netherlands

   

50

    

Albers et al. (1996)

Western Europe and other States

   

2.5

    

UNEP (2011)

The Americas

Antigua and Barbuda

  

2.6

     

UNEP (2009)

Brazil

  

23

     

Paumgartten et al. (2000)

Canada

  

11

1.1

    

Newsome and Ryan (1999)

Canada

  

9.8

8.5

    

Newsome et al. (1995)

Canada

    

30

   

Dewailly et al. (2000)

Chile

  

5.0

     

UNEP (2009)

Group of Latin America and Caribbean countries

   

4.9

    

UNEP (2011)

Mexico

   

30–50

    

Elvia et al. (2000)

Mexico

280

 

300

  

290

  

Rodas-Ortiz et al. (2008)

Nicaragua

  

18

  

3.0

  

Romero et al. (2000)

Uruguay

  

4.9

     

UNEP (2009)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

Table 10

Concentrations (ng/g fat) of pentachlorobenzene (PCBz), toxaphene, and mirex, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

PCBz

∑Toxaphene

Mirex

Reference

Mean

Median

Geo. mean

Mean

Median

Mean

Median

Geo. mean

Africa

Nigeria

   

4.1

    

UNEP (2009)

Asia and the Pacific region

Australia

      

0.21

 

Harden et al. (2007)

Australia

      

0.18

 

Mueller et al. (2008)

China

      

2.4

 

Zhou et al. (2011)

Hong Kong and South China

   

0.8

    

Hedley et al. (2010)

Korea

    

0.8

   

UNEP (2009)

Europe

Denmark

  

0.36

  

0.23

  

Shen et al. (2007)

Denmark

 

0.32

    

0.21

 

Shen et al. (2008)

Finland

  

0.27

  

0.31

  

Shen et al. (2007)

Finland

 

0.25

    

0.26

 

Shen et al. (2008)

Finland and Denmark

 

0.28

    

0.22

 

Damgaard et al. (2006)

Germany

   

16

    

Skopp et al. (2002)

Norway

        

Polder et al. (2008b)

Russia

   

10; 20

10; 19

0.5; 0.8

0.5; 0.7

 

Polder et al. (2008a)

The Americas

Antigua and Barbuda

   

1.3

    

UNEP (2009)

Canada

       

14

Dewailly et al. (2000)

Canada

       

3.0

Fitzgerald et al. (2001)

Canada

1.0

0.91

 

68

56

2.3

1.8

 

Newsome and Ryan (1999)

Canada

1.5a

1.2a

   

1.9a

1.6a

 

Newsome et al. (1995)

Mexico

     

200

  

Rodas-Ortiz et al. (2008)

Uruguay

     

9.8

  

UNEP (2009)

USA

      

1.0–5.8

 

Madden and Makarewicz (1996)

USA

       

1.4

Fitzgerald et al. (2001)

USA

      

2.4

 

Greizerstein et al. (1999)

USA

     

4.8

  

Kostyniak et al. (1999)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

Table 11

Concentrations (ng/g fat) of HBCDD and PBB, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

α-HBCDD

β-HBCDD

γ-HBCDD

∑HBCDD

∑PBB

Reference

Mean

Median

Mean

Median

Mean

Median

Mean

Median

Mean

Africa

Ghana

0.29–0.79

0.23–0.62

0.010

   

0.30–0.80

0.27–0.62

 

Asante et al. (2011)

South Africa

      

0.55

0.34

 

Darnerud et al. (2011)

Asia

China

0.33–2.8

   

0.46

 

0.33–2.8

  

Shi et al. (2009)

Japan

1.4

     

1.4

  

Kakimoto et al. (2008)

Philippines

0.58; 0.72

0.50; 0.67

0.052; 0.18

0.043; 0.12

0.14; 0.48

0.13; 0.23

0.81; 1.0

0.52; 0.89

 

Malarvannan et al. (2009)

Vietnam

 

0.33; 0.38

     

0.33; 0.38

 

Tue et al. (2010)

Europe

Denmark

        

0.26

Shen et al. (2008)

Finland

        

0.17

Shen et al. (2008)

Norway

      

1.7

0.86

 

Thomsen et al. (2010)

Russia

      

0.47; 0.71

0.45; 062

 

Polder et al. (2008a)

Spain

14

4.4

  

40

23

47

27

 

Eljarrat et al. (2009)

Sweden

      

0.45

0.30

 

Aune et al. (2002)

Sweden

      

0.63a; 0.80a

0.58a

 

Bergman et al. (2010)

Sweden

      

0.39

  

Fängström et al. (2008)

Sweden

       

0.3–0.4

 

Glynn et al. (2011)

Sweden

      

0.42

0.35

 

Lignell et al. (2003)

UK

4.9

3.2

0.32

0.30

0.49

0.50

6.0

3.8

 

Abdallah and Harrad (2011)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aQuantified using BDE-139 as surrogate standard

Table 12

PFOS concentrations in mothers’ milk, expressed in picograms per milliliter of milk as reported in studies from around the world, 1995–2011, are presented

Region

Country

Mean (pg/mL)

Median (pg/mL)

Reference

Asia and the Pacific

Cambodia

67

40

Tao et al. (2008a)

China

6–140

 

Liu et al. (2010)

China

120

100

So et al. (2006)

India

46

39

Tao et al. (2008a)

Indonesia

84

67

Tao et al. (2008a)

Japan

230

200

Tao et al. (2008a)

Malaysia

120

110

Tao et al. (2008a)

Philippines

98

100

Tao et al. (2008a)

South Korea

61

 

Kim et al. (2011a)

Vietnam

76

59

Tao et al. (2008a)

Europe

Germany

120; 130

110; 120

Volkel et al. (2008)

Germany

40

 

Fromme et al. (2010)

Hungary

310

330

Volkel et al. (2008)

Spain

120

110

Kärrman et al. (2010)

Spain

120

 

Llorca et al. (2010)

Sweden

120–260

170

Kärrman et al. (2007)

Sweden

120

 

Kärrman et al. (2006)

Sweden

75

 

Sundström et al. (2011)

The Americas

USA

130

110

Tao et al. (2008a)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

Table 13

Concentrations (ng/g fat) of endosulfan, in mothers’ milk, as reported in studies from around the world, 1995–2011, are presented

Region

Country

α-Endosulfan

β-Endosulfan

∑Endosulfan

Endosulfan sulfate

Reference

Mean

Median

Mean

Median

Mean

Median

Mean

Median

Africa

Egypt

 

4.8

      

Saleh et al. (1996)

Asia

India

    

9100a, b

   

Sanghi et al. (2003)

Turkey

50a

 

950a

 

1000a

   

Cok et al. (2011)

Europe

Spain

17a

22a

270a

180a

280a

200a

150a

120a

Cerrillo et al. (2005)

Denmark

7.4

       

Shen et al. (2007)

Denmark

 

7.4

      

Shen et al. (2008)

Denmark and Finland

 

6.8

      

Damgaard et al. (2006)

Finland

7.3

       

Shen et al. (2007)

Finland

 

6.4

      

Shen et al. (2008)

The Americas

Mexico

  

280

     

Rodas-Ortiz et al. (2008)

When concentrations from more than one sampling site in the same country and study have been reported, the concentrations are given as two values separated by a semicolon “;” (two concentrations) or a dash “–” (for more than two concentrations)

aRecalculated from fresh weight, assuming 4 % fat content

bNonspecified isomer/s

  • One reported concentration from one sample location is represented by a single value, e.g., “5.”

  • Two reported concentrations from one location are represented by two values separated by a semicolon, e.g., “3; 5.”

  • Three or more reported concentrations from one sample location are represented by giving the range, e.g., “3–5.”

  • If a study reports data from more than one sampling location, all are included, e.g., by presenting, “Sweden 5” and “Norway 4.”

  • In the case of a time series, i.e., more than one sample from one location, only the most recent value is included in the summary table.

  • A “sum value” is only given if more than one of the components of the “sum value” are reported.

  • If “sum values” are reported, the reported value is used. If not reported, the sum is calculated if possible.

  • If data from the same samples are presented in several studies, only the latest study is included in the table.

  • Three-letter country codes according to ISO 3166-1 alpha-3 are used in the figures, herein.

Spatial distribution diagrams

If mean or median values are given for different sampling locations within the same country or subgroups (e.g., age, primiparae versus multiparae), a weighted mean or median value is calculated based on the number of individuals in each group: for example, reported mean concentrations of 2, 3, and 5 ng/g fat of BDE-47, based on 10, 10, and 20 samples (total of 40 samples) from cities X, Y and Z in Sweden, respectively. The weighted mean value for study A will thus be a bar at 3.75 ng/g fat example given below.
$$ \frac{2\mathrm{ng}/\mathrm{g}\times 10}{40}+\frac{3\mathrm{ng}/\mathrm{g}\times 10}{40}+\frac{5\mathrm{ng}/\mathrm{g}\times 20}{40}=3.75\mathrm{ng}/\mathrm{g} $$

Equation 1. Example of how the weighted means were calculated.

In the spatial distribution diagrams, e.g., Fig. 3, the studies are sorted by rising concentrations within each region.

Methods applied for statistical reports

To test for significant log-linear trends, log-linear regression analyses were performed for the entire investigated time period and for the most recent 10 years using the annual arithmetic mean values. In cases where the regression line had a poor fit, a 3-point running mean smoother was checked for statistical significance in comparison with the regression through an ANOVA (Nicholson et al. 1998). Potential outliers in the temporal trends were detected using a method described by Hoaglin and Welsch (1978). The suspected outliers are merely indicated in the figures and were included in the statistical calculations. Values below level of quantification (LOQ) were replaced by LOQ/2 prior to the statistical analyses. Power analysis was also carried out. The power was fixed to 80 % and the minimum possible trend to be detected during a monitoring period of 10 years at a significant level of 5 % was estimated. A significance level of 5 % was used for all tests.

Results and discussion

A total of 253 scientific articles on POPs in mothers’ milk were identified on the basis of the applied methodology (cf. above). Several of the articles included data on more than one of the POPs. The diagram (Fig. 1) visualizes the number of reported concentrations of the corresponding POP that were available for this review. The results are presented in this review in descending order, starting from the POPs that are most well researched in relation to occurrence and concentrations in mothers’ milk, worldwide, i.e., going from DDT to SCCP and chlordecone (Fig. 1).
Fig. 1

Number of reported observations (total 744) in 253 scientific papers of the legacy POPs in mothers’ milk, from 1995 to 2011, subdivided on the POPs reported herein and presented in order of abundance of studies. Eighty percent of all studies are linked to seven of the POPs, DDT—chlordane. Note that a scientific paper may include observations of more than POP

Looking into the distribution of the scientific articles published on POPs in mothers’ milk in the chosen time period, it is clear that most of the studies originate from China, Japan, North America, and Western Europe (Fig. 2). However, publications are scattered throughout the globe making a spatial trend review possible. The results of the spatial distribution and concentrations of POPs are presented under the sections “DDT and DDT-related compounds” to “SCCPs,” including tables and figures when applicable. Temporal trend data on POPs in mothers’ milk are scarce but available data are reported herein under the sections “DDT and DDT related compounds” to “PFOS.” Some novel data are included for recent exposure assessments performed on mothers’ milk from Sweden.
Fig. 2

Global distribution of exposure assessment studies of POPs in mothers’ milk, up to year 2011. The circles are placed at the site of the capital city for each country, and the sizes of the circles visualize the abundance of studies from the countries on which this review is built. Black circle = 1 study, green circle = 2–5 studies, blue circle = 6–10 studies, red circle = 11–15 studies, and pink circle >15 studies

All concentration data given in Tables 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, and 13 are presented on a weight basis (ng or pg) per gram extracted fat, with the exception of perfluorooctane sulfonate (PFOS) which is presented in pg/mL.

It is of importance to consider that a reported concentration might not be generally applicable to a country as a whole, for instance, samples might originate from a farming area where pesticides have been in use. This could be more important to consider for countries with large diversity, either geographically and/or cultural, i.e., rural versus urban life styles. In smaller, more homogenous countries such as Sweden, POP concentrations have been found to be quite uniform, independent of geographical distribution (Glynn et al. 2011).

DDT and DDT-related compounds

A very large total number of reports are dealing with DDT and related compounds in mothers’ milk. Related compounds are 2,4′-DDT and the transformation products 4,4′-DDE, 4,4′-DDD, 2,4′-DDE, and 2,4′-DDD. The data shown in Table 2 refer only to the three individual compounds 4,4′-DDT, 4,4′-DDE, and 4,4′-DDD as well as ∑DDT. However, the ∑DDT may consist of some very different sums, sometimes including only the three main 4,4′-substituted DDTs mentioned but occasionally also including 2,4′-substituted DDTs. This makes the sum data less reliable for comparisons. However, we have still chosen to include sum data to visualize the larger data set, but avoiding the confusion with further differentiated data. Concentration data on 4,4′-DDT, 4,4′-DDE, and 4,4′-DDD are presented in detail in Table 2, subsectioned into four geographically large areas, i.e., Africa; Asia, Australia, and the Pacific region; Europe; and The Americas. Some of the results on DDT and related compounds in mothers’ milk are highlighted below.

Table 2 includes calculated ratio values of 4,4′-DDT/4,4′-DDE based on reported mean or median concentrations of the two compounds and gives an indication for recent discharges of DDT (with ratio values of 0.5 and above) or more historical use (ratios below 0.2) of this pesticide. Figure 3 displays the 4,4′-DDT and 4,4′-DDE concentrations as reported throughout the world.
Fig. 3

The sum of p,p-DDE and p,p-DDT reported worldwide is given in the figure, where contribution p,p-DDE is represented in dark blue and the contribution p,p-DDT is represented in orange

Africa

Concentrations of 4,4′-DDE are the highest among the three individual DDT compounds reported in Table 2, although the 4,4′-DDT/4,4′-DDE ratio indicates similar levels between the two major constituents in mothers’ milk. The highest concentrations of 4,4′-DDT and 4,4′-DDE are reported from Zimbabwe (Chikuni et al. 1997) and South Africa (Okonkwo et al. 2008; Sereda et al. 2009). Still, a few studies indicate low concentrations of DDTs in mothers’ milk. It is particularly clear that African mothers have high concentrations of 4,4′-DDT compared to most other samples from other regions. This is of course implying present or recent use of DDT for spraying, potentially indoors (Channa et al. 2012).

Asia, Australia, and the Pacific region

Reports from Asia, Australia, and the Pacific Region indicate that certain mothers have been highly exposed to both 4,4′-DDT and 4,4′-DDE (Nair et al. 1996; Nasir et al. 1998; Stuetz et al. 2001; Wong et al. 2002), while overall levels are above the common European concentrations, but below the concentrations reported for milk from African mothers (Table 2 and Fig. 3). The data indicate primarily old releases of DDT based on the low 4,4′-DDT/4,4′-DDE ratio, although there are exceptions (e.g., Nair et al. 1996; Nasir et al. 1998; Stuetz et al. 2001; Wong et al. 2002). Accordingly, direct exposure to DDT cannot be excluded.

Europe

The majority of studies on DDT in mothers’ milk are originating from Europe. The levels are in the lowest end (e.g., 20–250 ng/g fat of 4,4′-DDE) of all studies reviewed except for studies on DDTs in milk from the Eastern part of Europe, 250–2800 ng/g fat, as shown in Table 2. The higher concentrations in Eastern Europe is also followed by higher 4,4′-DDT/4,4′-DDE ratios indicating more recent use or unintentional release of DDT. However, the ratio is generally low indicating successful elimination of this POP from use in the society. The DDT and related compounds still present in mothers’ milk are a mirror of intake via food. Some high exposure levels to DDT among Eastern European citizens, as determined by analysis of blood, are supporting the higher levels in mothers’ milk from countries in this part of Europe (Hovander et al. 2006).

The Americas

Low concentrations of DDTs are reported from Canada and the USA, while Mexico in Central America (Table 2) reported levels that are similarly high as in Africa and some Asian countries. It is notable that in the countries from which the mothers’ milk contain the highest concentrations of DDTs, there is a more recent input of DDT (Fig. 3), which is confirmed by higher 4,4′-DDT/4,4′-DDE ratios, 0.12–0.4 (Table 2). A Brazilian study is reporting the highest ratio among all studies reviewed, i.e., 12 (Azeredo et al. 2008), indicating the present use of DDT. However, the actual concentration of ∑DDTs is lower than many other studies.

PCBs

Polychlorinated biphenyls (PCBs) reported as CB-153, sum of the six indicator CBs (CB-28, CB-52, CB-101, CB-138, CB-153, and CB-180, only if the concentrations of all six were reported), or the estimated total sum of PCB (∑PCB, the method of estimating the sum may vary between studies) in all 116 studies were tabulated (Table 3). Dioxin-like PCBs are not reported here but instead discussed together with the dioxins and furans (“PCDDs, PCDFs, and DL-PCBs”). Since PCBs are showing decreasing trends after the bans came into effect, studies from different time periods (1995–2011) may not be altogether comparable (Fig. 4).
Fig. 4

ac Graphical presentation of PCB concentrations in mothers’ milk from countries worldwide

Africa

Five studies of PCBs from Africa were found in the database search. CB-153 ranges from approximately 2 to 120 ng/g fat in South Africa (Darnerud et al. 2011) and Tunisia (Ennaceur et al. 2008), respectively. The reported ∑PCB ranges from about 3 to 750 ng/g fat in Zimbabwe (Chikuni et al. 1997) and Tunisia (Ennaceur et al. 2008), respectively.

Asia, Australia, and the Pacific region

No less than 36 studies were found from this region and the majority report estimated ∑PCB. The lowest concentrations are from China (Kunisue et al. 2004a; Xing et al. 2009), India (Devanathan et al. 2009), Indonesia (Sudaryanto et al. 2006), and Cambodia (Kunisue et al. 2004a). Higher concentrations of ∑PCB were reported from Australia, 160–480 ng/g fat (Quinsey et al. 1995); Japan, 120–200 ng/g fat (Kawashiro et al. 2008; Kunisue et al. 2006; Nagayama et al. 2007a; Nakamura et al. 2008); Kazakhstan, 220–820 ng/g fat (Hooper et al. 1997; Lutter et al. 1998; She et al. 1998); and Russia, 160–240 ng/g fat (Tsydenova et al. 2007). The lowest concentrations of CB-153, 0.5 ng/g fat, were reported from China (Zhang et al. 2011) and the highest in Iran, over 200 ng/g fat (Behrooz et al. 2009).

Europe

Over 50 % of the included studies came from Europe. The lowest concentrations of CB-153 in Europe, lower than 50 ng/g fat, came from Belgium (Colles et al. 2008), Italy (Ulaszewska et al. 2011), Latvia (Bake et al. 2007), Norway (Polder et al. 2008b), Poland (Jaraczewska et al. 2006), and Sweden (Lignell et al. 2003). The highest concentrations (more than 300 ng/g fat) were reported from the Czech Republic (Bencko et al. 1998; Cerna et al. 2010; Schoula et al. 1996) and Slovak Republic (Petrik et al. 2001). This is also true for the estimated ∑PCB, when reported. Concentrations >1000 ng/g fat are reported from the Czech Republic (Bencko et al. 1998; Cerna et al. 2010; Schoula et al. 1996), Germany (Schlaud et al. 1995), and the Slovak Republic (Petrik et al. 2001). Although the ban of PCB that was introduced stepwise during the 1970s and 1980s has led to significantly lowered concentrations in the environment, leakage due to inappropriate handling of waste material or from, e.g., building material, large capacitors, and hydraulic systems, still in use or stored at dumping sites, can still be expected and can thus cause elevated concentrations in mothers’ milk from highly industrialized countries.

The Americas

The concentrations of CB-153 reported from most of the 14 studies from the Americas were fairly low to moderate, around or below 50 ng/g fat: Brazil (Paumgartten et al. 2000), Canada (Dewailly et al. 1996; Newsome et al. 1995), and the USA (Fitzgerald et al. 1998; Pan et al. 2010). The highest concentration of CB-153, 110 ng/g fat (Rodas-Ortiz et al. 2008), as well as of the estimated ∑PCB, 1500 ng/g fat (Rodas-Ortiz et al. 2008), was reported from Mexico.

HCB and HCHs

Mothers’ milk concentrations of hexachlorobenzene (HCB) and the three more common hexachlorocyclohexane (HCH) isomers, α-HCH, β-HCH, and γ-HCH, are presented in Table 4, as well as the less commonly reported levels of δ-HCH. α-HCH, β-HCH, and γ-HCH represent the HCHs present in the “old” technical-grade HCH pesticide, while the commonly used pesticide, lindane, corresponds to γ-HCH. All the HCH isomers are related to pesticide use, while HCB has both a pesticide history and is also an abundant by-product from industrial activities and poorly controlled incineration/backyard burning. The pattern of HCH in the world is highly influenced by recent use of HCH as a pesticide. It is notable that the β-HCH isomer is the most abundant of the HCH isomers in mothers’ milk even though this compound is related to the historical HCH pesticide use and not to lindane (γ-HCH). However, the half-life of γ-HCH is much shorter in humans and wildlife than the half-life of β-HCH, and the observations confirm the higher persistency and lower reactivity of the β-HCH isomer compared to the others.

The data for HCB and the HCHs are dominated by studies of mothers’ milk from Asia and Europe (Table 4) and are reported in 94 and 113 scientific reports worldwide, respectively (Figs. 5 and 6).
Fig. 5

ac Graphical presentation of HCB concentrations in mothers’ milk from countries worldwide

Fig. 6

ad Graphical presentation of HCH concentrations in mothers’ milk from countries worldwide. Note that “RUS, Asia” refers to samples from a location in the Asian part of the Russian Federation

Africa

Most reported HCB concentrations from African countries range from about 2 to 5 ng/g fat, on either mean or median basis. Somewhat higher levels are reported in Ghananese mothers’ milk, 2.5–40 ng/g fat (Darko and Acquaah 2008; Ntow 2001; UNEP 2009). The highest concentrations are reported from Tunisia, mean concentration of 0.4–290 ng/g fat (Ennaceur et al. 2007, 2008).

In general, one could consider the ∑HCH levels in African mothers’ milk to be on the lower end on a global scale and comparable to concentrations reported from the Americas. There are quite few studies from Africa reporting levels of ∑HCH in mothers’ milk. Most of the studies report mean concentrations of approximately 10–100 ng/g fat (Table 4), the exceptions being one study from Ghana (Saleh et al. 1996) and one study from Libya (Elafi et al. 2001), reporting concentrations of 210 and 500 ng/g fat, respectively.

Asia, Australia, and the Pacific region

A few countries have reported HCB mean concentrations below 10 ng/g fat: Cambodia (Kunisue et al. 2004a), India (Devanathan et al. 2009), Korea (UNEP 2009), and the Philippines (Malarvannan et al. 2009). However, the majority of countries have reported mean values in the range 10–100 ng/g fat (Table 4). In the higher end of reported HCB, concentrations from the region include Australian levels between 370 and 460 ng/g fat (Behrooz et al. 2009; Quinsey et al. 1995), with levels up to 1500 ng/g fat, as well as Kazakhstan (Hooper et al. 1997) and Thailand (Stuetz et al. 2001), reporting concentrations above 100 ng/g fat (Table 4).

The reported levels of HCHs, both individual isomers as well as ∑HCH, are the highest in Asia, Australia, and the Pacific region, compared to the rest of the world, although there are a few studies reporting comparatively low mean concentrations, i.e., below 10 ng/g fat: Cambodia (Kunisue et al. 2004a), Kuwait (Saeed et al. 2000), the Philippines (Malarvannan et al. 2009), and Taiwan (Chao et al. 2006) but also studies from Japan (Nagayama et al. 2007a) and Australia (Khanjani and Sim 2006; Kunisue et al. 2004a). On the contrary, other studies from Japan and Australia report higher concentrations (Table 4). The majority of studies from Asia, Australia, and the Pacific region report ∑HCH concentrations in the range of hundreds of nanogram per gram fat, but a large number report concentrations in the range of thousands of nanogram per gram fat (Table 4). In India, there is a high HCH contamination according to the mothers’ milk concentrations, which range from 120 to 22,000 ng/g fat ∑HCH, with several studies reporting values of thousands of nanogram per gram fat (Table 4). The highest concentrations of the HCH isomers in mothers’ milk have been reported from India with means of 1800, 16,000, 1300, and 2300 ng/g fat for α-HCH, β-HCH, γ-HCH, and δ-HCH, respectively (Siddiqui et al. 2002).

Europe

In general, the HCB concentration in European mothers’ milk is higher than the rest of the world, although the most extreme values of HCB in mothers’ milk are not from Europe. Only two European countries, Croatia (Frkovic et al. 1996) and Finland (Shen et al. 2007), report mean HCB concentrations below 10 ng/g fat, while several Croatian studies report median concentrations above 10 ng/g fat (Krauthacker et al. 1998, 2009; Romanic and Krauthacker 2006). The majority of the HCB concentrations reported from European countries are in the range of 10–100 ng/g fat, reported on either mean and median basis (Table 4). In Europe, it is primarily the Eastern countries that report highly elevated HCB levels in the analyzed mothers’ milk, with the highest levels from the Czech Republic, median values up to 370 ng/g fat (Cajka and Hajslova 2003; Cerna et al. 2010). However, high levels are also reported in Spanish mothers’ milk with medians of 630 and 910 ng/g fat (Ribas-Fito et al. 2005).

The HCH concentrations in mothers’ milk from European mothers in general show significantly lower concentrations than milk from Asia, Australia, and the Pacific regions, but higher than concentrations reported from Africa and the Americas. The reported European levels of ∑HCH are for the most part homogenous, and the majority of mean and/or median concentrations are in the range 10–100 ng/g fat. However, there are a number of studies from Denmark (Shen et al. 2007), Finland (Shen et al. 2007), Romania (Covaci et al. 2001), and Russia (Polder et al. 1998; Tsydenova et al. 2007) that report ∑HCH concentrations of several hundreds of nanogram per gram fat (Table 4). The highest reported mean concentration is 1000 ng/g fat, in a study from Russia (Tsydenova et al. 2007).

The Americas

Overall, the HCB contamination seems to be lower in the Americas than any of the other regions with a higher portion of studies below 10 ng/g fat and no study reporting concentrations above 100 ng/g fat (Table 4). Antigua and Barbuda (UNEP 2009) along with a number of studies from the USA report levels below 10 ng/g fat. However, two studies report a mean concentration of 15 ng/g fat (Greizerstein et al. 1999) and a median concentration of 14 ng/g fat (Fitzgerald et al. 2001). The two highest mean concentrations of HCB were reported in studies of Mexican mothers’ milk, reaching 92 and 53 ng/g fat (Rodas-Ortiz et al. 2008; Waliszewski et al. 1998), and the third highest was reported from Canada, 43 ng/g fat (Newsome and Ryan 1999).

In the Americas, the ∑HCH concentrations are similar to the concentrations in Europe, albeit there are fewer reported observations. The two lowest concentrations are from Antigua and Barbuda (UNEP 2009) and Nicaragua (Romero et al. 2000), 5 and 7 ng/g fat, respectively. The majority of studies report values in the lower end of the range 10–100 ng/g (Table 4), although exceptions to this are reported concentrations in the range of hundreds of nanogram per gram from Brazil (Paumgartten et al. 2000) and Mexico (Elvia et al. 2000; Rodas-Ortiz et al. 2008; Waliszewski et al. 1998), with the highest mean concentration reported in mothers’ milk from Mexico, at 750 ng/g fat.

Chlordane

Chlordane concentrations reported as oxychlordane, α-chlordane, γ-chlordane, and ∑chlordanes from 63 studies, were selected and tabulated (Table 5).

Africa

Only ∑chlordanes from four countries on the African continent were reported. The highest concentrations were from Senegal, with a mean concentration of 11.7 ng/g fat (UNEP 2009).

Asia, Australia, and the Pacific region

Concentrations of oxychlordane vary greatly between countries, mostly between 0.5 and 10 ng/g fat. Extreme concentrations (140 and 150 ng/g fat) are reported from one Australian study (Quinsey et al. 1995), whereas the other studies from Australia report concentrations below 20 ng/g fat. Banned in most countries in 1997, chlordane was still allowed to be used as a termiticide in the Northern Territory (Australia) (UNEP Chemicals). Concentrations of α- and γ-chlordane are only reported from a few countries, whereof extreme concentrations are reported from Jordan 460 and 590 ng/g fat, respectively (Nasir et al. 1998). The highest concentrations of ∑chlordanes were reported from Japan (Konishi et al. 2001; Kunisue et al. 2006), while studies from the rest of the countries in the region report concentrations generally below 10 ng/g fat.

Europe

Fourteen studies from Europe report mean concentrations of oxychlordane, most of them close to or below 5 ng/g fat, and the reported median concentrations are in general of the same magnitude. The highest values of oxychlordane in Europe are reported from Ukraine (16–22 ng/g fat) (Gladen et al. 1999, 2003). Only very few countries reported ∑chlordanes, whereof the highest values, 10–60 ng/g fat, are reported from Russia (Polder et al. 1998, 2008a; Tsydenova et al. 2007). One study reports concentrations below 4 ng/g fat from Western, Central, and Eastern Europe (UNEP 2011).

The Americas

A few studies from the American continent in general show higher concentration of oxychlordane (Johnson-Restrepo et al. 2007; Newsome et al. 1995; Newsome and Ryan 1999) compared to Europe. The highest concentrations are between 40 and 60 ng/g fat from Canada (Newsome and Ryan 1999) and Mexico (Elvia et al. 2000). A few studies reporting concentrations of α- and γ-chlordane give values below 3 ng/g fat, except extreme concentrations reported from Mexico, 260 and 930 ng/g fat, respectively (Rodas-Ortiz et al. 2008).

PCDDs, PCDFs, and DL-PCBs

The polychlorinated dibenzo-p-dioxin/polychlorinated dibenzofuran (PCDD/PCDF) and dioxin-like PCB (DL-PCB) concentrations are reported as toxic equivalents (TEQs) based on WHO TEF values from 1998 (Van den Berg et al. 1998) and 2005 (Van den Berg et al. 2006). Total mean TEQ2005 varies between 3.1 and 7.2 pg TEQs/g fat for the three countries studied in Africa (UNEP 2009). The use of mean or median concentrations applying TEF1998 or TEF2005 results in four different total TEQs. Still, some spatial comparisons are possible. Both Brazil (Paumgartten et al. 2000) and Chile (UNEP 2009) show higher total TEQ2005 than the African countries. When comparing these total TEQ2005 concentrations with mothers’ milk from Europe (Table 6), we confirm generally higher TEQs from Europe than the countries mentioned in Africa and South America. Further comparisons are not made here due to the extensive complications in doing so.

PBDEs

Concentrations of PBDEs, BDE-47, BDE-209, and ∑PBDE data are summarized in Table 7 and Figs. 7 and 8.
Fig. 7

Graphical presentation of BDE-47 concentrations in mothers’ milk from countries worldwide

Fig. 8

Graphical presentation of BDE-209 concentrations in mothers’ milk from countries worldwide.

Africa

Only two studies of PBDEs in mothers’ milk from Africa were identified, and both studies confirm the occurrence of BDE-47 in mothers’ milk at mean or median concentrations below 2 ng/g fat (Asante et al. 2011; Darnerud et al. 2011). BDE-209 was only reported in one study from Ghana (Asante et al. 2011).

Asia and the Pacific region

The concentrations of BDE-47 are rather uniform and low (below 2 ng/g fat) in mothers’ milk in Asia and the Pacific region, even though a very large geographical area is covered. One study from Japan reports the highest level of BDE-47 outside the USA with a mean concentration of 19 ng/g fat (Akutsu and Hori 2004). From the Philippines, a study reports somewhat elevated levels, mean concentrations of 1.2 and 4.9 ng/g fat (13). Both low and high BDE-47 concentrations have been determined in samples from Turkey, with mean concentrations reaching 6.0 ng/g fat (Erdogrul et al. 2004; Ozcan et al. 2011).

BDE-209 was reported in 6 out of 16 studies with similar levels (<1 ng/g fat) independent of the study (cf. Table 7). The highest BDE-209 concentrations are reported in mothers’ milk from the Philippines and Vietnam with levels of around 2 ng/g fat (Malarvannan et al. 2009; Tue et al. 2010).

The reported ∑PBDEs in Asian mothers’ milk confirm the observations of BDE-47 concentrations, with the highest concentrations from the Philippines, mean concentrations of 5–10 ng/g fat (Malarvannan et al. 2009; Sudaryanto et al. 2008b), as well as from Japan and Turkey with mean concentrations of 31 and 67 ng/g fat, respectively (Akutsu and Hori 2004; Ozcan et al. 2011). These concentrations are comparable with the levels reported in mothers’ milk from the USA.

Europe

In general, the concentrations of BDE-47 in mothers’ milk in Europe (approximately 1–2 ng/g fat) are higher compared to the levels in Asia and the Pacific region and Africa but lower than in the Americas. The lowest levels of BDE-47 in Europe are reported in samples from the Czech Republic, Germany, Italy, and Russia, with mean concentrations below 1 ng/g fat (Alivernini et al. 2011; Kazda et al. 2004; Polder et al. 2008a; Raab et al. 2008). The highest levels are reported in mothers’ milk from the UK with median concentration of 2.7 ng/g fat (Kalantzi et al. 2004), and the remaining results from Europe are in between the mentioned BDE-47 concentrations (Table 7). Hence, the differences in the levels are rather small.

As few as 7 out of 25 of the European mothers’ milk samples report BDE-209, with the highest concentrations in samples from France, 1.5 ng/g fat (Antignac et al. 2008; Athanasiadou and Bergman 2008). Since BDE-209 has a short half-life in humans, 14 days (Thuresson et al. 2006), the differences in concentrations of this PBDE congener vary greatly. Consequently, exposure levels of BDE-209 and nona-BDEs become uncertain when seen over time.

In Europe, the ∑PBDE concentrations are in general 3–4 ng/g fat, with a few exceptions (Table 7). The highest ∑PBDE concentrations are reported in mothers’ milk from the UK, with median levels of 6.3 ng/g fat, which is still three to five times lower than levels reported from the USA.

The Americas

Only studies from the USA could be found that report levels of PBDEs from the Americas and that met the criteria set for this review.

In general, the reported levels of BDE-47 are much higher in the mothers’ milk samples from the USA compared to the rest of the world. The concentrations are rather uniform, with mean values at 35–40 ng/g fat (Johnson-Restrepo et al. 2007; Schecter et al. 2003, 2005, 2010), but with levels reaching as high as 73 ng/g fat (Park et al. 2011). Also, the levels of BDE-209 are higher in the USA than the rest of the world (Table 7), which is indicating a higher prevalence of deca-BDE exposure.

Also, the concentrations of ∑PBDEs in the samples from the USA are overall similar, with means of 66–76 ng/g fat, and one median value of 51, reported in four different studies (Johnson-Restrepo et al. 2007; Schecter et al. 2003, 2005, 2010). However, one study reports a mean concentration as high as 130 ng/g fat (Park et al. 2011).

The results clearly show that US mothers’ milk contains the highest concentrations of PBDEs. This is in line with any other exposure study from the USA, showing mothers and other individuals being subjected to environmental exposures of PBDEs that are the highest in the world.

Heptachlor

Heptachlor concentrations reported as cis-HCL-epoxide, HCL-epoxide, and heptachlor from 49 studies were selected and tabulated (Table 8). Concentrations of cis-HCL-epoxide are only reported from one or a few countries from each continent/region, and they range between 0.7 ng/g fat in China (Hedley et al. 2010) and 8 ng/g fat in Brazil (Paumgartten et al. 2000).

Africa

Heptachlor was only reported from four regions of the African continent with concentrations ranging between 0.9 and 2.25 ng/g fat (UNEP 2009, 2011).

Asia, Australia, and the Pacific region

Fifteen studies report concentrations of HCL-epoxide. Most of these report concentrations below 10 ng/g fat, but higher concentrations are reported from Australia, 53 and 78 ng/g fat (Quinsey et al. 1995); Jordan, 190 ng/g fat (Nasir et al. 1998); Thailand, 60 ng/g fat (Stuetz et al. 2001); and Turkey, 61 ng/g fat (Cok et al. 2005). The highest reported concentration of heptachlor is from Jordan at 500 ng/g fat (Nasir et al. 1998).

Europe

Concentrations of HCL-epoxide reported from Europe are in most cases below or close to 3 ng/g fat, although higher concentrations are reported from Ukraine, 16–22 ng/g fat (Gladen et al. 1999, 2003), and the Netherlands, 30 ng/g fat (Albers et al. 1996).

The Americas

Concentrations of HCL-epoxide and heptachlor from the Americas are reported as less than 4 ng/g fat except for Mexico, 160 and 580 ng/g fat, respectively (Rodas-Ortiz et al. 2008).

Dieldrin, endrin, and aldrin

The OCPs discussed herein were regulated at an early stage in many countries. Despite of this, rather high concentrations of dieldrin are reported (Table 9).

Africa

No studies were retrieved that report aldrin and/or endrin in mothers’ milk from any African nation. Dieldrin was reported in seven studies, three of which were part of the UNEP screening program with the lowest levels in mothers’ milk from Ghana, Nigeria, and Senegal, with mean concentrations of 1.3–4.1 ng/g fat (UNEP 2009). However, some reports indicate levels of up to 25–120 ng/g fat (Ennaceur et al. 2007, 2008; Ntow et al. 2008).

Asia and the Pacific region

Although only few studies report aldrin concentrations in mothers’ milk, the variation is great. The most comprehensive study originates from Australia showing a large national spatial distribution in a range 0.01–0.68 ng/g fat (Harden et al. 2007). Somewhat higher levels of aldrin are found in Kuwait and the highest concentration are from India and Jordan with mean concentrations up to 860 ng/g fat (Nasir et al. 1998; Siddiqui et al. 2002).

Dieldrin is more frequently reported in mothers’ milk than aldrin and endrin and at rather high concentrations (Table 9). The levels of dieldrin are rarely above 100 ng/g fat, with the exceptions of one study from Jordan, which reports a mean concentration of 1400 ng/g fat (Nasir et al. 1998), and one study from China, 9300–10,000 ng/g fat (Wang et al. 2008). Only two studies have been retrieved reporting on endrin in mothers’ milk, one from Jordan and one from Kuwait (Nasir et al. 1998; Saeed et al. 2000).

Europe

A study from Croatia reports aldrin and endrin in their samples, with mean concentrations of 1.3 and 2.0 ng/g fat, respectively (Frkovic et al. 1996). Again, the occurrence of dieldrin in mothers’ milk is frequently reported from European countries in low concentrations, for example in samples from Germany and Croatia, with mean concentrations below 3.8 ng/g fat (Frkovic et al. 1996; Zietz et al. 2008). However, other studies from Germany show higher levels, with mean concentrations of 4 and 14 ng/g fat (Raab et al. 2008; Schlaud et al. 1995). Two reports investigating dieldrin levels in mothers’ milk, both in Denmark and Finland, show similar results (Shen et al. 2007, 2008) and likewise from the WHO-UNEP monitoring program (UNEP 2011). The highest levels are reported from the UK with a mean concentration of 48 ng/g fat (Harris et al. 1999) and the Netherlands with a median concentration of 50 ng/g fat (Albers et al. 1996).

The Americas

In the Americas, one study has reported levels of aldrin from a known pest-controlled area on the Yucatán peninsula in Mexico with a mean concentration of 280 ng/g fat (Rodas-Ortiz et al. 2008). In the lower end of reported levels of dieldrin in mothers’ milk are samples from the Americas, Antigua and Barbuda, Chile, and Uruguay, with mean concentrations of 2.6, 5.0, and 4.9 ng/g fat (UNEP 2009), respectively, as well as from the Group of Latin American and Caribbean countries, with a median concentration of 4.9 ng/g fat (UNEP 2011). The highest levels of dieldrin in mothers’ milk in the Americas are found in samples from a know pest-controlled area in on the Yucatán peninsula in Mexico with a mean concentration of 300 ng/g fat (Rodas-Ortiz et al. 2008). Endrin could only be found in a sample from Nicaragua (Romero et al. 2000) and from the abovementioned pest-controlled area on the Yucatán peninsula in Mexico (Rodas-Ortiz et al. 2008).

Pentachlorobenzene, toxaphene, and mirex

Pentachlorobenzene (PCBz), mirex, and toxaphene concentrations in mothers’ milk are only reported in a few studies (Table 10). Mirex levels are reported as 16, 20, and 68 ng/g fat in mothers’ milk from Germany, Russia, and Canada, respectively (Newsome and Ryan 1999; Polder et al. 2008a; Skopp et al. 2002). Both PCBz and mirex are reported in around 1 ng/g fat in most mothers’ milk samples, with a few exceptions (Table 10). The most profound exception is mirex found in a concentration of 200 ng/g fat in mothers’ milk from Mexico (Rodas-Ortiz et al. 2008).

It is notable that so few reports have been published on these POPs. Therefore, any assessments of spatial differences are impossible.

HBCDD and PBB

Concentrations of hexabromocyclododecane (HBCDD) and polybrominated biphenyl (PBB) reported in mothers’ milk are presented in Table 11 on a fat weight basis. From isomer-specific information, it is clear that α-HBCDD is the most abundant isomer of environmental HBCDDs (Eljarrat et al. 2009; Lankova et al. 2013). The spatial distribution of HBCDD is illustrated in Fig. 9.
Fig. 9

Graphical presentation of HBCDD concentrations in mothers’ milk from countries worldwide

Africa

Only two studies of HBCDDs in mothers’ milk from all of Africa were retrieved, both showing subnanogram per gram fat concentrations in the mothers’ milk analyzed (Asante et al. 2011; Darnerud et al. 2011). No study was found reporting on PBBs in mothers’ milk from any African nation.

Asia and the Pacific region

The lowest concentrations of ∑HBCDDs reported in mothers’ milk from Asia come from the Philippines and Vietnam with mean and median concentrations below 1 ng/g fat (Malarvannan et al. 2009; Tue et al. 2010). A study from China shows a greater range in ∑HBCDD concentrations, with means of 0.33–2.8 ng/g fat (Shi et al. 2009). In Japanese mothers’ milk, ∑HBCDDs levels of 1.4 ng/g fat (Kakimoto et al. 2008) are reported. No study was found reporting on PBBs in mothers’ milk from any nation in Asia or the Pacific region.

Europe

The levels of ∑HBCDDs in Europe are quite uniform and low (Table 11), i.e., <1 ng/g fat. However, the highest concentrations on a global scale are those reported from a Spanish study, with a mean concentration of 47 ng/g fat, in mothers’ milk from a population living close to a textile processing plant (Eljarrat et al. 2009). The ∑HBCDD concentrations in Swedish samples reported median concentrations within the range of 0.3–0.4 ng/g fat (Glynn et al. 2011). Somewhat higher concentrations, and comparable with the Japanese levels, are reported from Norway, with mean concentrations of 1.7 ng/g fat (Thomsen et al. 2010). The ∑HBCDDs in mothers’ milk from the UK report a mean concentration of 6.0 ng/g fat (Abdallah and Harrad 2011), which is the highest background level worldwide, apart from the Spanish “hot spot” samples. One study reports PBB concentrations from two countries, Denmark and Finland, both indicating mean concentrations below 0.3 ng/g fat (Shen et al. 2008).

The Americas

We have not found any study with our search criteria which has reported the presence of HBCDDs or PBBs in mothers’ milk from any nation in the Americas.

PFOS

Thirteen studies report PFOS concentrations in mothers’ milk from a total of 13 countries in Asia and Europe and one study from the USA (Table 12). The concentration of PFOS ranges between 39 and 200 pg/mL, with Hungary as the only exception, 330 pg/mL (Volkel et al. 2008). Due to the limited data, it is not possible to draw any conclusions regarding spatial exposure differences. The spatial distribution of PFOS is illustrated in the diagram in Fig. 10.
Fig. 10

Graphical presentation of PFOS concentrations in mothers’ milk from countries worldwide

Endosulfan

Only some scattered endosulfan mothers’ milk data are available (Table 13). The sum concentrations from India and Turkey are exceptionally high, i.e., concentrations above 1000 ng/g fat (Cok et al. 2011; Sanghi et al. 2003). These high levels are comparable to some data on DDT in mothers’ milk (cf. Table 2) and are likely due to the very recent use of endosulfan in these countries.

Chlordecone

No studies were found with our search criteria reporting chlordecone concentrations in mothers’ milk.

SCCPs

No studies were found with our search criteria reporting SCCP concentrations in mothers’ milk, even though there is an agency report on SCCPs in Swedish mothers’ milk (Darnerud et al. 2012) indicating their presence in this matrix.

Global distribution trends

The data collected and compiled within the study indicates that there is indeed a difference in the distribution and exposure to POPs which is dependent on where in the world one resides. These conclusions are more easily made when comparing the different spatial distribution diagrams, e.g., Fig. 3. In general, it was found that DDT/DDE pesticides were reported in higher concentrations in mothers’ milk from the regions of Africa, Asia, and Central America, with a propensity for agricultural economies and lower degree of industrialization. On the other hand, PCBs and dioxins were found to be reported to a higher degree in more industrialized regions, such as parts of Asia, Europe, and North America. A good example of this can be seen by comparing Figs. 3 and 4a–c, where the DDT/DDE concentrations clearly are lower, in general, in Europe and North America compared to the rest of the world (Fig. 3). Similarly, it can be seen from Fig. 4a–c that the PCB concentrations are higher in industrialized regions compared to the rest of the world. This pattern is also observed for HCHs, although there are a few observations of high concentrations in mothers’ milk samples from Eastern Europe, i.e., Russia, Romania, and Ukraine (Fig. 6a–d).This pattern is not surprising since PCBs and dioxins, not shown in spatial distribution diagrams, are related to a degree of industrialization, either as chemical products or impurities there within. DDT as well as HCHs has been used as pesticides in SC and has been used in the equatorial and subequatorial regions, which in general are less industrialized and more dependent on agriculture. Furthermore, it is clear that mothers’ milk from the USA contains more PBDEs than the rest of the world (Fig. 7). BDE-47 is a biomarker of PBDE exposure and the lowest reported concentration is around five times as big as the highest concentration in a sample from outside of the USA. This can be explained by the stricter flame retardant policy enforced within the USA, a policy which calls for a greater use of flame retardant substances such as PBDEs primarily in upholstery (GSPI 2013; State of California 2000, 2013). A new fire safety regulation has recently been adopted, January 1st 2014, which does not call for the use of flame retardant chemicals and perhaps this will lead to a decrease of PBDEs in mothers’ milk in the USA (GSPI 2013; State of California 2000, 2013). For the substances not mentioned, there are no observed, clear spatial distribution trends that can be explained by traditional/historical use of the substances in question. This could be since there are too few reported concentrations available or that the differences in use or emissions are too small to observe.

Temporal trends

Two distinct objectives can be identified concerning temporal trend monitoring of contaminants. One is to quantitatively estimate the rate of changes in contaminant concentration, e.g., as a change in percent per year or as half- or doubling time in number of years. An example of this could be to estimate the response of measures taken to reduce the discharges of various contaminants. Dissimilarities in comparisons between the rate of change in contaminant concentration in mothers’ milk and other environmental biological matrices (e.g., fish) can give information about the exposure patterns, i.e., if the mothers are exposed to contaminants not only from local food but also from imported food and the indoor environment, including a variety of man-made technical products. Another objective of temporal trend monitoring is to study emerging new substances and to detect renewed use of banned contaminants. In order to estimate the rate quantitatively with a high statistical power, it is essential to keep the random variation between years as low as possible. Compared to other matrices, mothers’ milk seems to show a relatively low random variation (UNEP 2004).

Inclusion of a time series in this review article requires a minimum of five reported data points. Only approximately half of the substance groups from only two countries, Sweden and Japan, fulfilled the described criteria. The temporal trends present data from 1972 to 2011.

In the graphs below, log-linear regression and a smoother test have been carried out. The smoother test checks if the smoother explains significantly more of the variation in concentration, than the regression line (Nicholson et al. 1998).The regression line and/or the smoother are plotted when significant (α = 0.05).

DDT and DDT-related compounds

In Fig. 11, the concentrations of DDE (ng/g fat) in the samples from Japan, 1972–1998 (Konishi et al. 2001), and Sweden, 1972–2010 (Athanasiadou and Bergman 2008; Bergman et al. 2010; Lundén and Norén 1998), show significant decreasing trends over the whole time period of −9.1 % (p < 0.001) and −8.5 % (p < 0.001), respectively. The Japanese samples also show significant decreasing concentrations for the last 10 years of −13 % (p < 0.001), while no trend is indicated in the Swedish samples for the last 10 years (estimated during a decade later than for the Japanese samples). The temporal trends for DDT in mothers’ milk from Japan and Sweden are of similar magnitude as for DDE. In addition, the trends observed in Swedish mothers’ milk for DDE coincide with the trends seen in Swedish freshwater (Nyberg et al. 2011) and marine (Bignert et al. 2012) biota.
Fig. 11

Temporal trends of DDE (ng/g fat) from Japan (Konishi et al. 2001) and Sweden (Lundén and Norén 1998; Athanasiadou and Bergman 2008; Bergman et al. 2010)

The ratio of DDT/DDE (Fig. 12) shows similar log-linear trends in the samples from Japan, 1972–1998 (Konishi et al. 2001), and Sweden, 1972–2010 (Athanasiadou and Bergman 2008; Bergman et al. 2010; Lundén and Norén 1998). The Japanese samples also show a significant nonlinear trend for the ratio of DDT/DDE, which might indicate that a new release of DDT has occurred during the monitoring period.
Fig. 12

Temporal trends of the ratio between DDT and DDE (ng/g fat) from Japan (Konishi et al. 2001) and Sweden (Lundén and Norén 1998; Athanasiadou and Bergman 2008; Bergman et al. 2010)

PCBs

In Fig. 13, the concentrations of ∑PCB (ng/g fat) in the samples from Japan, 1972–1998 (Konishi et al. 2001), and Sweden, 1972–2010 (Athanasiadou and Bergman 2008; Bergman et al. 2010; Lundén and Norén 1998), show significant decreasing trends over the whole time period of −7.5 % (p < 0.001) and −6.5 % (p < 0.001), respectively, and for the last 10 years of −7 % (p < 0.001) and −11 % (p < 0.011), respectively. The trends observed in Swedish mothers’ milk for ∑PCB coincide with the trends seen in Swedish freshwater (Nyberg et al. 2011) and marine (Bignert et al. 2012) biota.
Fig. 13

Temporal trends of ΣPCB (ng/g fat) from Japan (Konishi et al. 2001) and Sweden (Lundén and Norén 1998; Athanasiadou and Bergman 2008; Bergman et al. 2010)

Only one temporal trend study on congener basis was found for PCBs within this review (from Sweden). In Fig. 14, the temporal trend for CB-153 (ng/g fat) in the Swedish samples, 1972–2010 (Bergman et al. 2010; Lundén and Norén 1998), is presented. CB-153 shows a significant decreasing trend over the whole time period and for the last 10 years of −4.9 % (p < 0.001) and −5.9 % (p < 0.042), respectively.
Fig. 14

Temporal trend of CB-153 (ng/g fat) from Sweden (Lundén and Norén 1998; Athanasiadou and Bergman 2008; Bergman et al. 2010)

HCB and HCHs

In Fig. 15, the concentrations of β-HCH (ng/g fat) in the samples from Japan, 1972–1998 (Konishi et al. 2001), show a significant decreasing trend over the whole time period as well as for the last 10 years of −12 % (p < 0.001) and −11 % (p < 0.001), respectively.
Fig. 15

Temporal trends of β-HCH (ng/g fat) from Japan (Konishi et al. 2001)

PCDDs, PCDFs, and DL-PCBs

In Fig. 16, the concentrations of PCDD (pg WHO2005-TEQ/g fat) from Stockholm, 1972–1997 (Norén and Meironyte 2000) and 1972–2011 (Fång et al. 2013), show significant decreasing trends over the whole time period of −3.6 % (p < 0.005) and −6.0 % (p < 0.001), respectively. However, for the last 10 years, a significant decreasing trend of −10 % (p < 0.001) is only seen for the time series from 1972 to 2011 (Fång et al. 2013), covering the last decade in contrast to the study from 1972 to 1997 (Norén and Meironyte 2000), which might have too few samples during the last 10 years to detect a trend. It should be noted that the two studies by Norén and Meironyte and the study by Fång et al. are analyzing the same pooled mothers’ milk sample during 1972–1997.
Fig. 16

Two temporal trends of PCDD in WHO2005-TEQ (pg/g fat) from Sweden, on the left (Norén and Meironyte 2000) and on the right (Fång et al. 2013)

In Fig. 17, the concentrations of PCDF (pg WHO2005-TEQ/g fat) from Stockholm, 1972–1997 (Konishi et al. 2001; Norén and Meironyte 2000) and 1972–2011 (Fång et al. 2013), show significant decreasing trends over the whole time period of −5.2 % (p < 0.003) and −6.2 % (p < 0.001), respectively. However, for the last 10 years, a significant decreasing trend of −7.3 % (p < 0.001) is only seen for the time series from 1972 to 2011 (Fång et al. 2013), covering the last decade in contrast to the study from 1972 to 1997 (Norén and Meironyte 2000), which might have too few samples during the last 10 years (only 4) to detect a trend.
Fig. 17

Two temporal trends of PCDF in WHO2005-TEQ (pg/g fat) from Sweden, on the left (Norén and Meironyte 2000) and on the right (Fång et al. 2013)

In Fig. 18, the concentrations of DL-PCBs (pg WHO2005-TEQ/g fat) from Stockholm, 1972–1997 (Norén and Meironyte 2000) and 1972–2011 (Fång et al. 2013), show significant decreasing trends over the whole time period of −5.1 % (p < 0.001) and −7.0 % (p < 0.001), respectively. For the last 10 years, a significant decreasing trend of −12 % (p < 0.012) is seen for the samples from 1972 to 2011 (Fång et al. 2013), and a decreasing trend of −6.7 % (p < 0.107) is also indicated in the samples from 1972 to 1997 (Norén and Meironyte 2000).
Fig. 18

Two temporal trends of dioxin-like PCBs (DL-PCBs) in WHO2005-TEQ (pg/g fat) from Sweden, on the left (Norén and Meironyte 2000) and on the right (Fång et al. 2013)

The trends observed in Swedish mothers’ milk for DL-PCBs during the whole time period coincide with the trends seen in Swedish freshwater (Nyberg et al. 2011) and marine (Bignert et al. 2012) biota for the dioxin-like PCB congener CB-118 from the end of the 1970s to the beginning of the 1990s. However, during the last decade, the levels are decreasing at a higher rate in Swedish human milk than in marine and freshwater biota from Sweden.

PBDEs

In Fig. 19, the concentrations of BDE-47 (ng/g fat) in the samples from Japan, 1977–1999 (Akutsu et al. 2003), indicate an increasing trend over the whole time period of 9.1 % (p < 0.081). In contrast, a decreasing trend of −5.7 % (p < 0.093) is indicated in the Swedish samples from Stockholm (Athanasiadou and Bergman 2008; Bergman et al. 2010; Fängström et al. 2008) for the last 10 years of the study. This decreasing trend of BDE-47 coincides with the trends seen in Swedish marine (Bignert et al. 2012) and freshwater (Nyberg et al. 2011) biota over the last decade. PentaBDE was first phased out voluntarily by the industry in Germany in 1986 and end in Sweden in 1999 (Alcock and Busby 2006). Subsequently, BDE-47 was partially banned within the EU countries in 2004 and the declining concentrations in human milk and biota could to some extent be explained by these events. No trend could be observed in the Swedish time trend from Uppsala during 1996–2001 (Lind et al. 2003).
Fig. 19

Temporal trends of BDE-47 (ng/g fat) from Japan (Akutsu et al. 2003) and from Stockholm (Athanasiadou and Bergman 2008; Fängström et al. 2008; Bergman et al. 2010) and Uppsala (Lind et al. 2003), Sweden

Heptachlor

In Fig. 20, the concentrations of heptachlorepoxide (ng/g fat) in the samples from Japan, 1986–1998 (Konishi et al. 2001), show significant decreasing trends over the whole time period and for the last 10 years of −9.7 % (p < 0.001) and −4.9 % (p < 0.049), respectively.
Fig. 20

Temporal trend of heptachlorepoxide (ng/g fat) from Japan (Konishi et al. 2001)

Dieldrin, endrin, and aldrin

In Fig. 21, the concentrations of dieldrin (ng/g fat) in the samples from Japan, 1972–1982 (Konishi et al. 2001), show a significant decreasing trend over the whole time period of −14 % (p < 0.001).
Fig. 21

Temporal trend of dieldrin (ng/g fat) from Japan (Konishi et al. 2001)

HBCDD

The concentrations in Fig. 22 of HBCDD (ng/g fat) in the samples from Japan, 1987–2007 (Kakimoto et al. 2008) and Sweden, 1987–2010 (Athanasiadou and Bergman 2008; Bergman et al. 2010; Fängström et al. 2008), show increasing trends over the whole time period of 5.4 % per year (p < 0.061) and 7.6 % per year (p < 0.001), respectively. The increasing trend of HBCDD seen in the Swedish milk samples coincides with trends in Swedish marine biota from the Baltic Sea (Bignert et al. 2012). HBCDD is still in use within the EU but is listed in REACHs authorization list as substance of very high concern (SVHC) and, since November 2014, included in the SC.
Fig. 22

Temporal trends of HBCDD (ng/g fat) from Japan (Kakimoto et al. 2008) and Sweden (Athanasiadou and Bergman 2008; Fängström et al. 2008; Bergman et al. 2010)

PFOS

In Fig. 23, the concentrations of PFOS (pg/ml) in the samples from Stockholm, 1972–2008 (Sundström et al. 2011), show a significant increasing trend over the whole time period of 3.3 % (p < 0.012). In contrast, a significant decreasing trend of −11 % (p < 0.002) is observed for the last 10 years. In the study with samples from Uppsala, Gothenburg, Lund, and Lycksele, 1996–2004 (Kärrman et al. 2007), a decreasing trend is indicated (p < 0.059) for the whole time period. The trends observed in Swedish mothers’ milk for PFOS coincide with the trends seen in Swedish marine (Bignert et al. 2012) and freshwater (Nyberg et al. 2011) biota over the last decade.
Fig. 23

Two temporal trends of PFOS (pg/mL) from Stockholm (Sundström et al. 2011) and Uppsala, Gothenburg, Lund and Lycksele (Kärrman et al. 2007), Sweden

Critical remarks and conclusions

Some of the legacy POPs are the most well-researched environment pollutants among all. This is due to their global distribution and occurrence in humans and wildlife, being classified as CMRs, having endocrine disruption effects and/or having other toxic effects. Some early efforts focused on the transfer of these chemically stable and bioaccumulative compounds to nursing children. The transfer of POPs via mothers’ milk initiated a still ongoing debate on risks for the newborn babies. In contrast to the strict recommendations to nursing mothers to avoid smoking and drinking alcohol, it is not possible to change the mothers’ body burdens of POPs as their levels of these compounds have been built up over the mothers’ whole lifetime. However, in some countries, there are at least dietary recommendations on how to limit the intake of POPs from some major food sources, in particular fatty fish. These recommendations are primarily targeting young women and women in child-bearing ages. Due to the many positive effects of nursing, WHO recommends mothers to breast feed their newborns for a minimum of 6 months (WHO and UNICEF 2014).

WHO also initiated a monitoring program for POPs in mothers’ milk in 1976 (WHO 2009), but at this point, researchers had already started to do exposure studies of nursing infants, as reviewed by Norén and Meironyte (2000). In the present review, it becomes clear how abundant mothers’ milk is a matrix for POP analysis, although only a limited number of POPs are assessed, i.e., 7 of the 24 (HCHs counted individually) POPs in Table 1 contribute with 80 % of the exposure studies discussed herein. There are no studies covering all, or even a majority of the POPs in the same study. The most comprehensive results for POP exposure analyses are when the same milk samples are utilized for assessments of as many POPs as possible. In reality, it is much more common with scattered studies globally, regionally and country-wise. This means that the cohorts are defined by different means and the objectives vary. This leads to the conclusion that there are very few studies that allow reliable comparisons, e.g., the temporal trend studies from Japan and Sweden. However, the temporal trend studies from Japan and Sweden presented did not cover POP analyses in an optimal manner, i.e., several of the POPs were not included in these studies. Another issue regarding comprehensive time trend analysis is the need to establish environmental specimen banks whose goal is to collect and store environmental relevant samples, including mothers’ milk, in a structured manner. In time, samples collected will allow a high qualitative time trend analysis on current POPs and currently unknown pollutants. Further, this is only the start of the problem comparing POPs in mothers’ milk from around the world. Below, we list and shortly discuss some of the major shortcomings in some studies which, if rectified, would allow proper comparisons of POPs in mothers’ milk.

Reporting base for POP concentrations in mothers’ milk

This is relevant for all POPs that are produced, used, and/or occur as mixtures of halogenated homologues and isomers-congeners. These POPs are PCBs, PCDFs, PCDDs, PBDEs, PBBs, chlordanes, toxaphen, and CPs. HCHs may be included even though only isomers of hexachlorinated cyclohexane is included. Similarly, HBCDD has three diastereomers (α-, β-, and γ-HBCDD), which are commonly discussed and often reported individually. DDTs and endosulfan, on the other hand, are both produced as two main isomers. However, both 4,4′-DDT and 2,4′-DDT are transformed to and occur in the environment, including mothers’ milk, as the corresponding DDD and DDE compounds. This has led to a similar handling of the DDTs as of true congeners of, e.g., PCBs. For all of these compounds/compound classes, it is common to report concentration sums (e.g., sPCB or ∑PCB), sometimes indicating how many PCB congeners are included in the sum and presented as ∑PCB(7), indicating that seven congeners were included. However, highly variable sums are reported for the POPs. For PCBs, for example, a number of different sum values have been found in the review including 3, 4, 6, 7, 8, 12, 15, 16, 19, 32, and 35 PCB congeners. Sometimes, the reported sum concentrations are referred to as “total PCBs” without any further specification. However, it is clear that it is still a summation of a defined number of PCB congeners, i.e., those quantified. To further complicate the issue, PCBs can also be reported as DL-PCBs and non-DL-PCBs or as non-ortho-PCBs, mono-ortho-PCBs, and di-ortho-PCBs. Hence, it is realistically not possible to compare ∑PCB concentrations unless they are reported in a similar manner. In this review article, we have used ∑PCB data but these are the weakest, the most unreliable, while the ∑PCB(6) and CB-153 concentration data are comparable if reported similarly by other means (mean, median, fat or fresh weight basis, cf. below).

The concentration reports for PBDEs follow a similar pattern as for the PCBs, often reporting ∑PBDEs but with differences in number and identity of PBDE congeners. Still, we have chosen to show ∑PBDE levels in Table 7, but for the purpose of comparison, BDE-47 and BDE-209 are recommended for use. The reporting variability applies for all POPs that have isomers and congeners and for which individual reference standards for analysis are available. The latter allows congener-, or isomer-, specific analysis, but the complexity of data generated call for simplifications.

Two classes of POPs, DDTs and dioxins, require further attention regarding concentration reports. The DDTs are commonly reported as the sum of 4,4′-DDT and its metabolites, 4,4′-DDE (major transformation product) and 4,4′-DDD. However, the ∑DDT may also include the true isomers, 2,4′-DDT and 4,4′-DDT or even the two isomers plus their metabolites. Concentrations of the abundant compounds 4,4′-DDT, 4,4′-DDE, and 4,4′-DDD are however quite frequently reported. This allows proper comparisons of the concentrations and to calculate comparable ratios of DDT versus either DDE or DDE and DDD, which can be done using different methods. In Table 2, we have applied the ratio 4,4′-DDT/4,4′-DDE due to the abundance of individual concentration data for these two pollutants.

The reporting of dioxin concentrations is another problem, even though individual concentration data are generated from the chemical analyses. The actual concentrations of dioxins (PCDDs, PCDFs, and DL-PCBs) are commonly reported as sum of their TEQs, after recalculation of the concentrations utilizing the TEF values—the most commonly used nowadays are the WHO TEFs from 1998 and 2005 (Van den Berg et al. 1998, 2006). However, if the ∑PCDDs, ∑PCDFs, and ∑DL-PCBs, or worse ∑dioxins, are presented, it is strongly limiting any comparisons, unless the actual concentration data of the individual congeners are presented as well.

In conclusion, POPs in mothers’ milk, as well as in other matrices, must be reported on a congener- or isomer-specific basis to promote proper trend studies. Unfortunately, this is not done in a structured manner today, which is strongly hampering the comparisons in the present data set on POPs in mothers’ milk.

Concentration base for POPs in mothers’ milk

The most common way of reporting concentrations of POPs in human matrices and wildlife is on weight basis, i.e., microgram, nanogram, picogram per weight of the matrix (gram or kilogram), or on volume (e.g., mL) of the matrix, which relates to a fresh weight, volume, or extracted lipids/fats. The concentrations are rarely reported on a molar base (e.g., nmol/g or pmol/g). Despite the fact that this is the correct way of assessing exposures used for risk assessments and for correct comparisons, this means reporting is only found in very few studies of POPs in mothers’ milk. This problem is particularly evident for the polybrominated pollutants, where the molecular weight varies greatly between the different congeners. The implications are shown in Fig. 24, where it is clear that the “number of molecules” (molar base) of CB-153 is 2.5 times the number of BDE-209, although the masses of the two are equal. Since there is such an extensive span in molecular masses among the POPs, it is crucial that this must be considered for future studies/reports on POPs.
Fig. 24

Comparison between CB-153 and BDE-209 on a weight (ng/g) and molar (pmol/g) basis

Another obstacle for comparisons of POPs in mothers’ milk is how to handle more water-soluble POPs, e.g., PFOS, other perfluorinated compounds, and organohalogen phenols. PFOS is commonly reported on a fresh weight basis, i.e., picograms per milliliter, while other POPs are reported on a fat weight basis (e.g., ng/g fat). To allow conversions, it is necessary to know the fat content of the matrix analyzed.

In conclusion, a change from weight- to molar-based reporting on POPs is needed in order to avoid unnecessary errors in exposure assessments and to allow accurate trend analyses. Furthermore, the fresh weight of mothers’ milk samples as well as concentrations on fat weight basis, and vice versa, should be mandatory since this would facilitate comparisons between studies.

Reporting

The reported measure of central tendency of the concentrations of POPs is not consistent, i.e., the arithmetic mean, the geometric mean, or median values, and sometimes, only a range is given without a mean or a median. This hampers the possibilities to compare data. However, if a log-normal distribution can be assumed, which is common for contaminant data (see, e.g., Esmen and Hammad 1977), the geometric mean and the median can be considered equal. The arithmetic mean is, with the same assumption of log-normality, always higher than the median. Some guidance of how to adjust for this bias is given by Caudill (2010, 2012). In conclusion, commonly agreed upon guidelines for this part in reporting exposure data are also required.

Overall conclusions

Unfortunately, reporting of POPs in mothers’ milk differs greatly between the studies. This has limited the comparisons for both spatial and temporal trend studies.

Acknowledgments

The financial support from the Swedish EPA is acknowledged for enabling this work.

Copyright information

© The Author(s) 2015

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  • Johan Fång
    • 1
    • 2
  • Elisabeth Nyberg
    • 2
  • Ulrika Winnberg
    • 1
  • Anders Bignert
    • 2
  • Åke Bergman
    • 1
    • 3
  1. 1.Department of Environmental Science and Analytical ChemistryStockholm University106 91 StockholmSweden
  2. 2.Department of Environmental Research and MonitoringSwedish Museum of Natural HistoryStockholmSweden
  3. 3.Swedish Toxicology Sciences Research Center (Swetox), Forskargatan 20SödertäljeSweden

Personalised recommendations