Skip to main content
SpringerLink
Log in

Health risk assessments of heavy metals and trace elements exposure in the breast milk of lactating mothers in the Northeastern Iran

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Mother’s breast milk is a natural and complete food for infants but can be a main source of exposure to toxic pollutants. These pollutants can negatively affect the health of the infant. Therefore, conducting biomonitoring surveys is essential to evaluate such health effects in toxicological research. This study aimed to estimate the probable health risks for infants exposed to essential and non-essential trace elements through breast milk ingestion. This descriptive-analytical, cross-sectional study was performed on 90 breastfeeding mothers referred to the health centers in Mashhad, Iran in January 2021. The health risk assessments (carcinogenic and non-carcinogenic risk) were estimated using chronic daily intake (CDI), hazard quotient (HQ), hazard index (HI), and lifetime carcinogenic risk (CR), which were recommended by the US Environmental Protection Agency (US EPA). The results of the HQ values of trace elements through ingestion exposure for arsenic (90%), copper (90%), zinc (40%), and iron (10%) exceeded the threshold of HQ, and arsenic (66.59%), copper (16.91%), and zinc (9.68%) and iron (4.57%) had the highest contribution to increasing the HI index. The average value of CR was 5. 08 × 10−3. Chromium and iron showed significant relationships (P<0.05) with education level and disease background in this study, and the concentration of chromium, iron, and zinc in the breast milk samples significantly changed during lactation stages (P<0.05). Overall, the risk of carcinogenicity through exposure to breast milk for infants was higher than the safety level of US EPA risk. Therefore, there could be a potential health risk of trace elements, particularly arsenic, copper, and zinc for infants in Mashhad, Iran through the consumption of mothers' breast milk. More efforts are required to control and reduce routes of receiving trace elements in breastfeeding mothers by the competent authorities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

We declare that all data relating to this manuscript are truthful and we will gladly share it with any interested readers or at the request of the editor board.

References

  • Alidadi H, Tavakoly Sany SB, Oftadeh BZG, Mohamad T, Shamszade H, Fakhari M (2019) Health risk assessments of arsenic and toxic heavy metal exposure in drinking water in northeast Iran. Environ Health Prev Med 24(1):1–17

    CAS  Google Scholar 

  • Almeida AA, Lopes CM, Silva AM, Barrado E (2008) Trace elements in human milk: correlation with blood levels, inter-element correlations and changes in concentration during the first month of lactation. J Trace Elem Med Biol 22(3):196–205

    CAS  Google Scholar 

  • Al-Saleh I (2021) Health risk assessment of trace metals through breast milk consumption in Saudi Arabia. Biol Trace Elem Res 199(12):4535–4545

  • Ashley-Martin J, Iannotti L, Lesorogol C, Hilton CE, Olungah CO, Zava T, Needham BL, Cui Y, Brindle E, Straight B (2022) Heavy metal blood concentrations in association with sociocultural characteristics, anthropometry and anemia among Kenyan adolescents. Int J Environ Health Res 32(9):1935–1949

    Google Scholar 

  • Aung H, Soe K, Smithuis FF, Lamb T, Aung MW, Smithuis FM (2021) Case Report: children with severe nutritional rickets in the Naga Region in Northwest Myanmar, on the border with India. Am J Trop Med Hyg 105(1):217

    Google Scholar 

  • Bahmani P, Maleki A (2018) Investigation of mercury, cadmium and arsenic levels in breast milk and their relationship with the studied parameters in Sanandaj, Iran. Zanko J Med Sci 19(62):84–97

  • Bassil M, Daou F, Hassan H, Yamani O, Abi Kharma J, Attieh Z, Elaridi J (2018) Lead, cadmium and arsenic in human milk and their socio-demographic and lifestyle determinants in Lebanon. Chemosphere 191:911–921

    CAS  Google Scholar 

  • Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9):124–152

  • Carignan CC, Karagas MR, Punshon T, Gilbert-Diamond D, Cottingham KL (2016) Contribution of breast milk and formula to arsenic exposure during the first year of life in a US prospective cohort. J Expo Sci Environ Epidemiol 26(5):452–457

    CAS  Google Scholar 

  • Chandravanshi L, Shiv K, Kumar S (2021) Developmental toxicity of cadmium in infants and children: a review. Environ Anal Health Toxicol 36(1):2311–139

  • Chien L-C, Han B-C, Hsu C-S, Jiang C-B, You H-J, Shieh M-J, Yeh C-Y (2006) Analysis of the health risk of exposure to breast milk mercury in infants in Taiwan. Chemosphere 64(1):79–85

    CAS  Google Scholar 

  • Choi J, Chang JY, Hong J, Shin S, Park JS, Oh S (2017) Low-level toxic metal exposure in healthy weaning-age infants: association with growth, dietary intake, and iron deficiency. Int J Environ Res Public Health 14(4):388

    Google Scholar 

  • Czarnek K, Terpiłowska S, Siwicki AK (2015) Selected aspects of the action of cobalt ions in the human body. Cent Eur J Immunol 40(2):236

    Google Scholar 

  • De Rezende Pinto M, Almeida AA (2018) Trace elements in the human milk. Trace Elements-Human Health Environ 85 (3):413–426

  • DesMarias TL, Costa M (2019) Mechanisms of chromium-induced toxicity. Curr Opin Toxicol 14:1–7

    Google Scholar 

  • Ekeanyanwu CL, Alisi CS, Ekeanyanwu RC (2020) Levels of Aflatoxin M1 and selected heavy metals (Pb, Cd, Cr, Cu, Zn, Fe, As, and Hg) in the breast milk of lactating mothers in South Eastern, Nigeria. Food Control 112:107150

    CAS  Google Scholar 

  • Faith DK, Glory B, Nyebuchi J, Fyneface Amadi C, Eedee Konne F (2021) Comparative study of heavy metals in breast milk of breast feeding mothers in urban and sub-urban subjects in rivers state

  • Ghasemi S, Hashemi M, Gholian Aval M, Khanzadi S, Safarian M, Orooji A, Tavakoly Sany SB (2022) Effect of Baking Methods Types on Residues of Heavy Metals in the Different Breads Produced with Wheat Flour in Iran: A Case Study of Mashhad. J Chem Health Risks 12(1):105–113

    CAS  Google Scholar 

  • Goudarzi M, Parsaei P, Nayebpour F, Rahimi E (2013) Determination of mercury, cadmium and lead in human milk in Iran. Toxicol Ind Health 29(9):820–823

    CAS  Google Scholar 

  • Goyer R (2004) Issue paper on the human health effects of metals. US Environmental Protection Agency 2(3):92–107

  • Hadiani MR, Dezfooli-Manesh S, Shoeibi S, Ziarati P, Mousavi Khaneghah A (2015) Trace elements and heavy metals in mineral and bottled drinking waters on the Iranian market. Food Addit Contam Part B 8(1):18–24

    CAS  Google Scholar 

  • Ijomone OM, Olung NF, Akingbade GT, Okoh CO, Aschner M (2020) Environmental influence on neurodevelopmental disorders: potential association of heavy metal exposure and autism. J Trace Elem Med Biol 62:126638

  • Islam MR, Attia J, Alauddin M, McEvoy M, McElduff P, Slater C, Islam MM, Akhter A, d’Este C, Peel R (2014) Availability of arsenic in human milk in women and its correlation with arsenic in urine of breastfed children living in arsenic contaminated areas in Bangladesh. Environ Health 13(1):1–10

    Google Scholar 

  • Jadaa W, Mohammed H (2023) Heavy metals--definition, natural and anthropogenic sources of releasing into ecosystems, toxicity, and removal methods--an overview study. J Ecol Eng 24(6):23–34

  • Javad MT, Vahidinia A, Samiee F, Elaridi J, Leili M, Faradmal J, Rahmani A (2018) Analysis of aluminum, minerals and trace elements in the milk samples from lactating mothers in Hamadan, Iran. J Trace Elem Med Biol 50:8–15

    Google Scholar 

  • Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes C, Valko M (2011) Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 31(2):95–107

    CAS  Google Scholar 

  • Jyothi NR (2020) Heavy metal sources and their effects on human health. Heavy Metals, Their Environmental Impacts and Mitigation 12(4):34–39

  • Khan S, Ismail A, Gong YY, Akhtar S, Hussain M (2018) Concentration of Aflatoxin M1 and selected heavy metals in mother milk samples from Pakistan. Food Control 91:344–348

    CAS  Google Scholar 

  • Khanjani N, Jafari M, Ahmadi Mousavi E (2018) Breast milk contamination with lead and cadmium and its related factors in Kerman, Iran. J Environ Health Sci Eng 16(2):323–335

    CAS  Google Scholar 

  • Khodavirdipour A, Haddadi F, Keshavarzi S (2020) Chromium supplementation; negotiation with diabetes mellitus, hyperlipidemia and depression. J Diabetes Metab Disord 19(1):585–595

    CAS  Google Scholar 

  • Kianpoor S, Sobhanardakani S (2017) Evaluation of Zn, Pb, Cd and Cu concentrations in wheat and bread consumed in Hamedan city. Food Hygiene 7(4 (28)):83–92

    Google Scholar 

  • Kogianni E, Kouras A, Samara C (2021) Indoor concentrations of PM 2.5 and associated water-soluble and labile heavy metal fractions in workplaces: implications for inhalation health risk assessment. Environ Sci Pollut Res 28:58983–58993

    CAS  Google Scholar 

  • Kunter İ, Hürer N, Gülcan HO, Öztürk B, Doğan İ, Şahin G (2017) Assessment of aflatoxin M1 and heavy metal levels in mothers breast milk in Famagusta, Cyprus. Biol Trace Elem Res 175(1):42–49

    CAS  Google Scholar 

  • Lin H-H, Jung C-R, Lin C-Y, Chang Y-C, Hsieh C-Y, Hsu P-C, Chuang B-R, Hwang B-F (2023) Prenatal and postnatal exposure to heavy metals in PM2. 5 and autism spectrum disorder. Environ Res 237:116874

    CAS  Google Scholar 

  • Magnano GC, Marussi G, Pavoni E, Adami G, Filon FL, Crosera M (2022) Percutaneous metals absorption following exposure to road dust powder. Environ Pollut 292:118353

    CAS  Google Scholar 

  • Mandić Z, Mandić ML, Grgić J, Grgić Z, Klapec T, Primorac L, Hasenay D (1997) Copper and zinc content in human milk in Croatia. Eur J Epidemiol 13(2):185–188

    Google Scholar 

  • McDermott S, Salzberg DC, Anderson AP, Shaw T, Lead J (2015) Systematic review of chromium and nickel exposure during pregnancy and impact on child outcomes. J Toxic Environ Health A 78(21-22):1348–1368

    CAS  Google Scholar 

  • Mohammadi S, Shafiee M, Faraji SN, Rezaeian M, Ghaffarian-Bahraman A (2022) Contamination of breast milk with lead, mercury, arsenic, and cadmium in Iran: a systematic review and meta-analysis. BioMetals 35(4):711–728

    CAS  Google Scholar 

  • Motas M, Jiménez S, Oliva J, Cámara MÁ, Pérez-Cárceles MD (2021) Heavy Metals and Trace Elements in Human Breast Milk from Industrial/Mining and Agricultural Zones of Southeastern Spain. Int J Environ Res Public Health 18(17):9289

    Google Scholar 

  • Nazlıcan E, Arıca E, Gören İE, Kılınçlı B, Mete B, Daglioglu N (2022) The risk estimation and assessment of heavy metal exposure by biomonitoring in the breast milk of mothers in the Cukurova Region, Turkey. Environ Sci Pollut Res 29(10):13963–13970

    Google Scholar 

  • Olowoyo JO, Macheka LR, Mametja PM (2021) Health Risk Assessments of Selected Trace Elements and Factors Associated with Their Levels in Human Breast Milk from Pretoria, South Africa. Int J Environ Res Public Health 18(18):9754

    CAS  Google Scholar 

  • Pajewska-Szmyt M, Sinkiewicz-Darol E, Gadzała-Kopciuch R (2019) The impact of environmental pollution on the quality of mother’s milk. Environ Sci Pollut Res 26(8):7405–7427

    CAS  Google Scholar 

  • Park Y, Lee A, Choi K, Kim H-J, Lee JJ, Choi G, Kim S, Kim SY, Cho GJ, Suh E (2018) Exposure to lead and mercury through breastfeeding during the first month of life: A CHECK cohort study. Sci Total Environ 612:876–883

    CAS  Google Scholar 

  • Peiravi R, Dehghan AA, Vahedian M (2013) Heavy metals concentrations in Mashhad drinking water network. Zahedan J Res Med Sci 15(9):112–134

  • Rodríguez J, Mandalunis PM (2018) A review of metal exposure and its effects on bone health. J Toxicol 3(2):45–67

  • Sadeghi N, Jannat B, Behzad M, Oveisi MR, Hajimahmoodi M, Ahmadi F (2020) Determination of zinc, copper, lead and cadmium concentration in breastmilk by anodic stripping voltammetry method and investigating their impact on infants’ growth indicators. Hum Health Halal Metrics 1(2):24–30

    CAS  Google Scholar 

  • Samanta G, Das D, Mandal BK, Chowdhury TR, Chakraborti D, Pal A, Ahamed S (2007) Arsenic in the breast milk of lactating women in arsenic-affected areas of West Bengal, India and its effect on infants. J Environ Sci Health A 42(12):1815–1825

    CAS  Google Scholar 

  • Samiee F, Vahidinia A, Javad MT, Leili M (2019) Exposure to heavy metals released to the environment through breastfeeding: a probabilistic risk estimation. Sci Total Environ 650:3075–3083

    CAS  Google Scholar 

  • Shad R, Khorrami M, Ghaemi M (2017) Developing an Iranian green building assessment tool using decision making methods and geographical information system: case study in Mashhad city. Renew Sust Energ Rev 67:324–340

    Google Scholar 

  • Sharma N, Sodhi KK, Kumar M, Singh DK (2021) Heavy metal pollution: insights into chromium eco-toxicity and recent advancement in its remediation. Environ Nanotechnol Monit Manag 15:100388

    CAS  Google Scholar 

  • Siabani S, Siabani S, Siabani H, Arya MM, Rezaei F, Babakhani M (2018) Determinants of compliance with iron and folate supplementation among pregnant women in West Iran: a population based cross-sectional study. J Family Reprod Health 12(4):197–205

  • Tolins M, Ruchirawat M, Landrigan P (2014) The developmental neurotoxicity of arsenic: cognitive and behavioral consequences of early life exposure. Ann Glob Health 80(4):303–314

    Google Scholar 

  • Torchi M, Seyedain Ardabili M, Azizi Nejad R, Nematollahi F (2016) Assessing the effect of baking methods on the levels of heavy metals in Iranian traditional breads. J Food Technol Nutr 14(1):5–12

    Google Scholar 

  • U.S. EPA (2002) A review of the reference dose and reference concentration processes. U.S. Environmental Protection Agency, Risk Assessment Forum, Washington, DC, EPA/630/P-02/002F

  • U.S.EPA (2008) Child-specific exposure factors handbook (2008, Final Report). U.S. Environmental Protection Agency, Washington, DC, EPA/600/R-06/096F

  • U.S. EPA (2011) Exposure factors handbook edition (Final Report). U.S. Environmental Protection Agency, Washington, DC, EPA/600/R-09/052F

  • U.S. EPA (2018) Guidelines for carcinogen risk assessment EPA/630/P-03/001F

  • U.S.EPA (2023) Risk assessment guidance for superfund: volume 1- human health evaluation manual (part b, development of risk-based preliminary remediation goals) from https://www.epa.gov/risk

  • Vahidinia A, Samiee F, Faradmal J, Rahmani A, Taravati Javad M, Leili M (2019) Mercury, lead, cadmium, and barium levels in human breast milk and factors affecting their concentrations in Hamadan, Iran. Biol Trace Elem Res 187:32–40

    CAS  Google Scholar 

  • Visconti V, Gasperini B, Greggi C, Battistini B, Messina A, Renzi M, Bakhtafrouz K, Iundusi R, Botta A, Palombi L (2023) Plasma heavy metal levels correlate with deregulated gene expression of detoxifying enzymes in osteoporotic patients. Sci Rep 13(1):10641

    CAS  Google Scholar 

  • WHO (1986) Principles for evaluating health risks from chemicals during infancy and early childhood: the need for a special approach. World Health Organization 12:23–45

  • WHO (1989) Minor and trace elements in breast milk: report of a joint WHO/IAEA collaborative study. Minor and trace elements in breast milk: report of a joint WHO/IAEA collaborative study

  • WHO (2010) Body mass index-BMI. A healthy lifestyle - WHO recommendations, Fact Sheet. http://www.euro.who.int/en/health-topics/diseaseprevention/nutrition/a-healthy-lifestyle/body-mass-index-bmi

  • WHO (2018) Guideline Counselling of women to improve breastfeeding practices. World Health Organization. Committee, Nutrition and Food Safety (NFS)

  • Xia W, Hu J, Zhang B, Li Y, Wise JP Sr, Bassig BA, Zhou A, Savitz DA, Xiong C, Zhao J (2016) A case-control study of maternal exposure to chromium and infant low birth weight in China. Chemosphere 144:1484–1489

    CAS  Google Scholar 

  • Zhang S, Sun L, Zhang J, Liu S, Han J, Liu Y (2020) Adverse impact of heavy metals on bone cells and bone metabolism dependently and independently through anemia. Adv Sci 7(19):2000383

    CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the vice president of research at the Mashhad University of Medical Sciences, the chiefs of the health centers affiliated with the university. We would also like to extend our appreciation to all participants and data collectors.

Funding

This project was generously supported financially by the Mashhad University of Medical Sciences. Grant number: 4022086.

Author information

Author notes

  1. Shiva Rahati and Asma Afshari contributed equally as first author

Authors and Affiliations

  1. Department of Food Sciences and Technology, Faculty of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran

    Shiva Rahati

  2. Medical Toxicology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Mohammad Hashemi & Asma Afshari

  3. Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Mohammad Hashemi & Asma Afshari

  4. Department of Epidemiology and Biostatistics, Faculty of Health Sciences, Mashhad University of Medical Sciences, Mashhad, 13131-99137, Iran

    Arezoo Orooji

  5. Department of Health, Safety, Environment Managment, School of Health Mashhad University of Medical Sciences, Mashhad, Iran

    Seyedeh Belin Tavakoly Sany

  6. Social Determinants of Health Research Center, Mashhad University of Medical Sciences, Mashhad, 13131-99137, Iran

    Seyedeh Belin Tavakoly Sany

Authors
  1. Shiva Rahati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Hashemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arezoo Orooji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Asma Afshari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seyedeh Belin Tavakoly Sany
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MH, SBTS, and AA contributed to the design of the study and the interpretation of the results. SHR and SBTS drafting of the manuscript. SHR and AA conducted the collection of the data. AO conducted the statistical analyses. SBTS, conducted uncertainty and sensitivity analysis and revised the manuscript based on reviewer’s comments. All authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Seyedeh Belin Tavakoly Sany.

Ethics declarations

Ethical approval

The study protocol was approved by the Ethics Committee of Mashhad University of Medical Sciences based project number 4022162 after obtaining the required permit for the research. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee with the 1964 Helsinki declaration.

Consent to participate

The participants provided written informed consent and were assured of confident.

Consent to publish

The authors consent to publish this manuscript entitled “Health Risk Assessments of Heavy Metals and Trace Elements Exposure in Human Breast Milk in Iran” to the Environmental Science and Pollution Research (ESPR).

Competing interests

The authors declare that they have no competing interests

Disclosure

The manuscript is not submitted to more than one journal for simultaneous consideration. The manuscript is original and has not been published elsewhere in any form or language (partially or in full), unless the new work concerns an expansion of previous work. The manuscript is not split up into several parts to increase the quantity of submissions and submitted to various journals or to one journal over time. Results are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. We adhere to discipline-specific rules for acquiring, selecting, and processing data. We have provided all data and proper mentions of other works.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahati, S., Hashemi, M., Orooji, A. et al. Health risk assessments of heavy metals and trace elements exposure in the breast milk of lactating mothers in the Northeastern Iran. Environ Sci Pollut Res 31, 25892–25906 (2024). https://doi.org/10.1007/s11356-024-32795-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-024-32795-z

Keywords

Search

Navigation