Skip to main content

Occurrence of aflatoxin M1 in conventional and organic milk offered for sale in Italy

Abstract

In the present study, 58 samples of milk were analyzed for the presence of aflatoxin M1 (AFM1). The samples were purchased during the period April–May 2013 in a random manner from local stores (supermarkets, small retail shops, small groceries, and specialized suppliers) located in the surrounding of Bologna (Italy). The commercial samples of milk were either organic (n = 22) or conventional (n = 36); fresh milk samples and UHT milk samples, whole milk samples, and partially skim milk samples were present in both the two considered categories. For the quantification of AFM1 in milk, the extraction-purification technique based on the use of immunoaffinity columns was adopted and analyses were performed using HPLC-FD. AFM1 was detected in 35 samples, 11 from organic production and 24 from conventional production. No statistically (P > 0.05) significant differences were observed in the concentration of AFM1 in the two categories of product. The levels of contamination found in the positive samples ranged between 0.009 and 0.026 ng mL−1. No sample exceeded the limit defined at community level for AFM1 in milk (0.05 μg kg−1). This demonstrates the effectiveness of the checks before the placing on the market of these food products. Thus, the “aflatoxins” problem that characterized the summer of 2012 does not seem to have had effect on the contamination level of the considered milk samples.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  • ANSA.it (2013) Latte tossico, arrestato leader Cospalat. Altri 4 ai domiciliari. Latte avariato venduto come buono. http://www.ansa.it/web/notizie/rubriche/cronaca/2013/06/20/Latte-tossico-arrestato-leader-Cospalat_8900234.html. Accessed 1 July 2016

  • Applebaum RS, Brackett RE, Wiseman DW, Marth EH (1982) Aflatoxin: toxicity to dairy cattle and occurrence in milk and milk products. A review J Food Protect 45:752–777

    CAS  Google Scholar 

  • Aycicek H, Aksoy A, Saygi S (2005) Determination of aflatoxin levels in some dairy and food products which consumed in Ankara, Turkey. Food Control 16:263–266

    CAS  Article  Google Scholar 

  • Battacone G, Palomba M, Usai MG, Pulina G (2003) Transfer of aflatoxin from feed to milk and curd in Sarda ewes with different milk production level. Ital J Anim Sci 2:530–532

    Google Scholar 

  • Bilandžić N, Božić D, Ðokić M, Sedak M, Kolanović BS, Varenina I, Tanković S, Cvetnić Z (2014) Seasonal effect on aflatoxin M1 contamination in raw and UHT milk. Food Control 40:260–264

    Article  Google Scholar 

  • Bognanno M, La Fauci L, Ritieni A, Tafuri A, De Lorenzo A, Micari P, Di Renzo L, Ciappellano S, Sarullo V, Galvano F (2006) Survey of the occurrence of aflatoxin M1 in ovine milk by HPLC and its confirmation by MS. Mol Nutr Food Res 50:300–305

    CAS  Article  PubMed  Google Scholar 

  • Bolzoni G, Zanardi G, Bertocchi L, Delle Donne G (2013) Risultati delle analisi dell’autocontrollo per la contaminazione da Aflatossina M1 nel latte in Lombardia. Large Anim Rev 19:251–255

    Google Scholar 

  • Capei R, Neri P (2002) Occurrence of aflatoxin M1 in milk and yoghurt offered for sale in Florence (Italy). Ann Ig 14:313–319

    CAS  PubMed  Google Scholar 

  • Caruso M, Mariotti A, Zizzadoro C, Zaghini A, Ormas P, Altafini A, Belloli C (2009) A clonal cell line (BME-UV1) as a possible model to study bovine mammary epithelial metabolism: metabolism and cytotoxicity of aflatoxin B1. Toxicon 53:400–408

    CAS  Article  PubMed  Google Scholar 

  • Casadio M, Tosi G, Massi P, Mazzotti E, Fiorentini L (2015) Evaluation of the risk of aflatoxin M1 contamination in bovine milk for human consumption in Romagna, Italy. Large Anim Rev 21:187–190

    Google Scholar 

  • Cavaliere C, Foglia P, Guarino C, Nazzari M, Samperi R, Laganà A (2007) A sensitive confirmatory method for aflatoxins in maize based on liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 21:550–556

    CAS  Article  PubMed  Google Scholar 

  • CLAL.it (2016) Dairy market—per capita consumption. http://www.clal.it. Accessed 13 April 2016

  • Corriere della Sera (2013) Latte tossico dal Friuli ai supermarket: 7 arresti. In manette anche il leader del Cospalat. http://www.corriere.it/cronache/13_giugno_20/latte-tossico-arresto_d1ee712a-d995-11e2-8116-cce4caac965d.shtml. Accessed 1 July 2016

  • Creppy EE (2002) Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol Lett 127:19–28

    CAS  Article  PubMed  Google Scholar 

  • Danieli PP, Giangolini G, Giontella D, Bernabucci U, Ronchi B (2005) Approccio epidemiologico allo studio delle contaminazioni da aflatossine B1 e M1 nel sistema di allevamento del bovino da latte. In: Istituto Superiore di Sanità. 1st National conference. Mycotoxins in agri-food chain. Istituto Superiore di Sanità. Rome, November 2004. Proceedings edited by Marina Miraglia and Carlo Brera 2005, vii, 357 p. Rapporti ISTISAN (in Italian) 05/42: 29–30

  • Decastelli L, Lai J, Gramaglia M, Monaco A, Nachtmann C, Oldano F, Ruffier M, Sezian A, Bandirola C (2007) Aflatoxins occurrence in milk and feed in Northern Italy. Food Control 18:1263–1266

    CAS  Article  Google Scholar 

  • European Commission (2006) Commission Regulation (EC) No. 401/2006 of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Off J Eur Union L. 70:12–34

    Google Scholar 

  • European Commission (2010) Commission Regulation (EC) No. 165/2010 of 26 February 2010 amending Regulation (EC) No. 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards aflatoxins. Off J Eur Union L 50:8–11

    Google Scholar 

  • European Commission (2013) Summary report of the standing committee on the food chain and animal health held in Brussels on 21 March 2013–22 March 2013 (section animal nutrition). http://ec.europa.eu/food/animals/docs/reg-com_ani-nutrit_20130221_sum.pdf. Accessed 5 July 2016

  • Fink-Gremmels J (2008) Mycotoxins in cattle feeds and carry-over to dairy milk: a review. Food Addit Contam 25:172–180

    CAS  Article  Google Scholar 

  • Fusi F, Scalvenzi A, Angelucci A, Bolzoni G, Bertocchi L (2013) Aflatossina/2: La fase di allerta non può dirsi conclusa. Informatore Zootecnico (Edagricole) 9:54–60 http://www.izsler.it/izs_bs/allegati/415/aflatossineIZ_2013_09.pdf. Accessed 1 July 2016

    Google Scholar 

  • Galvano F, Galofaro V, Galvano G (1996) Occurrence and stability of aflatoxin M1 in milk and milk products. A worldwide review J Food Protect 59:1079–1090

    CAS  Google Scholar 

  • Galvano F, Galofaro V, Ritieni A, Bognanno M, De Angelis A, Galvano G (2001) Survey of the occurrence of aflatoxin M1 in dairy products marketed in Italy: second year of observation. Food Addit Contam 18:644–646

    CAS  Article  PubMed  Google Scholar 

  • Ghidini S, Zanardi E, Battaglia A, Varisco G, Ferretti E, Campanini G, Chizzolini R (2005) Comparison of contaminant and residue levels in organic and conventional milk and meat products from Northern Italy. Food Addit Contam 22:9–14

    CAS  Article  PubMed  Google Scholar 

  • Haouet MN, Altissimi MS (2003) Micotossine negli alimenti e micotossicosi animale e umana. Elaborazione dei dati ottenuti dal 1992 al 1998. Webzine – Sanità Pubblica Veterinaria, 4, 19. http://spvet.it/arretrati/numero-40/003.html. Accessed 13 April 2016

  • Hernández-Martínez R, Navarro-Blasco I (2010) Aflatoxin levels and exposure assessment of Spanish infant cereals. Food Addit Contam 3:275–288

    Article  Google Scholar 

  • Hoogenboom LAP, Bokhorst JG, Northolt MD, Van de Vijver LPL, Broex NJG, Mevius DJ, Meijs JAC, Van der Roest J (2008) Contaminants and microorganisms in Dutch organic food products: a comparison with conventional products. Food Addit Contam 25:1195–1207

    CAS  Article  Google Scholar 

  • Huber M, Rembiałkowska E, Średnicka D, Bügel S, Van De Vijver LPL (2011) Organic food and impact on human health: assessing the status quo and prospects of research. NJAS-Wagen J Life Sc 58:103–109

    Article  Google Scholar 

  • Hussein HS, Brasel JM (2001) Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 167:101–134

    CAS  Article  PubMed  Google Scholar 

  • IARC (International Agency for Research on Cancer) (2002) Monograph on the evaluation of carcinogenic risk to humans: some traditional herbal medicines, some mycotoxins, naphthalene and styrene, vol 82. IARC Press, Lyon, pp. 1–556

    Google Scholar 

  • International Dairy Federation (2014) The World Dairy Situation 2014. Bulletin of the International Dairy Federation 476/2014. 25–26. http://www.fil-idf.org/Public/Download.php?media=41080. Accessed 20 July 2016

  • ISO (2008) ISO 9001:2008. Quality management systems—requirements. International Organization for Standardization, Geneva

    Google Scholar 

  • Jouany JP, Diaz DE (2005) Effects of mycotoxins in ruminants. In: Diaz DE (ed) The mycotoxin blue book. Nottingham University Press, Nottingham, pp. 295–321

    Google Scholar 

  • Kos J, Mastilovi J, Hajnal EJ, Sari B (2013) Natural occurrence of aflatoxins in maize harvested in Serbia during 2009-2012. Food Control 34:31–34

    CAS  Article  Google Scholar 

  • La Repubblica (2013) Latte tossico e cancerogeno in vendita in Friuli: 24 gli indagati, arrestato il leader di Cospalat. http://www.repubblica.it/cronaca/2013/06/20/news/latte_tossico_e_cancerogeno_in_vendita_in_friuli_24_gli_indagati_arrestato_il_leader_di_cospalat-61500569/. Accessed 1 July 2016

  • Martins ML, Martins HM (2000) Aflatoxin M1 in raw and ultra high temperature-treated milk commercialized in Portugal. Food Addit Contam 17:871–874

    CAS  Article  PubMed  Google Scholar 

  • Masoero F, Gallo A, Moschini M, Piva G, Diaz D (2007) Carryover of aflatoxin from feed to milk in dairy cows with low or high somatic cell counts. Animal 1:1344–1350

    CAS  Article  PubMed  Google Scholar 

  • Ministero della Salute (2013) Nota DGSAF 0000855-P-16/01/2013 Contaminazione da aflatossine nel mais e nella catena alimentare. http://www.unionalimentari.com/website/law.aspx?id=1287. Accessed 1 July 2016

  • Nachtmann C, Gallina S, Rastelli M, Ferro GL, Decastelli L (2007) Regional monitoring plan regarding the presence of aflatoxin M1 in pasteurized and UHT milk in Italy. Food Control 18:623–629

    CAS  Article  Google Scholar 

  • Park DL (2002) Effect of processing on aflatoxin. Adv Exp Med Biol 504:173–179

    CAS  Article  PubMed  Google Scholar 

  • Pietri A, Piva G (2007) Aflatoxins in foods. Ital J Public Health 1:32–38

    Google Scholar 

  • Pleadin J, Vuli A, Persi N, Skrivanko M, Capek B, Cvetni Z (2014) Aflatoxin B1 occurrence in maize sampled from Croatian farms and feed factories during 2013. Food Control 40:286–291

    CAS  Article  Google Scholar 

  • Ramos Catharino R, de Azevedo ML, Silva Santos L, Baptista AS, Glória EM, Calori-Domingues MA, Facco EMP, Eberlin MN (2005) Aflatoxin screening by MALDI–TOF mass spectrometry. Anal Chem 77:8155–8157

    Article  PubMed  Google Scholar 

  • Santini A, Raiola A, Ferrantelli V, Giangrosso G, Macaluso A, Bognanno M, Galvano F, Ritieni A (2013) Aflatoxin M1 in raw, UHT milk and dairy products in Sicily (Italy). Food Addit Contam Part B 6:181–186

    CAS  Article  Google Scholar 

  • Sarica DY, Has O, Tasdelen S, Ezer Ü (2015) Occurrence of aflatoxin M1 in milk, white cheese and yoghurt from Ankara, Turkey markets. Biol Chem Research 2015:36–49

    Google Scholar 

  • Schirone M, Visciano P, Olivastri AMA, Tofalo R, Perpetuini G, Suzzi G (2015) A one-year survey on aflatoxin M1 in raw milk. Ital J Food Sci 27:271–276

    CAS  Google Scholar 

  • Shenasi M, Candlish AAG, Aidoo KE (2002) The production of aflatoxins in fresh date fruits and under simulated storage conditions. J Sci Food Agr 82:848–853

    CAS  Article  Google Scholar 

  • Sifuentes dos Santos J, Ribeiro ABC, França VR, Katto S, Santana EHW (2015) Levels of aflatoxin M1 in dairy products from Londrina supermarkets and its estimated daily intake. ADSA-ASAS Joint Annual Meeting 2015. J Anim Sci 93, Suppl. s3/J. Dairy Sci. 98, Suppl. 2: 369 http://www.jtmtg.org/JAM/2015/abstracts/369.pdf. Accessed 1 July 2016

  • Škrbić B, Živanćev J, Antić I, Godula M (2014) Levels of aflatoxin M1 in different types of milk collected in Serbia: assessment of human and animal exposure. Food Control 40:113–119

    Article  Google Scholar 

  • Tam J, Mankotia M, Mably M, Pantazopoulos P, Neil RJ, Calway P, Scott PM (2006) Survey of breakfast and infant cereals for aflatoxins B1, B2, G1 and G2. Food Addit Contam 23:693–699

    CAS  Article  PubMed  Google Scholar 

  • Torović L (2015) Aflatoxin M1 in processed milk and infant formulae and corresponding exposure of adult population in Serbia in 2013–2014. Food Addit Contam Part B: 235–244.

  • USDA (United States Department of Agriculture) (2014) Gain Report Number RB1403. Serbia-Grain and Feed Annual http://gain.fas.usda.gov/Recent%20GAIN%20Publications/Grain%20and%20Feed%20Annual_Belgrade_Serbia_3-31-2014.pdf. Accessed 12 July 2016

  • US FDA (Food and Drug Administration) (2005) Compliance Policy Guides (GPG) Section 527.400. Whole Milk, Lowfat Milk, Skim Milk-Aflatoxin M1. http://www.fda.gov/ICECI/ComplianceManuals/CompliancePolicyGuidanceManual/ucm074482.htm. Accessed 13 April 2016

  • Veldman A, Meijs JAC, Borggreve GJ, Heeres-van der Tol JJ (1992) Carry-over of aflatoxin from cows’ food to milk. Anim Prod 55:163–168

    CAS  Article  Google Scholar 

  • Virdis S, Corgiolu G, Scarano C, Pilo AL, De Santis EPL (2008) Occurrence of aflatoxin M1 in tank bulk goat milk and ripened goat cheese. Food Control 19:44–49

    CAS  Article  Google Scholar 

  • Virdis S, Scarano C, Spanu V, Murittu G, Spanu C, Ibba I, De Santis EPL (2014) A survey on aflatoxin M1 content in sheep and goat milk produced in Sardinia Region, Italy (2005-2013). Ital J Food Saf 3:206–209

    Google Scholar 

  • Westlake K, Mackie RI, Dutton MF (1989) In vitro metabolism of mycotoxins by bacterial, protozoal and ovine ruminal fluid preparations. Anim Feed Sci Tech 25:169–178

    CAS  Article  Google Scholar 

  • Zanardi G, Bolzoni G, Delle Donne G, Biancardi A, Piro R, Bertocchi L (2013) Andamento e gestione dell’allerta aflatossina M1 nel latte in Lombardia nel 2012–2013. Atti XV Congresso Nazionale SIDiLV, Monreale (PA) - 23-25 Ottobre 2013:504–505. http://www.izsler.it/izs_bs/allegati/415/SIDILV_2013_Zanardi.pdf. Accessed 1 July 2016

  • Zinedine A, Brera C, Elakhdari S, Catano C, Debegnach F, Angelini S, De Santis B, Faid M, Benlemlih M, Minardi V, Miraglia M (2006) Natural occurrence of mycotoxins in cereals and spices commercialized in Morocco. Food Control 17:868–874

    CAS  Article  Google Scholar 

  • Zöllner P, Mayer-Helm B (2006) Trace mycotoxin analysis in complex biological and food matrices by liquid chromatography-atmospheric pressure ionisation mass spectrometry. J Chromatogr A 1136:123–169

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Paola Roncada.

Ethics declarations

Conflict of interest

None

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Armorini, S., Altafini, A., Zaghini, A. et al. Occurrence of aflatoxin M1 in conventional and organic milk offered for sale in Italy. Mycotoxin Res 32, 237–246 (2016). https://doi.org/10.1007/s12550-016-0256-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12550-016-0256-8

Keywords

  • Aflatoxin M1
  • Conventional milk
  • Organic milk
  • HPLC-FD
  • Immunoaffinity columns