Skip to main content
SpringerLink
Log in

Two-year survey on the seasonal incidence of aflatoxin M1 in traditional dairy products in Egypt

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

The most popular and economically important traditional dairy products in Egypt are raw milk, Karish cheese (an Arabian dairy product made from defatted cow milk) and Zabady (an Arabian yoghurt made from buffalo and cow milk). In this study, 302 traditional dairy samples including raw milk (120), white Karish cheese (118), and Zabady (64) were analyzed for aflatoxin M1 (AFM1) during different seasons in 2016 and 2017. Contamination of raw milk samples with AFM1 was 21.6% and 18.3% in samples collected in the two respective years with percentages of 100% and 90.9% exceeding the legal European limit (0.05 µg L−1). In Karish cheese samples, the contamination level was 33.9% and 44.6%, in the 2 years examined with percentages of 90.47% and 80% that were above the European limit (0.25 µg kg−1). In the case of Zabady, the AFM1-positive samples were 12.5% and 18.75%, and all of them were above the European limit (0.25 µg kg−1). However, average toxin concentration in Zabady was lower than that detected in milk and cheese. Despite the seasonal variations influencing the occurrence of AFM1 in the three dairy products, the AFM1 levels in samples collected in winter were significantly (P ≤ 0.001) greater than those collected in summer. The contamination levels of AFM1 in the traditional dairy products consumed in Egypt; represent a serious health risk. It is urgent to inspect dairy farms for contamination with aflatoxins in a regular manner.

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

Similar content being viewed by others

References

  • Abd El-Latif ME (2012) Economic study of milk production and consumption in Egypt. Egyptian Documentation and Information Centre for Agriculture (EDICA). http://agris.fao.org

  • Abou-Donia SA (2008) Origin, history and manufacturing process of Egyptian dairy products: an overview. J Food Sci Technol 5:51–62

    Google Scholar 

  • Assaf JC, Nahle S, Chokr A, Louka N, Atoui A, El Khoury A (2019) Assorted methods for decontamination of aflatoxin M1 in milk using microbial adsorbents. Toxins. https://doi.org/10.3390/toxins11060304

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahrami R, Shahbazi Y, Nikousefat Z (2016) Aflatoxin M1 in milk and traditional dairy products from west part of Iran: occurrence and seasonal variation with an emphasis on risk assessment of human exposure. Food Control 62:250–256

    Article  CAS  Google Scholar 

  • Capei R, Neri P (2002) Occurrence of aflatoxin M1 in milk and yoghurt offered for sale in Florence (Italy). Annali Di Igiene: Medicina Preventiva e Di Comunita 14:313–319

    CAS  Google Scholar 

  • Codex Alimentarius Commission (2001) Comments submitted on the draft maximum level for aflatoxin M1 in milk. Codex Committee on Food Additives and Contaminants 33rd Session, Hague, The Netherlands Commission Regulation (EC) No 257

  • Dashti B, Al-Hamli S, Alomirah H et al (2009) Levels of aflatoxin M1 in milk, cheese consumed in Kuwait and occurrence of total aflatoxin in local and imported animal feed. Food Control 20:686–690

    Article  CAS  Google Scholar 

  • El-baradei G, Delacroix-buchet A, Ogier JC (2008) Bacterial biodiversity of traditional Zabady fermented milk. Int J Food Microbiol 121:295–301

    Article  CAS  Google Scholar 

  • Elgerbi AM, Aidoo KE, Candlish AAG, Tester RF (2004) Occurrence of aflatoxin M1 in randomly selected North African milk and cheese samples. Food Addit Contam 21:592–597

    Article  CAS  Google Scholar 

  • El-Sayed AAA, Neamat-Allah AA, Aly SE (2000) Situation of mycotoxins in milk, dairy products and human milk in Egypt. Mycotoxin Res 16:91–100

    Article  Google Scholar 

  • Elzupir AO, Abas ARA, Fadul MH et al (2012) Aflatoxin M1 in breast milk of nursing Sudanese mothers. Mycotoxin Res 28:131–134

    Article  CAS  Google Scholar 

  • European Commission (2001) Commission Regulation (EC) No 466/2001 of 8 March 2001 setting maximum levels for certain contaminants in foodstuffs. European Commission, Brussels

  • Fallah AA (2010a) Aflatoxin M1 contamination in dairy products marketed in Iran during winter and summer. Food Control 21:1478–1481

    Article  CAS  Google Scholar 

  • Fallah AA (2010b) Assessment of aflatoxin M1 contamination in pasteurized and UHT milk marketed in central part of Iran. Food Chem Toxicol 48:988–991

    Article  CAS  Google Scholar 

  • Fallah AA, Rahnama M, Jafari T, Saei-Dehkordi SS (2011) Seasonal variation of aflatoxin M1 contamination in industrial and traditional Iranian dairy products. Food Control 22:1653–1656

    Article  CAS  Google Scholar 

  • FDA US (1996) Sec. 527.400 whole milk, low fat milk, skim milk-aflatoxin M1 (CPG 7106.210). FDA compliance policy guides. FDA, Washington, DC, 219

  • Hussain I, Anwar J (2008) A study on contamination of aflatoxin M1 in raw milk in the Punjab province of Pakistan. Food Control 19:393–395

    Article  CAS  Google Scholar 

  • IARC, International Agency for Research on Cancer (2002) Monograph on the evaluation of carcinogenic risks to humans, vol 82. World Health Organization, IARC, Lyon, p 171

    Google Scholar 

  • Iqbal SZ, Asi MR (2013) Assessment of aflatoxin M1 in milk and milk products from Punjab, Pakistan. Food Control 30:235–239

    Article  CAS  Google Scholar 

  • Iqbal SZ, Jinap S, Pirouz AA, Ahmad Faizal AR (2015) Aflatoxin M1in milk and dairy products, occurrence and recent challenges: a review. Trends Food Sci Technol 46:110–119

    Article  CAS  Google Scholar 

  • Ismaiel A, Papenbrock J (2015) Mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture 5:492–537

    Article  CAS  Google Scholar 

  • Kuboka MM, Imungi JK, Njue L, Mutua F, Grace D, Lindahl JF (2019) Occurrence of aflatoxin M1 in raw milk traded in peri-urban Nairobi, and the effect of boiling and fermentation. Infect Ecol Epidemiol 9:1–8. https://doi.org/10.1080/20008686.2019.1625703

    Article  Google Scholar 

  • Langat G, Tetsuhiro M, Gonoi T et al (2016) Aflatoxin M1 contamination of milk and its products in Bomet County, Kenya. Adv Microbiol 6:528–536

    Article  CAS  Google Scholar 

  • Mahosotanand B (2002) Relationship between aflatoxin M1 in milk and aflatoxin B1 in feedstuffs. In: Proceedings of evaluation and management of integrated problems solving of afltoxins in food and feedstuffs Thai Industrial Standards Institute Ministry of Industry, Bangkok, pp 67–69

  • Martins ML, Martins HM (2004) Aflatoxin M1 in yoghurts in Portugal. Int J Food Microbiol 91:315–317

    Article  CAS  Google Scholar 

  • Martins HM, Guerra MM, Bernardo F (2005) A six year survey (1999–2004) of the occurrence of aflatoxin M1 in dairy products produced in Portugal. Mycotoxin Res 21(3):192–195

    Article  CAS  Google Scholar 

  • Mikkelsen P (2014) World Cheese Market Report 2000–2020. PM Food and Dairy Consulting

  • Mohajeri FA, Ghalebi SR, Rezaeian M et al (2013) Aflatoxin M1 contamination in white and Lighvan cheese marketed in Rafsanjan, Iran. Food Control 33:525–527

    Article  Google Scholar 

  • Motawee MM, Bauer J, McMahon DJ (2009) Survey of Aflatoxin M1in Cow, Goat, Buffalo and camel milks in Ismailia-Egypt. Bull Environ Contam Toxicol 83:766–769

    Article  CAS  Google Scholar 

  • Oluwafemi F, Badmos AO, Kareem SO et al (2014) Survey of aflatoxin M1in cows’ milk from free-grazing cows in Abeokuta, Nigeria. Mycotoxin Res 30:207–211

    Article  CAS  Google Scholar 

  • Oruc HH, Cibik R, Yilmaz E, Kalkanli O (2006) Distribution and stability of aflatoxin M1 during processing and ripening of traditional white pickled cheese. Food Addit Contam 23:190–195

    Article  CAS  Google Scholar 

  • Öztürk Yilmaz S, Altinci A (2019) Incidence of aflatoxin M1 contamination in milk, white cheese, Kashar and butter from Sakarya, Turkey. Food Sci Technol 39:190–194

    Article  Google Scholar 

  • Panahi P, Kasaee S, Mokhtari A, Sharifi A, Jangjou A (2011) Assessment of Aflatoxin M1 Contamination in Raw Milk by ELISA in Urmia, Iran. Am Eurasian J Toxicol Sci 3:231–233

    Google Scholar 

  • Rodriguez Velasco ML, Calonge Delso MM, Ordonez Escudero D (2003) ELISA and HPLC determination of the occurrence of aflatoxin M 1 in raw cow’s milk. Food Addit Contam 20:276–280

    Article  CAS  Google Scholar 

  • Ruangwises S, Ruangwises N (2009) Occurrence of aflatoxin M1 in pasteurized milk of the school milk project in Thailand. J Food Prot 72:1761–1763

    Article  CAS  Google Scholar 

  • SAS (2004) SAS/STAT® 9.1 User’s Guide. SAS Institute Inc., New York

    Google Scholar 

  • Shundo L, Sabino M (2006) Aflatoxin M1 in milk by immunoaffinity column cleanup with TLC/HPLC determination. Braz J Microbiol 37:164–167

    Article  Google Scholar 

  • Stubblefield RD (1979) The rapid determination of aflatoxin M1 in dairy products. J Am Oil Chemists’ Soc 56:800–802

    Article  CAS  Google Scholar 

  • Tekinşen KK, Eken HS (2008) Aflatoxin M1 levels in UHT milk and kashar cheese consumed in Turkey. Food Chem Toxicol 46:3287–3289

    Article  Google Scholar 

  • Unusan N (2006) Occurrence of aflatoxin M1 in UHT milk in Turkey. Food Chem Toxicol 44:1897–1900

    Article  CAS  Google Scholar 

  • Van der Fels-Klerx HJ, Vermeulen LC, Gavai AK, Liu C (2019) Climate change impacts on aflatoxin B1 in maize and aflatoxin M1 in milk: a case study of maize grown in Eastern Europe and imported to the Netherlands. PLoS ONE 14:1–14

    Google Scholar 

  • Venâncio RL, Ludovico A, deSantana EHW, de Toledo EA, de Almeida Rego FC, dos Santos JS (2019) Occurrence and seasonality of aflatoxin M1 in milk in two different climate zones. J Sci Food Agric 99:3203–3206

    Article  Google Scholar 

Download references

Acknowledgements

The author thanks Dr. Reda E. Hamouda, Department of Animal Production Systems Research, Animal Production Research Institute, Agricultural Research Center, Ministry of Agriculture, Dokki, Giza, Egypt for performing the statistical analyses. The work employed herein was supported in part by the Department of Botany and Microbiology, Faculty of Science, Cairo University, Cairo, Egypt.

Author information

Authors and Affiliations

  1. Department of Botany and Microbiology, Faculty of Science, Zagazig University, Zagazig, 44519, Egypt

    Ahmed A. Ismaiel

  2. Department of Botany and Microbiology, Faculty of Science, Cairo University, Cairo, Egypt

    Nagwa A. Tharwat, Mohsen A. Sayed & Sara A. Gameh

Authors
  1. Ahmed A. Ismaiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nagwa A. Tharwat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohsen A. Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sara A. Gameh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed A. Ismaiel.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

13197_2020_4254_MOESM1_ESM.jpg

HPLC chromatogram of AFM1 showing Rt of 8.70 min. a Standard solution from Sigma-Aldrich, Taufkirchen, Germany. b Naturally contaminated Karish cheese sample (KCA 50). The sample was extracted with saturated NaCl and chloroform and the dried crude extract was dissolved in methanol and spotted with AFM1 standard on TLC. A 20 µL of standard and sample solution was injected separately into HPLC under the conditions described in Materials and methods section. (JPEG 919 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ismaiel, A.A., Tharwat, N.A., Sayed, M.A. et al. Two-year survey on the seasonal incidence of aflatoxin M1 in traditional dairy products in Egypt. J Food Sci Technol 57, 2182–2189 (2020). https://doi.org/10.1007/s13197-020-04254-3

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-020-04254-3

Keywords

Search

Navigation