Assessment of aflatoxin M1 in maternal breast milk in Eastern Turkey

doi:10.1016/j.fct.2014.01.037

Food and Chemical Toxicology

Volume 66, April 2014, Pages 147-149

https://doi.org/10.1016/j.fct.2014.01.037 Get rights and content

Highlights

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The exposure of mothers and neonates to AFM1.
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No significant correlation between moldy cheese consumption and AFM1 levels in maternal breast milk.
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Necessity of future research on micotoxin contamination to develop protection strategies.

Abstract

Breastfeeding may be considered as a risk factor for aflatoxin M1 (AFM1) exposure in early infancy. Hence, AFM1 levels in maternal breast milk (MBM) and the correlation between moldy cheese consumption of lactating mothers and infant exposure to AFM1 were investigated in this study. MBM samples from 73 lactating women randomly selected in hospitals located in Eastern Turkey were analysed for the presence of AFM1 using competitive ELISA. Out of 73 lactating mothers, 44 of them had the habit of cheese consumption (at least once a week), while remaining 29 had no such habit. AFM1 was detected in MBM of 18 out of 73 samples (24.6%); 12 MBM of 44 lactating mothers with moldy cheese consumption habit (27.2%) and 6 MBM of 29 mothers with no such habit (20.6%) with the range of 1.3–6.0 ng/l. None of the samples exceeded the limit set by EU and Turkish legislations. Moldy cheese consumption habit of lactating mothers exhibited no significant correlation with the presence of AFM1 in their milk (p > 0.05). The results indicated that the relative risk of infant AFM1 exposure via MBM of moldy cheese consuming mother was not higher than MBM of mothers with no such habit.

Introduction

Human milk is ultimately the best source of nutrition for infants. Breastfeeding offers many advantages to both babies and mothers from psychological, immunological and economic point of view. Although breast milk contains optimally balanced fats, carbohydrates and proteins, it may also contain toxic chemicals caused by pollution and other sources. People including mothers in lactation period are exposed to different naturally occurring and/or synthetic contaminants and nearly all nutrients are also polluted with these kinds of contaminants in different degrees (Gürbay et al., 2010). It has been recognized that the children exposed to aflatoxin M1 (AFM1) through milk or it is by products may become prone to the infectious diseases, underweight, and stunted during infancy and for the rest of their life (IARC, 2002).

Aflatoxin M1 is usually considered to be a detoxification by product of aflatoxin B1 (AFB1), which may be found in milk products obtained from the livestock fed with AFB1-contaminated feed (Creppy, 2002). Among more than three hundred aflatoxins, AFB1 is the most prevalent and toxic one. AFM1 acute toxicity is less severe than that of AFB1 and it belongs to Group 2B as “a potentially carcinogenic agent for human” (IARC, 1993). Although AFM1, a genotoxic carcinogen, is less toxic (about 10 times) than AFB1, exposure of infants to AFM1 exhibits an alarming condition. High metabolic rate, lower detoxifying ability, low body weights and incomplete development of vital organs (especially the central nervous system) makes infants more susceptible than adults for the adverse effects of AFM1.

The occurrence of AFM1 in cheese may be due to AFM1 contamination of raw milk used in cheese manufacture or synthesis of aflatoxins by Aspergillus flavus and Aspergillus parasiticus growing on cheese (Zerfiridis, 1985). As moldy cheese is not generally produced by using starter cultures under controlled conditions in Turkey, the presence of AFM1 in this kind of cheese type is of concern.

In Turkey, there exist a few data (Keskin et al., 2009, Gürbay et al., 2010) about AFM1 incidence on human breast milk. The aim of this study was therefore; (i) to determine the presence and level of AFM1 in human milk in Eastern Turkey and (ii) to evaluate any possible correlation between moldy cheese consumption of mother and AFM1exposure of their infants.

Section snippets

Sample preparation

Milk samples were collected from women between December 2008 and April 2009. A total of 73 human breast milk samples were obtained from mothers whose infants were inpatient in Department of Pediatrics, Section of Neonatology, Ataturk University, Faculty of Medicine, Erzurum, Turkey.

Equal amounts of breast milk (20 ml) were obtained from a total of 73 volunteer lactating mothers who were asked to complete a questionnaire to provide information whether they had the habit to consume moldy cheese at

Results

Among the examined MBM of volunteer lactating mothers for their containment of AFM1, 18 out of 73 samples (24.6%) were found to be positive with the range of 1.3 and 6.0 ng/l (Table 1). AFM1 was determined from 12 MBM of 44 lactating mothers with moldy cheese consumption habit (27.2%) and 6 MBM of 29 mothers with no such habit (20.6%) ranging from 1.3 to 6.0 ng/l and 2 to 4.5 ng/l, respectively. No significant difference was observed between the groups for their AFM1 contents (p > 0.05) (Table 1).

Discussion

Mycotoxins are one of the most critical naturally occuring toxins in various foods under proper conditions. Review of literature shows that, because of the immunologic and nutritional effects of aflatoxin, there is a reasonable probability that the 6 top WHO risk factors for short lifespan, as well as the risks of liver cancer, are modulated by aflatoxin (Williams et al., 2004). Indeed, even small amounts of this metabolite in milk are of importance for the consumers of large quantities of

Conclusion

These results pointed out the exposure of mothers and neonates to AFM1. Low amount of AFM1 found in this study supports the need for continuous breastfeeding of infants from the food safety point of view. It is recommended that further studies be extended to the large quantity of human milk samples, infant formulas, milk-based products and other edible products destined to children. There is need to continue to monitor the level of contamination both in food and biological fluids to ensure

Conflict of Interest

The authors declare that there are no conflicts of interest.

Transparency Document

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Aflatoxin M1 (AFM1) is the hydroxylated metabolite of aflatoxin B1 (AFB1) formed in the liver of mammals and subsequently excreted in breastmilk (BM) of mammals. Humans are exposed to AFM1 mainly through the consumption of aflatoxin contaminated milk and foods. Determining levels of AFM1 is of significant public health importance due to the risk of exposure to breastfeeding infants. The objective of this study is to determine the prevalence of AFM1 in BM and assess factors associated with BM AFM1 levels in mothers. Data, collected between July 2015 and July 2017, were derived from the Aflacohort study (n = 1675) in Banke district, of Province 5 in the south-west region of Nepal. AFM1 was analyzed using ultra-high-performance liquid chromatography with a lower limit of detection of 0.04 ng/L (ng/L). Multivariate linear and quantile regression models were used to examine the relationship of factors with AFM1, including mother's age, food consumption and body mass index, as well as, seasonality and wealth quintiles. Approximately 94% of BM samples had detectable levels of AFM1 (geometric mean 0.78 ng/L and range 0.04 ng/L to 315.99 ng/L). The consumption of particular foods such as yogurt, milk, hydrogenated oil and ripe pumpkin was positively associated with BM AFM1 levels (p-value <0.05), while consumption of legumes was associated with lower BM AFM1 levels (p-value <0.05). Seasonal influences were significant, with BM collected in the pre-winter and winter seasons exhibiting significantly higher AFM1 levels compared to the spring (p-value <0.05). These results suggest near-ubiquitous presence of aflatoxin in the food supply of this part of Nepal, and possible exposure of AFM1 to infants through BM of mothers. The findings justify integrated strategies across the value chain and at household level to identify dietary sources of aflatoxin exposure, proper post-harvest management and monitoring for aflatoxin control and mitigation.
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This research investigated the occurrence of aflatoxin M1 (AFM1), ochratoxin A (OTA), and zearalenone (ZEN) in human milk samples in the Hamadan city, Iran. The study was carried out using the milk of nursing mothers from ten governmental health care centers. Mycotoxin content of ninety milk samples measured using enzyme-linked immunosorbent assay (ELISA). All samples that tested positive for AFM1 with the ELISA test were subsequently analyzed by high-performance liquid chromatography (HPLC). The mean ± SD concentrations of AFM1, determined by ELISA and HPLC were 5.98 ± 1.47 and 4.36 ± 1.23 ng/L, respectively. OTA and ZEN levels were below the detection limit (<5 ng/L) in all samples. None of the contaminated samples exceeded the regulation limit set by the European Commission (25 ng/L) for AFM1 in infant formula. We found a significant correlation between the AFM1 concentration in breast milk and infant age and milk consumption by the nursing mother (p < 0.05). These findings revealed that infants are susceptible to AFM1 exposure from their mother's milk. The authors recommend that additional research be conducted on the analysis of foodstuff and biological fluids for various mycotoxins.
Aflatoxin M1 prevalence in breast milk in Morocco: Associated factors and health risk assessment of newborns “CONTAMILK study”
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The kit was used according to the manufacturer's instructions. AFM1 standard solutions were provided by the AFM1 test kit manufacturer in 0, 5, 10, 20, 40, 80 ng/L. Indeed, the RIDASCREEN AFM1 test kit was used in many previous studies to assess the level of AFM1 in BM (Al Tras et al., 2011; Atasever et al., 2014; Cantú-Cornelio et al., 2016; Elaridi et al., 2017; Ghiasian and Maghsood, 2012; Jafarian-Dehkordi and Pourradi, 2013; Kunter et al., 2017; Mahdavi et al., 2010). Milk samples were thawed gradually to room temperature, and then 10 mL of sample was centrifuged for 10 min at 3500 rpm at 10 °C.
The aim of this study was to assess the contamination of breast milk by aflatoxin M1 among nursing mothers from Rabat, Morocco, and to explore its association with several maternal parameters and dietary habits. In addition, the health risk assessment of the newborns by the estimation of the daily intake.
A competitive Enzyme Linked Immunosorbent Assay method was used for the analysis of aflatoxin M1 in breast milk samples. Analytical results indicate that out of 82 total samples, 43 samples (52.4%) of milk were positive. Aflatoxin M1 levels ranged from undetectable to 13.33 ng/L, while the mean level was 5.75 ± 3.44 ng/L. Besides, several factors and foodstuffs seem to increase the level of AFM1 in breast milk. As regards the estimated daily intake of aflatoxin M1, it varies between immeasurable and a maximum of 1.16 ng/kg.bw.
The degree of exposure to AFB1 and the levels of its metabolite AFM1 in breast milk were low, compared to some studies from other countries. Further investigations and periodic monitoring programs are recommended in large samples and in many cities of morocco to assess the level of exposure of the Moroccan population.
Levels of Aflatoxin M<inf>1</inf> and selected heavy metals (Pb, Cd, Cr, Cu, Zn, Fe, As, and Hg) in the breast milk of lactating mothers in South Eastern, Nigeria
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However, the prevalence in Nigeria was lower than those reported in Brazil (5.35% by Ishikawa et al., 2016) and Portugal (32.8% by Bogalho et al., 2018). The concentration range of Aflatoxin M1 in breast milk in our study was 2.33–7.08 ng/L, which is lower than that reported for Turkey (9.5–8.0 ng/L by (Kiliç et al., 2016)(Bogalho et al., 2018) Portugal (5.1–10.6 by Bogalho et al., 2018), Jordan (9.71–137.18 ng/L by Omar, 2012), Iran (11.1–39.3 ng/L by Jafari, Fallah, Kheiri, Fadei, & Amini, 2017), Egypt (7.3–328.5 ng/L by El-trans et al., 2011), Cyprus (5.36–28.44 ng/L by Kunter et al., 2017), Brazil (13–25 ng/L by Ishikawa et al., 2016) but lower than that reported for Turkey (1.3–6.0 ng/L by Atasever, Yildirim, Atasever, & Tastekin, 2014). The mean concentration of Aflatoxin M1 in our study was 4.02 ± 1.12 ng/L which was lower than the recent reports from other countries (Altun et al., 2016; Bogalho et al., 2018; Diaz & Sanchez, 2015; El-Tras, El-Kady, & Tayel, 2011; Elaridi, Bassil, Abi Kharma, Daou, & Hassan, 2017; Ghiasain & Maghsood, 2012; Ishikawa et al., 2016; Jafari et al., 2017; Kiliç; Kunter et al., 2017; Maleki et al., 2015; Omar, 2012) except for the report from turkey in 2014 (3.01 ± 1.42 ng/L) by Atasever et al. (2014).
In this study, the level and frequency of breast milk AfM₁ and selected heavy metals as biomarkers of maternal exposure was assessed. Selected heavy metals (Pb, Cd, Cr, Cu, Zn, Fe, As, and Hg) were analyzed using Atomic Absorption Spectrophotometry while AfM₁ levels were assessed by HPLC with fluorescence detection after aflatoxin extraction. The mean (±standard deviation) concentration of AfM₁ in the breast milk samples was 4.02 ± 1.12 ng/L and 100% of all the samples contained AfM₁ at 2.33–7.08 ng/L. AfM₁ concentration was positively and significantly (p < 0.01) associated with the daily consumption of cassava-based foods, groundnut oil, maize, tomatoes and dry fruit (p < 0.05). The mean (±standard deviation) values of these heavy metals were Cd: 0.029 ± 0.013 mg/L, Cr: 0.019 ± 0.011 mg/L, Cu: 0.035 ± 0.013 mg/L, Fe: 0.049 ± 0.039 mg/L, Pb: 0.038 ± 0.013 mg/L and Zn: 0.009 ± 0.008 mg/L. The result of the estimated daily intake of breast milk by the breastfed infant show that heavy metals such as Pb, Fe, and Cd are ingested more daily than other metals analyzed. There was a weak positive but non-significant correlation between heavy metal content and daily intake of maternal diet except for beans where a significant correlation (p < 0.01) was found with Cr, Cu, and Zn exposure. A weak positive but non-significant correlation was also observed between exposure to heavy metals such as Cu, Fe and Pb and maternal diets. None of the samples exceeded the national and international legal regulatory limits for AfM₁ and the selected heavy metals in breast milk except chromium. Nevertheless, the presence of these contaminants still presents a health risk.
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Breast milk is considered an essential food segment for children up to 6 months; however, it can be contaminated with some mycotoxins, such as aflatoxin M₁ (AFM₁) and ochratoxin A (OTA) as a consequence of ingestion of dietary mycotoxins by lactating mothers. Moreover, the health of infants can be threatened due to simultaneous exposure to a mixture of mycotoxins mainly due to their potential synergistic effects.
An overview of the prevalence of mycotoxins in breast milk and infant formula, fruit- and cereal-based products as routine diets of infants during the last 10 years, besides the associated health risks, were presented. In this regard, the relevant citations published in international databases such as PubMed, Science direct from 2008 to 2019 were screened by the aid of a systematic review approach.
The high prevalence of AFM₁ and OTA in breast milk reported in several countries highlighted the extent of mycotoxin occurrence in the diet of lactating mothers. Furthermore, the exposure rates of infants to mycotoxins in breast milk and infant formula while generated a margin of exposure values lower than 10,000, indicating a huge public health concern. Thus, reducing the dietary exposure of mycotoxins for lactating mothers and approaching the required controlling steps during the processing and distribution of infant formulas are crucial. Further studies are recommended to evaluate the health risks to infants due to dietary exposure to multiple mycotoxins in infant foods.
Aflatoxin, fumonisin, ochratoxin, zearalenone and deoxynivalenol biomarkers in human biological fluids: A systematic literature review, 2001–2018
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Similarly, AFM1 was present in 5% of maternal breast milk samples of Italian residents (Galvano et al., 2008). Controversial findings were reported for the nursing mothers in Turkey, where one study reported the presence of AFB1 and AFM1 in all breast milk samples (Gurbay et al., 2010) while a more recent one identified AFM1 in 25% breast milk samples (Atasever et al., 2014). This discrepancy could be most likely attributed to the different mycotoxin detection method used, i.e. the first study used HPLC with fluorescence detection and the later one used ELISA assay.
Human exposure to mycotoxins occurs mostly through dietary intake, although exposure through dermal and inhalation routes has also been shown. Depending on the type of mycotoxins, the applied dose and duration of exposure, a particular toxin can cause either chronic or acute illnesses such as kidney failure and cancer. Thus, understanding the biotransformation of mycotoxins and identification of reliable biomarkers in the human body is important for accurate risk assessment of mycotoxin exposure. This review provides a comprehensive overview of worldwide aflatoxins, fumonisins, ochratoxin, zearalenone and deoxynivalenol mycotoxin biomonitoring studies reported in the last 18 years. The studies performed in Africa, Europe, Asia and America are based on the measurement of a limited number of mycotoxin biomarkers and do not provide a comprehensive risk assessment of the mycotoxin exposure. Although the findings represent a small segment of a much larger health risk of mycotoxins exposure, it is acknowledged that a multianalyte approach covering bioconjugated and other metabolites of most often occurring mycotoxins would better reflect the extent of the global exposure problems with these highly toxic compounds.

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Assessment of aflatoxin M1 in maternal breast milk in Eastern Turkey

Highlights

Abstract

Introduction

Section snippets

Sample preparation

Results

Discussion

Conclusion

Conflict of Interest

Transparency Document

Food Chem. Toxicol.

Food Control

Int. J. Food Microbiol.

Toxicol. Lett.

Food Chem. Toxicol.

Food Control

Food Chem.

Food Chem. Toxicol.

J. Food Protect.

Food Chem. Toxicol.

Food Control