78 ISSN 1120-1770 online, DOI 10.15586/ijfs.v33iSP2.2053 P U B L I C A T I O N S CODON Italian Journal of Food Science, 2021; 33 (SP2): 78–91 P U B L I C A T I O N S CODON Biodecontamination of milk and dairy products by probiotics: Boon for bane Razieh Sadat Mirmahdi1, Alaleh Zoghi2, Fatemeh Mohammadi1, Kianoush Khosravi-Darani2*, Shima Jazaiery3, Reza Mohammadi4, Yasir Rehman5 1Student Research Committee, Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Science and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, Iran; 2Department of Food Science and Technology, National Nutrition and Food Technology; 3Department of Nutrition, School of Public Health, Iran University of Medical Sciences, Tehran, Iran; 4Department of Food Science and Technology, School of Nutrition Sciences and Food Technology, Research Center for Environmental Determinants of Health (RCEDH), Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran; 5Department of Life Sciences, School of Science, University of Management and Technology, Lahore, Pakistan *Corresponding Author: Kianoush Khosravi-Darani, Prof. Food Biotechnology. Shahrake gharb, Farahzadi Blv., Hafesi St. No7, Tehran Iran, P. O. Box: 19395-4741, Tehran, Iran. Email: k.khosravi@sbmu.ac.ir and kiankh@yahoo.com Received: 17 April 2021; Accepted: 31 May 2021; Published: 1 July 2021 © 2021 Codon Publications OPEN ACCESS REVIEW ARTICLE Abstract In recent decades, “contamination of the environment, food, and feed by different contaminants such as heavy metals and toxins is increasing due to industrial life.” Commercial milk and milk products can be contaminated with heavy metals and mycotoxins. Biosorption is a low-cost method and has good potential for decontamination. In dairy products, “various starters, especially probiotics, can be used as biosorbants, while microorganisms are able to bind to heavy metals and toxins and decrease their bioavailability and hazards in the human body.” In this article, the key role of dairy starters and probiotics in the decontamination of toxins and heavy metals, and the best probiotics for decontamination of aflatoxins and heavy metals has been reviewed. After a quick glance at introducing dairy products and the main risks in association with the intake of some hazardous materials from dairy products, the application of biological systems is mentioned. Then, the article is focused on the role of ben- eficial microorganisms as the last chance to decrease the risk of exposure to toxins and heavy metals in dairy products. This review can be helpful for biotechnologists and scientists who have challenges about the existence of heavy metals and toxins in milk and dairy products, and help them to find the best method to decrease the con- tent of the usual contaminants. Keywords: aflatoxins; biosorption; decontamination; heavy metals; dairy products Introduction The World Health Organization (WHO) defines food safety as, “Approaches and methods for certifying the manufac- ture, maintenance, distribution and utilization of food hap- pen in an assured system.” However, some people defined safe food as food without any contamination (El Sheikha, 2015). Heavy metals naturally exist in the environment. Industrial activities can increase their content in air and soil, leading to phytotoxicity of plants (Asati et al., 2016; Yang et al., 2018). Milk and dairy products have an important role in the human food chain, especially chil- dren’s food; so, contamination of dairy products by toxins and heavy metals is one of the most important issues that can negatively impact consumers’ health. Milk and dairy mailto:k.khosravi@sbmu.ac.ir mailto:kiankh@yahoo.com Italian Journal of Food Science, 2021; 33 (SP2) 79 Biodecontamination of milk and dairy products dairy products is aflatoxin M1 (AFM1). AFM1 is a metab- olite of aflatoxin B1 (AFB1) after ingestion of contami- nated feed (AFB1) by livestock. About 0.3 to 6.2% of AFB1 (Abdelmotilib et al., 2018) can be bio-transformed into AFM1 (4-hydroxy- AFB1) and can excrete into milk and urine (Iha et al., 2013; Karazhiyan et al., 2016). AFM1 is carcinogenic and toxicogenic, and can resist pasteur- ization and sterilization processes (Gonçalves et al., 2020). AFM1 compared with AFB1 is approximately 10 times less mutagenic, genotoxic, and toxigenic. Its car- cinogenic effects are displayed in different kinds of spe- cies (Elsanhoty et al., 2014). AFM1 can also cause gene mutation, DNA damage, cell transformation in mamma- lian cells, and chromosomal anomalies. Food and Drug Administration (FDA) and the European Commission recommended that the maximum permissible limits of AFM1 in milk are 0.5 μg/kg and 0.05 μg/kg, respectively (Commission, 2006; FDA, 2019) It is reported that mycotoxins in milk and dairy products, which can be produced by different kinds of fungi are: Aflatoxins (by Aspergillus), Compactin (by Penicillium), Cyclopaldic acid (by Penicillium), and Patulin (by Penicillium) (El Sheikha, 2019). Many reports have investigated regarding contamination of milk by heavy metals and toxins all over the world. According to Tables 1 and 2, which present some of the above reports, the amount of lead in Iraq, Brazil, China, Spain, and Italy was more than the maximum permissible products can be contaminated with heavy metals under certain conditions through contamination of water and animal feed with environmental contaminants such as metal and cement smelters, sewage effluents, and indus- trial waste. Heavy metals’ accumulation in milk can easily enter the human body and be dangerous for consumer’s health (Abedi et al., 2020). Dairy product contamination (heavy metal and aflatoxin) is very common all over the world (Ziarati et al., 2018). Heavy metals’ toxicity occurs in levels of about 1.0–10 mg/L; however, lead and cadmium could have a toxic effect in 1–100 μg/L (Alkorta et al., 2004). For example, different levels of exposure to cadmium could cause renal dysfunction, hepatic injury, and lung damage (Miura et  al., 2017; Naidoo et al., 2019; Zhang et al., 2014). Arsenic poisoning can cause death through disorder in essential metabolic enzymes (Khairul et al., 2017). Maximum permissible limits of heavy metal contents in milk (considered by International Dairy Federation) are 2.6 µg/kg for cadmium, 10 µg/kg for Copper, 20 µg/kg for lead, and 328 µg/kg for zinc (Malhat et al., 2012). Aflatoxins directly (through eating contaminated food) and indirectly (primary contaminated products such as milk of contaminated livestock) can enter into the human body by the use of contaminated dairy products. Aflatoxins can cause negative effects on human health, such as liver or kidney cancer and chronic intoxications (Karazhiyan et al., 2016). The most common aflatoxin in Table 1. Some important data about milk contamination to heavy metals (from 2014 to 2021). Country Contamination Concentration Reference Egypt Pb Cd 0.044–0.751 mg/L 0.008–0.179 mg/L Meshref et al., 2014 Serbia Pb Cd 54.3–95.2 lg/kg 2.13–4.82 lg/kg Suturović et al., 2014 Iraq Pb 32 µg/L Alani and Al-Azzawi, 2015 Pakistan Pb Cd 0.014 mg/Kg 0.001 mg/Kg Ismail et al., 2015 Bangladesh Pb Cd 0.2 mg/L 0.073 mg/L Muhib et al., 2016 Iran Pb Cd 14.0 µg/kg 1.11 µg/kg Shahbazi et al., 2016 Brazil Pb 2.12–37.36μg/L de Oliveira et al., 2017 Mexico Pb As 0.03 mg/Kg 0.12 mg/Kg Castro-González et al., 2018 Poland Pb Cd 5.24 μg/L 0.15 μg/L Halagarda et al., 2018 Turkey Pb Cd As 0.0055 mg/L 0.088 mg/L 0.002 mg/L Seğmenoğlu and Baydan, 2021 As: Arsenic, Cd: Cadmium, Pb: Lead 80 Italian Journal of Food Science, 2021; 33 (SP2) Mirmahdi RS et al. Table 2. Some important data about milk contamination to mycotoxins in world from 2014 to 2021. Country Contamination Concentration Reference Croatia AFM 1 0.003–1.135 μg/L Bilandžić et al., 2014 China AFM 1 OA ZEA α-ZEA 80.4 ng/kg 56.7 ng/kg 14.9 ng/kg 24.3 ng/kg Huang et al., 2014 Serbia AFM 1 0.01–1.2 μg/kg Kos et al., 2014 Iran AFM 1 > 0.05 μg/L Fallah et al., 2015 Macedonia AFM 1 408.1 ng/L Dimitrieska-Stojković et al., 2016 Pakistan AFM 1 >2610 ng/L Aslam et al., 2016 Argentina AFM 1 293 ng/L Michlig et al., 2016 Bosnia and Herzegovina AFM 1 60 ng/L Bilandžić et al., 2016 Italy AFM 1 52 ng/L De Roma et al., 2017 Tanzania AFM 1 0.627 ng/mL Karczmarczyk et al., 2017 Malaysia AFM 1 144 ng/L Shuib et al., 2017 Kosovo AFM 1 83 ng/L Camaj et al., 2018 El Salvador AFM 1 Approximately 100 ng/L Peña-Rodas et al., 2018 Turkey AFM 1 78.69 ng/L Eker et al., 2019 Ethiopia AFM 1 207 ng/L Zakaria et al., 2019 Kenya AFM 1 4563 ng/L Kuboka et al., 2019 Brazil AFM 1 45.18 ng/L Venâncio et al., 2019 Ecuador AFM 1 0.0774 μg/kg Puga-Torres et al., 2020 Spain AFM 1 0.009–1.36 μg/kg Rodríguez-Blanco et al., 2020 India AFM 1 1116 ng/L Sharma et al., 2020 Morocco AFM 1 4.46 ± 14.09 ng/L Mannani et al., 2021 Malawi AFM 1 0.551 μg/L Njombwa et al., 2021 Spain AFM 1 AFB 1 12.6 ng/kg 0.61 μg/kg Bervis et al., 2021 AFM 1 : Aflatoxin M 1, AFB 1 : Aflatoxin B 1, OA: Ochratoxin A, ZEA: Zearalenone, α-ZEA: α-zearalenone. limits. Also, AFM1 in China and India, and cadmium in Poland and Spain, were higher than permissible limits. This information confirms the importance of decontami- nation in milk and dairy products. There are different methods for the decontamination of dairy products, such as physical, chemical (reverse osmo- sis, ion exchange, freeze concentration, and evaporation) (Patterson and Minear, 2013), and biological methods (using different biomaterials such as bacteria and yeasts biomass, plants, and seaweeds) (Abdelmotilib et al., 2018; Hashim and Chu, 2004; Hayat et al., 2017; Satyapal et al., 2016; Sulaymon et al., 2013; Vishnoi et al., 2014). Adsorption is one of the most important decontami- nation strategies in dairy products (Giovati et al., 2015; Massoud et al., 2019; Milanowski et al., 2017; Porova et  al., 2014). There are different biosorbents, such as “algae, plants, yeasts, fungi, and bacteria,” for the biore- moval of toxins and metals in fermented dairy products (e.g., kefir, kumis, yogurt, and doogh). Probiotic bacte- ria can also be used for this purpose. Fermented dairy products are very popular, and they have a perfect taste (El Sheikha et al., 2018; Yerlikaya, 2014). Probiotics can reduce contamination (heavy metals and aflatoxins) in fermented dairy products (Zoghi et al., 2014). They are widely used for bioremoval of toxins (Massoud et al., 2018; Zoghi et al., 2017, 2019) as well as heavy metals (arsenic, mercury, lead, and cadmium) (Hadiani et al., 2018, 2019; Khosravi-Darani et al., 2019), heterocyclic aromatic amines (Khosravi-Darani et al., 2019; Sarlak, 2020), and even pesticides (Wochner et al., 2018). In this article, reports about the influence of adding start- ers and probiotics into the formulation of dairy products on the bioremoval of contaminations such as toxins and heavy metals are reviewed. Starters and Probiotics in Dairy Products Food fermentation by microorganisms is one of the most economic and widely practiced methods for improving Italian Journal of Food Science, 2021; 33 (SP2) 81 Biodecontamination of milk and dairy products via the manufacture of lactic acid and/or the sprinkling of secondary metabolites in the product matrix (Ryan et  al., 2015). Different starters have been used for pro- ducing various dairy products all around the world. Some of these products and their starters are mentioned in Table 3. texture, flavor, and functionality, and also for enhancing the shelf life of food products (Ray et al., 2014; Salque et  al., 2013). The fermentation process can be carried out with starter cultures to certify consistency in com- mercial products by using familiar microorganisms with favorable traits, such as a high amount of acidification Table 3. Some fermented dairy products and related starters. Fermented dairy products Country/Region of origin Starters Reference Acidophilus milk — Lactobacillus acidophilus, Lactobacillus casei, Bifidobacterium bifidum, Lactobacillus bulgaricus, Streptococcus thermophilus Raftaniamiri et al., 2010 Buttermilk Egypt and Ethiopia (cultured buttermilk) Lactic acid bacteria (e.g., Lactococcus, Lactobacillus, Streptococcus, and Leuconostocs) El Sheikha and Montet, 2014; Kumar et al., 2015 Cheese — (cheddar cheese) Lactic acid bacteria starter culture (Lactococcus lactis ssp. lactis, Lactococcus lactis ssp. cremoris, and Streptococcus salivarius spp. thermophilus) Ferreira and Viljoen, 2003 Matzoon Armenia Lactic acid bacteria Macori and Cotter, 2018 Leben Arab World (Leben from camel milk) Lactococcus lactis, Lactobacillus pentosus, Lactobacillus plantarum, Lactobacillus brevis, and Pediococcus pentosaceus Fguiri et al., 2013 Kishk Arab World Freeze-dried yogurt starter culture Tamime et al., 2000 Kumis Central Asia Turkic countries Central Asia Lactococcus lactis subsp. lactis, Streptococcus thermophilus, Lactobacillus delbrueckii subsp. bulgaricus, Lactobacillus helveticus, Lactobacillus casei subsp. Pseudoplantarum, and Lactobacillus brevis Kluyveromyces marxianus var. lactis, Saccharomyces cerevisiae, Candida inconspicua, and Candida maris Simova et al., 2002 Ymer Denmark Streptococcus lactis, Streptococcus diacetilaclis., Streptococcus cremoris, and Leuconostoc citrovorum Poulsen, 1970 Kefir Estonia, Hungary, Greece, Latvia, Romania, Slovakia, Bosnia and Herzegovina Lactobacilli Lactococcus Acetic acid bacteria and yeast Garrote et al., 2001 Dahi India Lactobacillus case or Lactobacillus acidophilus Yadav et al., 2005 Mishti doi India Streptococcus salivarius ssp. Thermophiles, Lactobacillus acidophilus, Lactobacillus delbrueckii ssp. bulgaricus, Lactobacillus acidophilus, Lactococcus lactis ssp. lactis, Saccharomyces cerevisiae Gupta et al., 2000 Matsoni Georgia Lactobacillus Streptococcus, Kluyveromyces marxianus, Candida famata, Saccharomyces cerevisiae, Lodderomyces elongisporus, Kluyveromyces lactis Bokulich et al., 2015 Wara Africa Lactobacillus sp., Leuconostoc sp., Pediococuus sp., Lactococcus sp., yeasts El Sheikha and Montet, 2014 Biruni Sudan Lactic acid bacteria El Sheikha and Montet, 2014 Mish Sudan and Egypt Lactic acid bacteria El Sheikha and Montet, 2014 Rob Sudan Lactic acid bacteria El Sheikha and Montet, 2014 Doogh Iran Lactobacillus acidophilus, Lactobacillus rhamnosus, Lactobacillus casei, Bifidobacterium lactis Sarlak et al., 2017 Yogurt Serbia Streptococcus thermophilus and Lactobacillus bulgaricus Elsanhoty et al., 2014 Clabber United States Starters like Kefir Dyomina et al., 2017 82 Italian Journal of Food Science, 2021; 33 (SP2) Mirmahdi RS et al. FAO (2001) defined probiotics as, “viable microorgan- isms, that while ingested in sufficient amounts, exert health benefits on the host (FAO/WHO, 2001).” The main beneficial effects of probiotics on human health include mucosal immunity support, decreasing lactose intol- erance, preventing respiratory infections or diarrheas, feasible hypocholesterolemia effects, prevention of intes- tinal pathogens, inhibition of colon cancer or inflamma- tory bowel disease (Sanders et al., 2014; Yu et al., 2015). The application of microorganisms, especially probiotics, recently has been investigated for their potential to heavy metals and aflatoxins reduction (Zoghi et al., 2014). Most species known as probiotic bacteria are Bifidobacterium (B.), Lactobacillus (L.), Bacillus, and yeast Saccharomyces (S.) cerevisiae, and some strains of Escherichia (E.) coli. A practical taxonomy of nonpathogenic, fermentative, and nontoxigenic probiotic bacteria is lactic acid bacteria (LAB), which are used widely in food industries (Zoghi et al., 2017). LAB usually have gram-positive cell walls, and peptidoglycan is their main cell wall structural com- ponent; teichoic acid, lipoteichoic acid, some neutral polysaccharides, and a proteinous S-layer are their minor components (Zoghi et al., 2014). Toxins’ Bioremoval in Milk and Dairy Products In recent decades, several scientific studies have been done regarding decontamination in dairy products, espe- cially the biological decontamination method. Some of these researches are mentioned in Table 4. El Khoury et al. (2011) investigated the application of LAB including L. bulgaricus and Streptococcus ther- mophiles on the reduction of AFM1. They showed that using LAB is a potential method to decrease AFM1 with the higher efficiency of L. bulgaricus compared to Streptococcus thermophiles. They also mentioned that the level of AFM1, which is bound by LAB, enhanced with increasing the time of inoculation (El Khoury et al., 2011). The binding ability of yogurt cultures was differ- ent. It is suggested that the difference in the binding abil- ity of LAB is attributed to the difference in their cell-wall structure (Sarimehmetoğlu and Küplülü, 2004). In addition to LAB, using S. cerevisiae is considered as an effective way for microbial detoxification (Karazhiyan et al., 2016). A systematic review by Campagnollo et al. (2020) focused on parameters influencing the binding process of AFM1 by yeast. The overall binding level of yeast was reported as 52.05%, in which the lowest bind- ing capacity was related to the yeast extract peptone and the highest binding was associated with the ruminal fluid. Also, different factors, including temperature, yeast, pH, and the type of aflatoxin, have been mentioned as the major parameters in the process of decontamination (Campagnollo et al., 2020). Moreover, the effect of differ- ent treated S. cerevisiae, including heat, acid, and ultra- sound treated, on the binding with AFM1 was assessed by Karazhiyan et al. (2016). Among all treated yeasts, acid treatment had the most positive impact on yeast cells for improving their binding ability to aflatoxins which can be attributed to the release of monomers from polysaccha- rides under acidic conditions and their further changes into aldehydes after breaking down of glycosides link- ages. After acid treatment, heat-treated yeasts showed the highest binding ability due to protein denaturation and Maillard reaction product formation, which caused an increase in the permeability of cell walls. Comparison between viable and unviable yeasts (heat, acid, and ultra- sound treated) exhibited higher efficiency of unviable cells, which indicates that such treatments increase the binding capacity of yeasts (Karazhiyan et al., 2016). In a study performed by Taheur et al. (2017), a novel strategy for the reduction of mycotoxins using kefir grains was examined. The results showed that kefir microorgan- ism grains could adsorb 82 to 100% of AFB1, zearalenone, and ochratoxin A after cultivation in milk. The main strains that were able to adsorb mycotoxins were L. kefiri, Kazachstania servazzii, and Acetobacter syzygii. The L. kefiri KFLM3 was found to be the most active strain with an adsorption rate of 80 to 100% of the mycotox- ins, and K. servazzii KFGY7 was found to retain higher mycotoxin than others after the desorption experiments. As a result, kefir consumption can assist in diminishing gastrointestinal absorption of mycotoxins and their toxic effects (Taheur et al., 2017). Heavy Metals’ Bioremoval in Milk and Dairy Products In Table 5, investigations regarding heavy metal biore- moval in milk and dairy products are illustrated. In two different studies by Massoud et al. (2019, 2020a), application of S. cerevisiae to reduce the concentrations of lead and cadmium in milk was examined. The optimi- zation process was also performed considering three fac- tors including contact time, concentrations of biomass, and initial content of heavy metals (Massoud et al., 2019, 2020a). Generally, the rate of removal of heavy metals increased with an increase in the biomass, contact time, and concentration of heavy metals. They concluded that optimized conditions for lead removal were obtained after 4 days (at the end of storage time) with the content of 22×108 CFU/mL of yeast and 70 μg/L of lead in milk (Massoud et al., 2019). Similarly, the optimized process for cadmium bioremoval was achieved after 4 days with 80 μg/L of cadmium and 30×108 CFU/mL of S. cerevisiae Italian Journal of Food Science, 2021; 33 (SP2) 83 Biodecontamination of milk and dairy products Table 4. Aflatoxin decontamination in milk and dairy products. Product Microorganism Removal w/w% Contaminant Conditions Reference Milk Lactobacillus rhamnosus (milk whey medium) 46.0% AFB 1 Optimal condition: 60 min in pH 3.0 Bovo et al., 2014 Milk Kefir starters 1. L. acidophilus, Bifidobacterium, & Streptococcus thermophiles (thermophilic lactic culture) 2. Lactococcus lactis subsp. cremoris, Leuconostoc, Lactococcus lactis subsp. lactis biovar diacetylactis, Lactococcus lactis, subsp. lactis, 3. Debaryomyces hansenii, Kluyveromyces marxianus subsp. marxianus., yeast pool, Lactic acid bacteria pool Full kefir starters 11.67–34.66% Yeast pool 65.33–68.89% LAB pool 65% AFM 1 Toxin Concentration: 150, 200, and 250 ng/L Temperature: 4 °C Time: 7 days Kamyar and Movassaghghazani, 2017 Milk Lactobacillus helveticus 85% AFM 1 Time: 60 min Ismail et al., 2017 Milk Saccharomyces cerevisiae 81.3% AFM 1 Time: 48 h Foroughi et al., 2018 Yogurt A: S. thermophilus & L. bulgaricus B: 50% S. thermophilus & L. bulgaricus 50% L. planetarum C: 50% S. thermophilus and L. bulgaricus, 50% L. acidophilus Treatment B: Highest reduction 31.5–87.8% AFM 1 Temperature: 5°C, Storage time: 1, 3, 5, and 7 days Elsanhoty et al., 2014 Yoghurt Lactobacillus acidophilus 90% AFM 1 108 CFU/ mL, Initial concentration of AFM 1 :0.1, 0.5, 0.75 μg/L Adibpour et al., 2016 Yoghurt Saccharomyces cerevisiae 76.46% AFM 1 Aflatoxin M 1: 100, 500, and 750 g/ M l , in 1, 7, 14, and 21 days, yeast treatments: heat, acid, and ultrasound Karazhiyan et al., 2016 Yoghurt Lactobacillus plantarum, Bifidobacterium animalis, Bifidobacterium bifidum Yogurt starters and B. bifidum, B. animalis (60.8%), Yogurt starters and L. plantarum, B. Bifidum 55.1%) AFM 1 Storage time: 1 or 10 days Sevim et al., 2019 Yogurt L. plantarum, B. animalis, & B. bifidum, L. plantarum 49–60% AFM 1 Contact time: 4 h Temperature: 42°C Sevim et al., 2019 Kefir Lactobacillus casei & kefir starter 88.17% AFM 1 Aflatoxin M 1 500 pg, Kefir starters 2, 4, 6, 8, 10%, L. casei: 0.1, 0.3, 0.5, 0.7, 0.9 % in 48 h Sani et al., 2014 Kefir Kefir-grains 96.8% AFG 1 Toxin concentration 5, 10, 15, 20, 25 ng/g, Kefir grain:5, 10, 20, 10, 25%, in 0, 2, 4, 6, 8 h, at 20, 30, 40, 50, 60°C Ansari et al., 2015 (continues) 84 Italian Journal of Food Science, 2021; 33 (SP2) Mirmahdi RS et al. Table 4. Continued Product Microorganism Removal w/w% Contaminant Conditions Reference Kefir Kefir grains: Lactobacillus kefiri, Kazachstania servazzii, Acetobacter syzygii 82–100% AFB 1, ZEA, OA 1 μg/Ml mycotoxin, Kefir grains 10% w/v in 24 at 25°C Taheur et al., 2017 UHT skim milk Lactic acid bacteria (Lactobacillus rhamnosus, Lactobacillus delbrueckii spp. Bulgaricus, Bifidobacterium lactis), Saccharomyces cerevisiae LAB pool (30 min): 11.5 ±2.3% LAB (60 min): 11.7 ± 4.4%, Saccharomyces: (30 min), 90.3 ± 0.3%, Saccharomyces: 60 min, 92.7 ± 0.7% AFM 1 0.5 ng AFM 1 mL−1, LAB pool: 1010 cells mL−1 Yeast: 109 cells mL−1 Contact time: 30 min or 60 min Corassin et al., 2013 Fermented milk drink Lactobacillus casei Shirota AFB 1 -lys reduction: 82.37% Serum AFB 1 - lysine adduct 4-week intervention phases, (A): probiotic drinks 2 twice a day (B): placebo for 6, 8, or 10 weeks Redzwan et al., 2016 Doogh Lactobacillus acidophilus, Lactobacillus rhamnosus, Lactobacillus casei, , Bifidobacterium lactis Day 28, Lactobacillus acidophilus: 98.8 ± 1.3% AFM 1 0.500 ppb toxin, 1,14, or 28 days at 5 °C, L. acidophilus 9 log cfu/mL Sarlak et al., 2017 Ergo fermented milk L. plantarum Lactobacillus acidophilus, Lactobacillus brevis, Lactobacillus casei subsp. casei, Lactobacillus helveticus, Streptococcus faecalis, Streptococcus thermophiles, Leuconostoc mesenteroides, subsp. cremoris 57.33% 54.04% AFM 1 Time: 1–5 days Temperature: 25°C Shigute and Washe, 2018 AFM 1 : Aflatoxin M 1, AFB 1 : Aflatoxin B 1, OA: Ochratoxin A, ZEA: Zearalenone, AFG 1 : Aflatoxin G 1 . Table 5. Heavy metals decontamination in milk and dairy products. Product Microorganism Contaminant Removal% W/W Conditions Reference Milk Saccharomyces cerevisiae Pb 70% Opt. at 22×108 CFU inoculation of yeast, Lead content 70 μg/l Massoud et al., 2019 Kefir Lactococcus lactis, Kluyveromyces marxianus, co-culture Ni, Cu, Cd, Pb, Fe 81.53%, 73.45%, 79.48%, 68.53%, 58.17% Time: 10 days Cherni et al., 2020 Milk Saccharomyces cerevisiae Cd 70% Cadmium content in milk 80 μg/L, 30×108 CFU Saccharomyces cerevisiae, storage time the 4th day, Masoud et al., 2020 Milk Lactobacillus acidophilus Pb Cd 80% 75% 1 × 1012 CFU of L. acidophilus, in 4 days with the initial pollution of 100 µg/L. Massoud et al., 2020b Milk Saccharomyces cerevisiae Hg 70% Contact time: 30 days, initial concentration of Hg: 80 µg/L and biomass dosage 22 × 108 CFU Massoud et al., 2021 Lead: Pb, Nickel: Ni, Copper: Cu, Cadmium: Cd, Iron: Fe, Mercury: Hg. Italian Journal of Food Science, 2021; 33 (SP2) 85 Biodecontamination of milk and dairy products (Massoud et al., 2020a). Therefore, they have introduced applying S. cerevisiae as a novel and useful technology for the bioremoval of heavy metals from foodstuff (Massoud et al., 2019, 2020a) Different treatments, such as caustic, ethanol, acidic, and heat, can enhance the biosorption of heavy metals by microorganisms. In a study by Yekta Göksungur et al. (2005), “potential of baker’s yeast in bioremoval of cad- mium and lead with 3 pretreatments (caustic, heat and ethanol)” was examined. Ethanol-treated yeast strains could remove the most content of metals and it can be explained by improving the availability of yeast bind- ing sites and maybe enhancing the metals accessibility (Göksungur et al., 2005). Mechanisms of Bioremoval and Stability of Complexes (Probiotics/Starters-heavy Metal/Toxin) AFM1 and other toxins are accumulated in milk and dairy products because they are able to bind to milk protein components such as casein (Dyomina et al., 2017; Granados-Chinchilla, 2016; Sarlak et al., 2017). Therefore, numerous investigations have been focused on the removal of toxins using microorganisms, such as LAB (Dyomina et al., 2017; Sarlak et al., 2017). Although the mechanism of bioremoval of toxins and heavy metals by LAB was not well known until now, it is proposed that toxins are highly linked by cell wall com- ponents of microorganisms and are not metabolically degraded (Zoghi et al., 2014). Yeast and LAB are used widely to reduce toxins and metal ions. As both viable and dead cells are capable of adsorbing toxins, it is sensi- ble to conclude that the removal of toxins is by adhesion to the components of microorganism’s cell wall relative to covalent binding, as reviewed by Shetty et al. (2006) (Shetty and Jespersen, 2006). It is indicated that man- nan components of the S. cerevisiae cell wall play an important role in toxin binding (Devegowda et al., 1996). Generally, the cell wall proteins of S. cerevisiae are bound to β-1,3-glucans by covalent linkage by β-1,6-glucan chains (Shetty and Jespersen, 2006). Apart from this, the major part of the LAB cell is made up of peptidoglycan, which contains teichoic and lipoteichoic acids. Also, a proteinous S-layer and neutral polysaccharides as com- ponents of the LAB cell wall have been recognized and reviewed by Lahtinen et al. (2004). A study by Yiannikouris et al. (2004) indicated the inter- actions between zearalenone and β-D-glucans, in which β-1,3 D-glucan chains constitute a stable helical link with zearalenone and stabilized by β-1,6 D-glucan chains (Yiannikouris et al., 2004). In order to investigate the mechanism of binding of aflatoxins to L. rhamnosus it is indicated that carbohydrates in the cell wall are predom- inantly responsible for binding to aflatoxins. In samples treated by urea, it is shown that hydrophobic interactions play a significant role in binding, and treatment by NaCl and CaCl2 showed that electrostatic interactions played a minor role (Haskard et al., 2000). Also, it is stated that AFM1 is bound to LAB cell wall components by weak noncovalent interactions. The dif- ference in the binding ability among different microor- ganisms is attributed to the cell wall and cell envelope structures (El Khoury et al., 2011). Similarly, Turbic et al. (2002) mentioned that the different binding ability of LAB highly depended on the strain of the microorgan- isms (Turbic et al., 2002). Another study associated with the mechanism of bio- sorption illustrated that nonviable cells, including heat and acid-treated cells, produced complexes with higher stability, which means better access of groups in treated cells rather than viable ones. This phenomenon empha- sizes that the viability of cells is not an important fac- tor for the binding ability of cells (Haskard et al., 2001). Furthermore, it is shown that acids might be capable of breaking amine binding in peptides and proteins, which leads to the production of peptides and even amino acids, and consequently, more accessible aflatoxin binding sites will be available (El-Nezami et al., 2002). Similarly, it is noted that hydrophobic interactions are highly expected in LAB, which is treated by acid because acid treatment leads to denaturation of proteins and enhanced hydro- phobic binding sites (Haskard et al., 2000). Moreover, the mechanisms of bioremoval could be influ- enced by various factors including types of microorgan- isms or even the status of biomass (living or nonliving microorganism), chemical properties of toxic materials, and environmental factors, such as temperature as well as pH (Javanbakht et al., 2014). For more illustration, Javanbakht et al. (2014) investigated the mechanism of removal of heavy metals by microor- ganisms. They suggested that two different types of path- ways are involved in biosorption, which depends on cell metabolism and is divided into metabolism-dependent and metabolism-independent groups. The first pathway only occurs in viable cells through the transformation of metals across the cell wall. The second mechanism is involved in the physicochemical interaction between metals and functional groups of cell surface such as phys- ical adsorption and ion exchange without depending on the cell metabolisms (Javanbakht et al., 2014). To investigate the stability of complexes, Haskard et al. (2001) evaluated the stability of 12 complexes between 86 Italian Journal of Food Science, 2021; 33 (SP2) Mirmahdi RS et al. in  vivo and in vitro conditions. Also, more experiments should be done for finding optimum conditions for special starters in special dairy products for better decontamination. Declarations Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for- profit sectors. Conflicts of interest/Competing interests The authors declare that they have no conflicts of interest. Availability of data and material Not applicable. Code availability Not applicable. Authors’ Contributions RM was involved in writing and original draft prepara- tion; AZ was responsible for writing, review, and editing; KKD was concerned with conceptualization and supervi- sion; FM was involved in writing and editing; and SJ, RM, and YR were responsible for review and editing. References Abdelmotilib, N.M., Hamad, G.M., Elderea, H.B., Salem, E.G. and El Sohaimy, S.A., 2018. Aflatoxin M1 reduction in milk by a novel combination of probiotic bacterial and yeast strains. European Journal of Nutrition & Food Safety 8(2):83–99. https://doi. org/10.9734/EJNFS/2018/39486 Abedi, A.-S., Nasseri, E., Esfarjani, F., Mohammadi-Nasrabadi,  F., Moosavi, M.H. and Hoseini, H., 2020. A systematic review and meta-analysis of lead and cadmium concentrations in cow milk in Iran and human health risk assessment. Environmental Science and Pollution Research 27: 10147–10159. https://doi. org/10.1007/s11356-020-07989-w Adibpour, N., Soleimanian-Zad, S., Sarabi-Jamab, M. and Tajalli, F., 2016. Effect of storage time and concentration of aflatoxin m1 on toxin binding capacity of L. acidophilus in fermented milk product. Journal of Agricultural Science and Technology 18: 1209–1220. Available from: http://jast.modares.ac.ir/article-23-4462-en.html LAB and AFB1 considering both viable and nonviable cells and concluded that 71% of AFB1 remained bound, indicating the high stability of the complexes. Also, they showed that nonviable cells retained a higher amount of AFB1, as mentioned above (Haskard et al., 2001). Based on their results, the stability of complexes depends upon three factors including strain, treatment type, and envi- ronmental conditions. Fazeli et al. (2009) conducted a study to investigate the effect of strains, including L.  casei, L. plantarum, and L. fermentum, on the reduc- tion of AFB1 and concluded that all the strains were able to remove AFB1, although L. casei was found to be a stronger binder of AFB1 rather than other bacteria (Fazeli et al., 2009). A Study by Zoghi et al. (2020) showed that adsorption of patulin by LAB can be reversible in simulated gastroin- testinal conditions. The reversibility of binding between LAB and patulin can be explained by the sense of non- covalent electrostatic bonds (Van der Waals and hydro- gen bonds) (Zoghi et al., 2020). Similarly, in another study, the adsorption of AFB1, zearalenone, and ochra- toxin A by kefir grains in simulated gastrointestinal pH was reversible. In pH 3, further amounts of toxins were released (Taheur et al., 2017). Moreover, reduction of AFB1 from a gastrointestinal model by several cells, including L. rhamnosus, L. plantarum, and L. acidophi- lus, were examined by Motameny et al. (2012), and they concluded that L. plantarum was the most active cell (Motameny et al., 2012). Conclusions Aflatoxins and heavy metals frequently contaminate milk and dairy products at different levels. In the food indus- try, controlling aflatoxin and heavy metal levels in dairy products is a challenge for researchers. According to the recent studies summarized in this review, it is revealed that using different microorganisms (such as probiotics) in different dairy products could result in the removal of toxins and heavy metals by creating bonds between con- taminants and these microorganisms. Using the starters in fermented dairy products can be helpful in the decon- tamination of toxins and heavy metals. 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