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  • Research
  • Open Access

Functional role of selenium-fortified yogurt against aflatoxin-contaminated nuts in rats

Agriculture & Food Security20187:21

https://doi.org/10.1186/s40066-018-0171-7

  • Received: 5 January 2018
  • Accepted: 15 February 2018
  • Published:

Abstract

Background

Aflaxions are a group of chemically toxic fungal metabolites produced by species of the genus Aspergillus. Nuts can be contaminated by fungi, resulting in the production of mycotoxins. The present study was performed to investigate the ability of selenium-fortified yogurt to counteract the adverse effects of consuming 3% experimental nuts (pistachios, cashews, walnuts, almonds and hazelnuts) contaminated with aflatoxins in experimental rats. First, the total aflatoxins concentrations were estimated in fresh nuts, and in nuts after 6 months of storage, and selenium-fortified yogurt was prepared. Rats were classified into a negative control group (fed a standard diet with a 3% mixture of fresh safe nuts), a positive control group (fed a standard diet with a 3% mixture of nuts contaminated with aflatoxins after storage at 25 °C for 6 months) and treated groups that fed on pistachios with selenium-fortified yogurt, cashews with selenium-fortified yogurt, walnuts with yogurt fortified with selenium, almonds with selenium-fortified yogurt and hazelnuts with selenium-fortified yogurt (fed a standard diet with 3% individual nuts contaminated with aflatoxins and 160 ml/kg body weight of selenium-fortified yogurt daily through a stomach tube).

Results

The negative effects of aflatoxins on weight gain and food intake were reversed by selenium-fortified yogurt. This yogurt also led to a significant decrease in serum cholesterol, TG, LDLc, VLDLc, total lipids, phospholipids, glucose and atherogenic indexes (CHO/HDLc and LDLc/HDLc) and an increase in serum HDLc, haemoglobin, PCV, liver TG and glycogen at p < 0.05. In addition, the study showed a significant decrease in liver cholesterol and total lipids compared to the positive control rat group, which consumed 3% mixed nuts contaminated with aflatoxins and simultaneously restored these parameters to be close to those in the control group. The results were corroborated by histopathological examination of the liver and kidneys.

Conclusions

The most prominent conclusion is that selenium-fortified yogurt reduces side effects from consumption of nuts contaminated with aflatoxins. It is recommended to consume functional selenium-fortified yoghurt for its nutritional values and for alleviating the harmful effect of aflatoxins in nuts.

Keywords

  • Nuts
  • Aflatoxins
  • Lipids pattern
  • Selenium
  • Yogurt
  • Liver
  • Kidney
  • Rats

Background

Aflatoxins (AF) are mycotoxins produced by Aspergillus flavus and Aspergillus parasiticus that affect livestock and humans and occur as natural contaminants in foods containing peanuts and corn meal [1]. Aflatoxin-contaminated foods (i.e., grains and nuts) are more commonly observed in tropical regions, including sub-Saharan Africa and Southeast Asia [2]. There are four major types of aflatoxins (B1, B2, G1 and G2), all of which are carcinogenic, teratogenic, hepatotoxic, immunosuppressive and capable of inhibiting several metabolic systems, causing liver, kidney and heart damage [3]. Aflatoxin B1 (AFB1) is the most frequently occurring and most toxic. Its toxic effects may be due to the generation of free radicals resulting in lipid peroxidation, which is a damaging process for all biological systems since cell membranes contain fatty acids that serve as substrates for free radical oxidation [4, 5]. Although the liver is the principal target organ for AF, the kidney and testis can also be affected following dietary and inhalational exposure. The majority of the toxin is metabolized in the liver, where AFB1 is converted by hepatic cytochrome P450 enzymes into the reactive and electrophilic exo-AFB1-8,9-epoxide. This highly unstable intermediate quickly reacts with DNA, RNA and proteins, which leads to cell death [6, 7]. Chronic AFB1 exposure, especially in combination with hepatitis B infection, severely increases the risk of hepatocellular carcinoma in humans [8].

Yogurt contains many probiotic bacteria, including Lactobacillus bulgaricus and Streptococcus thermophilus, which provide benefit through existing as microflora in the intestines and by acting directly on bodily functions such as digestion and immunity [9, 10]. Fermented dairy products contain live lactic acid bacteria, and these bacteria and their metabolites have been shown to modulate the immune response in animals, suppress carcinogenesis in rodents, inhibit the activity of enzymes related to carcinogenesis and bind mutagenic and carcinogenic heterocyclic amines. The fermentation process leads to a reduction in the lactose content of the milk and an increase in lactic acid [11, 12]. Yogurt has been documented as therapeutic for a variety of disorders including lactose intolerance, which is ameliorated due to a reduced cholesterol level, alimentary tract diseases, constipation, diarrhoea, gastroenteritis, indigestion, intoxication, hypercholesteremia, kidney and liver disorders and cancer [1315].

Selenium is essential for the immune system in both animals and humans and has emerged as an important element for dietary protection from various toxic agents [16, 17]. Moreover, selenium has been reported to be protective against the toxic effects of aflatoxins. Early studies revealed that selenium can modify the disease process and counteract AFB1-induced adverse effects, such as impaired development and histopathological lesions in immune organs [18]. Selenium might enhance the conjugation of aflatoxins by increasing excretion of the aflatoxins and by preventing the formation of AFB1-DNA adducts. The protective effect of selenium is mediated through a cellular mechanism related to glutathione detoxification pathways [1921].

The present study uses a rat model to investigate whether selenium-fortified yogurt can counteract the adverse effects resulting from consuming nuts contaminated with aflatoxins.

Methods

Nuts

Five kilograms of most edible nuts and more susceptible to mould growth (pistachios, cashews, walnuts, almonds and hazelnuts) was obtained from a local market in Riyadh, Saudi Arabia.

Chemicals

All materials used in this experiment were of analytical grade. BioMerieux kits were purchased from Alkan Co. for Chemicals and Biodiagnostics. Selenium was obtained from Sigma Chemical Company (St. Louis, MO, USA).

Probiotic bacteria

Cow milk was purchased from a local market in Riyadh, Saudi Arabia. Lactobacillus delbrueckii bulgaricus CH-2 and Streptococcus thermophilus ST-36 were obtained from Chr. Hansen’s Laboratory in Rich, Denmark.

Experimental animals

Seventy adult male white Sprague-Dawley strain albino rats, 130 ± 10 g, were purchased from the experimental animals centre in the Research Centre in Prince Sultan Military Medical City, Riyadh. Rats were housed in groups in wire cages under the normal laboratory conditions and fed a standard diet for a week as an adaption period. Food and water were provided ad libitum. Ethical guidelines were maintained in animal handling during the study, and permission was obtained from the relevant department.

Standard diet

The standard experimental diet was composed of corn starch (598 g/kg), casein (200 g/kg), soybean oil (100 g/kg), vitamins mixture (10 g/kg), salts mixture (40 g/kg), cellulose (50 g/kg) and choline chloride (2 g/kg) according to the Second Report of the American Institute of Nutrition [24].

Preparation of yogurt

Lactobacillus delbrueckii subsp. bulgaricus CH-2 was cultivated in 25 ml of MRS broth medium at 37 °C for 24 h. Streptococcus thermophilus ST-36 was grown in 25 ml of M17 broth at 40 °C for 24 h. The whole milk was boiled to reduce its volume by approximately 20%, then heated at 90 °C for 5 min, cooled to 42 °C and inoculated with 1% of Lactobacillus delbrueckii subsp. bulgaricus CH-2, Streptococcus thermophilus and 1 g of selenium/litre of milk and then incubated at 40 °C for approximately 4 h until coagulation. The yogurt samples were stored at 5 ± 1 °C for 2 days [25].

Sensory evaluation

The selenium-fortified yogurt was evaluated for its sensory characteristics including aroma, taste, texture, colour and overall acceptability. A total of 20 trained voluntary panellists were involved in the hedonic test. The results are represented by the following scores: excellent, 9–10 (90–100%); very good, 8–9 (80–90%); good, 6–7 (60–70%); fair, 4–5 (40–50%); poor, 2–3 (20–30%); and very poor, 0–1 (0–10%).

Estimation of aflatoxins

Nuts were crushed separately, and equal amounts of ever crushed nut were mixed to estimate the total aflatoxins at zero time of storage (fresh) as nuts can be naturally infected with Aspergillus fungi that produce aflatoxins [22, 23]. Individual raw experimental nuts and mixture nuts were stored separately in glass dishes at 25 °C and 70% relative humidity for 6 months. The total aflatoxins after 6 months of storage were estimated. According to these aflatoxin levels, the biological study was designed.

Grouping of rats and experimental design

Animals were divided into seven groups as follows:
  • The negative control group was fed a standard diet with a 3% fresh mixture of the five experimental nuts (zero time of storage, safe nuts).

  • The positive control group was fed a standard diet with a 3% mixture of five nuts contaminated with aflatoxins after storage at 25 °C for 6 months.

  • The pistachio with selenium-fortified yogurt rat group was fed a standard diet with 3% pistachios contaminated with aflatoxins after storage at 25 °C for 6 months and 160 ml/kg body weight daily of selenium-fortified yogurt through a stomach tube [25].

  • The cashew with selenium-fortified yogurt group was fed a standard diet with 3% cashews contaminated with aflatoxins and 160 ml/kg body weight daily of selenium-fortified yogurt through a stomach tube.

  • The walnut with selenium-fortified yogurt group was fed a standard diet with 3% walnuts contaminated with aflatoxins and 160 ml/kg body weight daily of selenium-fortified yogurt through a stomach tube.

  • The almond with selenium-fortified yogurt group was fed a standard diet with 3% almonds contaminated with aflatoxins and 160 ml/kg body weight daily of selenium-fortified yogurt through a stomach tube.

  • The hazelnut with selenium-fortified yogurt group was fed a standard diet with 3% hazelnuts contaminated with aflatoxins and 160 ml/kg body weight daily of selenium-fortified yogurt through a stomach tube.

After completion of the experimental period (60 days), rats were fasted overnight and killed to obtain blood, kidneys and liver.

Biological determination

Biological evaluation of the different diets was carried out by determination of the initial body weight, body weight gain (BWG%) and feed intake and calculation of the feed efficiency ratio (FER) by dividing the daily body weight gain by the daily feed intake. Serum cholesterol (CHO), triglycerides (TG), high-density lipoprotein cholesterol (HDLc) and total lipids (T. lipids) were determined by enzymatic colourimetric methods [2628]. Very low-density lipoprotein cholesterol (VLDLc) was calculated as TG/5, and low-density lipoprotein cholesterol (LDLc) was calculated as total cholesterol minus HDLc + VLDLc [29]. Blood haemoglobin (HG), packed cell volume (PCV) and glucose were estimated in heparinized blood. Atherogenic indexes (CHO/HDLc and LDLc/HDLc) and phospholipids were calculated. Livers were immediately perfused with 50–100 of ice-cold 0.9% NaCl solution for estimation of liver cholesterol, triglycerides, total lipids and glycogen. Fresh portions of liver and kidney from every rat were immersed in 10% neutral buffered formalin for future histopathological examination. The fixed specimens were later trimmed, washed and dehydrated in ascending grades of alcohol, cleared in xylene, embedded in paraffin, sectioned at 4–6 µm thickness and stained with haematoxylin and eosin before microscopic examination. In addition, Masson’s trichrome and Sudan Black B methods were also used to stain collagen tissues and to demonstrate changes in fatty tissues [30].

Precautions with aflatoxins

Laboratory surfaces were cleaned with 1% sodium hypochlorite. Suitable protective clothes such as laboratory masks, coats and gloves were worn. All laboratory instruments were washed with 10% sodium hypochlorite before cleaning or discarding and after use. Aflatoxins were deactivated by autoclaving in the presence of ammonium and by treatment with hypochlorite [31, 32].

Statistical analysis

Collected data are presented as the mean ± SD and statistically analysed using one-way analysis of variance (ANOVA) with the level of significance indicated at p < 0.05. Student’s t test was used for evaluating the significance of paired observations [33].

Results and discussion

The total aflatoxin concentration was 4.97 μg/kg in the mixture of fresh nuts at zero time of storage, which is considered to be safe according to the European Union standard, Iran standard and Australia New Zealand Food Standards Code. The total aflatoxins in the mixed nuts after 6 months of storage were 24.84 μg was 24.84 μg/kg, which is not considered safe by the European Union standard, Iran standard, and Australia New Zealand Food Standards Code. The estimated total aflatoxins were 23.25, 23.66, 22.07, 26.02 and 28.6 μg/kg in the pistachios, cashews, walnuts, almonds and hazelnuts, respectively. According to these aflatoxin levels, the biological study was designed.

In overall acceptability, the fresh selenium-fortified yogurt was rated very good (80–90%) and the commercial brand was rated excellent (90–100%; Table 1). Selenium-fortified yogurt was acceptable to the panellists as indicated by their mean score for overall acceptability.
Table 1

Sensory evaluation of selenium-fortified yogurt compared to the commercial brand

Attribute

Aroma

Taste

Texture

Colour

Overall acceptability (%)

Selenium-fortified yogurt

8.2 ± 1.52

8.4 ± 1.24

8.7 ± 1.33

8.5 ± 1.55

33.8 ± 3.20 (84.5%)

Commercial yogurt

9.1 ± 1.62

9.2 ± 1.73

9.3 ± 1.54

9.2 ± 1.65

36.8 ± 3.26 (92%)

The nutritional and therapeutic benefits of the consumption of dairy products containing live Lactobacillus acidophilus as a food or supplement have been the focus of studies for the last two decades [3436]. However, the production of high-quality fermented milk products containing these probiotic bacteria is a major challenge due to specific attributes of the bacteria such as rapid acid production from lactose and development of suitable quantities of volatile compounds such as diacetyl and acetaldehyde [37]. Selenium is an essential element in almost all biological systems. Although significant attention has been placed on the organoleptic characteristics of selenium-fortified yogurt, little emphasis has been placed on consumer acceptability and preference of the finished product. To enhance the consumption of yogurt, consumer satisfaction must be balanced with cost-effectiveness and health benefits [38].

The effect of consumption of aflatoxin-contaminated nuts on rat body weight, food intake and FER is illustrated in Table 2. The positive control rat group that consumed 3% mixed nuts contaminated with aflatoxins showed a significant decrease in body weight and FER at p < 0.05 compared to the negative control rat group that consumed 3% safe fresh mixed nuts. Consumption of 3% pistachios, walnuts, almonds, or hazelnuts contaminated with aflatoxins in addition to selenium-fortified yogurt produced body weight and feed intake that were within normal values of the negative control group, along with a significant decrease in the feed efficiency ratio compared to the negative control group and a significant increase in this value compared to that of the positive control rat group. Consumption of 3% cashews contaminated with aflatoxins in addition to selenium-fortified yogurt by experimental rats produced insignificant changes to body weight, feed intake and FER compared to the negative control group.
Table 2

Body weight, food intake and feed efficiency ratio in the experimental rat groups

Variables

Initial weight (g)

Body weight gain (g)

Food intake (g/w)

FER

Groups

Negative control consumed 3% mixed fresh nuts

130.77 ± 5.50a

120.2 ± 5.80a

15.11 ± 1.30a

0.132 ± 0.003a

Positive control consumed 3% mixed nuts contaminated with aflatoxins

131.87 ± 5.50a

100.21 ± 8.99d

14.50 ± 1.69a

0.114 ± 0.002c

Rat groups consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins

 Pistachios with selenium-fortified yogurt

131.91 ± 5.44a

110.33 ± 4.35a

14.90 ± 2.53a

0.123 ± 0.004b

 Cashews with selenium-fortified yogurt

131.71 ± 5.44a

112.45 ± 5.40a

14.09 ± 2.49a

0.133 ± 0.003a

 Walnuts with selenium-fortified yogurt

131.61 ± 5.44a

113.43 ± 3.85a

15.01 ± 2.30a

0.125 ± 0.004b

 Almonds with selenium-fortified yogurt

131.53 ± 5.44a

115.39 ± 3.50a

15.11 ± 1.90a

0.127 ± 0.005b

 Hazelnuts with selenium-fortified yogurt

131.49 ± 5.44a

114.82 ± 5.50a

15.39 ± 2.04a

0.124 ± 0.002b

(g/w): gram/week, FER feed efficiency ratio

Mean values in each column having different letters (a, b, c and d) are significantly different at p < 0.05

Aflatoxin B1 accumulates in the liver to very high concentrations and is metabolized through microsomal enzymes by hydroxylation, hydration, demethylation and epoxidation reactions. Aflatoxin B1 causes damage to the liver and adversely affects key metabolic pathways of carbohydrates, proteins and lipids [6, 39]. Aflatoxin ingestion can also lead to body weight loss by changing the activities of digestive enzymes, causing malabsorption syndrome, characterized by steatorrhea as well as hypocarotenoidemy, and lowering the bile, pancreatic lipase, trypsin and amylase levels [40]. Aflatoxin is known to impair protein biosynthesis by forming adducts with DNA, RNA and proteins, to inhibit RNA synthesis and DNA-dependent RNA polymerase activity and to cause degranulation of the endoplasmic reticulum. A reduction in protein content could also be caused due to increased hepatocellular necrosis. Other investigators have reported a decrease in protein concentration in the skeletal muscle, heart, liver and kidneys of aflatoxin-fed animals [41, 42]. Our results agreed with previous studies that reported that dietary exposure to AFB1 and other aflatoxins leads to less weight gain in both chickens and turkeys. A decreased efficiency of nutrient usage contributes to the impaired growth during aflatoxicosis. AFB1 dampens food conversion, causing poultry to require more feed to produce muscle and eggs [43, 44]. The body weight of the rats that declined due to the aflatoxin recovered after treatment with selenium-fortified yogurt. This is likely related to the composition of yogurt including proteins, fat, lactose and biogenic metabolites such as vitamins, peptides, oligosaccharides and organic acids [45, 46]. A separate study in rats suggested that probiotic treatment prevented weight loss and reduced the hepatotoxic effects caused by a high dose of AFB1 by increasing the excretion of orally administered aflatoxin in faeces [47]. Selenium added to yogurt, regarded as a basic trace element essential for the normal growth and development of humans and animals and acting as antioxidant, improves nutritional results. As a component of selenoproteins, selenium has both structural and enzymatic functions, protects cell lipids from the harmful effects of reactive oxygen species and can minimize the production of hydrogen peroxide by aflatoxins [48].

The positive control group that consumed 3% mixed nuts contaminated with aflatoxins showed significant increases in serum cholesterol, TG, LDLc and VLDLc and lower values of serum HDLc compared to the negative control group. Consumption of 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins along with selenium-fortified yogurt led to significant decreases in serum cholesterol, TG, LDLc and VLDLc and higher values of serum HDLc compared to the positive control group. Consumption of selenium-fortified yogurt could somewhat normalize these values compared to the negative control group (Table 3).
Table 3

Serum lipids profile of the experimental rat groups

Variables

CHO (mg/dl)

TG (mg/dl)

HDLc (mg/dl)

LDLc (mg/dl)

VLDLc (mg/dl)

Groups

Negative control consumed 3% mixed fresh nuts

95.17 ± 8.67bc

69. 41 ± 5.25bc

36.86 ± 5.41a

44. 43 ± 4.56d

13.88 ± 1.68bc

Positive control consumed 3% mixed nuts contaminated with aflatoxins

167.25 ± 15.24a

90.31 ± 8. 40a

24.31 ± 3.23c

124.34 ± 13. 81a

18.06 ± 1.45a

Rat groups consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins

 Pistachios with selenium-fortified yogurt

112.45 ± 11.22b

75.55 ± 3.44b

32.98 ± 3.50a

64.36 ± 5.99b

15.11 ± 1.33b

 Cashews with selenium-fortified yogurt

109.60 ± 12.75b

72. 41 ± 5. 73b

33.65 ± 3.24a

61.47 ± 8. 17b

14.48 ± 1.50b

 Walnuts with selenium-fortified yogurt

113.76 ± 10.64b

74.01 ± 4.55b

31.99 ± 4.03ab

66.9 ± 6.78b

14.80 ± 1.12b

 Almonds with selenium-fortified yogurt

103.80 ± 11.14b

73.61 ± 7.03b

34.11 ± 2.71a

54.97 ± 6. 40bc

14.72 ± 1.57b

 Hazelnuts with selenium-fortified yogurt

101.70 ± 10. 14b

70. 14 ± 5.11b

35.65 ± 4.81a

52.02 ± 5. 71bc

14.03 ± 1.35b

Mean values in each column having different letters (a, b, c and d) are significantly different at p < 0.05

Yogurt is recognized as a functional food, and its consumption correlates with a reduced risk of numerous cancers. Probiotic bacteria in yogurt, including lactobacilli and streptococci, can reduce serum cholesterol levels by metabolizing cholesterol and reducing its re-absorption in the gastrointestinal tract. Probiotics in yogurt can assimilate cholesterol by incorporating it into membranes and can deconjugate and precipitate bile acids, leading to excretion of free bile acids through the stool [49, 50]. Selenium compounds play an important role in neutralizing and removing a variety of toxic substances from the body. Research has shown a relationship between selenium deficiency in humans and an increased cancer risk. Selenium inactivates aflatoxins, thus protecting the body from their carcinogenic effects [51].

The positive control rat group showed significant increases in serum total lipids, phospholipids, CHO/HDLc and LDLc/HDLc compared to the negative control rat group. Rats that consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins along with selenium-fortified yogurt showed significant decreases in serum total lipids, phospholipids and atherogenic indexes (CHO/HDLc and LDLc/HDLc) compared to the positive control group. When compared to the negative control group, consumption of pistachios, cashews and almonds contaminated with aflatoxins and selenium-fortified yogurt produced significant increases in serum phospholipids and atherogenic index values (LDLc/HDLc) and insignificant increases in total lipids and CHO/HDLc. Consumption of walnuts contaminated with aflatoxins along with selenium-fortified yogurt produced insignificant differences in serum total lipids, phospholipids and atherogenic index (CHO/HDLc) and a significant increase in LDLc/HDLc. Consumption of hazelnuts contaminated with aflatoxins along with selenium-fortified yogurt produced insignificant differences in serum total lipids and atherogenic indexes (CHO/HDLc and LDLc/HDLc) and a significant increase in serum phospholipids (Table 4).
Table 4

Serum T. lipids, phospholipids, CHO/HDLc and LDLc/HDLc in the experimental rat groups

Variables

T. lipids (mg/dl)

Phospholipids (mg/dl)

CHO/HDLc

LDLc/HDLc

Groups

Negative control consumed 3% mixed safe nuts

322.17 ± 99.76b

157.59 ± 11.58c

2.58 ± 0.56 bc

1.20 ± 0.23c

Positive control consumed 3% mixed nuts contaminated with aflatoxins

578.41 ± 141.51a

320.85 ± 95.88a

6.87 ± 1.22a

5.11 ± 1.09a

Rat groups consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins

 Pistachios with selenium-fortified yogurt

360.71 ± 101.21b

172.71 ± 17.89b

3.40 ± 0.62b

1.95 ± 0.22b

 Cashews with selenium-fortified yogurt

350.45 ± 111.13b

168.44 ± 15.90b

3.25 ± 0.55b

1.82 ± 0.33b

 Walnuts with selenium-fortified yogurt

345.21 ± 99.61b

157.44 ± 14.45c

3.55 ± 0.57b

1.98 ± 0.45b

 Almonds with selenium-fortified yogurt

355.11 ± 109.51b

177.71 ± 18.87b

3.04 ± 0.70bc

1.61 ± 0.50b

 Hazelnuts with selenium-fortified yogurt

343.66 ± 105.64b

171.82 ± 18.03b

2.85 ± 0.61bc

1.45 ± 0.43bc

Mean values in each column having different letters (a, b, c and d) are significantly different at p < 0.05

Our results were in agreement with published reports [10, 52, 53]. Probiotic bacteria in yogurt can inhibit peroxidation of lipids through scavenging reactive oxygen radicals, such as hydroxyl radicals or hydrogen peroxide, and can produce antioxidant factors, such as superoxide dismutase or glutathione, as well as various peptides derived from α-lactalbumin, β-lactoglobulin and α-casein. It has been reported that some lactic acid bacteria in yogurt can remove or have protective effects against AFB1. Some relevant studies have demonstrated that lactobacilli can inhibit the production of aflatoxin as well as the growth of Aspergillus spp. Researchers have also analysed AFB1 removal by lactobacilli in vitro and noted that lactobacilli could rapidly remove AFB1 with a removal rate of approximately 50–80% [54, 55]. Ingestion yogurt regulated the expression of sterol regulatory element binding protein, other lipogenic enzymes and β-oxidation-related genes, which produce enzymes that are involved in the catabolism of fatty acids cholesterol in the rat liver. Selenium improves the activity of the selenoenzyme. Selenium is also present in the active centre of glutathione peroxidase, an antioxidant enzyme, which protects lipid membranes and macromolecules from oxidative damage produced by peroxides. Furthermore, glutathione peroxidase has the ability to counteract free radicals and protect the structure and function of proteins, DNA and chromosomes against oxidation [56].

The positive control group showed significant increases in liver cholesterol and total lipids and significant decreases in liver TG and glycogen compared to the negative control group. Consumption of 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins along with selenium-fortified yogurt resulted in significant decreases in liver cholesterol and total lipids and significant increases in liver TG and glycogen compared to the positive control group, which consumed 3% mixed nuts contaminated with aflatoxins, and produced values within the expected range established by the negative control group (Table 5).
Table 5

Liver cholesterol, T. lipids, TG and glycogen in the experimental rat groups

Variables

CHO (mg/g)

T. lipid (mg/g)

TG (mg/g)

Glycogen (mg/100 g)

Groups

Negative control consumed 3% mixed safe nuts

3.97 ± 0.66bc

35.58 ± 4.78bc

3.44 ± 0.51a

5.50 ± 1.20a

Positive control consumed 3% mixed nuts contaminated with aflatoxins

6.86 ± 0.91a

59.51 ± 8.55a

2.19 ± 0.23b

3.11 ± 0.36b

Rat groups consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins

 Pistachios with selenium-fortified yogurt

4.07 ± 0.64b

39.95 ± 4.77b

3.24 ± 0.25a

4.99 ± 0.50a

 Cashews with selenium-fortified yogurt

4.80 ± 0.65b

38.55 ± 4.44b

3.35 ± 0.25a

4.83 ± 0.55a

 Walnuts with selenium-fortified yogurt

4.96 ± 0.66b

36.97 ± 4.62b

3.39 ± 0.21a

4.96 ± 0.56a

 Almonds with selenium-fortified yogurt

4.06 ± 0.76b

37.79 ± 4.53b

3.30 ± 0.33a

4.88 ± 0.88a

 Hazelnuts with selenium-fortified yogurt

4.91 ± 0.76b

35.92 ± 4.69b

3.44 ± 0.43a

4.90 ± 0.95a

Mean values in each column having different letters (a, b, c and d) are significantly different at p < 0.05

Aflatoxins cause food poisoning, and acute doses are responsible for liver and kidney damage and, potentially, hepatocarcinoma. Exposure to aflatoxins can lead to liver injuries, liver fibrosis and hepatocellular carcinoma and therefore poses a considerable health risk for humans and livestock [57]. AFB1 exposure causes alterations in metabolic processes, such as glycogenolysis/glycolysis and phospholipidation, and changes in amino acid transportation. AFB1 exposure can also indirectly result in damage to cell membranes and ultimately lead to cell death [58]. AFB1 exposure also causes other metabolic alterations, especially in the metabolism of lipids, choline, nucleic acids and cholesterol. Aflatoxins cause oxidative stress by increasing lipid peroxidation and decreasing enzymatic and non-enzymatic antioxidants in aflatoxin-treated animals [59, 60]. Yogurt containing lactic acid bacteria (lactobacilli and streptococci) improves liver efficiency by lowering bacterial translocation and by stimulating the effects of intestinal mucosa and altering intestinal microflora that influence the intestinal barrier [61]. These yogurt bacteria inhibited the peroxidation of lipids through scavenging reactive oxygen species, such as hydroxyl radicals or hydrogen peroxide [52].

Table 6 shows the levels of haemoglobin, PCV and glucose in the control and experimental rat groups. Decreased haemoglobin and PCV and increased levels of glucose were observed in the positive control rat group that consumed 3% mixed nuts contaminated with aflatoxins. Consumption of 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins along with selenium-fortified yogurt produced significant increases in haemoglobin and PCV and a significant decrease in glucose compared to the positive control group, with this values appearing within the range of those of the negative control group.
Table 6

Blood HG, PCV and glucose in the experimental rat groups

Variables

HG (g/dl)

PCV %

Glucose (mg/dl)

Groups

Negative control consumed 3% mixed safe nuts

13.98 ± 1.89a

38.42 ± 4.53a

95.85 ± 5.99c

Positive control consumed 3% mixed nuts contaminated with aflatoxins

10.99 ± 1.25c

27.53 ± 2.60c

149.06 ± 10.37a

Rat groups consumed 3% pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins

 Pistachios with selenium-fortified yogurt

12.65 ± 1.26ab

34.38 ± 4.59ab

104.63 ± 13.29bc

 Cashews with selenium-fortified yogurt

12.79 ± 1.33ab

35.08 ± 4.87ab

105.76 ± 11.55bc

 Walnuts with selenium-fortified yogurt

12.45 ± 1.34ab

34.56 ± 4.50ab

107.09 ± 12.11bc

 Almonds with selenium-fortified yogurt

12.77 ± 1.55b

33.98 ± 4.08ab

106.70 ± 11.29bc

 Hazelnuts with selenium-fortified yogurt

12.88 ± 1.63ab

34.70 ± 4.80ab

110.03 ± 13.28bc

Mean values in each column having different letters (a, b, c and d) are significantly different at p < 0.05

The decreased haemoglobin and PCV indicate the severity of hepatic damage induced by aflatoxins. The decrease in haemoglobin levels might be due to increased catabolism and degradation of haemoglobin into bilirubin. The reduction in HG content could be related to decreases in red blood cell numbers, which is indicative of anaemia [62]. Our observations suggested that one of the consequences of aflatoxin exposure is accelerated rates of glycogenolysis and glycolysis. Rats exposed to aflatoxins exhibited significantly reduced hepatic glucose/glycogen levels and elevated plasma glucose. Previous investigations have also reported increased glucose utilization and that several enzymes metabolizing glycogen, such as glucose 6-phosphate dehydrogenase, were upregulated following AFB1 exposure [60]. In addition of nutritional values of selenium-fortified yogurt, selenium conferred protection against AFB1-induced testicular toxicity and effectively protected the liver and spleen against AFB1-induced toxicity. In previous studies, dietary selenium protected chicks from AFB1-induced liver injury, potentially through the synergistic actions of inhibition of the pivotal CYP450 isozyme-mediated activation of AFB1 to toxic AFBO and the increased antioxidant capacities caused by upregulation of selenoprotein genes coding for antioxidant proteins. Low selenium status can upregulate the activity of hepatic heme oxygenase-1, which catalyses the initial step of heme catabolism and reduces heme to biliverdin, carbon monoxide and free divalent iron [42, 63]. Thus, selenium could potentially play a role in the anaemia of chronic inflammation through its relationship with the upregulation of interleukin-6 that implicated in the upregulation of the iron regulatory hepcidin hormone that blocks iron absorption in the gut and iron release from macrophages and the liver [64]. Lactic acid bacteria have shown great ability to bind aflatoxin in contaminated medium. It has been suggested that a physical union through an adhesion of aflatoxin to bacterial cell wall components (polysaccharides and peptidoglycans) might be responsible for reducing the bioavailability of mycotoxins, instead of covalent binding or degradation [65].

Histopathological results

Microscopically, the liver of rats from the negative control group that consumed 3% mixed safe fresh nuts had the expected histological structure of hepatic lobules (Fig. 1a). In comparison, the livers of the positive control group that consumed 3% mixed nuts contaminated with aflatoxins showed congestion of hepatoportal blood vessels, portal oedema and focal hepatic necrosis associated with leucocytic cell infiltration (Fig. 1b). Consumption of selenium-fortified yogurt by rat groups that consumed pistachios, cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins resulted in liver histological structures with featured between those of healthy and injured cells. Livers of rats that consumed 3% pistachios contaminated with aflatoxins and selenium-fortified yogurt showed slight congestion of the central vein (Fig. 1c). However, livers from rats that consumed 3% cashews and walnuts contaminated with aflatoxins appeared healthy with no histopathological changes (Figs. 1d, e). The rats that consumed 3% almonds contaminated with aflatoxins had vacuolations of hepatocytes (Fig. 1f), but rats that consumed 3% hazelnuts only showed mild Kupffer cell activation (Fig. 1g).
Fig. 1
Fig. 1

Histological structure of the liver of the negative control group (a), in the positive control group (b), of the pistachio with selenium-fortified yogurt group (c), of the cashews with selenium-fortified yogurt group (d), of the walnuts with selenium-fortified yogurt group (e), of the almonds with selenium-fortified yogurt group (f) and of the hazelnuts with selenium-fortified yogurt group (g)

The kidneys filter and remove toxins from the body. Hence, a histopathological study of the kidneys was undertaken to evaluate the efficacy of selenium-fortified yogurt in ameliorating the harmful effects of aflatoxin. Microscopic examination of the kidneys from the negative control group that consumed 3% mixed fresh nuts showed the expected histological structure of renal parenchyma (Fig. 2a). Kidneys from the positive control group that consumed 3% mixed nuts contaminated with aflatoxins showed chronic interstitial nephritis and periglomerular fibroblast proliferation (Fig. 2b). Kidneys from rats that consumed 3% pistachios contaminated with aflatoxins and selenium-fortified yogurt showed a slight dilatation of renal tubules (Fig. 2c), while kidneys from rats that consumed 3% cashews, walnuts, almonds and hazelnuts contaminated with aflatoxins and selenium-fortified yogurt showed the expected normal histological structure of renal parenchyma (Figure 2d–g).
Fig. 2
Fig. 2

Histological structure of the kidneys of the negative control group (a), of the positive control group (b), of the pistachio with selenium-fortified yogurt group (c), of the cashews with selenium-fortified yogurt group (d), of the walnuts with selenium-fortified yogurt rat group (e), of almonds with selenium-fortified yogurt group (f) and of the hazelnuts with selenium-fortified yogurt group (g)

The histological results from this current study confirmed the biochemical analysis and indicated that consumption of mixed nuts contaminated with aflatoxins induces severe histological changes in the liver and kidneys of rats, as previously documented [5, 66]. Acute aflatoxin poisoning caused hepatocellular necrosis and derangement of hepatic functions. Subacute or chronic aflatoxicosis caused changes to fatty portions of the liver, enlargement of the gall bladder and periportal fibrosis with proliferative changes in the bile duct epithelium [67, 68]. The significant recovery of hepatic and kidney tissues through consumption of selenium-fortified yogurt is consistent with previous results in mice [69]. The improvements in the liver tissues have also already been seen in mice orally administered with viable L. plantarum C88 through the increase of faecal AFB1 excretion, which reversed deficits in antioxidant defence systems and regulated the metabolism of AFB1 [70].

Conclusions

Consumption of nuts stored in bad conditions leads to aflatoxin toxicity, primarily in the liver and kidneys. Consumption of selenium-fortified yogurt can successfully protect against this aflatoxin toxicity. Further researches and studies must be undertaken systematically and constantly to better understand the in vivo mechanisms by using other types of food which reduce aflatoxin toxicity and its side effects. Overall, the application of probiotic bacteria and selenium to improve safety in the food industry is a viable, vital therapeutic approach. Therefore, it is recommended to consume fresh nuts along with selenium-fortified yogurt to reduce the effects of aflatoxins.

Abbreviations

AF: 

aflatoxins

FER: 

feed efficiency ratio

CHO: 

serum cholesterol

TG: 

triglycerides

HDLc: 

high-density lipoprotein cholesterol

T. lipids: 

total lipids

VLDLc: 

very low-density lipoprotein cholesterol

LDLc: 

low-density lipoprotein cholesterol

HG: 

haemoglobin

PCV: 

packed cell volume

Declarations

Authors’ contributions

AMA conceived and designed the research, collected and analysed the data and wrote the manuscript. Additionally, she conceived the study, followed up the field work, supervised the animal experiments with technical specialists and reviewed and made editorial comments on the draft of the manuscript. In addition, she was involved in proof reading and editorial comments on the draft of the manuscript. The author read and approved the final manuscript.

Acknowledgements

The author (Amnah Mohammed ALsuhaibani) records her profound gratitude to Princess Nourah Bint Abdulrahman University for its financial and moral support in accomplishing this research paper.

Competing interests

The author declares that she has no competing interests.

Availability of data and materials

The dataset supporting the conclusions of this article is included within top of the article.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Ethical guidelines were maintained in animal handling during the study, and permission was obtained from the relevant department.

Funding

Princess Nourah Bint Abdulrahman University, Nutrition and Food Sciences Department.

Publisher’s Note

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Authors’ Affiliations

(1)
Nutrition and Food Sciences Department, Home Economic College, Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia

References

  1. Bennett JW, Klich M. Mycotoxins. Clin Microbiol Rev. 2003;16:497–516.View ArticlePubMedPubMed CentralGoogle Scholar
  2. Rawal S, Kim JE, Coulombe R Jr. Aflatoxin B1 in poultry: toxicology, metabolism and prevention. Res Vet Sci. 2010;89:325–31.View ArticlePubMedGoogle Scholar
  3. Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D. Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr. 2004;80:1106–22.View ArticlePubMedGoogle Scholar
  4. Zhang L, Ye Y, An Y, Tian Y, Wang Y, Tang H. Systems responses of rats to aflatoxin B1 exposure revealed with metabonomic changes in multiple biological matrices. J Proteome Res. 2011;10:614–23.View ArticlePubMedGoogle Scholar
  5. Wogan GN, Kensler TW, Groopman JD. Present and future directions of translational research on aflatoxin and hepatocellular carcinoma. A review. Food Addit Contam A Chem Anal Control Expo Risk Assess. 2012;29:249–57.View ArticleGoogle Scholar
  6. Bedard LL, Massey TE. Aflatoxin B1-induced DNA damage and its repair. Cancer Lett. 2006;241:174–83.View ArticlePubMedGoogle Scholar
  7. Cotty PJ, Jaime-Garcia R. Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int J Food Microbiol. 2007;119:109–15.View ArticlePubMedGoogle Scholar
  8. Wild CP, Montesano R. A model of interaction: aflatoxins and hepatitis viruses in liver cancer aetiology and prevention. Cancer Lett. 2009;286:22–8.View ArticlePubMedGoogle Scholar
  9. Spanhaak S, Havenaar R, Schaafsma G. The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr. 1998;52:899–907.View ArticlePubMedGoogle Scholar
  10. Fitzgerald RJ, Murray BA. Bioactive peptides and lactic fermentations. Int J Dairy Technol. 2006;59:118–25.View ArticleGoogle Scholar
  11. Keszei AP, Schouten LJ, Goldbohm RA, van den Brandt PA. Dairy intake and the risk of bladder cancer in the Netherlands cohort study on diet and cancer. Am J Epidemiol. 2010;171:436–46.View ArticlePubMedGoogle Scholar
  12. Knasmuller S, Steinkellner H, Hirschl AM, Rabot S, Nobis EC, Kassie F. Impact of bacteria in dairy products and of the intestinal microflora on the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Mutat Res. 2001;480–481:129–38.View ArticlePubMedGoogle Scholar
  13. Kato I, Tanaka K, Yokokura T. Lactic acid bacterium potently induces the production of interleukin-12 and interferon-gamma by mouse splenocytes. Int J Immunopharmacol. 1999;21:121–31.View ArticlePubMedGoogle Scholar
  14. Lim BK, Mahendran R, Lee YK, Bay BH. Chemopreventive effect of Lactobacillus rhamnosus on growth of a subcutaneously implanted bladder cancer cell line in the mouse. Jpn J Cancer Res. 2002;93:36–41.View ArticlePubMedGoogle Scholar
  15. Sangwan S, Singh R. Therapeutic effects of probiotic fermented milk (LGG and L casei NCDC 19) on progression of type 2 diabetes. J Innov Biol. 2014;1:78–83.Google Scholar
  16. Kukreja R, Khan A. Effect of selenium deficiency and its supplementation on DTH response, antibody forming cells and antibody titre. Indian J Exp Biol. 1998;36:203–5.PubMedGoogle Scholar
  17. Gill H, Walker G. Selenium, immune function and resistance to viral infections. Nutr Diet. 2008;65:S41–7.View ArticleGoogle Scholar
  18. Jakhar KK, Sadana JR. Sequential pathology of experimental aflatoxicosis in quail and the effect of selenium supplementation in modifying the disease process. Mycopathologia. 2004;157:99–109.View ArticlePubMedGoogle Scholar
  19. Shi CY, Chua SC, Lee HP, Ong CN. Inhibition of aflatoxin B1-DNA binding and adduct formation by selenium in rats. Cancer Lett. 1994;82:203–8.View ArticlePubMedGoogle Scholar
  20. Uysal H, Agar G. Selenium protective activity against aflatoxin B1 adverse affects on Drosophila melanogaster. Braz Arch Biol Technol. 2005;48:227–33.View ArticleGoogle Scholar
  21. Wang F, Shu G, Peng X, Fang J, Chen K, Cui H, et al. Protective effects of sodium selenite against aflatoxin B1-induced oxidative stress and apoptosis in broiler spleen. Int J Environ Res Public Health. 2013;10:2834–44.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Anonymous. Enzyme immunoassay for the quantitative analysis of aflatoxins. Aflatoxin Total Art. No. R-4701. Darmstadt: R-Biopharm GmbH; 2004.Google Scholar
  23. Senyuva HZ, Gilbert J. Immunoaffinity column cleanup with liquid chromatography using post-column bromination for determination of aflatoxins in hazelnut paste: interlaboratory study. J AOAC Int. 2005;88:526–35.PubMedGoogle Scholar
  24. Second Report of American Institute of Nutrition. Nutrient requirement of laboratory animals. J Nutr. 1980;110:1726–32.View ArticleGoogle Scholar
  25. Tamime AY, Robinson RK. Yoghurt–science and technology. Cambridge: Woodhead Publishers; 1999.Google Scholar
  26. Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem. 1974;20:470–5.PubMedGoogle Scholar
  27. Bucolo G, David H. Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem. 1973;19:476–82.PubMedGoogle Scholar
  28. Kostner GM. Enzymatic determination of cholesterol in high-density lipoprotein fractions prepared by polyanion precipitation. Clin Chem. 1976;22:695.PubMedGoogle Scholar
  29. Fruchart GG. LDL-cholesterol determination after separation of low density lipoprotein. Revue Française des Laboratoires. 1982;103:7–117.Google Scholar
  30. Coles EH. Veterinary clinical pathology. Philadelphia: Saunders Company; 1974.Google Scholar
  31. Nakai VK, Rocha LO, Gonçalez E, Fonseca H, Ortega EMM, Corrêa B. Distribution of fungi and aflatoxins in a stored peanut variety. Food Chem. 2008;106:285–90.View ArticleGoogle Scholar
  32. Leong Y-H, Ismail N, Latif AA, Ahmad R. Aflatoxin occurrence in nuts and commercial nutty products in Malaysia. Food Control. 2010;21:334–8.View ArticleGoogle Scholar
  33. Artimage GY, Berry WG. Statistical methods. 7th ed. Ames: Iowa Stata University Press; 1987.Google Scholar
  34. Mustapha A, Jiang T, Savaiano DA. Improvement of lactose digestion by humans following ingestion of unfermented acidophilus milk: influence of bile sensitivity, lactose transport, and acid tolerance of Lactobacillus acidophilus. J Dairy Sci. 1997;80:1537–45.View ArticlePubMedGoogle Scholar
  35. Anderson JW, Gilliland SE. Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr. 1999;18:43–50.View ArticlePubMedGoogle Scholar
  36. Andrade S, Borges N. Effect of fermented milk containing Lactobacillus acidophilus and Bifidobacterium longum on plasma lipids of women with normal or moderately elevated cholesterol. J Dairy Res. 2009;76:469–74.View ArticlePubMedGoogle Scholar
  37. Yeung PS, Sanders ME, Kitts CL, Cano R, Tong PS. Species-specific identification of commercial probiotic strains. J Dairy Sci. 2002;85:1039–51.View ArticlePubMedGoogle Scholar
  38. Ostlie HM, Helland MH, Narvhus JA. Growth and metabolism of selected strains of probiotic bacteria in milk. Int J Food Microbiol. 2003;87:17–27.View ArticlePubMedGoogle Scholar
  39. Preston RJ, Williams GM. DNA-reactive carcinogens: mode of action and human cancer hazard. Crit Rev Toxicol. 2005;35:673–83.View ArticlePubMedGoogle Scholar
  40. Osborne DJ, Huff WE, Hamilton PB, Burmeister HR. Comparison of ochratoxin, aflatoxin, and T-2 toxin for their effects on selected parameters related to digestion and evidence for specific metabolism of carotenoids in chickens. Poult Sci. 1982;61:1646–52.View ArticlePubMedGoogle Scholar
  41. Abdel-Wahhab MA, Ahmed HH, Hagazi MM. Prevention of aflatoxin B1-initiated hepatotoxicity in rat by marine algae extracts. J Appl Toxicol. 2006;26:229–38.View ArticlePubMedGoogle Scholar
  42. Sun LH, Zhang NY, Zhu MK, Zhao L, Zhou JC, Qi DS. Prevention of aflatoxin B1 hepatoxicity by dietary selenium is associated with inhibition of cytochrome P450 isozymes and up-regulation of 6 selenoprotein genes in chick liver. J Nutr. 2016;146:655–61.View ArticleGoogle Scholar
  43. Pandey I, Chauhan SS. Studies on production performance and toxin residues in tissues and eggs of layer chickens fed on diets with various concentrations of aflatoxin AFB1. Br Poult Sci. 2007;48:713–23.View ArticlePubMedGoogle Scholar
  44. Lee JT, Jessen KA, Beltran R, Starkl V, Schatzmayr G, Borutova R, et al. Mycotoxin-contaminated diets and deactivating compound in laying hens: 1. Effects on performance characteristics and relative organ weight. Poult Sci. 2012;91:2089–95.View ArticlePubMedGoogle Scholar
  45. Santosa S, Farnworth E, Jones PJ. Probiotics and their potential health claims. Nutr Rev. 2006;64:265–74.View ArticlePubMedGoogle Scholar
  46. Junaid M, Javed I, Abdullah M, Gulzar M, Younas U, Nasir J, et al. Development and quality assessment of flavored probiotic acidophilus milk. J Anim Plant Sci. 2013;23:1342–6.Google Scholar
  47. Gratz S, Täubel M, Juvonen RO, Viluksela M, Turner PC, Mykkänen H, et al. Lactobacillus rhamnosus strain GG modulates intestinal absorption, fecal excretion, and toxicity of aflatoxin B(1) in rats. Appl Environ Microbiol. 2006;72:7398–400.View ArticlePubMedPubMed CentralGoogle Scholar
  48. Rayman MP. The importance of selenium to human health. Lancet. 2000;356:233–41.View ArticlePubMedGoogle Scholar
  49. Agerholm-Larsen L, Raben A, Haulrik N, Hansen AS, Manders M, Astrup A. Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur J Clin Nutr. 2000;54:288–97.View ArticlePubMedGoogle Scholar
  50. Pereira DI, Gibson GR. Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol. 2002;68:4689–93.View ArticlePubMedPubMed CentralGoogle Scholar
  51. Debski B, Zachara B, Wasowicz W. Attempts to evaluate selenium level in Poland and its effect on human and animal health. Folia Universitas Agriculturae Stetinensis Zootechnica. 2001;224:31–8.Google Scholar
  52. Lin MY, Yen CL. Antioxidative ability of lactic acid bacteria. J Agric Food Chem. 1999;47:1460–6.View ArticlePubMedGoogle Scholar
  53. Kiessling G, Schneider J, Jahreis G. Long-term consumption of fermented dairy products over 6 months increases HDL cholesterol. Eur J Clin Nutr. 2002;56:843–9.View ArticlePubMedGoogle Scholar
  54. Chang I, Kim JD. Inhibition of aflatoxin production of Aspergillus flavus by Lactobacillus casei. Mycobiology. 2007;35:76–81.View ArticlePubMedPubMed CentralGoogle Scholar
  55. Gerbaldo GA, Barberis C, Pascual L, Dalcero A, Barberis L. Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiol Lett. 2012;332:27–33.View ArticlePubMedGoogle Scholar
  56. Akhtar MS, Farooq AA, Mushtaq M. Serum concentrations of copper, iron, zinc and selenium in cyclic and anoestrus Nili-Ravi buffaloes kept under farm conditions. Pak Vet J. 2009;29:47–8.Google Scholar
  57. Wild CP, Hall AJ. Primary prevention of hepatocellular carcinoma in developing countries. Mutat Res. 2000;462:381–93.View ArticlePubMedGoogle Scholar
  58. Diaz DE. A review on the use of mycotoxin sequestering agents in agricultural livestock production. In: Siantar DP, Trucksess MW, Scott PM, editors. Food contaminants: mycotoxins and food allergens. Washington: American Chemical Society; 2008. p. 125–50.View ArticleGoogle Scholar
  59. Rastogi R, Srivastava AK, Rastogi AK. Long term effect of aflatoxin B(1) on lipid peroxidation in rat liver and kidney: effect of picroliv and silymarin. Phytother Res. 2001;15:307–10.View ArticlePubMedGoogle Scholar
  60. Carvajal M. Aflatoxin-DNA adducts as biomarkers of cancer: nature, formation, kinds of AF-DNA adducts, methodology, effects and control. In: Siantar DP, Trucksess MW, Scott PM, editors. Food contaminants: mycotoxins and food allergens. Washington: American Chemical Society; 2000. p. 13–55.Google Scholar
  61. Adawi D, Ahrne S, Molin G. Effects of different probiotic strains of Lactobacillus and Bifidobacterium on bacterial translocation and liver injury in an acute liver injury model. Int J Food Microbiol. 2001;70:213–20.View ArticlePubMedGoogle Scholar
  62. Mohiuddin S, Reddy MV, Reddy MM, Ramakrishna K. Studies on phagocytic activity and haematological changes in aflatoxicosis in poultry. Indian Vet J. 1986;63:442–5.Google Scholar
  63. Cao Z, Shao B, Xu F, Liu Y, Li Y, Zhu Y. Protective effect of selenium on aflatoxin B1-induced testicular toxicity in mice. Biol Trace Elem Res. 2017;180:233–8.View ArticlePubMedGoogle Scholar
  64. Roy CN, Andrews NC. Anemia of inflammation: the hepcidin link. Curr Opin Hematol. 2005;12(2):107–11.View ArticlePubMedGoogle Scholar
  65. Elsanhoty RM, Salam SA, Ramadan MF, Badr FH. Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control. 2014;43:129–34.View ArticleGoogle Scholar
  66. Mayura K, Abdel-Wahhab MA, McKenzie KS, Sarr AB, Edwards JF, Naguib K, et al. Prevention of maternal and developmental toxicity in rats via dietary inclusion of common aflatoxin sorbents: potential for hidden risks. Toxicol Sci. 1998;41:175–82.View ArticlePubMedGoogle Scholar
  67. Weidenbörner M. Encyclopedia of food mycotoxins. Berlin: Springer; 2001.View ArticleGoogle Scholar
  68. Lakkawar AW, Chattopadhyay SK, Johri TS. Experimental aflatoxin B1 toxicosis in young rabbits-a clinical and patho-anatomical study. Slov Vet Res. 2004;41:73–81.Google Scholar
  69. Hathout AS, Mohamed SR, El-Nekeety AA, Hassan NS, Aly SE, Abdel-Wahhab MA. Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet. Toxicon. 2011;58:179–86.View ArticlePubMedGoogle Scholar
  70. Huang L, Duan C, Zhao Y, Gao L, Niu C, Xu J, et al. Reduction of aflatoxin B(1) toxicity by Lactobacillus plantarum C88: a potential probiotic strain isolated from Chinese traditional fermented food “Tofu”. PLoS ONE. 2017;12:e0170109.View ArticlePubMedPubMed CentralGoogle Scholar

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