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Abstract

Objective:

The present work aimed to investigate the relationship between occupational exposure to airborne molds, serum aflatoxin B₁ (AFB₁), and liver enzymes of workers handling wheat flour.

Methods:

The study included 90 bakers, 100 flour milling workers, and 100 controls with no exposure to flour dust. Workplace aspects such as temperature and relative humidity were measured. Airborne fungi were collected and identified. In all subjects included, the serum levels of AFB₁, serum albumin (Alb), aspartate aminotransferase (AST), alanine aminotransferase (ALT), and alkaline phosphatase (ALP) were measured.

Results:

Air temperature and relative humidity were found to be higher in bakeries than in flour mill sections. Airborne Aspergillus species were isolated in dust particles <8 µm in size. The concentration of Aspergillus flavus and Aspergillus niger were higher in bakeries than in the flour mill sections. They were higher in the grinding section than in other mill sections. The serum AFB₁-Alb adduct and ALP levels were significantly higher in bakers compared to milling workers (p < 0.0001, p = 0.05), respectively. The liver enzymes AST and ALT were significantly higher among milling workers and bakers than controls (p < 0.05, p < 0.0001), respectively. The duration of exposure was significantly correlated with serum AFB₁ in bakers. Moreover, there was significant correlation between serum AFB₁, each of ALT and AST levels in bakers.

Conclusions:

chronic occupational exposure to high concentrations of Aspergillus in workplaces may cause elevations in serum levels of AFB₁ and liver enzymes in workers exposed to flour dust. Hence, worker protection measures should be consistently adopted and enforced at the workplace.

Keywords

Flour milling workers bakers liver enzymes

Introduction

Wheat is one of the world’s most important food crops. Foods made from wheat and its derivatives are a major part of a diet for over a third of the world’s population. They are a very important staple food for North African populations.¹ Egypt is one of the countries with high wheat consumption.²

A wide diversity of fungi were isolated from flour of which Aspergillus and Penicillium were the predominant genera.³ Fusarium, Penicillium, Alternaria, Mucor, and Aspergillus were the common fungal species isolated from Algerian wheat. Wheat products dominated by Aspergillus nigri and Aspergillus flavus species displayed a worldwide distribution, particularly, in subtropical and warm temperate regions.¹

Fungi can produce a wide range of mycotoxins under environmental conditions which are conducive to growth. Aflatoxins are naturally occurring mycotoxins produced by certain fungi, mainly A. flavus and Aspergillus parasiticus. Aflatoxin commonly contaminates crops during production, harvest, and storage processes.^4,5 Aflatoxins B₁ (AFB₁), B₂ (AFB₂), G₁ (AFG₁), and G₂ (AFG₂) are the main aflatoxin types, based on their fluorescence under ultraviolet light and relative chromatographic mobility. Riba et al.¹ found that A. flavus was the predominant species in the analyzed Algerian wheat samples, and they could not isolate any of AFGs producing fungi (A. parasiticus, Aspergillus nomius, Aspergillus bombycis, Aspergillus toxicarius, and Aspergillus arachidicola). A. flavus and A. parasiticus are the main AFB₁ producer species.^1,6 Moreover, A. flavus species dominated in the wheat samples originating from Egypt.^7,8

Selim et al.,⁹ studied the prevalence of aflatoxins in some food products in Egyptian market. They reported the highest prevalence of AFB₁ in nuts and seeds (82%), followed by spices (40%), herbs and medicinal plants (29%), dried vegetables (25%), and cereal grains (21%). The highest mean concentration of AFB₁ was in herb and medicinal plants (49 ppb), followed by cereals (36 ppb), spices (25 ppb), nuts and seeds (24 ppb), and dried vegetables (20 ppb). Mycotoxin exposure occurs in parts of the world where poor methods of food handling and storage are common and where malnutrition is a problem, and few regulations exist to protect exposed population. People are commonly exposed to AFB₁ through consumption of food products contaminated with A. flavus. AFB₁ causes both acute hepatotoxicity and liver carcinoma in exposed humans and animals. Acute and chronic hepatotoxicity from AFB₁ is characterized by periportal hepatocellular necrosis, bile duct injury, and hemorrhage.⁴

Aflatoxin albumin (Alb) adduct in blood reflects exposure over the previous 2–3 months.¹⁰ This Alb adduct is formed following metabolism of aflatoxin in the liver and its level correlates with both dietary aflatoxin exposure and other exposure sources (percutaneous and airborne).^11,12

The adverse health consequences of ingestion of food contaminated with AFB₁ are known, however, relatively few studies are available on the adverse effects of inhalation exposure in occupational settings. Therefore, the objectives of this work were identification of the fungal species present in working environments of wheat flour mills and bakeries and investigation of the effects of occupational exposure to airborne fungi on the serum aflatoxin and liver enzymes among the exposed workers.

Subjects and methods

The study was a cross-sectional comparative study between three groups (milling workers, bakeries, and controls). The work was conducted during the period from August to November 2010.

Ethical approval number (10142) was obtained from the Research Ethics Committee of the National Research Centre, Egypt, before the beginning of the study.

Milling procedure can be summarized into the following steps: In the first step (storage), wheat is delivered to the mill and stored in special stores. In the second step (garbling), wheat is subjected to a cleaning process in order to remove coarse and fine impurities. The grain is separated by size, shape, and weight to prevent breakup of the bran. Conditioning takes place to produce uniform moisture content throughout the grain. After conditioning, different batches of wheat are blended together to make the mix capable of producing the required flour quality. In the third step (grinding), sequence of breaking, grinding, and separating operations are carried out to separate bran and germ from the endosperm and reduce endosperm to uniform particle size (flour). Finally, the fourth step involves packing of different milled products prior to marketing.

The process of baking starts by opening bales of flour. The flour is then poured into a big container. Temperature-controlled water and yeast are added, and a mixer is used to blend the ingredients. The dough is then cut into small balls and left aside on wooden tables to rise. Bakers dust their hands with flour while kneading the loaves. The loaves are then placed in the oven.

None of the bakers and the flour milling workers used personal protective equipment during the different processes of flour handling.

Air sampling

Air sampling was done in the workplace environments from 11 a.m. to 3 p.m. during the working days (6 days/week). Fungal air samples were collected using the two-stage viable cascade impactor sampler (TE-10-160, Tisch Environmental, Cleves, Ohio, USA), separating particles into two size ranges, for example, fine (<8 µm) and coarse (>8 µm). The particles ≥8 µm are usually deposited in the upper respiratory tract and can contribute to allergic rhinitis and asthma; however, particles ≤8 µm can penetrate into the alveoli contributing to allergies. Indoor samples were collected at a height of 1.5 m, the human breathing zone, above the floor level in the middle of the working room. The sampler was operated at the manufacturer recommended flow rate of 28.3 L/min for 2 min. Petri dishes containing malt extract agar (BD BioSciences, Sparks, Maryland, USA) were used to collect fungi.

The petri dishes were incubated at 28°C for 5–7 days, and colonies were counted. Positive hole correction ¹³ was applied to the raw colony-forming unit (CFU) recovered on each plate, then used along with the sampling time and flow rate to calculate the concentration with final concentration expressed as CFUs per cubic meter of air. Fungal isolates were purified and identified by direct observation on the basis of micro- and macro-morphological features, reverse and surface coloration of colonies on Sabouraud dextrose agar, Czapek Dox agar, and malt extract agar.¹⁴

Temperature and relative humidity were measured during the course of the study (SATO; PC-5000 TRH-II Sampler, China).

Subjects

This study included all the flour milling workers (100 workers) from the four sections of one of the biggest flour mills in Helwan District and 90 bakers from 7 different bakery stores located also in Helwan District, Cairo, Egypt. The controls (100 subjects) were not occupationally exposed to wheat dust or other organic dusts. They were matched with the milling workers and the bakers regarding their age, socioeconomic status, dietary habits, and smoking habits. Examined workers and controls who were hepatitis B vrus (HBV) and hepatitis C virus (HCV) positive by laboratory screening were excluded. Therefore, 10 workers and three control subjects did not participate as they were excluded from the start of the study.

Questionnaire

Written informed consent was obtained from all the included subjects and signed by the principal investigator and the participant. The questionnaire contained personal data, smoking habit, residential area, and detailed current and previous occupational history to find out work-related symptoms. Medical history of acute and chronic illness, drug abuse, and personal complaints related to liver and gastrointestinal system were also noted. Dietary habits concerning consumption of bread and other products that might be contaminated with aflatoxins were inquired about. The questionnaire was fulfilled during personal interview.

Examination

General and local abdominal examinations were done for all the included persons.

The blood samples were collected in sterile dry tubes, left to clot for 30 min at 37°C, and then centrifuged at 3000 r/min for 10 min. The separated sera were kept at −20°C for the laboratory investigations.

Screening for HBV and HCV

Hepatitis B surface antigen (HBsAg) was qualitatively detected using one-step HBsAgtest device (package insert) according to method used by Blumberg.¹⁵

HCV was also qualitatively detected using hepatitis C one-step test device (package insert) according to the method used by Choo et al.¹⁶

AFB₁ and serum Alb

Aflatoxin B₁ was firstly extracted using EASI-EXTRACT^® Aflatoxin immune affinity column (Scotland). AFB₁ concentrations of the samples were analyzed by microtiter plate enzyme-linked immunosorbent assay (ELISA) method using RIDASCREEN^® AFB₁ 30/15 ELISA, made in Germany. Serum albumin (Alb) was determined by colorimetric method according to Doumas and Biggs.¹⁷

Liver enzymes

The liver enzymes serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were determined according to the colorimetric method described by Reitman and Frankel¹⁸ using biodiagnostic kits (normal value up to 40 U/mL, 45 U/mL for AST and ALT, respectively). The serum alkaline phosphatase (ALP) was determined according to the colorimetric method described by Belfield and Goldberg¹⁹ using biodiagnostic kits (normal value 20–90 IU/L).

Statistical analysis

Statistical analysis was done through SPSS package version 14. Quantitative data were expressed as mean ± SD. Independent t-test was used for comparisons between two groups. Analysis of variance and the post hoc least significant difference were used for comparisons between more than two groups. The relationships between the different variable were studied through correlation coefficient. The difference was considered significant at p ≤ 0.05 levels.

Results

Air temperature ranged between 38°C and 42°C and relative humidity from 70% to 74% in bakeries. However, air temperature and relative humidity ranged from 30°C to 32°C and from 62% to 66%, respectively, in flour milling sections.

Table 1 shows the concentration and the identification of fungal genera in the size fraction <8 μm. Penicillium was not detected in the bakery stores; however, Penicillium concentrations were the highest in the grinding section and indoors than outdoors. A. flavus and A. niger were higher in bakeries than in the four sections of the flour milling factory. Results showed the highest concentration of A. flavus in the grinding section compared to the other miller sections.

Table 1.

The mean concentrations (CFU/m³) of airborne Penicillium and Aspergillus species in size <8 µm.

		Penicillium	Aspergillus flavus	Aspergillus niger	Other^a Aspergillus species
		CFU/m³	CFU/m³	CFU/m³	CFU/m³
Outdoor		512.8	11.5	153.8	44.9
Bakery stores		–	487.2	256.4	–
FlourMill	Storage	38.5	76.9	76.9	–
	Garbling	102.6	76.8	115.4	19.2
	Grinding	576.9	205.1	19.2	19.2
	Packaging	136.8	21.4	179.5	25.6

^aOther species include Aspergillus parasiticus, Aspergillus tereus and Aspergillus ochraceus.

The AFB₁-Alb levels were significantly higher in bakers compared to both the control subjects and milling workers and in the milling workers compared with the controls. All tested liver enzymes were within the normal range. However, AST and ALT were significantly higher in the milling workers and the bakers comparative to the controls. ALP was statistically significantly higher in the bakers compared with the control subjects and milling workers (Table 2).

Table 2.

Comparison of the AFB₁-Alb levels and the liver enzymes between the milling workers, the bakers, and their controls.

	Controls (100)		Milling workers (100)		Bakers (90)		ANOVA
	Mean	SD	Mean	SD	Mean	SD	p Value
AFB₁-Alb (ng/g)	0.04^a,b	0.008	0.06^c	0.003	0.10	0.01	p < 0.0001
Liver enzymes
AST (U/L)	16.2^a,b	10.9	26.5	8.70	26.0	8.33	p < 0.05
ALT (U/L)	18.2^a,b	7.56	37.5	10.66	37.6	11.14	p < 0.0001
ALP (IU/L)	77.4^b	24.50	76.7 ^c	25.71	90.0	32.11	p = .05

LSD: least significant difference; AFB₁: aflatoxin B₁; Alb: albumin; ANOVA: analysis of variance; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ALP: alkaline phosphatase.

^aAccording to LSD, significant difference between the controls and the milling workers.

^bAccording to LSD, significant difference the controls and the bakers.

^cAccording to LSD, significant difference between the milling workers and the bakers.

Table 3 shows that there was no significant difference in the levels of AFB₁-Alb and liver enzymes between the milling workers in the different sections. In the milling workers, there were no significant relationships between the levels of AFB₁-Alb and liver enzymes and the duration of exposure and between the liver enzymes and the AFB₁-Alb. AFB₁-Alb was significantly correlated with the duration of exposure in the bakers and each of the liver enzymes ALT and AST levels (Table 4).

Table 3.

The difference in the AFB₁-Alb and the liver enzymes levels between the different milling workers in the four sections.

	Storage (19)		Garbling (43)		Grinding (15)		Packaging (23)		ANOVA
	Mean	SD	Mean	SD	Mean	SD	Mean	SD	p Value
AFB₁-Alb (ng/g)	0.06	0.01	0.06	0.01	0.08	0.01	0.06	0.01	NS
Liver enzymes
AST (U/mL)	28.4	2.43	25.3	1.34	25.3	1.06	27.8	1.88	NS
ALT (U/mL)	39.0	2.48	36.5	1.49	36.6	1.99	38.4	2.97	NS
ALP (IU/L)	73.4	3.86	74.4	4.48	90.2	7.11	76.0	4.88	NS

AFB₁: aflatoxin B₁; Alb: albumin; ANOVA: analysis of variance; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ALP: alkaline phosphatase.

Table 4.

Relationships between the duration of exposure and AFB₁-Alb and the liver enzymes levels in the milling workers and the bakers.

	Milling workers (100)		Bakers (90)
	Duration of exposure (years)	AFB₁-Alb (ng/g)	Duration of exposure	AFB₁-Alb (ng/g)
AFB₁-Alb (ng/g)	−0.1	^a	0.4	^a
AFB₁-Alb (ng/g)	NS	^a	p = 0.001	^a
AST (U/mL)	−0.01	0.05	0.1	0.2
AST (U/mL)	NS	NS	NS	p < 0.05
ALT (U/mL)	−0.1	0.1	0.1	0.3
ALT (U/mL)	NS	NS	NS	p < 0.05
ALP (IU/L)	−0.1	0.1	0.1	0.2
ALP (IU/L)	NS	NS	NS	NS

AFB₁: aflatoxin B₁; Alb: albumin; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ALP: alkaline phosphatase; NS: not significant.

^aCannot be calculated.

Discussion

Molds are known to potentially produce mycotoxins. Until recently, human health effect studies for mycotoxin exposure have generally focused on the topic of ingestion. Consumption of mycotoxins has resulted in immunosuppression, mutagenicity, and cancer as well as adverse effects on various organs and systems of the body including kidney and liver, gastrointestinal, nervous, urogenital, and vascular.²⁰ Only a very limited number of studies have been conducted on the role of inhaled mycotoxins and human health.²¹

Workers in the agricultural food industries are at high risk of ingestion, transmucosal absorption, and inhalation of AFB₁ released during product preparation or processing. Riba et al.¹ revealed that A. flavus is the only aflatoxigenic fungus detected in Algerian wheat, and nearly 72% of the A. flavus strains produced AFB₁ ranging from 12.1 µg/g to 234.6 µg/g.

In a previous study, airborne fungal counts in a flour mill in Giza, Egypt, varied from 10³ to 10⁴ CFU/m³. Aspergillus and Penicillium were the predominant fungal types detected in this study.³ Those results are in accordance with our findings.

Moreover, A. flavus was the predominant species in both the bakeries and flour mill and in the grinding section compared to the other mill sections (Table 1). A. flavus has been particularly prevalent in the air of subtropical countries.¹ Climatic conditions markedly influence the prevalence of A. flavus in air.

The results pointed to the significant elevation of the serum levels of AFB₁-Alb in the bakers compared to the milling workers and in the bakers and milling workers compared with their controls. The level of AFB₁-Alb among flour mill grinding workers was nonsignificantly higher compared to the workers from the other mill sections. In this study, the three examined groups were of the same socioeconomic status, living conditions, and dietary habits. Thus, significant elevations of AFB₁-Alb among the workers could be attributed to their occupational exposure to relatively high concentrations of A. flavus detected in bakeries and in the flour mill grinding section.

A. flavus spores were detected at high counts in the air of textile pre-spinning and weaving departments but was not detected in the spinning department. Higher concentrations of AFM₁, the metabolite of AFB₁, were found in the urine samples of the workers in these two departments compared to the workers in the spinning department.²²

A study by Viegas et al.,²³ identified detectable AFB₁ levels in 18 poultry workers in Portugal (59%) from a total of 31 workers. AFB₁ was not detected in the serum sampled from any of the control. They concluded that aflatoxin inhalation poses an occupational risk in workers engaged in poultry production.

Detection of AFB₁-Alb levels in peripheral blood are a reliable indicator of long-term exposure to aflatoxin.¹⁰ Exposure to aflatoxin is known to cause both chronic and acute hepatocellular injury. Elevation in liver enzymes suggests either hepatic parenchymal cell injury (ALT and AST) or biliary tract alterations (ALP).⁴

In this study, all the positive cases for HbsAg and or HCV antibodies were excluded from the study. However, the present results revealed significant elevation in the liver enzymes ALT and AST in the milling workers and bakers compared with their controls and ALP of the bakers was significantly elevated than in the milling workers and controls. This means that hepatic parenchymal cells in the bakers and the milling workers and the biliary tract in the bakers are liable to injury due to their occupational exposures, so those workers should be under periodic follow up.

Wild et al.¹¹ demonstrated a positive association between AF-Alb level and ALT. They concluded that the hepatotoxic effects of aflatoxin could be the direct cause of the increased ALT level of the non-HBV carrier subjects and acts as additional cause in HBV carriers. In this study, significant correlations were found between the duration of exposure and AFB₁-Alb levels and between AFB₁-Alb levels and the liver enzymes ALT and AST among bakers. Nevertheless, the associations between the AFB1-Alb and the liver enzymes ALT and AST were much stronger in bakers than in millers. In this study, the dietary exposure to aflatoxin is considered the same in the workers of the two occupational groups as they lived in the same socioeconomic status and shared nearly the same food habits. Therefore, we suggest that the higher level of AFB₁-Alb in the bakers could be attributed to the much higher level of occupational exposure to Aspergillus in the bakeries than in the millers.

Our results confirm that workers handling flour dust are exposed to AB₁ through inhalation. This represents an additional exposure risk to those subjects than the general population. Literature concerning ingestion exposure is abundant, while studies entailing occupational exposure to aflatoxins are few. Individuals with positive HBsAg and HCV antibodies should not be employed in occupations that carries the risk of exposure to aflatoxins. Both factors may interact to increase the risk of hepatic damage and raise the possibility of developing hepatocellular carcinoma.

It could be concluded that the role of mycotoxins in indoor air and human health still remains controversial. This study was a brief contribution in order to highlight the role of airborne mycotoxins producing fungi on the health of workers handling wheat flour. The chronic occupational exposure to A. flavus in the flour mill and bakery workplaces may cause elevation in the serum levels of AFB₁ and the liver enzymes in workers inhaling flour dust during the different processes. These elevations increased with increasing environmental concentrations of A. flavus. Future studies in other populations are needed.

Thus, wherever there is a problem in the storage or in the processing of wheat and wheat-based feeds that allows fungal growth, the risk of aflatoxin contamination should be taken into account. Methods for controlling aflatoxin are largely preventive, including good agricultural practice, sufficient drying of crops after harvest and good ventilation during handling and processing. In addition, simple protective clothes must be used during the different processes. Studies on the chronic exposure to other toxigenic species are needed. Further studies on workers employed in various occupations imposing exposure to airborne molds are needed in the future. Safe work practices should be followed as no occupational exposure levels for aflatoxins have been established till now.

Footnotes

Acknowledgment

Authors are grateful to the flour mill workers, bakers, and control subjects for their cooperation in this research project. We also appreciate the sincere help and cooperation of the Occupational Safety and Health Teams in both flour mills and bakery stores while conducting this work. Moreover, the authors are greatly grateful to Dr Yousra Saeed, Researcher Assistant, at Air Pollution Department, National Research Centre (NRC) for collecting and identifying the airborne fungi, and to Dr Mohamed Hamshary, Researcher Assistant, Environmental and Occupational Department, NRC for his participation in the medical examination.

Conflict of interest

The authors declared no conflicts of interest.

Funding

This work was funded by the National Research Centre.

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Effects of airborne Aspergillus on serum aflatoxin B1 and liver enzymes in workers handling wheat flour