Foodborne Bacteria in Iran: A 23-year Systematic Review of High-risk Foods

Document Type : Review article

Authors

1 Medical Toxicology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran & Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

2 Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

Abstract

Foodborne diseases are a significant global public health concern due to their high prevalence, mortality, and economic losses. The aim of this study was to conduct a systematic review of identified foodborne pathogens and outbreaks in Iran over the past 23 years to provide an overview of the risk assessment and prevention approaches in the country. Using appropriate keywords and searching major databases, such as ScienceDirect, Scopus, PubMed, Google Scholar, and the Iranian Scientific Knowledge Database, we initially identified 4,740 articles. Finally, 328 articles were selected for evaluation. Among these articles, publications on Salmonella, Staphylococcus aureus, and Listeria were the most numerous. Poultry meat was found to be the main source of major foodborne pathogens in Iran, including Campylobacter (46.21%), Listeria monocytogenes (38.45), Salmonella (24.83%), and Yersinia enterocolitica (16.81%). Given the high prevalence of foodborne bacteria in Iranian foods, it is crucial to implement effective control measures to reduce the risk and burden of foodborne diseases. In particular, poultry meat, which poses a high risk for the occurrence of foodborne diseases in Iran, should be subjected to further risk assessment and control measures throughout the food chain. 

Keywords

Main Subjects

Abbreviations

EWHO: World Health Organization

CDC: Center for Disease Control and Prevention

RTE: Ready-To-Eat

EFSA: European Food Safety Authority

Introduction

Foodborne diseases typically result from the consumption of food or water contaminated with pathogens or their toxins [ 1 ]. These illnesses often present as acute health problems with diverse symptoms, such as gastrointestinal distress (e.g., diarrhea, vomiting, nausea, and abdominal cramps) or neurological symptoms (e.g., headache, paralysis, and paresthesia) [ 2 , 3 ]. The bacterial pathogens most commonly associated with foodborne illness worldwide include Listeria monocytogenes, Escherichia coli O157:H7, Staphylococcus aureus, Salmonella enterica, Bacillus cereus, Vibrio spp., Campylobacter jejuni, and Clostridium perfringens [ 2 , 4 , 5 ]. The food products most frequently implicated in outbreaks include poultry, ground meat, seafood, dairy products, as well as fruits and vegetables [ 6 ].

The food industry faces significant challenges in ensuring the safety and nutritional quality of food products for consumers due to various sources of contamination, such as animals, soil, water, air, and food handlers during production and storage [ 7 , 8 ]. However, the implementation of proper cold preservation methods (e.g., refrigeration and freezing) and appropriate thermal processing of foods can effectively prevent foodborne diseases [ 3 ].

In the contemporary era, regulatory frameworks and directives pertaining to food safety have been fortified and intensified. Nevertheless, foodborne diseases continue to represent a significant threat to global public health and an economic burden, particularly in developing countries [ 9 ]. In its inaugural estimation of the global burden of foodborne diseases in 2015, the WHO attributed 600 million cases of foodborne diseases, 420,000 deaths, and a loss of 33 million years of healthy life worldwide to unsafe food consumption [ 9 ].

In 2018, the United States documented 25,606 cases of foodborne infections, resulting in 5,893 hospitalizations and 120 deaths [ 10 ]. The burden of foodborne diseases is particularly significant in low- and middle-income countries. Identifying the source of contamination and transmission route is of paramount importance for preventing foodborne illnesses and implementing effective interventions in food safety. However, attributing an infection to specific food and identifying foodborne transmission is challenging and requires source attribution methodologies. Consequently, there is a dearth of studies identifying the sources of foodborne infections, particularly in developing countries [ 11 ].

In this study, we aimed to conduct a systematic review of the prevalence of foodborne pathogens in different types of foods in Iran. As a result, we can gain an overview of the role of food in the transmission of infections and emphasize the importance of food safety in controlling foodborne diseases and reducing their health and economic burden on society.  

Materials and Methods

Search strategy

A comprehensive and systematic search was conducted in various databases, including ScienceDirect, Scopus, PubMed, Google Scholar, and local Iranian databases, namely the Iranian Scientific Information Database (www.sid.ir). The literature review was limited to studies published during 2000-2023. The keywords used for searching included "prevalence", "detection", and "identification" in conjunction with terms, such as "food", "Iran", "foodborne pathogen", "food infection", "food poisoning", "food illness", "food disease", "foodborne bacteria", "Campylobacter", "Listeria", "Salmonella", "Helicobacter pylori", "Vibrio", "Clostridium botulinum", "Clostridium difficile", "Clostridium perfringens", "Mycobacterium tuberculosis", "Coxiella burnetii", "Staphylococcus aureus", "Shigella", "Pseudomonas", "Bacillus cereus", "Brucella", and "Yersinia enterocolitica".

Eligibility criteria

This systematic review included articles that focused on the prevalence of foodborne pathogens in any type of food in Iran. Duplicate reports and articles without a clear sample size or other essential data were excluded.

Data extraction

Data collection included extracting information, such as the year of publication, types of foods tested for pathogen contamination, sample size, and number of positive samples contaminated with foodborne pathogens.

Results and Discussion

Results and Discussion

Figure 1 illustrates the study selection process presented in the PRISMA diagram. A systematic literature search using Scopus, ScienceDirect, Google Scholar, SID, Magiran, and cross-references yielded an initial total of 4740 articles. After removing duplicates, 1719 articles remained for title/abstract screening. Following this screening, 655 articles were selected for full-text review. Finally, 328 eligible studies were included in the systematic review.

Figure 1. Flow diagram showing the results of search

1) Salmonella spp. prevalence in food

Salmonella (S.) enterica enterica has more than 2300 serotypes, with S. Enteritidis and S. Typhimurium being the most commonly reported serotypes. Symptoms of salmonellosis include abdominal pain, vomiting, nausea, diarrhea, and fever [ 12 ]. Raw meat, particularly poultry, and egg products, are the main sources of foodborne salmonellosis. Other reported foods that transmit Salmonella to humans include fish, peanuts, unpasteurized juice, and milk. It is important to cook raw foods thoroughly to a safe minimum internal temperature to prevent foodborne salmonellosis, as Salmonella is heat-sensitive. However, processed foods, such as RTE meats and salads can become contaminated through cross-contamination during processing [ 12 ]. In Europe in 2020, 0.15% of RTE food samples and 2.4% of non-RTE food samples were positive for Salmonella [ 13 ].

Table 1 presents the prevalence of Salmonella in different foods in Iran based on our review. The highest levels of contamination were found in poultry meat (23.03%), followed by red meat (14.13%), dairy products (11.66%), RTE foods (11.34%), eggs (9.93%), vegetables (7.8%), fish and shrimp (5.93%), raw milk (3%), and water (2.25%) (Figure 2). In a study conducted in China in 2019, out of 1035 different food samples, a total of 147 samples (14.2%) were positive for Salmonella. In their study, the highest prevalence of Salmonella was found in fresh meat samples (28%), followed by RTE foods (9%), frozen foods (7.1%), and fresh produce (4.5%) [ 14 ]. Fresh meat is a common source of Salmonella contamination due to the nature of its production and processing [ 15 ]. During the slaughter and processing of animals, there is a high risk of cross-contamination with various bacteria, such as Salmonella [ 16 ]. In addition, fresh meat products consumed raw or undercooked increase the risk of foodborne illness [ 17 ]. The handling and storage of fresh meat products can also contribute to Salmonella contamination [ 18 ]. In contrast, RTE foods and frozen foods undergo processing and packaging that can reduce the risk of Salmonella contamination [ 19 ]. However, it is still possible for Salmonella to be introduced during the processing or packaging of these products [ 20 ]. Fresh produce, while less likely to be contaminated with Salmonella compared to fresh meat, can still pose a risk if not properly handled and washed before consumption [ 18 ].

Year Sample type Sample size Positive samples (N) Prevalence (%) Type of Salmonella spp. References City
1 2023 Eggs 40 4 10 Salmonella Enteritidis [ 72 ] Qazvin
2 2023 poultry meat 440 39 9 Salmonella enteritidis and Salmonella typhimurium [ 73 ] Shahrekord
3 2022 Eggs 500 405 81 Salmonella spp. [ 74 ] Lahijan
4 2022 retail raw meat 60 16 26 Salmonella spp. [ 75 ] Urmia
5 2022 poultry products 80 11 13.75 Salmonella spp. [ 76 ] Ardabil
6 2022 Eggs duck 130 21 16.6 Salmonella spp. [ 77 ] Qazvin
7 2022 Chicken meat 150 4 2.7 Salmonella spp. [ 78 ] Zahedan
8 2022 cattle raw milk 100 2 2 Salmonella spp. [ 79 ] Mazandaran
9 2022 Red meat 300 35 11 Salmonella spp. [ 80 ] Shahrekord
10 2021 Chicken meat 100 6 6 Salmonella spp. [ 81 ] Ardabil
11 2021 poultry and egg 3125 250 8 Salmonella spp. [ 82 ] six provinces of Iran
12 2021 chicken meat, beef 450 40 8 Salmonella enterica [ 83 ] Tehran
13 2019 Olivier salad 26 6 23 Salmonella spp. [ 84 ] Mashhad
14 2019 Raw chicken meat 60 29 48.3 Salmonella spp. [ 85 ] Karaj
Egg yolk 30 0 0
15 2019 Eggs (shell & contents) 525 0 0 Salmonella spp. [ 86 ] Isfahan
16 2019 Traditional cheeses 100 0 0 Salmonella spp. [ 87 ] Mohabad
17 2018 Pastry 75 5 6.6 Salmonella spp. [ 88 ] Mashhad
18 2018 Chicken Meat 100 7 7 Salmonella spp. [ 89 ] Mahabad
19 2018 Industrial eggs (shell & contents) 60 0 0 Salmonella spp. [ 90 ] Zanjan
Local eggs shell 60 0 0
Local egg contents 60 2 1.6
20 2018 Industrial eggs (shell & contents) 34 0 0 Salmonella spp. [ 91 ] Sanandaj
Local eggs shell 42 6 4.2
Local egg contents 42 2 4.7
Bulk eggs shell 40 3 7.5
Bulk egg contents 40 0 0
21 2018 Industrial eggs (shell & contents) 60 0 0 Salmonella spp. [ 92 ] Qazvin
22 2018 Shrimp 245 33 13.4 Salmonella spp. [ 93 ] Khuzestan
23 2017 Pizza 90 8 8.8 S. arizonae [ 94 ] Ilam
Frankfurter 90 22 24.4
Sausages 90 19 21.1
24 2017 Camel meat 150 S. Typhimurium [ 95 ] Kohgiluyeh & Boyerahmad/ Isfahan
25 2017 Hamburgers 100 2 2 Salmonella spp. [ 96 ] Kashan
26 2016 Beef meat 190 7 3.6 S. Typhimurium [ 97 ] Gilan
Poultry meat 190 15 7.8 S. Typhimurium
27 2016 Poultry meat 183 52 28.4 S. Typhimurium [ 98 ] Zanjan
28 2016 Industrial Olovier salad 48 0 0 Salmonella spp. [ 99 ] Isfahan
Traditional Olovier salad 54 11 20.4
29 2016 Traditional ice cream 90 62 68.8 Salmonella spp. [ 100 ] Zabol
30 2015 Pastry cream 120 0 0 Salmonella spp. [ 101 ] Arak
31 2015 Olivier salad 50 9 18 S. Ttypimurium [ 102 ] Shahrekord
32 2015 Poultry meat 625 35 5.6 S. Enteritidis [ 103 ] Tehran
Eggs 625 25 4
33 2015 Eggs 50 5 10 S. Enteritidis [ 104 ] Shiraz
34 2015 Native eggs 64 0 0 Salmonella spp. [ 105 ] Yasuj
35 2015 Traditional & Industrial cheese 200 34 17 S. Enteritidis [ 106 ] Shahrekord
11 5.5
36 2015 Eggshells 150 2 1.3 S. Enteritidis [ 107 ] Tabriz
Egg contents 150 0 0
37 2014 Meat Products (Burgers, Sausages, &Kababs, Cutlets) 42 0 0 Salmonella spp [ 108 ] Urmia
38 2014 Unpasteurized cream 100 2 2 S. Paratyphi B [ 109 ] Tehran
39 2014 Chicken 190 86 45 Salmonella spp. [ 110 ] Tehran
Beef meat 189 38 20.2 Salmonella spp.
Beef meat 189 19 10 S. thompson
Chicken 190 65 34.2 S. thompson
40 2014 Chicken meat 200 58 29 Salmonella spp. [ 111 ] Alborz
Liver 120 26 21.6
Heart 120 17 14.1
41 2014 Poultry meat 89 28 31.6 Salmonella spp. [ 112 ] Shahrekord
Beef meat 98 26 26.1
42 2014 Olovier salad 50 9 18 S. Typhimurium [ 112 ] Shahrekord
43 2013 Tap water 144 5 3.4 Salmonella spp. [ 113 ] Isfahan
Bottled mineral water 304 5 1.1
44 2013 Poultry slaughtered 250 7 2.8 S. infantis [ 114 ] Birjand
45 2013 Local eggs 210 14 66.6 Salmonella spp. [ 115 ] Kohgiluyeh & Boyerahmad
46 2013 Industrial egg contents 100 0 0 Salmonella spp. [ 116 ] Talesh
Industrial eggshells 100 19 19
Local egg contents 100 0 0
Local eggshells 100 4 4
Local chicken meat 100 21 21
Industrial chicken meat 100 5 5
Red meat 150 5 3.3
47 2013 Industrial Olovieh salad 200 0 0 Salmonella spp. [ 117 ] Yazd
48 2013 Seafood 384 19 5 Salmonella spp. [ 118 ] Bushehr, Hormozgan, Khuzestan
49 2012 Chicken meat 150 14 9.3 Salmonella spp. [ 119 ] Isfahan & Shahrekord
Turkey meat 105 7 6.7
Ostrich meat 45 1 2.2
50 2012 Beef meat 60 7 11.6 S. Typhimurium [ 120 ] Sanandaj
4 6.6 Salmonella spp.
51 2012 Packed chicken meat 96 19 19.7 Salmonella spp. [ 121 ] Mazandaran
Unpacked chicken meat 104 24 23
52 2012 Salt water fish 70 2 2.9 Salmonella spp. [ 122 ] Ahvaz
Shrimp 70 3 4.3
Shrimp burge 10 1 10
53 2012 Raw cow’s milk 350 14 4 Salmonella spp. [ 123 ] Shahrekord
54 2011 Eggs 100 0 0 Salmonella spp. [ 124 ] Shahrekord
55 2010 Chicken meat 190 86 45 Salmonella spp. [ 125 ] Tehran
Beef meat 189 38 20
56 2010 Turkey meat 144 14 9.7 Salmonella spp. [ 126 ] Isfahan
Ostrich meat 65 3 4.6
Partridge meat 40 0 0
57 2010 Eggshells 250 4 1.6 S. Typhimurium [ 127 ] Mashhad
Egg contents 250 0 0 Salmonella spp.
58 2009 Poultry carcasses 60 5 8.3 Salmonella spp. [ 128 ] Mashhad
60 1 1.6 S. Typhimurium
59 2009 Egg contents 120 0 0 Salmonella spp. [ 129 ] Zanjan
Eggshells 120 68 56.6
Chicken meat 120 104 86.6
60 2009 Chicken meat 67 32 47.7 Salmonella spp. [ 130 ] Tehran
Beef meat 66 19 28.7
61 2009 Local egg contents 500 1 0.2 Salmonella spp. [ 131 ] Birjand
Local eggshells 500 2 0.4
62 2008 Raw poultry 134 24 17.9 Salmonella spp. [ 133 ] Tehran
Cooked poultry 56 3 5.3
Turkey 3 1 33.3
Quail 5 2 40
Red meat 101 8 7.9
Cooked meat 118 2 1.6
Vegetables 38 3 7.8
Fish 15 0 0
Yogurt 32 0 0
Olovieh salad 20 0 0
Hamburger 5 0 0
Mayonnaise souse 8 0 0
63 2008 Poultry carcasses 132 92 69 Salmonella spp. [ 133 ] Tehran
64 2007 Traditional cheeses 200 0 0 Salmonella spp. [ 134 ] Jahrom
65 2007 Liver 145 12 8.1 Salmonella spp. [ 135 ] Yazd
Meat (before chiller) 145 28 18.4
Meat (after chiller) 145 50 34.4
66 2006 Local eggs 500 3 0/6 Salmonella spp. [ 133 ] Birjand
Table 1. Summary of the studies reporting the prevalence of Salmonella spp. in Iran.

Figure 2. Prevalence of Salmonella spp. in different foods in Iran.

2) Staphylococcus aureus prevalence in food

Although Staphylococcus (S.) aureus is the primary causative agent of hospital and community-acquired infections, it has also been associated with foodborne diseases. S. aureus can cause various gastrointestinal illnesses, which are characterized by nausea, vomiting, abdominal cramps, weakness, and diarrhea [ 21 ]. Table 2 presents the findings of studies conducted in Iran regarding the prevalence of this pathogen in different food categories, including seafood (38.51%), meat products (35.47%), dairy products (31.70%), red meat (25.85%), RTE foods (23.59%), raw milk (23.32%), and poultry meat (14.32%) (Figure 3). Seafood and fish are conducive to microbial growth due to their abundant protein and water content. S. aureus is not typically found in the natural microflora of fish, therefore, its presence can indicate poor personal hygiene, new contamination, or potential disease in the fish [ 22 ]. Improper conditions in the fishery, storage, and non-standard transportation provide conditions for pathogens to grow [ 23 ]. Furthermore, the hot climate in Iran can facilitate the growth and proliferation of S. aureus bacteria in food products, such as meat and dairy items, particularly if they are not stored and refrigerated correctly [ 24 ].

Year Sample type Sample size Positive samples (N) Prevalence (%) Area
1 2023 Poultry meat 94 16 17 Shahrekord
2 2023 Sausages and Bologna 100 31 31 Tehran
3 2022 Raw and ready-to-eat green leafy vegetables 366 134 36.6 Tehran
4 2022 Retail raw meat 60 23 39 Urmia
5 2022 Raw Milk And Traditional Dairy 150 23 15.33 Alborz
6 2022 Ready To Eat Food 320 10 3.12 Tehran
7 2022 Raw Milk 380 42 11.05 Alborz
8 2022 Raw Cow Milk 90 35 38.88 Shahrekord
9 2022 Baghlava 112 3 2.67 Qazvin
10 2022 Raw milk 250 46 18.4 Mashhad
11 2021 Cheese, raw and pasteurized milk 100 10 10 -
12 2021 Meat Products 160 26 16.25 Shahrekord
13 2021 Milk and Cheese 200 23 11 Khuzestan
14 2021 Meat retail 90 31 34.5 Zanjan
15 2021 Ready‑to‑eat food 415 64 15.42 Tehran
16 2021 Chicken meat 24 6 25 Tehran
17 2019 Zoolbia & Bamieh 75 21 28 Mashhad
18 2019 Fowl meat 240 22 9.6 Tehran
19 2019 Traditional cheese 100 21 21 Maragheh
20 2018 Traditional cheese 100 45 45 Mahabad
21 2017 Raw foods with animal origin 84 20 23.8 Isfahan
Cooked foods with animal origin 132 12 9
Cooked foods without animal origin 269 15 5.7
22 2017 Season salad 18 0 0 Bandar Abbas
Pasta salad 5 2 40
Lettuce 16 0 0
Shirazi salad 7 0 0
23 2017 Pizza 90 11 12.2 Ilam
Frankfurter 90 25 27.7
Sausages 90 22 24.4
24 2016 Cheese 120 18 41.6 Hamedan
25 2016 Meat 380 78 20.5 Gilan
26 2016 Shrimp 300 84 28 Persian Gulf, Caspian Sea
Fish 300 122 47
27 2016 Red meat 379 36 9.4 Hamadan
Dairy products 671 62 7.2
28 2015 Raw milk 320 88 27.5 Chaharmahal va Bakhtiyari
Dairy products 350 87 24.8
29 2015 Shrimp 300 74 24.6 Persian Gulf, Tehran
30 2015 Raw milk 1930 248 12.8 Mazandaran
Dairy products 720 80 11.1
31 2015 Bovine milk 92 44 47 Maku
Sheep milk 86 32 37
32 2015 Industrial Olivier salad 30 15 50 Shahrekord
Traditional Olivier salad 20 8 40
33 2015 Cheese 80 80 100 Marand
34 2015 Chicken nuggets 420 24 5.7 Isfahan
35 2015 Different food 606 12 1.9 Gilan
36 2014 Cream pastry 450 194 43.3 Gorgan
37 2014 Milk 100 9 9 Tabriz
Cheese 100 45 45
38 2014 Traditional ice cream 30 2 6.7 Yasuj
Olovier salad 4 0 0
Cream suit 30 9 30
39 2014 Raw milk 300 125 41.6 Shahrekord
40 2014 Dairy product 460 127 27.6 Marand
41 2014 Cheese 80 80 100 Tehran, Gilan
42 2014 Doogh 126 86 68 Mazandaran
43 2014 Raw milk 120 49 40.8 Kurdistan
44 2014 Meat products 150 19 12.6 Tonekabon
45 2014 Traditional cheeses 100 16 16 East- Azerbaijan
46 2013 Dairy products 347 20 5.8 Isfahan, Chaharmahal va Bakhtyari, Khuzestan,
47 2013 Industrial Olivier salad 200 40 20 [ 117 ] Yazd
48 2013 Milk 200 22 11 [ 175 ] Fars
49 2012 Traditional white cheese butter 100 26 26 [ 176 ] Tabriz
150 24 16
50 2012 Ground-meat kebab 72 72 100 [ 177 ] Tehran
Bakkhtiyari Kebab 72 72 100
Fish 72 72 100
Salad 72 72 100
51 2012 Seafood products 245 22 8.9 [ 122 ]
52 2012 Packaged hamburger 256 64 25 [ 178 ] Tehran
53 2012 Raw milk 100 50 50 [ 176 ] Urmia
Pasteurized milk 100 2 2
Ice cream 100 26 26
54 2012 Raw milk 348 46 13.2 [ 179 ] Shahrekord
55 2010 Fruit juice 360 32 8.8 [ 180 ] Shahrekord
56 2008 Different food 216 30 55.6 [ 181 ] Tehran
57 2006 Fresh fish 67 15 22.3 [ 182 ] Gilan, Caspian Sea
Table 2.Summary of the studies reporting the prevalence of S. aureus in Iran.

Figure 3. Prevalence of S. aureus in different foods in Iran.

3) Listeria monocytogenes prevalence in food

Listeria (L.) monocytogenes represents a significant public health concern due to its ability to be transmitted from the environment to food, which can lead to foodborne listeriosis in humans [ 25 ]. In 2020, the EFSA reported a total of 1876 cases of listeriosis, with 97.1% of these cases necessitating hospitalization [ 26 ]. Moreover, the EFSA indicated an increase in the case fatality rate and hospitalization rate associated with L. monocytogenes infections in 2020. Among all the reported zoonoses in Europe in 2020, listeriosis had the highest case fatality rate of 13% [ 26 ]. Those at the greatest risk of developing listeriosis include pregnant women, the elderly, newborns, and patients with compromised immune systems [ 27 ]. Moreover, a multitude of food items were identified as potential sources of listeriosis outbreaks during this period. Specifically, 4.8% of RTE meat products and 0.44% of ed with L. monocytogenes [ 26 ]. Table 3 and Figure 4 present the findings of studies conducted in Iran regarding the prevalence of L. monocytogenes in various food types. As illustrated in Figure 4, poultry meat exhibited the highest contamination rate of 38.45%, followed by meat products (14.94%), red meat (13.45%), raw milk (9.77%), dairy products (9.48%), seafood (8.75%), and RTE foods (7.32%) (Figure 4). A previous review study conducted in Iran until 2015 yielded comparable results regarding the contamination of food with Listeria. The highest prevalence of L. monocytogenes was approximately 9.2%, which was observed in RTE foods [ 25 ]. Therefore, RTE foods should be considered a potential hazard to consumers [ 25 ]. Similarly, other developing countries have also yielded comparable results. For example, a study conducted in Ethiopia revealed that 28.4% of raw milk and milk products were contaminated with Listeria spp., with 5.6% of these samples testing positive for L. monocytogenes [ 23 ].

Year Sample type Sample size Positive samples (N) Prevalence (%) Type of Listeria spp. References Area
1 2023 Various Food 900 136 15.1 L. monocytogenes [ 183 ] Mazandaran and Golestan
2 2022 Retail raw meat 60 25 42 L. monocytogenes [ 75 ] Urmia
3 2022 Curd and cheese 150 14 9.33 L. monocytogenes [ 184 ] -
4 2021 Non-Pasteurized Milk 50 30 60 L. monocytogenes [ 185 ] Kerman
5 2021 Traditional cheeses 60 1 1.6 L. monocytogenes [ 186 ] Tehran
6 2021 Raw Milk 100 10 10 Listeria spp. [ 187 ] Tehran
7 2021 Seafood 350 40 11.42 Listeria spp. [ 188 ] Genaveh port
8 2020 Beef and chicken meat 90 45 50 L. monocytogenes [ 189 ] Zanjan
9 2019 Eggs 525 0 0 Listeria spp. [ 86 ] Isfahan
10 2019 Chicken meat retailers 811 257 30.5 Listeria spp. [ 190 ] Mashhad
11 2018 Traditional products dairy 545 64 11.7 Listeria spp. [ 191 ] Yazd
22 4.3 L. monocytogenes
12 2017 Food (sausage, milk, cheese, &chicken and meat) 267 8 2.9 Listeria spp. [ 192 ] Urmia
13 2017 Fresh chicken carcasses 200 80 40 Listeria spp. [ 193 ] Mashhad
14 2016 Dairy products 107 9 8.4 L. monocytogenes [ 194 ] Tehran
Processed meat 210 11 5.2 Karaj
15 2016 Seafood 237 7 2.9 L. monocytogenes [ 195 ] Karaj & Tehran
16 2016 Argyrosomus hololepidotus 240 30 12.5 Listeria spp. [ 196 ] Isfahan & Bandaranzali
5 16.6 L. monocytogenes
17 2015 Koozeh cheeses 100 3 3 L. monocytogenes [ 197 ] Urmia
18 2015 Minced beef 150 4 2.7 Listeria spp. [ 198 ] Ahvaz
1 0.6 Mazandaran
19 2015 Raw fish 488 104 21.3 Listeria spp. [ 199 ] Mazandaran
20 2015 Raw milk 60 0 0 L. monocytogene [ 200 ] Zanjan
21 2015 Traditional dairy products 292 21 19.7 Listeria spp. [ 201 ] Isfahan
22 2015 Raw milk 100 5 5 L. monocytogene [ 202 ] Kerman
23 2014 Ready to eat food (olovier salad, Yogurt stew, macaroni salad and meat salad) 235 20 8.5 Listeria spp. [ 203 ] Shahrekord
24 2014 Meat products 98 12 32.4 L. monocytogene [ 204 ] Qazvin
Milk products 84 25 29.7
25 2014 Bulk milk 260 27 10.4 Listeria spp. [ 205 ] Fars & Khuzestan
7 2.7 Bandar anzali
26 2014 Smoked fish 80 7 8.8 Listeria spp. [ 206 ] Isfahan & Bandar anzali
2 2.5 L. monocytogene
Salted Fish 40 6 15 Listeria spp.
1 2.5 L. monocytogene
27 2013 Meat and meat products 60 8 13.3 Listeria spp. [ 207 ] Khoramabad & Tehran
2 6.6 L. monocytogene
28 2013 Crayfish meat 40 3 7.5 L. monocytogene [ 208 ] Aras
29 2013 Raw cow milk 986 25 2.5 Listeria spp. [ 209 ] Isfahan
20 2 L. monocytogene
30 2013 Vegetables and ready mayonnaise salads 300 26 8.7 Listeria spp. [ 210 ] Tehran
21 7 L. monocytogene
31 2013 Raw seafood products 331 16 4.8 L. monocytogene [ 211 ] Shahrekord
RTE seafoods 321 46 14.5 L. monocytogene
32 2013 Raw milk 446 83 18.6 Listeria spp. [ 212 ] Tehran
33 2013 Dairy products 185 7 3.8 Listeria spp. [ 213 ] Kermanshah
Meat products 187 51 27.2
Ready-to-eat foods 158 8 5.1
34 2013 Seafood 300 24 8 Listeria spp. [ 214 ] Isfahan & Shahrekord
18 6 L. monocytogene
35 2013 Quail products 150 10 6.6 Listeria spp. [ 215 ] Isfahan
1 0.6 L. monocytogene
36 2013 Lamb 200 5 2.5 L.ivanovii [ 216 ] Shahrekord
37 2012 Different types of raw meat 1107 141 12.7 Listeria spp. [ 217 ] Shahrekord, Isfahan, Ahvaz ,Shiraz,Yazd,
27 2.4
38 2012 Poultry product 402 134 33.3 Listeria spp. [ 218 ] Shahrekord
39 2012 Seafood 264 20 7.6 Listeria spp. [ 219 ] Isfahan & Shahrekord
40 2012 Various seafood products 245 2 0.8 L. monocytogene [ 122 ] Different markets of Iran
41 2011 Eggs 100 0 0 L. monocytogene [ 124 ] Shahrekord
42 2011 Fish 194 24 12.3 Listeria spp. [ 220 ] Urmia
5 2.5 L. monocytogene
43 Raw cow milk 45 5 1.1 Listeria spp. [ 221 ] Shiraz
2 4.4 L. monocytogene
Raw goat milk 32 1 3.1 Listeria spp.
1 3.1 L. monocytogene
Traditional cheese 41 10 24.4 Listeria spp.
4 9.7 L. monocytogene
Traditional icecream 60 8 11.7 Listeria spp.
2 3.3 Listeria spp.
44 Raw milk 100 4 4 L. monocytogene [ 222 ]
45 Dairy products 360 6 1.6 L. monocytogene [ 223 ]
46 Chilled ready to eat foods 41 3 7.3 L. monocytogene [ 224 ]
Meat, meat products 332 4 1.2 L. monocytogene
Milk and dairy products 88 0 0 L. monocytogene
47 Cattle carcasses 203 6 3 L. monocytogene [ 225 ]
Table 3.Summary of the studies reporting the prevalence of Listeria spp. in Iran.

Figure 4. Prevalence of Listeria in different foods in Iran.

4) Coxiella burnetii prevalence in food

Coxiella burnetii is a zoonotic pathogen that causes Q fever in humans and coxiellosis in livestock. Cattle, goats, and sheep serve as the primary reservoirs for the pathogen, facilitating its transmission to humans [ 28 ]. The primary routes of human infection are through the inhalation of contaminated aerosols or the consumption of unpasteurized milk and dairy products [ 29 ]. In Europe, 523 cases of Q fever were identified in 2020, resulting in a case fatality rate of 2.1% [ 30 ]. Table 4 presents the results of studies conducted in Iran concerning the prevalence of C. burnetii in different food items. As illustrated in Figure 5, the foods with the highest contamination rates were raw milk (12.36%) and dairy products (6.40%). C. burnetii is a bacterium that causes Q fever, a zoonotic disease that can be transmitted from animals to humans. In numerous rural regions of Iran, milk is still produced and processed using traditional methods that fail to meet the requisite modern hygiene standards [ 31 ]. The absence of adequate hygiene protocols in milk production and processing facilities may result in the contamination of milk with C. burnetii. Moreover, the proximity of animals to humans in the rural areas of Iran contributes to the high levels of contamination of raw milk and dairy products with C. burnetii [ 32 ]. Animals, such as cows and goats, can carry the bacterium and shed it in their milk, which can then be transmitted to humans through consuming contaminated dairy products [ 33 ].

Year Sample type Sample size Positive samples (N) Prevalence (%) References Area
1 2022 Unpasteurized Camel Milk 100 6 6 [ 226 ] Mashhad
2 2022 Kope cheese and cattle milk 800 103 12.87 [ 227 ] West Azerbaijan
3 2021 Raw Milk 162 23 14 [ 228 ] Tehran, Hamadan, and Mazandaran
4 2021 Raw milk 100 27 27 [ 229 ] Mazandaran
5 2020 Raw milk 204 21 10.2 [ 230 ] Gilan
6 2020 Sheep and goats milk 420 51 12.1 [ 231 ] West Azerbaijan
7 2019 Milk 126 44 34.9 [ 232 ] Qom
8 2019 Milk 840 14 16.9 [ 233 ] West Azerbaijan
Cattle milk 14.4
Buffalo milk 19.3
9 2019 Cream & butter 200 6 3 [ 234 ] Shahrekord
Traditional bovine cream, 69 4 5.7
Traditional sheep butter, 20 1 5
Traditional bovine butter 39 1 2.5
10 2018 Raw milk 500 9 1.8 [ 235 ] Khorramabad
Sheep milk 3
Goat milk 6
11 2018 Bulk milk 100 3 3 [ 236 ] Shiraz
12 2018 Non-pasteurized dairy products 238 20 8.4 [ 29 ] Shiraz
13 2018 Raw milk 100 10 10 [ 237 ] Tehran
Traditional unpacked cheese 40 3 7.5
14 2016 Raw sheep milk 72 15 20.8 [ 238 ] Khorramabad
15 2015 Bovine bulk milk 70 12 17.4 [ 239 ] Jahrom
7 10
7 10
16 2015 Individual raw milk 60 7 11.6 [ 200 ] Zanjan
Bovine 38 5 8.3
Ovine 22 2 3.3
17 2015 Cow milk 150 18 12 [ 240 ] Tehran
18 2015 Goat milk 31 5 16.1 [ 241 ] Kerman
19 2015 Cow milk 80 20 25 [ 242 ] Ajabshir
20 2014 Cheese 28 2 7.1 [ 243 ] Mashhad
Yoghurt 26 2 7.6
Sheep milk 23 8 34.7
Cow milk 60 2 3.3
21 2014 Bovine bulk tank 100 5 5 [ 244 ] Mashhad
22 2014 milk 51 21 41.1 [ 245 ] Khoramabad.
23 2013 Goat milk 100 14 14 [ 246 ] Qom
24 2013 Bovine bulk milk 100 11 11 [ 247 ] Jahrom
25 2011 Bovine milk 247 8 3.2 [ 248 ] Kerman
Ovine bulk milk 140 8 5.7
Caprine bulk milk
Camel bulk milk 110 5 4.5
26 2010 Bulk milk 296 6 2 [ 249 ] Fars, Ghom, Kerman, Yazd Khuzestan
27 2010 Cow milk 210 13 6.2 [ 250 ] Chaharmahal va Bakhtiari
Sheep milk 110 0 0
Goat milk 56 1 1.8
Table 4.Summary of the studies reporting the prevalence of C. burnetii in Iran.

Figure 5. Prevalence of C. burnetii in different foods in Iran.

A study conducted in Italy in 2017 reported that 15% of milk samples were contaminated with C. burnetii, with a higher prevalence of contamination in bovine milk (41%) compared to sheep milk (12%) [ 34 ]. In Brazil, in 2020, 9.43% of cheese samples (out of 53 samples) were positive for C. burnetii DNA [ 35 ]. Another research in the United States reported that 94% of bulk milk samples from dairy herds were contaminated with C. burnetii [ 36 ]. Our review indicates that the data from Iran align with the reports from other countries. However, it should be noted that the prevalence of C. burnetii contamination varies depending on the type of dairy products, including specific variations within milk.

5) Bacillus cereus prevalence in food

Bacillus cereus spores are a well-documented contaminant of food that can survive high temperatures during cooking and pasteurization [ 37 ]. This bacterium is associated with two distinct types of gastrointestinal diseases: the emetic (vomiting) syndrome and the diarrheal syndrome [ 38 ]. In Europe, 835 cases of foodborne illness caused by B. cereus were reported in 2020, with a hospitalization rate of 1.2% and a mortality rate of 0.1% [ 30 ]. The diarrheal syndrome is typically attributed to the consumption of contaminated foods, including raw and cooked beef, meat products, fish, poultry, soups, sauces, stews, milk, and vegetables. In contrast, the emetic syndrome is associated with the consumption of a toxic dose of the pre-formed emetic (cereulide) toxin produced by B. cereus in starchy foods, such as rice, pasta, noodles, potatoes, bread, pastries, and sesame products [ 39 ]. Table 5 presents the results of studies conducted in Iran regarding the prevalence of B. cereus in different food items. As illustrated in Figure 6, the highest prevalence of B. cereus contamination was observed in rice (100%), followed by raw milk (48.8%), poultry meat (42.17%), spices (42%), infant food (32.62%), dried vegetables (31.42%), meat products (11.16%), red meat (9.33%), and dairy products (8.9%) (Figure 6). In Australia, B. cereus contamination was identified in a variety of food samples, including uncooked pizza bases (1.58%), cooked pizzas (4.57%), processed meats (0.28%), cooked meat pies (4.45%), cooked sausage rolls (3.26%), and raw diced chicken (5.45%) out of 1,263 retail food samples [ 40 ]. In China, B. cereus contamination was observed in 50% of rice and noodle samples, 34% of cooked meat samples, and 22% of cold vegetable dishes [ 41 ]. In Poland, the highest prevalence of B. cereus contamination was found in herbs and spices, with a rate of 63.3%. Moreover, other food items, including breakfast cereals, pasta, rice, pasteurized milk, infant formulas, as well as fresh and ripening cheeses, were also found to be contaminated with B. cereus [ 37].

Year Sample type Sample size Positive samples (N) Prevalence (%) References Area
1 2023 Various Spices 200 84 42 [ 251 ] Isfahan
2 2020 Individual meat 200 29 14.5 [ 252 ] Zanjan
Raw lamb
Raw beef 60 7 3.5
Cooked beef 60 10 5
80 12 6
3 2020 Traditional dairy products 150 16 10.6 [ 253 ] Tabriz
4 2019 Different rice 10 10 100 [ 254 ] Zanjan
5 2018 Cow‘s raw milk 120 13 10.8 [ 255 ] Tabriz
6 2018 Dried vegetable 140 44 31.4 [ 256 ] Tehran
7 2018 Cream 62 0 0 [ 257 ] Zanjan
8 2017 Different types of beef burgers 80 18 22.5 [ 258 ] Tehran
9 2017 Milk-based infant food 300 9 3 [ 259 ]
10 2017 Powdered infant formula milk 125 84 67.2 [ 260 ]
11 2017 Cow milk 42 41 97.6 [ 261 ]
12 2016 Cheese 200 10 5 [ 262 ]
13 2016 Beef meat and poultry 380 44 11.8 [ 97 ]
14 2016 Dairy products 230 46 20 [ 263 ]
15 2015 Poultry meat foods Frozen 104 80 76.5 [ 264 ] Tehran
Semi cooked 39 9 24.2
Refrigerated 46 26 56.2
16 2014 Rice 408 408 100 [ 265 ] Urmia
17 2013 Infant foods 200 84 42 [ 266 ] Isfahan
18 2012 Kefir type drinks 32 9 28 [ 267 ]
Pasteurized milk 32 12 38
19 2007 Infant formula 60 11 18.3 [ 268 ] Tehran
Table 5.Summary of the studies reporting the prevalence of B. cereus in Iran.

Figure 6. Prevalence of B. cereus in different foods in Iran.

6) Yersinia enterocolitica prevalence in food

In Europe, 236 cases of foodborne yersiniosis were reported in 2020, with 4.7% of cases necessitating hospitalization [ 30 ]. Yersinia enterocolitica contamination has been documented in a variety of foods in Europe, including red meat (beef, pork, and lamb), poultry, seafood, eggs, milk and milk products, bean sprouts, vegetables, tofu, and stewed mushrooms [ 42 ]. Table 6 presents the results of studies conducted in Iran regarding the prevalence of Y. enterocolitica in different food items. As illustrated in Figure 7, poultry meat exhibited the highest contamination rate of 16.81% in Iran. This was followed by raw milk (11.93%), red meat (11.63%), and dairy products (10%) (Figure 7). In Europe, 5.2% of RTE meat was found to be positive for Yersinia in 2020, which is a relatively high and concerning rate [ 30 ]. A study conducted in Argentina in 2019 reported chicken (12.4%) and bovine-originated foods (10.2%) as the most contaminated foods with Y. enterocolitica [ 43 ], which aligns with the findings in Iran. However, the latter study reported a lower prevalence of contamination in dairy products (0.7%) compared to the findings in Iran [ 43 ]. The elevated contamination rates of Y. enterocolitica in poultry meat observed in Iran and Argentina can be attributed to several factors, including the hygiene practices employed during the processing, transportation, and storage of these products [ 44 ]. Poultry meat has been identified as a significant source of Y. enterocolitica contamination due to the presence of the bacterium in the intestinal tracts of birds [ 45 ]. Inappropriate handling and processing of poultry can result in the cross-contamination of the meat with Y. enterocolitica. In addition, raw milk, red meat, and dairy products can serve as reservoirs for Y. enterocolitica if not properly pasteurized or handled [ 46].

Year Sample type Sample size Positive samples (N) Prevalence (%) References Area
1 2022 Raw Milk 360 3 0.83 [ 269 ] Tehran
2 2021 red meat 200 26 13 [ 270 ] Shiraz
3 2021 Bovine Raw Milk 100 33 33 [ 271 ] Mashhad
4 2021 Traditional Cheeses 200 38 19 [ 272 ] Khorasan Razavi and Golestan
5 2020 Raw milk 360 3 0.8 (Soltan Dallal, 2020) Tehran
6 2019 Cheeses 200 38 19 [ 273 ] Khorasan Razavi and Golestan
Raw milk 100 33 33
7 2018 Chicken meat 100 25 25 [ 274 ] Mashhad
8 2018 Raw milk (sheep & goats) 100 9 9 [ 275 ] Shahrekord
9 2018 Turkey meat 300 55 18.3 [ 276 ] Shahrekod
10 2015 Meat 450 56 12.4 [ 277 ] Tehran
Chicken meat 226 35 15.4
Beef meat 224 21 9.3
11 2015 Raw milk 446 19 4.3 [ 278 ] Varamin
12 2014 Dairy products 552 28 5 [ 279 ] Isfahan
13 2014 Raw chicken meat 300 65 21.6 [ 280 ] Shahrekod
14 2014 Unpasteurized cream 100 3 3 [ 281 ] Tehran
15 2013 Chicken meat 720 132 18.3 [ 282 ] Shahrekod
16 2012 Bulk raw milk 354 8 2.6 [ 283 ] Eastern Azerbaijan
Cheeses 200 8 4
17 2012 Chicken meat 200 18 9 [ 121 ] Mazandaran
18 2012 Broiler meat 120 19 15.8 [ 284 ] Tabriz
19 2011 Beef and chicken meat 379 48 12.6 [ 285 ] Tehran
Table 6.Summary of the studies reporting the prevalence of Y. enterocolitica in Iran.

Figure 7. Prevalence of Y. enterocolitica in different foods in Iran.

7) Campylobacter prevalence in food

Campylobacter spp. has been identified as the leading cause of foodborne gastroenteritis in Europe since 2005 [ 30 ]. In addition to acute gastroenteritis, Campylobacter infections can also result in chronic manifestations in humans [ 47 ]. Among the various species within the genus Campylobacter, C. jejuni and C. coli are the most commonly reported causes of Campylobacteriosis in humans [ 48 ]. Table 7 presents the results of studies conducted in Iran regarding the prevalence of Campylobacter in different food items. As illustrated in Figure 8, the most prevalent occurrence of Campylobacter contamination in Iran was observed in poultry meat (46.21%), followed by red meat (40%) and eggs (28.06%). The contamination of dairy products and raw milk was observed in 2.36% and 2.5% of samples, respectively (Figure 8). A study conducted in the United States in 2020 reported that while various broiler products carry the risk of Campylobacter spp. contamination, the highest prevalence of contamination was observed in chicken carcasses [ 49 ]. Similarly, in the European Union, C. jejuni has been identified as the most prevalent species (51%) in broiler meat, followed by C. coli (35.5%) [ 47 ]. Consequently, poultry meat represents the greatest risk of Campylobacter transmission to humans worldwide. The consistent reporting of the highest prevalence of Campylobacter contamination in poultry meat in multiple studies, including those conducted in Iran, the United States, and the European Union, underscores the importance of addressing this issue [ 47 , 49 ]. This finding highlights the necessity of implementing rigorous food safety measures and regulations in the poultry industry to prevent the transmission of Campylobacter to consumers.

Year Sample type Sample size Positive samples (N) Prevalence (%) Campylobacter spp. References Area
1 2023 chicken meat 100 81 81 Campylobacter spp. [ 286 ] Hamedan
2 2023 chicken meat 255 64 25.09 Campylobacter spp [ 287 ] Shahrekord
3 2023 Mushrooms 740 74 10 Campylobacter spp [ 288 ] -
4 2022 poultry meat 380 24 6.25 Campylobacter spp [ 289 ] Shahrekord
5 2022 poultry meat 100 35 35 Campylobacter spp [ 290 ] Tehran
6 2022 raw meat 200 27 13.5 Campylobacter jejuni [ 291 ] -
7 2022 cattle raw milk 100 7 7 Campylobacter jejuni [ 79 ] Mazandaran
8 2021 Poultry Carcasses 370 203 54.8 Campylobacter spp [ 292 ] south of Iran
9 2021 Camels meat 40 5 12.5 Campylobacter spp. [ 293 ] chaharmahal and Bakhtiari
10 2019 poultry meat 328 217 66.7 Campylobacter spp. [ 294 ] Jahrom
11 2019 Industrial chicken meat 1 0.6 Campylobacter spp. [ 295 ] Ahvaz
0 0
Traditional chicken meat 8 16 C. jejuni
3 37.5 Campylobacter spp
Fresh packed chicken meat 0 0 C. jejuni
Campylobacter spp
Beef meat 7 14 Campylobacter spp.
7 100
Mutton meat 12 24 C. jejuni
12 100
Water buffalo meat 50 4 8 Campylobacter spp.
4 100 C. jejuni
12 2019 Packed chicken meat 26 28.9 Campylobacter spp. [ 296 ] Shiraz
13 2016 Red meat 90 21 23 Campylobacter spp. [ 297 ] Zanjan
13 61.9
Chicken-meat 120 33 27.5 C. jejuni
22 66.6 Campylobacter spp.
Eggshells 90 38 31.6 C. jejuni
20 52.6 Campylobacter spp.
14 2015 Chicken wing 96 37 38.5 Campylobacter spp. [ 298 ] Urmia
15 2015 Meat 360 227 63.1 Campylobacter spp. [ 299 ] Mashhad
200 88.1 C. jejuni
16 2015 Raw ovine milk 38 0 0 C. jejuni [ 300 ] Zanjan
Raw bovine milk 22 0 0 C. jejuni
17 2014 Chickens 250 110 44 Campylobacter spp. [ 300 ] Tehran
87 79
18 2013 Pasteurized milk 30 0 0 Campylobacter spp. [ 301 ] Isfahan & Chaharmahal va Bakhtyari
Camel milk 37 0 0
Commercial dairy 290 0 0
Raw cow milk 80 5 6.2 Campylobacter spp.
Raw sheep milk 60 1 1.6 Campylobacter spp.
Raw goat milk 60 2 3.3 Campylobacter spp.
Traditional cheese 60 3 5 Campylobacter spp.
Traditional icecream 35 1 2.8 Campylobacter spp.
Traditional butter 25 1 4 Campylobacter spp.
19 2012 Packed chicken meat 96 29 22.9 Campylobacter spp. [ 121 ] Mazandaran
Unpacked chicken meat 104 31 28.8 Campylobacter spp.
20 2011 Eggs 100 0 0 C. jejuni [ 124 ] Shahrekord
21 2011 Raw bovine milk 120 3 2.5 Campylobacter spp. [ 302 ] Isfahan
22 2011 Chicken 200 94 47 Campylobacter spp. [ 303 ] Shahrekord
91 96.8 C. jejuni
Turkey 49 49 49 Campylobacter spp.
41 83.7 C. jejuni
Quail 33 37 43 Campylobacter spp.
33 89.2 C. jejuni
Partridge 6 6 35.3 Campylobacter spp.
6 100 C. jejuni
Ostrich 21 1 4.8 Campylobacter spp.
1 100 C. jejuni
23 2010 Chicken meat 60 37 61.7 Campylobacter spp. [ 304 ] Ahvaz
35 94.6 C. jejuni
Turkey meat 50 18 83.3 Campylobacter spp.
15 36 C. jejuni
Sheep meat 50 3 6 Campylobacter spp.
1 33.3 C. jejuni
Goat meat 45 17 4.4 Campylobacter spp.
17 100 C. jejuni
24 2010 Raw camel meat 107 1 0.9 Campylobacter spp. [ 305 ] Isfahan & Yazd
0 0 C. jejuni
Beef meat 190 5 2.4 Campylobacter spp.
3 60 C. jejuni
Lamb meat 225 27 12 Campylobacter spp.
23 92 C. jejuni
Goat meat 180 17 9.4 Campylobacter spp.
16 94.1 C. jejuni
25 2008 Raw chicken meat 280 157 56.1 Campylobacter spp. [ 306 ] Isfahan
140 89.2 C. jejuni
Quail meat 248 68 27.4 Campylobacter spp.
53 77.9 C. jejuni
Turkey meat 212 145 68.4 Campylobacter spp.
92 63.4 C. jejuni
Ostrich meat 60 7 11.7 Campylobacter spp.
3 42.9 C. jejuni
Table 7.Summary of the studies reporting the prevalence of Campylobacter spp. in Iran.

Figure 8. Prevalence of Campylobacter in different foods in Iran.

8) Helicobacter pylori prevalence in food

Helicobacter pylori is associated with several digestive diseases, including peptic ulcer, mucosa-associated lymphoid tissue lymphoma, gastritis, and an increased risk of gastric cancer [ 50 ]. It is estimated that approximately 50% of the global population is infected with H. pylori [ 51 ]. The prevalence of H. pylori infection is observed to be higher in developing countries, with rates ranging from 70% to 90%, compared to developed countries, where rates are reported to be 25%-50%. Iran is considered a high-risk region for H. pylori infection due to the high prevalence (60%-90%) among its population [ 52 ]. H. pylori can be found in a variety of animal-derived foods, vegetables, and water sources, which contribute to its transmission [ 50 ]. Table 8 presents the findings of studies conducted in Iran regarding the prevalence of H. pylori in various food items. As illustrated in Figure 9, the highest prevalence of H. pylori in food samples in Iran was observed in RTE foods (25.5%) and vegetables (22.14%), followed by raw milk (16.06%), red meat (15.82%), dairy products (7.93%), meat products (6.26%), and water (3.8%) (Figure 9). In other countries, studies have also identified the presence of H. pylori in a variety of food sources. In Japan, the ureA gene of H. pylori was found in 72.2% of raw milk samples and 55% of pasteurized milk samples [ 53 ]. In Italy, the glmM gene of H. pylori was identified in 34.7% of raw milk samples [ 54 ]. In the United States, H. pylori was detected in 44% of RTE raw tuna meat and 36% of raw chickens using a multiplex PCR assay [ 55 ]. These findings underscore the potential presence of H. pylori in various food sources and the significance of food as a potential route of transmission.

Year Sample type Sample size Positive samples (N) Prevalence (%) References Area
1 2023 Raw Poultry Meat 320 20 6.25 [ 307 ] Shahrekord
2 2020 Red meat 600 52 8.6 [ 308 ] Tehran
3 2018 Traditional dairy products 800 31 3.8 [ 309 ] Isfahan
4 2017 Red meat 220 11 5 [ 310 ] Isfahan
5 2017 Meat 150 11 7.3 [ 311 ] Alborz
Milk 150 24 16
Vegetable 40 5 12.5
6 2016 Cream-candy 50 9 18 [ 312 ] Isfahan
Traditional bread 50 3 6
Sausage 50 0 0
Salami 50 0 0
Hamburger 50 1 2
Soup 50 11 22
Restaurant salad 50 15 30
Falafel 50 3 6
Olivier salad 50 18 36
Chicken nugget 50 0 0
Fruit salad 50 14 28
7 2016 Milk 420 92 21.9 [ 313 ] Shahrekord
Meat 400 105 26.2
8 2016 Meat products 150 11 7.3 [ 314 ] Isfahan
9 2016 Drinking water (total) 120 5 4.2 [ 315 ] Isfahan, Shiraz, Yazd, Shahrekord
110 2 1.8
100 3 3
10 2016 Ready to eat fish 70 2 2.8 [ 316 ] Shiraz
Ham 60 9 15
Chicken sandwich 60 5 8.3
Vegetable sandwich 40 2
Meat sandwich 40 18 5
Minced meat 50 10 45
50 16 20
32
11 2015 Raw milk 210 28 13.3 [ 317 ] Tehran
12 2015 Bovine milk 120 20 16.6 [ 318 ]
Traditional cheese 80 10 [ 318 ]
Traditional cream 40 3 7.5
Total 40 3 [ 319 ]
13 2014 Vegetable and salad 460 44 9.5 [ 319 ] Shahrekord
14 2014 Vegetable and salad 430 59 13.7 [ 320 ] Isfahan
15 2013 Water 200 14 7.2 [ 51 ] Isfahan
16 2012 Milk 447 56 12.5 [ 321 ] Isfahan, Fars, Chaharmahal & Bakhtiari, Khuzestan
Table 8.Summary of the studies reporting the prevalence of H. pylori in Iran.

Figure 9. Prevalence of H. pylori in different foods in Iran.

9) Clostridium prevalence in food

Clostridium botulinum

Clostridium botulinum is a gram-positive, anaerobic bacterium that is capable of producing spores. It is known to cause botulism, a severe illness characterized by the production of a potent neurotoxin. Table 9 presents the findings of research conducted in Iran on the prevalence of C. botulinum in various food items. As illustrated in Figure 10, the most prevalent contamination of C. botulinum in Iran was observed in seafood (12.56%), followed by red meat (12.23%), dairy products (9.02%), and honey (2%) (Figure 10). Honey is recognized as a reservoir for C. botulinum spores, particularly types B and A, and has been implicated in cases of neonatal botulism [ 30 ]. Studies conducted in various countries, including Turkey, Brazil, Denmark, Sweden, and Norway, have demonstrated the presence of C. botulinum spores in honey samples, with prevalence rates ranging from 2% to 26% [ 30 ]. In Iran, the prevalence of C. botulinum contamination in honey samples was reported to be 2% (Figure 10), indicating a relatively lower level of contamination compared to some other regions.

Year Sample type Sample size Positive samples (N) Prevalence (%) Clostridium spp. References Area
1 2023 Meat native birds 300 35 11.6 C. difficile [ 322 ] Shahrekord
2 2022 Meat Nuggets 600 7 1.17 C. difficile [ 323 ] Isfahan
3 2022 Ground Beef 133 24 18.04 C. perfringens [ 324 ] Qazvin
94 3 3.22
4 2022 Raw Meat 240 7 2.91 C. difficile [ 325 ] Mazandaran
5 2022 Raw Beef Meats 133 18 13.53 C. perfringens [ 326 ] Qazvin
6 2021 raw and ready-to-eat green leafy vegetables 366 66 18 C. perfringens [ 139 ] Tehran
7 2019 Olivier Salad 26 0 0 C. perfringens [ 327 ] Mashhad
8 2018 Cattle and sheep carcasses 200 61 30.5 C. perfringens. [ 328 ] Shiraz
9 2017 Broiler chickens 122 95 77.8 C. perfringens [ 329 ] Kerman
10 2017 Broiler chickens 400 169 42.2 C. perfringens [ 330 ] Chaharmahal & Bakhtiari
11 2017 Honey 130 0 0 C. Botulinum [ 331 ]
12 2017 Traditional curds Commercial curds 50 12 25 C. perfringens [ 332 ] Shahrekord
Commercial curds 50 5 10
Beef meat 20 1 6
Lamb meat 23 3 13
13 2015 Broiler meat 200 31 15.5 C. perfringens [ 333 ] Mashhad
14 2015 Minced meat 200 25 12.5 C. perfringens [ 334 ] Mashhad
15 2013 Honey 100 2 2 C. Botulinum [ 335 ] Shiraz
16 2013 Fish 80 4 5 C. Botulinum [ 336 ] Shiraz
Honey 50 2 4
Kashk 80 2 2.5
Dough 80 1 1.2
17 2013 Dairy products 57 12 21 C. Botulinum [ 337 ] Gilan, Tehran, Golestan, Hamedan
Fish 68 18 26.4
Meat 14 1 7.1
18 2010 Cheese 57 2 3.5 C. Botulinum [ 338 ] Gillan
Kashk 11 0 0
Salted fish 63 4 6.3
Table 9.Summary of the studies reporting the prevalence of Clostridium spp. in Iran.

Figure 10. Prevalence of Clostridium in different foods in Iran.

While C. botulinum spores may be present in certain foods, the risk of botulism is contingent upon the conditions that facilitate the germination of spores and toxin production, such as inadequate food processing, storage, or handling. Proper food safety practices, including adequate cooking, storage at appropriate temperatures, and hygienic handling, can help prevent the growth and toxin production of C. botulinum in food.

Clostridium perfringens

C. perfringens is a significant contributor to foodborne gastrointestinal illnesses in both humans and animals. The spores of C. perfringens exhibit remarkable resilience to external influences. In Europe in 2020, there were 682 reported cases of food poisoning caused by C. perfringens toxins, with a hospitalization rate of 1.5%. Conversely, there were fewer cases (n = 34) of food poisoning due to C. botulinum toxins, yet the hospitalization rate for botulism cases was 100%. It is noteworthy that no fatalities were reported in these cases. Early diagnosis, hospitalization, and treatment are essential for reducing the severity of botulism [ 30 ]. Table 9 presents the findings of studies conducted in Iran regarding the prevalence of C. perfringens in various food items. C. perfringens type A is the most prevalent cause of food poisoning associated with this bacterium. The available data indicate that C. perfringens was most commonly isolated from red meat in Iran. It is of paramount importance to ensure that meat is cooked and handled properly to minimize the risk of contamination with C. perfringens and subsequent foodborne illnesses. In Europe in 2019, two outbreaks were associated with pig meat and products, one caused by toxins produced by C. perfringens and the other by C. botulinum. Conversely, vegetables, juices, and other related products were linked to a greater number of outbreaks, with two outbreaks reported for each category during the same period [ 30 ]. Nevertheless, only one study has been conducted in Iran regarding the presence of C. perfringens in vegetables and juices, and other related products. Further research and surveillance are necessary to gain a more comprehensive understanding of the prevalence and sources of C. perfringens in various food items in Iran.

10) Brucella prevalence in food

Brucella spp. are the causative agents of brucellosis [ 56 ], an infectious disease of humans that presents with chronic and recurring febrile symptoms that can be life-threatening [ 57 ]. The primary etiological agent of the disease is B. melitensis, although other species, including B. abortus, B. canis, and B. suis, can also result in human brucellosis [ 58 ]. The infection can be transmitted to humans from various animals, including buffalo, cattle, yak, elk, camel, domestic pig, and rodents [ 58 ]. Globally, approximately 500,000 cases of human brucellosis are reported annually, with animals and animal-derived foods serving as the primary sources of infection [ 57 ]. A global systematic review conducted in 2020 revealed that the Southeast Asia region exhibited the highest prevalence of Brucella spp. at 25.55% [ 57 ]. The consumption of unpasteurized dairy products plays a significant role in the transmission of Brucella spp. to humans [ 57 ]. Table 10 presents the results of studies conducted in Iran on the prevalence of Brucella spp. in food. As illustrated in Figure 11, the primary sources of reported contamination with Brucella spp. are dairy products (34.28%) and raw milk (16.64%). Dairy products, particularly unpasteurized or inadequately pasteurized ones, can serve as reservoirs for Brucella contamination [ 57 ]. This can occur due to infected dairy animals shedding the bacteria in their milk. Raw milk, in particular, has been identified as a common source of Brucella infection in various parts of the world, including Iran. Improper handling and processing of raw milk can contribute to the transmission of Brucella spp. to humans [ 59 ].

Year Sample type Sample size Positive samples (N) Prevalence (%) Brucella spp. References Area
1 2022 Unpasteurized Milk and Dairy 291 12 4.1 Brucella spp. [ 339 ] Hamadan
2 2021 Bovine Milk 240 16 6.66 Brucella spp. [ 340 ] Kurdistan
3 2020 Dairy products 227 9 4 Brucella spp. [ 341 ] Hamadan
Non boiling milk 43 1 2.3
Fresh cheese Cream 21 2 [ 341 ]
4 2019 Raw camel milk 96 3 3 Brucella spp. [ 342 ] Isfahan, Semnan
51 2 [ 342 ]
41 1
5 2018 Dairy Products 208 60 28.8 Brucella spp. [ 58 ] Tehran
Goat raw milk 33 15 45.5
Non-pasteurized cheese 23 9 39.1
Sheep raw milk 33 9 27.3
Cow raw milk 57 15 26.3
Pasteurized cheese 28 7 25
Pasteurized milk 34 5 14.7
6 2017 Dairy Products 14 11 78.6 Brucella spp. [ 343 ] Tehran
8 72.7 B. melitensis
3 27.3 B. abortus
7 2017 Sheep raw milk Goat raw milk 530 43 8.1 Brucella spp. [ 344 ] Kerman
8 2017 Raw milk 700 9 1.28 B.melitensis [ 345 ] Kerman
Sheep’s raw milk 300 3 1
Goats raw milk 400 6 1.5
9 Unpasteurized milk 132 4 3 Brucella spp. [ 346 ] Isfahan
Dairy products 65 1 1.5
10 2016 Cow‘s raw milk 48 4 8.3 Brucella spp. [ 347 ] Kerman
11 2016 Milk 225 20 8.9 B. melitensis [ 348 ] Shahrekord & Isfahan
Sheep milk 125 12 9.6
Goat milk 100 18 18
12 2016 Raw goat milk 470 51 10.8 Brucella spp. [ 344 ] Southeast region of Iran
Raw sheep milk 330 18 5.4
13 2015 Raw milk 60 32 53.3 Brucella spp. [ 200 ] Zanjan
14 2014 Raw cow milk 57 19 33 Brucella spp. [ 349 ] Tehran
Pasteurized cow milk 34 10 29
Pasteurized cheese 28 8 28
Traditional cheese 23 14 60
Raw goat milk 33 21 63
Raw sheep milk 33 19 57
15 2013 Cattle milk 1117 18 1.6 Brucella spp [ 350 ] Urmia
Sheep milk 598 99 16.5
Table 10.Summary of the studies reporting the prevalence of Brucella spp. in Iran.

Figure 11. Prevalence of Brucella in different foods in Iran.

In Iran, where dairy products hold cultural and dietary significance, ensuring the safety of these products from Brucella contamination is crucial for public health [ 60 ]. Implementing stringent control measures in dairy production, processing, and distribution can help mitigate the risk of Brucella transmission through dairy products and raw milk [ 57 , 59 , 60 ].

11) Vibrio prevalence in food

Vibrio spp. are halophilic marine bacteria. Some species, including V. cholerae, V. parahaemolyticus, and V. vulnificus, have the potential to cause gastroenteritis or septicemia in humans. The primary mode of transmission for this foodborne illness is the ingestion of raw, undercooked, or mishandled seafood contaminated by bacteria [ 61 ]. Table 11 presents the results of studies conducted in Iran on the prevalence of Vibrio spp. in different types of food. Vibrio spp. were predominantly detected in seafood, including lobster, fish products, crayfish, fish, and shrimp, as well as drinking water. As illustrated in Figure 12, the prevalence of Vibrio spp. was highest in seafood, with fish exhibiting the greatest incidence (49.33%), followed by lobster (21.53%), crayfish (8.63%), shrimp (8.12%), fish products (7.8%), and drinking water (1.3%) (Figure 12). The findings from Iran are in alignment with those from other countries. For instance, a comprehensive systematic review conducted in 2016 revealed that V. parahaemolyticus contamination was observed in 63.4% of oysters, 52.9% of clams, 51% of fish, and 48.3% of shrimps [ 62 ]. A similar study in China in 2020 reported that 15.34% of shrimp samples, 14.17% of fish samples, and 3.67% of RTE food were contaminated with V. parahaemolyticus [ 63 ]. However, there are no reports available from Iran regarding the prevalence of V. parahaemolyticus in RTE foods.

Year Sample type Sample size Positive samples (N) Prevalence (%) Type of Vibrio spp. References Area
1 2021 Fish 64 61 95 Vibrio species [ 351 ] Isfahan
2 2020 Frozen fish 200 0 0 V. parahaemolyticus [ 352 ] Mazandaran
3 Shrimp 70 12 17.1 V. parahaemolyticus [ 353 ] Zanjan
4 2018 Cold Smoked Salted Fishes 200 46 23 Vibrio spp. [ 354 ] Mazandaran
5 2016 Fish 58 18 31 V. parahaemolyticus [ 355 ] Persian Gulf
Shrimps 55 7 12.7
6 2015 Fresh shrimps 30 2 6.6 V. parahaemolyticus [ 356 ] Genaveh
Salted shrimps 30 2 6.6 seaport
7 2014 Shrimps 36 7 19.4 Vibrio spp. [ 357 ] South coast of Iran
8 2014 Fish 100 22 22 V. parahaemolyticus [ 358 ] Bushehr, Persian Gulf
Lobster 60 13 21.6
Crab caught 40 7 17.5
9 2014 Crayfish 97 11 11.3 V. vulnificus [ 357 ] Aras
7 7.2 V. harveyi
2 2 V. alginolyticus
1 1 V. mimicus
10 2013 Tap-water water 144 3 2 V. cholerae [ 360 ] Isfahan
Bottled mineral 304 3 0.6
11 2012 Fresh shrimp 70 5 7.1 V. parahaemolyticus [ 122 ]
Salted fishes 70 2 2.9
Fish nugget 10 0 0
Shrimp burger 10 0 0
12 2012 Lobsters 100 40 40 Vibrio spp. [ 361 ] Persian Gulf
100 3 3 V. parahaemolyticus
Crab 32 4 12.5 Vibrio spp.
32 1 3.1 V. parahaemolyticus
13 2010 Fresh shrimp 300 29 9.6 V. parahaemolyticus [ 361 ] Bohsher. Hormozgan,Khoozcstan
14 2004 Fresh shrimp 770 16 2.1 Vibrio spp. [ 361 ] Bohsher. Hormozgan, Khoozestan
Table 11.Summary of the studies reporting the prevalence of Vibrio spp. in Iran.

Figure 12. Prevalence of Vibrio in different foods in Iran.

12) Shigella prevalence in food

The Shigella genus encompasses four known species: S. dysenteriae, S. boydii, S. flexneri, and S. sonnei, which have also been classified as subgroups A to D, respectively [ 64 ]. While S. flexneri has traditionally been reported as the main cause of shigellosis in developing countries, recent studies have shown that S. sonnei has become the predominant species of Shigella in Iran [ 64 ]. According to the WHO, Shigella spp. cause approximately 165 million cases of bacillary dysentery and 1 million deaths worldwide each year [ 64 ]. In general, Shigella spp. are among the most prevalent causes of acute diarrhea in Iran, with a particularly high incidence among children and young adults. A diverse array of foods, encompassing meat, dairy products, and vegetables, have been identified as potential sources of shigellosis outbreaks worldwide [ 64 ]. Table 12 presents the results of studies conducted in Iran on the prevalence of Shigella spp. in different types of food. As illustrated in Figure 13, contamination with Shigella spp. is most commonly reported in RTE foods (1.72%) and vegetables (1.05%), followed by red meat (0.4%). In contrast to the data from Iran, a high prevalence of Shigella spp. contamination has been reported in vegetables (25.25%) in India [ 65 ], and in beef, chicken, and dairy products in Egypt [ 66 ]. According to our review, poultry meat should be considered a high-risk food with the potential to spread foodborne zoonoses in Iran. In general, poultry meat is more susceptible to contamination during processing and handling due to its higher water content and pH levels, which provide an optimal environment for the proliferation of bacteria [ 67 ]. Moreover, poultry meat is frequently sold and consumed in its raw state, thereby increasing the probability of contamination if the requisite hygiene standards are not observed during slaughter, processing, and storage. In contrast, red meat and seafood have lower contamination rates compared to poultry meat, likely due to differences in processing and handling practices [ 68 ]. These findings underscore the necessity of developing strategies to reduce the contamination levels of poultry meat to effectively control and prevent foodborne illnesses in Iran.

Year Sample type Sample size Positive samples (N) Prevalence (%) Type of Shigella spp. References Area
1 2022 raw milk, ground meat, and raw vegetable 580 13 2.24 Shigella sonnei [ 364 ] Tehran and Qazvin
2 2021 Vegetable salad, ground meat, and raw cow's milk 405 18 4.44 Shigella spp. [ 365 ] Qazvin
3 2021 meat, vegetable salad and raw milk 165 8 4.84 Shigella spp. [ 366 ] Qazvin
4 2019 Ready to eat food 250 2 0.8 S. sonnei [ 64 ] Isfahan, Fars, Hormozgan, Kohkiloyeh va Boyer Ahmad
0 0 S. dysenteriae
0 0 S. boydii
0 0 S. flexneri
Fresh meat 150 1 0.7 S. sonnei
2 1.3 S. flexneri
0 0 S. dysenteriae
0 0 S. boydii
Frozen meat 150 0 0 Shigella spp.
Cow milk 100 0 0 Shigella spp.
Domestic cheese 100 0 0 Shigella spp.
Vegetables 650 8 1.2 S. sonnei
6 0.9 S. flexneri
0 0 S. dysenteriae
0 0 S. dysenteriae
100 19 1.4 Shigella spp.
5 2018 Ready-to-Eat Salad 90 7 7.8 Shigella spp. [ 367 ] Tehran
6 2018 Food (vegetables, chicken, minced meat, fish) 100 6 6 Shigella spp. [ 368 ] Shiraz
7 2014 Camel milk 18 0 0 Shigella spp. [ 369 ] Golestan
Table 12.Summary of the studies reporting the prevalence of Shigella spp. in Iran.

Figure 13. Prevalence of Shigella in different foods in Iran.

The risk of food contamination, particularly in meat products, is significant. However, to effectively underscore the importance of foodborne diseases, it is imperative to document the consequences of infection with these pathogens and generalize this information to the population in Iran. Currently, foodborne diseases in Iran are not generally reported, leading to a likely gross underestimation of their burden. This underestimation is attributable to the fact that many foodborne illnesses do not exhibit sufficient severity, duration, or specific diagnostic criteria for accurate identification and intervention. Similar circumstances exist in developed countries, such as the United States. For instance, the CDC estimates that foodborne pathogens cause approximately 48 million illnesses, 128,000 hospitalizations, and 3,000 deaths annually in the US [ 70 ].

Therefore, it is crucial to emphasize the necessity of establishing robust monitoring systems in Iran. Such a surveillance network would require the collaboration of multidisciplinary teams comprising medical doctors, veterinarians, microbiologists, public health specialists, and other relevant experts, in alignment with the One Health concept. By adopting a methodology similar to that employed by the CDC's Foodborne Diseases Active Surveillance Network (FoodNet), which monitors the incidence of nine foodborne pathogens in ten US cities, representing approximately 15% of the American population [ 71 ], Iran can enhance the awareness of foodborne disease events and trends. These practices enable the implementation of effective intervention and prevention strategies.

Authors' Contributions

MH suggested the topic and supervised the conduction of the systematic review. SA wrote the first draft of the manuscript. FA and SA performed the literature review. GS was the major contributor in writing the manuscript. AA gave advice for conducting and writing the manuscript. All authors read and approved the final manuscript.

Competing Interests

The authors declare that there is no conflict of interest.

Acknowledgements

It is not applicable

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Iranian Journal of Veterinary Science and Technology
Volume 16, Issue 3 - Serial Number 36
This issue XML files are being prepared.
September 2024
Pages 1-47

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History

  • Receive Date: 17 March 2024
  • Revise Date: 15 July 2024
  • Accept Date: 21 July 2024

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