REVIEW

Etiological Agents Implicated in Foodborne Illness World Wide

Heeyoung Lee1https://orcid.org/0000-0001-6115-9179, Yohan Yoon2,*https://orcid.org/0000-0002-4561-6218
Author Information & Copyright
1Food Standard Research Center, Korea Food Research Institute, Wanju 55365, Korea
2Department of Food and Nutrient, Sookmyung Women’s University, Seoul 04310, Korea
*Corresponding author : Yohan Yoon, Department of Food and Nutrient, Sookmyung Women’s University, Seoul 04310, Korea, Tel: +82-2-2077-7585, Fax: +82-2-710-9479, E-mail: yyoon@sookmyung.ac.kr

© Korean Society for Food Science of Animal Resources. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Jul 31, 2020 ; Revised: Aug 23, 2020 ; Accepted: Aug 23, 2020

Published Online: Jan 01, 2021

Abstract

This mini review focuses on foodborne illnesses and outbreaks caused by food-producing animals because statistical information of the foodborne illnesses is important in human health and food industry. Contaminated food results in 600 million cases of foodborne diseases and 420,000 deaths worldwide every year. The world population is currently 7.8 billion, and 56 million people die every year; of these, every year, 7.69% of people experience foodborne diseases, and 7.5% of annual deaths (56 million deaths) was died by foodborne illness in the world. A majority of such patients are affected by norovirus and Campylobacter. Listeria monocytogenes is the most fatal. In the United States, except for those caused by Campylobacter, the number of foodborne diseases did not decrease between 1997 and 2017, and cases caused by Toxoplasma gondii are still being reported (9 cases in 2017). The percentage of foodborne illnesses caused by food-producing animals was 10.4%–14.1% between 1999 and 2017 in the United States. In Europe, foodborne illnesses affect 23 million people every year and cause approximately 5,000 deaths. Europe has more Campylobacter- and Salmonella-related cases than in other countries. In Australia, the highest number of cases are due to Campylobacter, followed by Salmonella. In Korea, Escherichia coli followed by norovirus. Campylobacter- and Clostridium perfringens-related cases have been reported in Japan as well. This review suggests that Campylobacter, Salmonella, L. monocytogenes, and E. coli, which are usually isolated from animal-source food products are associated with a high risk of foodborne illnesses.

Keywords: Campylobacter; foodborne illness; norovirus; Listeria monocytogenes; Salmonella

Introduction

Every individual requires nutrients for survival; however, consuming certain types of food could cause diseases and even death in individuals with symptoms of diarrhea, headache, vomiting, nausea, abdominal cramps, etc. Recently, foodborne outbreaks have become more serious owing to globalization and active food trade among countries. One such example is the 2011 Escherichia coli O104:H4 outbreak in Germany, which was spread to other countries like France, Denmark, Sweden, Switzerland, the Netherlands, the United Kingdom, Canada, the Czech Republic, Greece, Luxembourg, Norway, Austria, Poland, Spain, and the United States, causing 2,987 non-hemolytic uremic syndrome (HUS) cases, 855 HUS cases, and 53 deaths (RKI, 2011). Thus, every country has certain food safety and foodborne disease control regulations, although the level of control varies according to the economic conditions.

However, despite these regulations, the number of foodborne illnesses is continuously increasing. Products manufactured from food-producing animals are considered the major cause of bacterial foodborne illnesses (Heredia and García, 2018); the pathogens involved are enterohemorrhagic E. coli, Salmonella, Listeria monocytogenes, Campylobacter, Staphylococcus aureus, etc. This mini review discusses on foodborne illnesses and outbreaks in different regions worldwide caused by consumption of products manufactured from food-producing animals.

The World Health Organization

Food unsafe for consumption causes 600 million cases of foodborne diseases and 420,000 deaths every year, and 56 million people die each year (Ritchie and Roser, 2018; WHO, 2015). This data indicates that 7.69% (600 million) individuals of world populations (7.8 billion) suffer from foodborne diseases every year and 7.5% (420,000 death) of all deaths (56 million) annually are due to foodborne illnesses. This is almost equivalent to 31.1% of annual deaths caused by road traffic accidents (1.35 million) worldwide (WHO, 2020).

Globally, foodborne illnesses caused by bacteria (226,526,634) were more common than those caused by viruses (138,513,782) and parasites (10,284,561) (WHO, 2015). However, norovirus caused the highest annual cases (124,803,946) and 34,929 deaths, indicating that it has a fatality rate of 0.028 (WHO, 2015). Even though norovirus infects people by consumption of vegetables, fruits, and raw oysters, there were also norovirus outbreaks related to processed meat (Boxman et al., 2007; Malek et al., 2009). Hence, norovirus should be considered a risk microorganism in meat products. Hepatitis A virus causes 13,709,836 cases and 27,731 deaths with 0.202 of fatality rate (WHO, 2015). This result suggests that viruses are also high-risk microorganisms, infecting humans by the consumption of meat products. Among bacteria, Campylobacter caused the highest annual cases (95,613,970), although with a low fatality rate (0.022), followed by Salmonella (78,707,591) (WHO, 2015). In general, fatality rates due to bacteria were low, except for that due to L. monocytogenes. Although the number of L. monocytogenes-related cases was lower than that caused by other bacteria, the fatality rate (22.41%) was much higher than that caused by other bacteria (WHO, 2015). Campylobacter and L. monocytogenes are usually found in meat and processed animal source food products (Kim et al., 2017).

Regarding parasite-related foodborne illnesses, Toxoplasma gondii-related cases are still high, much higher than those caused by Trichinella. T. gondii causes 10,280,089 cases and 684 deaths annually and infects animals (WHO, 2015); thus, humans can be infected through the consumption of uncooked meat or raw meat.

The United States

In the United States, albeit with a low fatality rate, norovirus causes the highest number of cases; 4 deaths were observed in 2017 (Table 1). Salmonella is the second leading cause, resulting in 3–8 deaths every year (Table 1). Although L. monocytogenes causes fewer cases, the associated fatality rate is higher (3–35 deaths annually; 9.4%–20.8%) than that due to other bacteria (Table 1). The number of foodborne illness cases remained unaltered between 1997 and 2017, except for those caused by Campylobacter (Table 1). The number of Campylobacter-related foodborne outbreaks, particularly due to poultry products, decreased from 483 cases in 1998 to 147 cases in 2017 (Table 1). Regarding hepatitis A virus-related cases, the numbers are low compared to other microorganisms, and the virus generally causes 1 death annually (Table 1). Regarding the parasite T. gondii, there were no cases in 1998, 2002, and 2011, but in 2017, there were 9 cases (Table 1), probably due to the consumption of not fully cooked meat; this parasite mainly infects via pork consumption and is rarely found in pigs from developed countries. However, the 2017 outbreak has indicated that the risk of T. gondii infection through pork consumption may exist.

Table 1. Number of reported foodborne illnesses and deaths in the United States
Hazards 1998 2002 2011 2017
Foodborne illnesses Foodborne deaths Foodborne illnesses Foodborne deaths Foodborne illnesses Foodborne deaths Foodborne illnesses Foodborne deaths
Bacteria Bacillus cereus 213 0 42 0 100 0 341 0
Campylobacter 483 0 350 0 291 0 147 0
Clostridium botulinum 8 0 14 0 11 0 17 2
Clostridium perfringens 1,328 0 2,207 0 667 0 843 0
Pathogenic Escherichia coli 1,613 0 486 2 411 2 562 1
Listeria monocytogenes 105 21 54 8 168 35 32 3
Non-typhoidal Salmonella 2,731 6 4,636 3 3,047 5 3,061 8
Shigella 1,266 0 318 0 40 0 54 0
Staphylococcus aureus 615 0 495 0 113 0 128 0
Yersinia enterocolitica 9 0 13 0 16 1 0 0
Parasites Trichinella 0 0 5 0 2 0 5 0
Toxoplasma gondii NA NA NA NA NA NA 9 0
Virus Hepatitis A 293 1 50 1 7 0 35 1
Norovirus 2,563 0 6,559 0 5,135 0 6,340 4

Adopted from CDC (2014, 2019) with public domain; Lynch et al. (2006) with public domain.

NA, not applicable.

Download Excel Table

The European Union (EU)

In Europe, 23 million people are infected with foodborne illnesses and 5,000 people die due to it every year (WHO, 2015). Norovirus causes the highest number of cases annually (approximately 15 million), followed by Campylobacter (approximately 5 million) (WHO, 2015). Interestingly, in the European Union (EU), the number of Campylobacter-related foodborne illnesses is the highest. Campylobacter is the most commonly reported gastrointestinal disease-causing bacterium in the EU, followed by Salmonella (Table 2). In 2007, the incidence of Campylobacter-related foodborne illnesses was 45.2 cases per 100,000 people, and broiler and fresh poultry meat were identified as the largest sources of infections (ECDC, 2020). The total annual cases of the associated illnesses and deaths increased gradually from 2012 to 2016 (Table 2). In the case of the Salmonella outbreak, 31.1 cases per 100,000 people were reported (ECDC, 2020). The temperature was the most influential factor (ECDC, 2020). In 2012, 2014, and 2016, the number of Salmonella-related cases was 91,034, 88,715, and 94,530, respectively, with a 0.14–0.25 fatality rate, similar to that of Shiga toxin-producing E. coli (Table 2). In the EU, higher fatality rates (15%–17.8%) due to L. monocytogenes have been reported, and the number cases due to Shiga toxin-producing E. coli were between 5,671 and 6,378 with 7–12 deaths (Table 2). The most commonly reported Shiga toxin-producing E. coli serogroup in the EU is O157, although its proportion appears to be decreasing relative to other serogroups (EFSA-ECDC, 2015). Regarding parasite-related foodborne illnesses, Trichinella caused 2 deaths in 2014 (Table 2).

Table 2. Number of foodborne illnesses in the European Union
Hazards Years
2012 2014 2016
Foodborne illnesses Foodborne deaths Fatality rates Foodborne illnesses Foodborne deaths Fatality rates Foodborne illnesses Foodborne deaths Fatality rates
Bacteria Campylobacter 214,268 31 0.03 236,851 25 0.01 246,307 62 0.03
Non-typhoidal Salmonella 91,034 61 0.14 88,715 65 0.15 94,530 128 0.25
Listeria monocytogenes 1,642 198 17.8 2,161 210 15 2,536 247 16.2
Shiga toxin-producing Escherichia coli 5,671 12 0.36 5,955 7 0.20 6,378 10 0.27
Yersinia enterocolitica NA NA NA 6,625 5 0.13 6,861 5 0.11
Parasite Trichinella 301 0 0 319 2 0.84 101 0 0

Adopted from EFSA-ECDC (2014, 2015, 2017) with CC-BY-ND.

NA, not applicable.

Download Excel Table

Korea

Unlike that in the countries reviewed above, in Korea, the pathogen causing the highest number of cases is pathogenic E. coli (1,784–2,754 cases from 2010 to 2018) (Table 3). The second highest number of cases are due to norovirus (Table 3). Besides, the number of S. aureus-related cases decreased from 2010 to 2018 (Table 3). Previously, S. aureus ranked the first or the second in Korea; thus, the Ministry of Food and Drug Safety made serious efforts to control S. aureus. This may have gradually decreased the numbers.

Table 3. Number of foodborne illnesses in Korea
Hazards Years
2010 2012 2014 2016 2018
Bacteria Pathogenic Escherichia coli 1,926 1,844 1,784 2,754 2,715
Non-typhoidal Salmonella 677 147 1,416 354 3,516
Campylobacter 380 639 490 831 453
Staphylococcus aureus 372 35 195 4 52
Clostridium perfringens 171 297 1,689 449 679
Virus Norovirus 1,994 1,665 739 1,187 1,319

Adopted from MFDS (2020) with public domain.

Download Excel Table

Regarding L. monocytogenes, which is a serious problem in other countries, in Korea, no foodborne outbreak had been reported until 2018 (Table 3). However, recalls of processed meat products due to L. monocytogenes contamination are continuously occurring. Thus, the risk of L. monocytogenes-related foodborne illness may increase, which may result in foodborne outbreaks of L. monocytogenes.

Australia

In Australia, Campylobacter caused the highest number of cases, with the number ranging from 15,640 to 15,973 from 2004 to 2012 (OzFoodNet 2005, 2010, 2018). This was followed by Salmonella. The number of L. monocytogenes-related cases increased from 66 to 93 from 2004 to 2012 (OzFoodNet 2005, 2010, 2018). The trend in terms of etiological agents in Australia is very similar to that observed in the EU and the United States. In Korea and Japan, Campylobacter was not an agent, causing the highest number of cases. This is the different one among Korea and Japan, Australia, the EU, and the United States.

Japan

In general, the number of cases, especially those caused by pathogenic E. coli, Salmonella, and S. aureus, decreased between 2000 and 2018 (PSOSJ, 2020). This might be due to the ban on raw beef liver served at a restaurant in 2012. In Japan, norovirus causes the highest number of cases, and the number of cases caused by Campylobacter is also high, ranging from 551 to 2,643 between 2000 and 2018 (PSOSJ, 2020). Unlike that in other countries, in Japan, Clostridium perfringens causes a relatively high number of cases, higher than that caused by Campylobacter in 2018, among others.

Conclusion

In summary, norovirus causes the highest number of foodborne illness cases worldwide, followed by Campylobacter, Salmonella, and L. monocytogenes. The trend observed was mostly similar to the EU, the United States, and Australia. However, in Korea, pathogenic E. coli caused the highest number of cases, and L. monocytogenes was not reported to be as fatal. In Japan, the number of Campylobacter-, norovirus-, and C. perfringens-related cases was high. These data suggest that apart from norovirus, Campylobacter, Salmonella, pathogenic E. coli, and L. monocytogenes, which are generally isolated from food-producing animals, are associated with foodborne illnesses and outbreaks in the world.

Conflict of Interest

The authors declare no potential conflict of interest.

Author Contributions

Conceptualization: Lee H, Yoon Y. Data curation: Lee H. Writing - original draft: Lee H. Writing - review & editing: Lee H, Yoon Y.

Ethics Approval

This article does not require IRB/IACUC approval because there are no human and animal participants.

References

1.

Boxman ILA, Tilburg JJHC, Loeke NAJ, Vennema H, de Boer E, Koopmans M. 2007; An efficient and rapid method for recovery of norovirus from food associated with outbreaks of gastroenteritis. J Food Prot. 70:504-508

2.

Centers for Disease Control and Prevention [CDC]. 2014 Surveillance for foodborne disease outbreaks, United States, 2011, annual report. US Department of Health and Human Services, CDC. Atlanta, GA, USA: .

3.

Centers for Disease Control and Prevention [CDC]. 2019 Surveillance for foodborne disease outbreaks, United States, 2017, annual report. US Department of Health and Human Services, CDC. Atlanta, GA, USA: .

4.

European Centre for Disease Prevention and Control [ECDC]. 2020 Food-borne disease. Available fromhttps://www.ecdc.europa.eu/en/climate-change/climate-change-europe/food-borne-diseasesAccessed at July 1, 2020

5.

European Food Safety Authority-European Centre for Disease Prevention and Control [EFSA-ECDC]. 2014; The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J. 12:3457

6.

European Food Safety Authority-European Centre for Disease Prevention and Control [EFSA-ECDC]. 2015; The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 13:4329

7.

European Food Safety Authority-European Centre for Disease Prevention and Control [EFSA-ECDC]. 2017; The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J. 15:e05077

8.

Heredia N, García S. 2018; Animals as sources of food-borne pathogens: A review. Anim Nutr. 4:250-255

9.

Kim S, Oh H, Lee H, Lee S, Ha J, Lee J, Choi Y, Yoon Y. 2017; Polymer hydrogels formulated with various cross-linkers for food-surface application to control Listeriamonocytogenes. J Food Hyg Saf. 32:443-446

10.

Lynch M, Painter J, Woodruff R, Braden C. 2006; Surveillance for foodborne-disease outbreaks: United States, 1998–2002. MMWR. 55:1-34.

11.

Malek M, Barzilay E, Kramer A, Camp B, Jaykus LA, Escudero A, Derrick G, White P, Gerba C, Higgins C, Vinje J, Glass R, Lynch M, Widdowson MA. 2009; Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clin Infect Dis. 48:31-37

12.

Ministry of Food and Drug Safety [MFDS]. 2020 Food safety Korea-statistics of foodborne illness. Available fromhttps://www.foodsafetykorea.go.kr/portal/healthyfoodlife/foodPoisoningStat.do?menu_no=3724&menu_grp=MENU_NEW02Accessed at July 30, 2020

13.

OzFoodNet. 2005; Reported foodborne illness and gastroenteritis in Australia: Annual report of the OzFoodNet network, 2004. Commun Dis Intell Q Rep. 29:165-192.

14.

OzFoodNet. 2010; Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of the OzFoodNet network, 2009. Commun Dis Intell Q Rep. 34:396-426.

15.

OzFoodNet. 2018; Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of the OzFoodNet network, 2012. Commun Dis Intell. 42:S2209-6051.

16.

Portal Site of Official Statistics of Japan [PSOSJ]. 2020 e-Stat. Available fromhttps://www.e-stat.go.jp/stat-search/files?page=1&toukei=00450191&tstat=000001040259Accessed at July 30, 2020

17.

Ritchie H, Roser M. 2018 Causes of death. Our World in Data. Available fromhttps://ourworldindata.org/causes-of-deathAccessed at July 30, 2020

18.

Robert Koch Institute [RKI]. 2011 Final presentation and evaluation of epidemiological findings in the EHEC O104:H4 outbreak, Germany 2011. RKI. Berlin, Germany: .

19.

World Health Organization [WHO]. 2015 WHO estimates of the global burden of foodborne diseases. Available fromhttps://apps.who.int/iris/bitstream/handle/10665/199350/9789241565165_eng.pdf?sequence=1Access at July 21, 2020

20.

World Health Organization [WHO]. 2020 Global health observatory data repository-Road traffic deaths data by country. Available fromhttps://www.who.int/gho/road_safety/mortality/traffic_deaths_number/en/Accessed at June 28, 2020


Change of publication charge


As day of June 1, 2021 (based on date of article submission), article processing charges (APC) will be applied to papers accepted after peer review as follows:
 

Author APC Remark
Member 1,000,000 KR won First and corresponding authors should pay membership fee to Korean Society for Food Science of Animal Resources.
Non-member in Korea 1,200,000 KR won
Other countries except Korea 500 US $ Affiliation of corresponding author

I don't want to open this window for a day.

Special Issue: 67th ICoMST 2021


The 67th International Congress of Meat Science and Technology (ICoMST) is currently accepting abstracts.

The deadline for submitting abstracts has been extended to April 15th, 2021, and FSAR will apply a 50% publishing fee discount to this special issue.

For more information, please check the website below.

https://www.icomst2021.com/

 


I don't want to open this window for a day.