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Gastroenterology & Hepatology: Open Access

Review Article Volume 8 Issue 3

Thermophilic Campylobacter - Neglected Foodborne Pathogens in Cambodia, Laos and Vietnam

Ngoc Huy Nguyen*,1 Tuan Ngoc Minh Nguyen,2,3,4# Helmut Hotzel,2 Hosny El Adawy,2,5 An Quang Nguyen,1 Hanh Thi Tran,6 Minh Thi Hong Le,7 Herbert Tomaso,2 Heinrich Neubauer,2 Hafez M Hafez4

1Phutho General Hospital, Vietnam
2Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Bacterial Infections and Zoonoses, Germany
3Hung Vuong University, Vietnam
4Institute for Poultry Diseases, Free University Berlin, Germany
5Department of Poultry Disease, Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt
6Biodiversity Conversation and Tropical Disease Research Institute (BioD), Vietnam
7Institute of Marine Biochemistry, Vietnam Academy of Science and Technology, Vietnam

Correspondence: Tuan Ngoc Minh Nguyen, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany

Co-correspondence: Huy Ngoc Nguyen, Phutho General Hospital, Vietnam

Received: November 28, 2017 | Published: December 20, 2017

Citation: Nguyen TNM, Hotzel H, El-Adawy H, Tran HT, Hong Le MT, et al. (2017) Thermophilic Campylobacter - Neglected Foodborne Pathogens in Cambodia, Laos and Vietnam. Gastroenterol Hepatol Open Access 8(3): 00279. DOI: 10.15406/ghoa.2017.08.00279

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Abstract

Thermophilic Campylobacter are the most common bacterial cause of gastroenteritis in humans worldwide. Poultry and poultry products are the main sources for human infections. Epidemiological data concerning campylobacteriosis in Asia are limited. Overall, it is difficult to accurately assess the burden of Campylobacter infections. South-East Asia including Cambodia, Laos and Vietnam is known as a hotspot for emerging diseases. Campylobacteriosis is a problem of public health concern in these countries, hence. Epidemiological data are scarce. This is influenced by the limited number of laboratory facilities and lack of equipment and awareness in physicians and veterinarians resulting in the lack of surveys. This review lists articles and reports on Campylobacter and campylobacteriosis in these developing third world countries. Subjects are prevalence of thermophilic Campylobacter in humans, animals and food and their resistance to several antibiotics.

Keywordscampylobacter, foodborne zoonoses, Cambodia, laos; Vietnam, antibiotic resistance

Highlights

This review gives an overview about articles and reports on Campylobacter and campylobacteriosis in Cambodia, Laos and Vietnam. The knowledge about these objects is limited for the three countries. One topic in the literature is prevalence of thermophilic Campylobacter in humans and their relation to diarrhea. In Vietnam a prevalence rate up to 11% was reported. In Cambodia and Laos it was ever higher. Especially, children under fiveyears of age were affected. Animals and food as source for human infections play an important role. Carriage of Campylobacter by different animal species and contamination rate of meat are generally high and can reach more than 70%. Resistance to antibiotics is of public health concern. High rates of resistance to nalidixic acid, erythromycin, tetracycline and ciprofloxacin were detected reaching sometimes 100% of isolates.

Introduction

Zoonoses are diseases and infections which can be transmitted from animals to humans or vice versa. Over 200 pathogens are recognized as zoonotic agents and classified as foodborne and non-foodborne agents. Zoonotic foodborne pathogens may cause human diseases after uptake of contaminated food or water. Several of these microorganisms can be found in the intestinal tract of healthy food-producing animals e. g. thermophilic Campylobacter species.

Thermophilic Campylobacter species are the most common bacterial cause of gastroenteritis in humans worldwide. Incidence and prevalence of campylobacteriosis have increased in both, developed and developing countries, over the last 10years.1 A dramatic increase in the number of reported cases was recognized in Australia, Europe, and North America. In the United States, an incidence of 14.3 campylobacteriosis cases per 100.000 inhabitants was reported for the period between 1996 and 2012.2 In Quebec, Canada an annual incidence of 35.2 cases per 100,000persons was reported.3 In Europe, Campylobacter has become the most frequently reported bacterial pathogen causing gastrointestinal infections in humans since 2005. In 2013, 214,779 confirmed cases were reported by the member states of the European Union (EU) which correlated with a notification rate of 64.8 per 100,000 inhabitants.4 Hence, the number of fatal cases was very low with 0.05%. Data from African countries are limited and indicate that Campylobacter infections are most prevalent in children. In a study in Malawi, 14% of non-diarrheic children and 28% children with diarrhea were PCR positive for C. jejuni and C. coli.5 C. jejuni and C. coli were also found to be endemic in children in Madagascar and Kenya 6,7. Epidemiological data concerning campylobacteriosis in Asia are limited. A study from China reported that 5% of diarrheic patients were PCR positive for C. jejuni. The highest prevalence was detected in the cohort of children younger than 7years.8 Also in Japan and India Campylobacter infections occur quite frequently.9,10 Overall, it is difficult to accurately assess the burden of Campylobacter infections in Asia owing to insufficient epidemiological data.1

International travel, consumption of undercooked chicken and products thereof, environmental exposure, and direct contact with farm animals were recognized as risk factors for human campylobacteriosis.11 The most important sources of foodborne campylobacteriosis are consumption of contaminated food, especially poultry products, unpasteurized milk and water. Broilers are the main source for thermophilic campylobacters to humans.12 Studies in Switzerland estimated that 71% of human cases were caused by uptake of contaminated chicken meat.13,14 The UK Food Standards Agency found 72.9% of fresh retail chicken Campylobacter positive with nearly 20% being highly contaminated.15 Besides broilers, turkeys and ducks, and also cattle and pigs serve as reservoirs of thermophilic CampylobacterCampylobacter contaminated water was responsible for outbreaks of human campylobacteriosis, but also for transmission within animal populations.1

South-East Asia is known as a hotspot for emerging diseases. Part of the region is former French Indochina including Cambodia (Kingdom of Cambodia), Laos (Lao People´s Democratic Republic) and Vietnam (Socialist Republic of Vietnam) with a shared history since the 19th century. All three countries are developing third world countries suffering the aftermath of the Vietnam War. Campylobacteriosis is a problem of public health concern in these countries, hence. Epidemiological data are scarce. This may be caused by the limited number of laboratory facilities and lack of equipment and awareness in physicians and veterinarians resulting in the lack of surveys. A recent review of foodborne bacterial and parasitic zoonosis in Vietnam summarized a number of studies on thermophilic Campylobacter infections16 but no data on the prevalence of campylobacteriosis are available for Laos and Cambodia.

Therefore, in this review we summarize literature on Campylobacter affecting human and animal populations, their prevalence as foodborne pathogen and the resistance to antibiotics in these countries from 1971 to 2016. We delineate knowledge and capability gaps, which will foster new research and surveillance programs. This will help to tackle the impact on public health that is caused by Campylobacter infections in the respective countries.

Methods and research data

Information presented in this review was collected by searching published studies on database including CABDIRECT, Science Direct, Pubmed and Google with keywords “Campylobacter and Vietnam”, “Campylobacter and Laos”, “Campylobacter and Cambodia”. The searched publications were reviewed and relevant information was retrieved. All Articles or studies provided information on prevalence of thermophilic Campylobacter in humans, animals or food and/or information on antibiotic resistance in these bacteria. All articles and studies were in relation to South-East Asian countries of Cambodia, Laos and/or Vietnam.

Results and discussion

Articles on campylobacter in cambodia, laos and vietnam

Thirty one publications were retrievable in Pubmed and other database concerning Campylobacter in Cambodia, Laos and Vietnam between 1971 and 2016. Nineteen articles were related to Vietnam, 3 articles to Laos and 9 articles to Cambodia. Eleven articles were related to antibiotic resistance but most of the papers dealt with investigations of the prevalence of Campylobacter in humans, animals and food.

Campylobacterin humans

An overview about papers concerning Campylobacter in humans in Vietnam, Laos and Cambodia is given in Table 1. The main source of human campylobacteriosis is the consumption of chicken meat, but meat of other species can also be contaminated with Campylobacter. Identification of thermophilic campylobacters was carried out by cultivation in combination with biochemical methods. Only recently, identification and differentiation by PCR assays was introduced. Detection rates ranged between 0 and 12% depending on country and the method of detection. C. jejuni was detected more often than C. coli. Children under 5years of age are most frequently affected. The risk of infections seems to be correlated with undernutrition, poor hygiene, keeping of animals in the house, manure and wet litter in house yards and contaminated drinking water.17 In Cambodia, 12% of 681human faecal samples were tested positive by PCR assays.18 Rates for Vietnam and Laos were below 5%. In an investigation in children with and without diarrhea in Ho Chi Minh City, Vietnam, 2.2% of stool samples were positive, but in the control group without diarrhea 2.6% samples were also found positive.19 A similar result was reported from Cambodia. In Phnom Penh 4.7% C. jejuni and 1.5% C. coli were detected in diseased children at an age under 5years and 6.2% C. jejuni and 2.4% C. coli in the control group.20 It seems that Campylobacter is widespread in the population, but the mere presence of the bacteria in the gut is not inevitable related to clinical symptoms of campylobacteriosis.

Country

Region

Group

Method

Result

Reference

Vietnam

Red River

1,655 children under 5 years (one year of investigation)

Cultivation

150 C. jejuni and C. coli (43.2%) from 347 cultures isolated from 2,160 cases of diarrhoea

36

Vietnam

Hanoi

83 children under 3 years with persistent diarrhoea

 

No Campylobacter

37

Vietnam

Hanoi

291 children under 5 years with acute diarrhoea (one year of investigation)

Cultivation, enzyme immunoassay

4% Campylobacter positive stool samples

38

Vietnam

Ho Chi Minh City, southern Vietnam

1,309 stool samples of children up to 12 months with diarrhoea

Real-time PCR

152 Campylobacter positive (11.6%)

39

Vietnam

Ho Chi Minh City

1,419 stool samples of children under 5 years with diarrhoea

Cultivation

Campylobacter positive in 293 norovirus positive samples

40

Vietnam

Da Nang

987 U. S. Marines

 

No Campylobacter

41

Vietnam

Ho Chi Minh City

1,419 children with and 609 without diarrhoea over a one- year period

Cultivation

31 Campylobacter sp. in stools of diarrheal cases (2.2%) and 16 in samples without diarrhea (2.6%)

19

Vietnam

Hanoi

636 adults observed for 18 months

Cultivation

0.6 % of stool samples Campylobacter positive

42

Laos

Vientiane

880 patients with diarrhea in an 11 months period

Cultivation

2.4% C. jejuni and 2.0% C. coli

43

Laos

Vientiane

70 patients with diarrhoea in a 13 months period (most of them < 5 years)

Cultivation

2.9% C. jejuni

44

Cambodia

Thai-Cambodian border

65 stool specimen from children younger 2 years

Cultivation, latex agglu-tination test

16% Campylobacter positive

45

Cambodia

Thai-Cambodian border

487 children with diarrhoea under 5 years

Cultivation

107 out of 487 Campylobacter positive (22.0%)

46

Cambodia

Phnom Penh

600 children under 5 years with diarrhea and 578 children without diarrhoea

Cultivation

4.7% C. jejuni and 1.5% C. coli in diseased children; 6.2% C. jejuni and 2.4% C. coli in control group

20

Cambodia

No information

25 C. jejuni from children under 5 years

Multiplex PCR

Detection of capsule type

47

Cambodia

Villages in 3 provinces

681 stool samples

Cultivation, multiplex PCR

No C. detection by cultivation; 12% Campylobacter positive in PCR

17,18

Table 1 Studies concerning presence of thermophilic Campylobacter in humans

In a detailed study from Cambodia, Osbjer et al.,18 could not detect Campylobacter in 681 stool samples by cultivation of frozen samples.18 Hence, 66 C. jejuni and 16 C. coli were identified by multiplex PCR. In the group of children up to 15 years, Campylobacter was detected in 18.8% of the samples whereas only 7% to 8% of those of male and female group over 15years were C. positive. Risk factors for human campylobacteriosis were slaughtering of domestic animals, allowance of animal access to sleeping and food preparation areas and eating of undercooked meat.17

Campylobacterin animals and meat

In an investigation from the Mekong delta, Vietnam, the prevalence of Campylobacter in faeces of chickens, ducks and pigs was reported to be 31.9%, 23.9%, and 53.7%, respectively.21 Similar results were found in Cambodia.18 In 41.3% of swab and faeces samples of chickens, ducks, pigs and cattle Campylobacter was detected by multiplex PCR. 56.1% of chicken and 23.8% of duck samples were positive. 72.2% of pigs but only 5.3% of cattle samples were tested positive for C. jejuni and C. coli, respectively. C. jejuni was the dominant species in chickens and ducks, C. coli was more prevalent in pigs. The low prevalence rate of Campylobacter in cattle (5.3%) was similar to that in buffaloes in Laos i. e. 2%.22 A remarkable difference was observed between cultivation and PCR assays. In contrast to 352 samples that were assessed to be positive by PCR assays (41.3%) only 106 samples were identified as Campylobacter positive by cultivation (12.4%). Cultivation of Campylobacter is difficult at least under field conditions because of their sensitivity to oxygen and changes in temperature.

Contamination rates of poultry products with thermophilic Campylobacter were determined to be between 15% and 35% in Vietnam (Table 2). Schwan, 2010 found 76.0% of swabs of chickens positive for Campylobacter, but none of the investigated meat samples was contaminated.23 In Phnom Penh, Cambodia, was shown that 80.9% of poultry carcasses were contaminated.24 The result was obtained by cultivation of Campylobacter. A lower contamination rate of 35.0% was reported for poultry products from markets in the capital of Cambodia.25 C. jejuni (44.4%), C. coli (36.5%), C. lari (15.9%) and C. upsaliensis (3.2%) were identified among 63 Campylobacter isolates.

Country

Region

Source

Number of Isolates
Method of Investigation

Resistance Rate to

Reference

Vietnam

-

Human

88 isolates;
MIC agar-plate dilution test

NA: 7%
CIP: 7%
AZM: 0%

27

Vietnam

Hanoi

Human

 

CIP: 27%

38

Vietnam

Mekong delta

Chicken

22 C. jejuni and 6 C. coli;
Broth microdilution test

NA: 64% b); 100% c)
ERY: 0%b); 33% c)
CIP: 64% b); 100% c)
GEN: 9% b); 33% c)
STR: 14% b); 50% c)
TET: 68% b); 83% c)

23

Vietnam

Ho Chi Minh City

Chicken

20 chicken neck-skin samples; Disc diffusion test

AMP: 40%
ERY: 25%
NA: 95%
CIP: 95%

51

Vietnam

Mekong delta

Chicken, ducks, pigs

202 Campylobacter isolates
(C. jejuni and C. coli);
Disc diffusion method

ERY: 100%
SXT: 99%
NA: 92%
CIP: 20.8%
CHL: < 10%

21

Vietnam

Ho Chi Minh City

Human

66 Campylobacter isolates from children with diarrhea; 16 isolates from non-diarrheal control;
E-test using disc diffusion

AMP: 26.3%
CIP: 80.0%
CHL: 1.5%
NA: 84.8%
ERY: 7.8%
CIP: 68.7% a)
NA: 62.5% a)
CHL: 18.7% a)

19

Vietnam

Hanoi

Chicken and pig meat

Campylobacter isolates (8 C. jejuni and 1 C. coli);
Broth microdilution test

CIP: 62.5% b)
NA: 87.5% b)
STR: 62.5% b)
TET: 75.0% b)
CHL: 25.0% b)
ERY: 25.0% b)
GEN: 25.0% b)

29

Cambodia

Phnom Penh

Poultry carcasses

139 Campylobacter isolates (C. jejuni, C. coli, C. lari);
Disc diffusion method

CIP: 25.9%
ERY: 4.3%
GEN: 1.4%
NA: 58.3%

24

Cambodia

Phnom Penh

Human

23 C. coli and 64 C. jejuni isolates;
Disc diffusion method

NA: 34% b); 57% c)
ERY: 2% b); 9% c)
CIP: 31% b); 57% c)
AMP: 14% b); 22% c)
GEN: 0% b); 17% c)
SXT: 75% b); 87% c)
TET: 27% b); 44% c)

20

Cambodia

Phnom Penh and peri-urban areas

Poultry, carcasses, environment

63 Campylobacter isolates (C. jejuni; C. coli; C. lari, C. upsaliensis) from markets;
Agar dilution method

CIP: 61.9%
ERY: 22.2%
TET: 50.8%

25

Cambodia

Kampong Thom d)

Cynomolgus monkeys

15 Campylobacter isolates;
Agar dilution method

CIP: 100% b); 100%c)
STR: 0% b); 44% c)
GEN: 0% b); 44% c)
TET: 13% b); 78% c)

26

Table 2 Studies concerning antibiotic resistance of thermophilic Campylobacter of different origin

NA: Nalidixic Acid; CIP: Ciprofloxacin; AZM: Azithromycin; AMP: Ampicillin; ERY: Erythromycin; SXT: Sulfamethoxazole-Trimethoprim; CHL: Chloramphenicol; STR: Streptomycin; TET: Tetracycline; GEN: Gentamicin

Resistance rates of Cambodian campylobacters from chicken to ciprofloxacin reached 90.0% for C. lari isolates and was lower for C. jejuni and C. coli with 60.7% and 52.2%, respectively.25 C. coli (30.4%) showed a higher resistance rate to erythromycin in comparison to C. jejuni (17.9%). Resistance to tetracycline varied around 50% whereupon C. coli showed the highest value (56.5%). Campylobacter isolated from faeces of monkeys were 100% sensitive to erythromycin and chloramphenicol.26 Archawakulathep et al.,30 2014 gave a good overview of perspectives on antimicrobial resistance in livestock and livestock products in ASEAN countries.30

Consequence of finding of fluoroquinolone in imported basa catfish from Vietnam was the stop of sale of 350 tons of seafood in the US by the U. S. Food and Drug Administration (FDA) in 2005.31 Motivation was the emerging of resistance to enrofloxacin in Campylobacter causedby treatment of chickens and turkeys with this antimicrobial agent in poultry production and the risk for human health.

Other topics

Recently, five genomes of Campylobacter jejuni isolates from Vietnam were sequenced. Some of these isolates had a cluster of genes of the type-6 secretion system (T6SS) which play roles in pathogen-pathogen and host-pathogen interactions. T6SS is associated with virulence, cell adhesion and cytotoxicity toward erythrocytes. Using the marker gene hcp (haemolysin co-regulated protein) the T6SS was detected in more than 70 % of Vietnamese human and chicken isolates.32

Another study gave a detailed characterization of Vietnamese Campylobacter isolates.29 Investigations concerning genotyping and antimicrobial resistance of Campylobacter isolates were carried out using flaA typing, MLST and DNA microarray assays. Resistance of Campylobacter to several antibiotics was determined phenotypically and by molecular biological methods. A limitation was the low number of isolates. In a study concerning the regional risks and seasonality in travel-associated campylobacteriosis in East Asia including Cambodia, Laos and Vietnam the risk was estimated to be 386 infections per 100,000 Swedish travelers per year. This is the highest value in the world apart from the Indian subcontinent with 1,253 cases per 100,000 travelers per year.33

In an evaluation study of gastrointestinal pathogens in stool samples from diarrheic patients the usefulness of a multipanel pathogen identification system was shown. It represented a sensitive, specific and easy approach as an alternative to classical detection methods.34

Conclusion

Little information about Campylobacter was reported in the past in the three South East Asian countries of Cambodia, Laos and Vietnam. Often, investigations were related to human infections especially in children of young age in big cities like Hanoi, Vientiane, Phnom Penh or Ho Chi Minh City. Knowledge about the prevalence of Campylobacter in humans and poultry and the antibiotic resistance is much better in Vietnam than in Laos or Cambodia. However, there exist no data about the prevalence of Campylobacter in milk or water sources, although Campylobacter contamination in both could be a risk for humans. Moreover, the common habit of consumption of unpasteurized milk in children under 5year of age underlines the relevance of this potential route of transmission in these countries. However, food safety awareness and concepts are existing.35 Surveillance and collaborative research within the South East Asian countries can clarify the epidemiology of foodborne infections like campylobacteriosis in humans. It can be also important for control of bacterial contamination in livestock and food of animal origin.

Prerequisite of improvement of food safety and as a consequence of human health is the introduction of modern diagnostics. PCR assays are rapid, reliable and comparably cheap, but especially in Laos molecular techniques are practically not in use yet and there is a substantial lack of laboratory infrastructure and equipment in all three countries. An increasing problem is antibiotic resistance in bacteria like Campylobacter. In the EU, antibiotic use of antibiotics as growth promotors in food animals was completely banned several years ago. National monitoring and control programmes for antimicrobial resistance in foodborne pathogens have not been established in ASEAN countries yet.30,36–51 Limited data on the amount of antibiotics used in the farming industry exist, because there is no effective control, policy or regulation. In summary, national surveillance programs and international collaborations are needed to address the substantial gaps in knowledge about the epidemiology of campylobacteriosis in developing countries such as Cambodia, Laos and Vietnam. Establishment of at least one National Reference Laboratory with modern equipment and well trained personnel in each country is recommended.

Acknowledgements

This work was supported by Friedrich-Loeffler-Institut, Institute of Bacterial Infections and Zoonoses, Germany and Vietnam Ministry of Agriculture and Rural Development.

Conflicts of interest

No competing financial interests exist.

Funding

None.

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