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Review ArticleOpen Access

Campylobacteriosis: A Global Threat Volume 11 - Issue 5

Muhammad Hanif Mughal*

  • Homeopathic Clinic, Rawalpindi, Islamabad, Pakistan

Received: November 30, 2018;   Published: December 10, 2018

*Corresponding author: Muhammad Hanif Mughal, Homeopathic Clinic, Rawalpindi-Islamabad, Pakistan

DOI: 10.26717/BJSTR.2018.11.002165

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Abstract

Campylobacter species account for most cases of human gastrointestinal infections worldwide. In humans, Campylobacter bacteria cause illness called Campylobacteriosis. It is a common problem in the developing and industrialized world in human population. Campylobacter species extensive research in many developed countries yielded over 7500 peer reviewed articles. In humans, most frequently isolated species had been Campylobacter jejuni, followed by Campylobactercoli (5-18.6 % of all Campylobacter cases), Campylobacterlari, and lastly Campylobacter fetus. C. jejuni colonizes important food animals besides chicken, which also includes cattle. The spread of the disease is allied to a wide range of livestock which include sheep, pigs, birds and turkeys. The organism has been responsible for diarrhoea in an estimated 400 - 500 million people globally each year. The most important Campylobacter species associated with human infections are C. jejuni, C. coli, C. lari and C. upsaliensis. Campylobacter colonize the lower intestinal tract, including the jejunum, ileum, and colon. The main sources of these microorganisms have been traced in unpasteurized milk, contaminated drinking water, raw or uncooked meat; especially poultry meat and contact with animals.

Keywords: Campylobacteriosis; Gasteritis; Campylobacter jejuni; Developing countries; Emerging infections; Climate change

Introduction

Campylobacter cause an illness known as Campylobacteriosis is a common infectious problem of the developing and industrialized world. Campylobacteiosis accounts for most of the cases of human gastrointestinal infections worldwide and extensive research on Campylobacter species yielded over 7500 peer reviewed articles [1]. In humans, the most frequent reported species of Campylobacter had been Campylobacter jejuni (C.jejuni), followed by Campylobacter coli (C. coli), Campylobacter lari (C. lari), and lastly Campylobacter fetus (C. fetus). C. jejuni colonizes in most of the livestock which include sheep, pigs, turkeys etc [2]. In a closely watched study, differences in risk factors between the two species showed that C. coli infection occurs more with drinking bottled water, while C. jejuni is more associated with the tendency in eating habits [3]. Campylobacter can colonize in most of the warm blooded animals, and poultry. The world’s poultry production is colonized by Campylobacter species and these bacterial species have also been isolated from different wildlife i.e. birds, wolves, cats, dogs etc [4,5]. Campylobacteriosis has been responsible for diarrhea in an estimated 400 - 500 million people globally each year and has been identified as zoonotic infection associated with asymptomatic illnesses [6,7]. Annual financial costs for the management of Campylobacteriosis in the US has also swelled up to 1.2 - 4 billion [8]. Campylobacter is small, 0.2-5.0 𝜇m long by 0.2-0.9 𝜇m wide spirally curved, gram’s negative, motile bacteria. The genus Campylobacter comprises of 21 species of which C. jejuni and 12 species of C. coli have been associated with the diseases in over 95% of human’s infections [9, 10].

Transmission of Campylobacter

In last 35 years, world have witnessed emergence of numerous new pathogens that have spread quickly in the communities along with new indications [11,12]. Among them, Campylobacter is one, besides, Legionella, E. coli, Rotavirus and Norovirus. Together they are now one of the leading causes of morbidity in humans. Among Campylobacter species, C. jejuni, C. coli, and C. lari are associated with human infection [13] and C. upsaliensis. It is usually sporadic, but some outbreaks may occur. Campylobacter colonize the lower intestinal tract, including the jejunum, ileum, and colon. In contrast to other enteropathogenic bacteria, Campylobacter possess relatively few virulent factors, and host factors are important in determining the severity of clinical signs that develop. Campylobacter can invade intestinal epithelial cells and produce cytolethal distending toxin, which causes cell cycle arrest and apoptosis. Moreover it is believed that in children, the number of C. jejuni responsible for the illness is even lower than in adults [14].

Campylobacteriosis is normally a self-limiting disease, but in some cases complications may occur, such as GuillainBarr´e (GB) syndrome - a post infectious polyneuropathy, reactive arthritis (1 - 5% of Campylobacter infected patients) with the mortality of 2-7% and Fisher syndrome that can also lead to paralysis as a result of autoimmune damage in 0.01 - 0.03% of Campylobacter enteritis patients [15,16]. Furthermore, it can also trigger an acute respiratory (22-53%) or gastrointestinal (6-26%) infections. Although Campylobacteriosis is quite well considered and accepted as foodborne pathogen but it is also transmitted through contact with colonized animals, contaminated environments by animal waste or poor hygiene. Cross contamination during food manufacturing is considered as an important transmission route [17,18]. C. coli and C. jejuni species have the tendency to be both human and zoonotic pathogens and these microorganisms have been traced in unpasteurized milk, contaminated drinking water, raw or uncooked meat; especially poultry meat along with contact with animals [19].

Campylobacteriosis Prevalence in the Developed World

North America

United States of America: The incidence of reported Campylobacter disease in industrialized countries, like United States, has risen steadily over the past 2 decades with most reported cases being sporadic. In 2013 from five Campylobacter out breaks, mostly outbreaks were associated with raw milk consumption [20]. Moreover, presence of active food borne surveillance system estimates that one out of 30 cases were reported. In March, 2013 CDC reported 14% rise in the incidence of food-borne infections caused by C. jejuni. The data from FoodNet→(2009) indicates that the number of infections by Campylobacter has reached a total of 6,033, or 13 per 100,000 people and it is reported that up to 39% of dogs are carriers of Campylobacter. Interestingly, Campylobacter has also been isolated from free living American crows. If the data from 2013 is compared with 2010-2012, clearly indicates that the incidence for Salmonella decreased, but there is a considerable increase in Campylobacteosis [21]. From 2009-2013, an average of about 105 cases of Campylobacter infection has been reported each year from Alaskawith increase of roughly 50% in recent years compared to older data in the region [22].

Canada

In Canadianterritories, the cases of Campylobacteriosis have been mostly sporadic. Investigations into causative agent lead to identification of improper domestic food preparation. In Ontario (Walkerton, ONT) 2,500 people got sick with Campylobacter gastroenteritis due to cross contaminated of a supply with the thermophilic Campylobacter species (C. jejuni, C. coliand C. lari) [23].

South America

Small, community-based study in Guatemala suggests that Campylobacter is acommon cause of diarrhea in children. In Peru, C. coli and C. jejuni were isolated in highnumbers in both cases and controls,from the urban community [24].

European Countries

In European countries, human Campylobacter infections incidence has continued to increase since last sixyears and is considered as the most common reported zoonotic disease since 2009. The disease has a clear seasonal trend [25]. In all Eurpean Union (EU) countries the prevalence and incidence of Campylobacteriosis has a large variation. In 2011, total of 11 waterborne outbreaks had been documented with Campylobacter and other species in the regionwith an estimated increase of 2.2% cases compared to 2010. Austrian surveillance program on zoonotic bacteria fromfarm animals has revealed as high as 59% Campylobacterspecies positivity in broiler flocks during 2002-2007 [26]. Campylobacter species has been recognized as important pathogens since last 20 years and considered as the most common reported bacterial cause of acute gastroenteritis [27, 28].

In a large study on 33967 infections, from 2000-2006, in Scotland showed that rural children are at greater risk to Campylobacter infection [29]. The survey on Campylobacter infections has shown steady increase in cases since surveillance program began in 1977. In 1999, there has been >60,000 cases with an incidence rate of 103.7 per 100,000. Today incidence of Campylobacteriosis has risen to be 9.3 per 1000 person per years (2008-2009). The financial cost of Campylobacter infection to the nation has been estimated as ÂŁ314.00 million (1994-95 prices). It is estimated that 20 - 40% of sporadic disease might result from eating chicken. In an interesting survey, Campylobacter has been identified in 637 ready to eat pies and 55 other cooked meat products [28]. Italy shows a statistically significant increasing trend since 2008. It has been further estimated that the incidence of true cases are586 per year (per 100,000 inhabitants/years [30]. Number of animal studies has shown the presence of Campylobacter species in Italian peninsula. A survey has demonstratedthe presence of C. jejuni in stray cats with a prevalence of 16.8%, in Southern Italy [31].

Scandinavian Countries

In a telephonic survey it was found that in almost 4000 interviews, 61% have been affected in a Campylobacteriosis out breaking Denmark [32]. Water samples obtained from the community water works contained C. jejunisero type HS:2. In 1999, a legislation has been adopted to reduce the spread and distribution of Campylobacter species in contaminated poultry by freezing to reduce bacterial counts before being supplied to customers. This simple solution resulted in 72% reduction in Campylobacteriosis in following year [10]. Iceland comparable mitigation strategies have been adopted by Norway and Denmark to control the cross contamination and spread of Campylobacteriosis. In Sweden, a study on Campylobacter infections has found association of Campylobacter incidence to average water pipe length per person and ruminant density. In the same study negative association was also reported between the percentage of population receiving water from a public water supply [33,10].

Campylobacteriosis Prevalence in The Developing World

The incidence of Campylobacter in the developing world has been high, as these countries lack sophisticated surveillance systems in line seen in many developed countries making an assessment of true incidence very difficult [34,35]. Even with the development of improved modalities, the true burden of Campylobacteriosis especially in children has seriously been underestimated with recent reports of association between Campylobacter infection with malnutrition. One study showed an alarming high rate of infection of 60,000 per 100,000children < 5 years of age [36]. Poultry specifically has accounted for 50%-70% infection with an increase during summers due to undercooked meat from outdoor cooking facilities [35].

African Countries

Numerous studies have reported that in South Africa, diarrheas by Campylobacter has been clinically less severe than other developing countries. In a relatively large study in Malawi, Campylobacter species had been detected in 415/1,941 (21%) of diarrhea children. Species identification accounted for 85% being C. jejuni. Importantly median age of these children was 11 months. In Botswana, estimates from the prevalence data indicates that Campylobacter diarrheal infection of hospitalized < 5 year children has range as low as 1.5%. In Mozambique it is, 1.7%, 9% in Uganda, 11% in The Central African Republic. Highest rate has been found in Tanzania where it is 18%. Where as, 3.3% in Djibouti and 0.8% in Guinea-Bissau. These low rates may be due to their socioeconomic status but still needs further evaluation [36]. In Africa, from 1993 to 2011, five studies had been conducted to assess the extent of colonizationof chickens and ducks in Tanzania. All studies found to be positivelyassociated to Campylobacter; and specifically to C. jejuni followed by C. coli. Two of these studies also looked at seasonalvariation on human infections and did not found any difference. Previousstudy conducted in the Congo, had reported high prevalence of Campylobacter during the wet season [37].

Middle East

Campylobacter infection ranked among the top three etiological agents of bacterial enteritis in the region. In Jeddah, Saudi Arabia, Campylobacter infection has the second in prevalence to Salmonella with 69% cases being due to C. jejuniand 31% due to C. coli. In Kuwait, Campylobacter ranked third after Salmonella and Enterotoxigenic E. coli [38]. In Israel, Campylobacteriosis is a reportable disease and microbiology laboratories of thecountrysubmithuman isolates from all sources to the National Campylobacter reference Laboratory working under Ministry of Health. Recently a sharp increase in the incidence of Campylobacter species infection was noted with rates tripling withinjust 12 years. These infections have been mostly among children < 2 years of age. During that period, most (>99%) infections were C. jejuni followed by C. coliand remaining < 1% have been identified as C. fetus, C. upsaliensis, C. lari and some unidentified cultures [39].

Antibiotic Resistance

Macrolides are considered the first drug of choice in enteritis from C. jejuni and C. coli while Erythromycin and Ciprofloxacin are the preferred drugs for treatment of human Campylobacteriosis. Genera Campylobacter is recognized as reservoirs for antimicrobial resistance genes that potentially can be exchanged between other pathogenic and other common bacteria [40]. Since last few decades antibiotics have been in use in animal food production for control, prevent, and treatment of infections that enhance growth. This usage has caused an increase in resistance to multiple antibiotics by members of Campylobacter species in food production animals and surrounding environment. The development of antimicrobial resistance in Campylobacter species is a serious threat to human health because of its prevalence in general. The worldwide rapid increase in the proportion of Campylobacter strains resistant to antimicrobial agents has evolved. Campylobacter jejuni and C. coli are almost intrinsically resistant to penicillins, cephalosporins (with exception of a few 3rdgenerationcephalosporins), Trimethoprim, Sulfamethoxazole, Rifampicin and Vancomycin.

For patients infected with Campylobacter species, the prognosis occurs in them without specific treatments other thanreplacement of fluids and electrolytes. It is believed that increasing resistance to fluoroquinolones and Erythromycin by C. jejuni and C. coli might compromise the effectiveness of these treatments. Acquired antimicrobial resistance to macrolides, fluoroquinolones and other antibiotics has given us a challenge in Campylobacteriosis control worldwide [41].

This increasing resistance of Campylobacter to relevant antibiotics; macrolides and fluoroquinolones has become a serious public health concern in developed as well as the developing world. The adverse effects of an infection with quinoloneresistant Campylobacter on severity and extent of infection are the subject of de¬bate [42]. In children suffering from diarrhea in Guatemala; antimicrobial resistance was high, and treatmentregimens in the ambulatory setting were metronidazole and trimethoprimsulfamethoxazole [24]. Korolik et al. [43] reported that human strains collected between 1989-1990and 1994-1995,79-81 strains of C. jejuni and 6-8of C. coli showed resistance to Erythromycin.

Strategies for Control of Campylobacteriosis in Climate Change

Warming trend due to the changes in the global climate is affecting in increase of various important infections and on the other hand the extreme weather conditions lead to outbreaks of clusters of different diseases as a surprise. Most studies indicated about a positive association between temperature and enteric infections such as Salmonella, Campylobacter and Bacillary infections. It is reported that 1°C increase in temperature can increase the risk of severe diarrhea by 5-15% [44]. The food consumption habits due to increase in the cost affected by the climate change also affect food safety protocols (pesticide and chemical residues) resulting in foodborne illness. The increase in cost of food will force more people to shift from expensive but fresh poultry to relatively cheap but frozen chicken that can lead to increase in incidence of Salmonella but on the contrary may lead to less cases of Campylobacterosis [45].

One study has reported that minimizing or complete elimination of animal proteins from the diet and proper sanitization of the water supply has been found effective in preventing the infections [46]. The use of antibiotics are no longer recommended due to high incidence of antibiotic resistant strains which will limit the sensitivity and specificity of the drugs while treating human diseases. However, the use of Pre- and Pro-biotics have been reported to have shown results by some groups and need further evaluation. Interestingly, bacteriocins-producing bacteria (paenibacilluspolymyxma) has shown some interesting results and further researches are required to fully validate these results [47].

Conclusion

More research is required in this field to refine our understanding of the pathophysiology of Campylobacter infections in the developed as well as developing countries. The findings of these few studies indicate a need for increased surveillance and Campylobacter screening both at the slaughter houses and at the sales levels. Collaborative efforts from veterinary and human medicine targeting different aspects of the infections are need of the hour, to allow for efficient and more effective strategies for prevention and/or control of the disease. Thoroughly washing of hands with soap especially before eating or drinking can avoid hand-to-mouth contact, after handling of a companion animal and it can further help in prevention of transmission of the zoonotic disease.

References

  1. Khan IU, Edge TA (2009) Development of a novel triplex PCR assay for the detection and differentiation of thermophilic species of Campylobacter using 16S-23S rDNA internal transcribed spacer (ITS) region. Journal of Applied Microbiology 103(6): 2561-2569.
  2. Mahdavi J, Pirinccioglu N, Oldfield NJ, Carlsohn E, Stoof J, et al. (2014) A novel O-linked glycan modulates Campylobacter jejuni major outer membrane protein-mediated adhesion to human histo-blood group antigens and chicken colonization. Open Biol 4(1): 130202.
  3. Rasschaert G, Houf K, Van Hende J, De Zutter L (2007) Investigation of the concurrent colonization with Campylobacter and Salmonella in poultry flocks and assessment of the sampling site for status determination at slaughter. Vet Microbiol 123(1-3): 104-109.
  4. O Mahony E, Buckley JF, Bolton D, Whyte P, Fanning S (2011) Molecular epidemiology of Campylobacter isolates from poultry production units in southern Ireland. PLoS One 6(12): e28490.
  5. Roux F, Sproston E, Rotariu O, Macrae M, Sheppard, et al. (2013) Elucidating the aetiology of human Campylobacter coli infections. PLoS One 8(5): e64504.
  6. Allos BM (2001) Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32(8): 1201-1206.
  7. Ruiz Palacios GM (2007) The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clinical Infectious Diseases 44(5): 701-703.
  8. Eberle KN, Kiess AS (2012) Phenotypic and genotypic methods for typing Campylobacter jejuni and Campylobacter coli in poultry. Poultry Science 91(1): 255-264.
  9. Campero CM, Anderson M, Walker R, Blanchard P, Barbano L, et al. (2005) Immunohistochemical identification of Campylobacter fetus in natural cases of bovine and ovine abortions. Zoonoses Public Health 52(3): 138-141.
  10. Engberg J, Aarestrup FM, Taylor DE, Gerner Smidt P, Nachamkin I (2001) Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg Infect Dis 7(1): 24-34.
  11. Murray PR (2010) Matrix-assisted laser desorption ionization time-offlight mass spectrometry: usefulness for taxonomy and epidemiology. Clin Microbiol Infect 16(11): 1626-1630.
  12. Morand, S, Owers KA, Szkuta AW, McIntyre KM, Baylis M (2013) Climate variability and outbreaks of infectious diseases in Europe. Sci Rep 3: 1774.
  13. Man SM (2011) The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 8(12): 669-685.
  14. Kalischuk LD, Inglis GD (2011) Comparative genotypic and pathogenic examination of Campylobacter concisus isolates from diarrheic and nondiarrheic humans. BMC Microbiol 11: 53.
  15. Nyati KK, Nyati R (2013) Role of Campylobacter jejuni infection in the pathogenesis of Guillain-Barré syndrome: an update. Biomed Res Int 852195.
  16. Pope JE, Krizova A, Garg AX, Thiessen Philbrook H, Ouimet JM (2007) Campylobacter reactive arthritis: a systematic review. Semin Arthritis Rheum 37(1): 48-55.
  17. Ross AG, Olds GR, Cripps AW, Farrar JJ, McManus DP (2013) Enteropathogens and chronic illness in returning travelers. N Engl J Med 368(19): 1817-1825.
  18. Hong Y, ME Berrang, T Liu, CL Hofacre, S Sanchez, et al. (2003) Rapid detection of Campylobacter coli, C. jejuni, and Salmonella enterica on poultry carcasses by using PCR-enzyme-linked immunosorbent assay. Appl Environ Microbiol 69(6): 3492-3499.
  19. Adedayo O, Kirkpatrick BD (2008) Campylobacter jejuni Infections: Update on presentation, diagnosis, and management. Hospital Physician p. 9-15.
  20. Sanad YM, Kassem II, Z Liu, J Lin, JT Lejeune, et al. (2011) Occurrence of the invasion associated marker (iam) in Campylobacter jejuni isolated from cattle. BMC Res Notes 4: 570.
  21. Sharon VR Epps, Roger B Harvey, Michael E Hume, Timothy D Phillips, Robin C Anderson, et al. (2013) Foodborne Campylobacter: Infections, Metabolism, Pathogenesis and Reservoirs. Int J Environ Res Public Health 10(12): 6292-6304.
  22. Taylor EV, KM Herman, EC Ailes, C Fitzgerald, JS Yoder, et al. (2013) Common source outbreaks of Campylobacter infection in the USA, 1997- 2008. Epidemiol Infect 141(5): 987-996.
  23. Galanis E (2007) Campylobacter and bacterial gastroenteritis. CMAJ 177(6): 570-571.
  24. Benoit SR, Lopez B, Arvelo W, Henao O, Parsons MB, et al. (2014) Burden of laboratory-confirmed Campylobacter infections in Guatemala 2008– 2012: Results from a facility-based surveillance system. J Epidemiol Glob Health 4(1): 51-59.
  25. Ishihara K, R Takahashi, M Andoh, H Ueno, Y Muramatsu, et al. (2012) Seasonal variation in Campylobacter-contaminated retail chicken products: a year-round investigation in Japan. J Vet Med Sci 74(1): 117- 120.
  26. Feierl G, S Jelovcan (2009) Campylobacteriosis in Austria; Situation and Trends. Weiner Klinische Wochenschrift 121(3-4): 103-107.
  27. Gormley FJ, Little CL, Rawal N, Gillespie IA, Lebaigue S, et al. (2011) ADAK: A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992–2008). Epidemiol Infec 139(5): 688-699.
  28. Little CL, Gormley FJ, Rawal NJ, Richardson F (2010) A recipe for disaster: outbreaks of Campylobacteriosis associated with poultry liver pâté in England and Wales. Epidemiol Infec 138(12): 1691-1694.
  29. Bessell PR, L Matthews, A Smith Palmer, O Rotariu, NJ Strachan, et al. (2010) Geographic determinants of reported human Campylobacter infections in Scotland. BMC Public Health 10: 423.
  30. Havelaar AH, Ivarsson S, Löfdahl M, Nauta MJ (2013) Estimating the true incidence of Campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol Infect 141(2): 293-302.
  31. Gargiulo, A, Rinaldi L, D Angelo, L Dipineto, L Borrelli, et al. (2008) Survey of Campylobacter jejuni in stray cats in southern Italy. Letters in Applied Microbiology 46(2): 267-270.
  32. Wingstrand A, Neimann J, Engberg J, Nielsen EM, Smidt PG, et al. (2006) Fresh Chicken as Main Risk Factor for Campylobacteriosis, Denmark. Emerg Infect Dis 12(2): 280-284.
  33. Newell DG, Elvers KT, Dopfer D, Hansson I, Jones P, et al. (2011) Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol 77(24): 8605-8614.
  34. Oberhelman RA, Taylor DN (2000) Campylobacter infections in developing countries. In: Nachamkin I, Blaser MJ, editors. Campylobacter, 2nd edition. American Society for Microbiology pp. 139-153.
  35. Coker AO, Isokpehi RD, Thomas BN, Amisu KO (2001) International collaboration on Campylobacters: Experience from Lagos, Nigeria. [Abstract S-05]. In: Hacker J, editor. Abstracts of scientific presentations of the 11th International Workshop on Campylobacter, Helicobacter and related Organisms, Freiburg, Germany, Sept 1-5, 2001. Int J Med Microbiol 291(31): 168.
  36. Yu JH, NY Kim, NG Cho, JH Kim, YA Kang, et al. (2010) Epidemiology of Campylobacter jejuni outbreak in a middle school in Incheon, Korea. J Korean Med Sci 25(11): 1595-1600.
  37. Komba EVG, RH Mdegela, PLM Msoffe, H Ingmer (2013) Human and animal Campylobacteriosis in Tanzania: a review. Tanzan J Health Res 15(1): 40-50.
  38. Senok AC, GA Botta (2009) Campylobacter enteritis in the Arabian Gulf. J Infect Dev Ctries 3(2): 74-82.
  39. Weinberger M, Lerner L, Valinsky L, Moran Gilad J, Nissan I, et al. (2013) Increased Incidence of Campylobacter spp. Infection and High Rates among Children, Israel. Emerg Infect Dis 19(11): 1828-1831.
  40. Alfredson DA, Korolik V (2007) Antibiotic resistance and resistance mechanisms in Campylobacter jejuni and Campylobacter coli. Fed Microbiol Socie 277(2): 123-132.
  41. Marshall BM, Levy SB (2011) Food Animals and Antimicrobials: Impacts on Human Health. Clin Microbiol Rev 24(4): 718-733.
  42. Moore JE, Barton MD, Blair IS, Corcoran D, Dooley JS, et al. (2006) The epidemiology of antibiotic resistance in Campylobacter. Microbes Infect 8(7): 1955-1966.
  43. Korolik V, Alderton MR, Smith SC, Chang J, Coloe PJ (1998) Isolation and molecular analysis of colonising and non-colonising strains of Campylobacter jejuni and Campylobacter coli following experimental infection of young chickens. Veterinary Microbiol 60(2-4): 239-249.
  44. Zhang M, Y Gu, L He, L Ran, S Xia, et al. (2010) Molecular typing and antimicrobial susceptibility profiles of Campylobacter jejuni isolates from north China. J Med Microbiol 59(10): 1171-1177.
  45. Kovats RS, Edwards SJ, Charron D, Cowden J, D Souza RM, et al. (2005) Climate variability and Campylobacter infection: an international study. Int J Biometeorol 49(4): 207-214.
  46. Humphrey T, O Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117(3): 237-257.
  47. Stern NJ, Svetoch EA, Eruslanov BV, Kovalev YN, Volodina LI, et al. (2005) Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. J Food Prot 68(7): 1450-1453.