Zoonotic Enteropathogens
World Small Animal Veterinary Association World Congress Proceedings, 2014
Melanie Craven, BVetMed, PhD, DSAM, DECVIM-CA, MRCVS

Zoonotic diseases are contagious diseases spread between animals and people, and can be caused by bacteria, viruses, parasites, and fungi.1,2 A zoonotic enteropathogen is an infectious disease affecting the gastrointestinal (GI) tract. Since the emergence of H5N1 bird flu, risk of zoonotic pandemics has been acknowledged as a major global threat to human health. Most pandemics, e.g., HIV/AIDS, severe acute respiratory syndrome, pandemic influenza, originate in animals, are caused by viruses and are driven to emerge by ecological, behavioural, or socioeconomic changes. Despite their substantial effects on global public health, no pandemic has been predicted before infecting people. Numerous research and surveillance programs have been established to overcome these challenges and move the global pandemic strategy from response to preemption.3

Bacteria

Campylobacters are gram-negative rods and commensal flora of the canine and feline gut, and cause bacterial-mediated diarrhoea in around 400–500 million people globally each year.4 Uncooked meat is the main source of infection, transmitted via the faecal-oral route from food or water sources. After an incubation period of 1–5 days, self-limiting symptoms including diarrhoea, abdominal pain, and fever occur. Serious complications can arise, such as reactive arthritis (1 to 5% of people) and Guillain-Barre syndrome, a postinfectious polyneuropathy capable of paralysis and death. Remarkably, campylobacteriosis has been experimentally induced in people with as few as 500 bacterial cells and a clinical trial using a well-characterized outbreak of C. jejuni, CG8421 strain, in 23 people who received 1 × 10e6 colony forming units of C. jejuni, documented attack rates of 93%.4,5 In dogs and cats, infection is common and often asymptomatic. C. jejuni is frequently isolated from dogs or cats in pet shops, kennels and animal shelters. Children less than 5 years old with a newly acquired puppy have the highest risk of infection.6 Many observational and experimental studies have examined the association between diarrhoea and the presence of Campylobacter in dog and cat faeces, and have rarely confirmed a positive association.4,7,8 Diagnosis of pathogenic campylobacteriosis in dogs and cats is a real challenge because of the high prevalence in healthy animals, and faecal culture is perhaps most helpful in excluding infection.

Salmonella

Salmonellosis is caused by gram-negative, motile, non-spore-forming facultative anaerobic bacilli from the family Enterobacteriaceae. Salmonella genus includes more than 2,400 different serotypes, the majority serotypes of S. enterica subspecies enterica. Human salmonellosis cases have doubled in the U.S. over the past 2 decades, involving 1.4 million people. Most infections are foodborne, and the incidence of disease attributable to dogs and cats is unknown, though Salmonella is a pathogen in dogs and cats. The prevalence of Salmonella in healthy dogs (carriers) ranges from 0 to 3.6%; in diarrhoeic dogs 0 to 3.5%, and cats 0 to 8.6%; in stray or shelter dogs and cats 0–51.4% (much higher in dogs fed raw food diets) (5). Transmission of Salmonella from dogs and cats to people has been documented in households, shelters, and veterinary clinics, causing disease ranging from mild self-limiting diarrhoea to severe haemorrhagic gastroenteritis (HGE) and septicaemia. Due to the 'carrier' state, the mere isolation of Salmonella alone is insufficient to make a diagnosis of Salmonella-induced enteritis in animals. It is generally accepted that culture of a single faecal sample underestimates the prevalence of Salmonella, whether or not from low test sensitivity, low-level shedding, intermittent shedding, or other reasons. In horses, testing of at least 5 serial samples is recommended, and in cats and dogs, culture of 3 samples is advised. Conventional and real-time PCR assays are widely available, but suffer from a lack of validation for use with dog and cat faeces, hence sensitivity and specificity are unclear. Management is supportive and choice of antimicrobial is based on in vitro5 susceptibility testing. There is no evidence that antimicrobials decrease severity or duration of diarrhoea, though may prevent or treat bacteraemia associated with bacterial translocation. When carriers of Salmonella spp. are identified, there is no evidence that antimicrobials are of use, but pro- and prebiotics may be helpful to reduce bacterial shedding.

Clostridial Species

Clostridia are anaerobic spore-forming gram-positive rods. Two species, C. perfringens (CP) and C. difficile (CDI) are associated with disease. C. difficile is an important human pathogen and a leading cause of hospital-associated infection. It causes antibiotic-associated colitis and pseudomembranous colitis in people, which can progress to toxic megacolon and death.

CDI produces toxin A (an enterotoxin) and toxin B (a cytotoxin), which cause bloating, diarrhoea, and abdominal pain. CDT is a binary toxin, of unknown significance.5,8 C. difficile exists as vegetative cells and spores. Vegetative cells are the actively growing form responsible for disease in the intestinal tract. Spores are highly resistant, can survive in the environment for years, and are responsible for most or all transmission of C. difficile. The risk of zoonotic transmission is currently unclear, however there is circumstantial evidence suggesting that interspecies transmission can occur. CDI can be carried by asymptomatic dogs and cats, though some studies cite it as a leading cause of enteritis in dogs, and an outbreak has been reported in a veterinary teaching hospital5. The strains of C. difficile recovered from dogs and cats are almost always indistinguishable from those found in people with CDI5 and can cause mild self-limiting diarrhoea to potentially fatal HGE. The clinical standard for diagnosis of CDI in humans has been detection of C. difficile toxins A and/or B in stool, by cell culture cytotoxicity assay, ELISA, and PCR. Treatment is supportive, and metronidazole is the antimicrobial of choice.

C. perfringens (CP) is a gram-positive, spore-forming anaerobic bacterium. Isolates are divided into 5 major types (A–E) based on the presence of toxin genes, cpa (alpha toxin), cpb (beta toxin), etx (epsilon toxin), and iap (iota toxin). CP is found in up to 11%–100% of healthy dogs and 27%–86% of diarrhoeic dogs and thus is a normal component of the intestinal microflora. Several studies have shown an association between immunodetection of CP toxin in faecal specimens and diarrhoea, but the pathogenesis of C. perfringens-associated diarrhoea in dogs and cats is not fully understood. Little is known about the potential for transmission from pets to people, and pets probably play little to no role in human disease. Foodborne transmission is more important. It is possible that C. perfringens from dogs and cats could be inadvertently inoculated into food through poor hygiene practices.5,8 Because of the prevalence of CP in healthy animals, the most useful aspect of faecal culture is to rule out disease, as this indicates an extremely low likelihood of infection. Currently, the only commercially available tests for detection of C. perfringens toxin in faeces are CPE immunoassays (RPLAA and ELISA), but neither has been adequately scrutinized in dogs and cats. Treatment is supportive and with metronidazole or tylosin.

E. coli

Escherichia coli is prevalent in the intestinal flora (~10 cfu/mL). Most strains are commensals, but some pathotypes cause GI disease, with 7 mechanisms described: enteropathogenic (EPEC), enterotoxigenic (ETjm EC), enterohaemorrhagic (EHEC), necrotoxigenic (NTEC), enteroinvasive (EIEC), enteroaggregative (EAEC), and adherent-invasive (AIEC) strains.5,9 In general, only EHEC strains (e.g., Escherichia coli O157) are regarded as food and waterborne zoonotic pathogens that cause diarrhoea, haemorrhagic colitis, and haemolytic uremic syndrome (HUS) in humans. Human infections result from contaminated foods of animal (especially bovine) origin, contact with shedding or contaminated animals, and environmental (water) contaminants. The O157:H7 strain is distinguished microbiologically from other E. coli by its inability to ferment sorbitol and, most importantly, by its production of "shiga-like" toxins (SLT I and II). Cattle are the main reservoir for human infection, but the O157:H7 strain has been isolated from two asymptomatic dogs on a farm in Washington (along with cattle, a horse, two batches of stable flies and biofilms on water troughs on the farm). There have been reports of dog-to-human transmission of O157 in Canada and the U.K., and a report of O157 isolation from a veterinary student's dog.5

AIEC strains are a relatively new E. coli pathotype. They have been shown to invade the colon mucosa in Boxer dog colitis (GC), and in people with Crohn's disease and colitis of chronic granulomatous disease (CGD). A direct cause and effect for AIEC is implied by response to antimicrobials, especially in Boxer dog GC, where a complete cure can be achieved using enrofloxacin.10 AIEC can be highly responsive to antimicrobials, but multidrug resistance is common. The zoonotic potential of Boxer dogs harbouring AIEC is unknown, as is the potential for reverse zoonosis. AIEC are 'resident' strains in people and animals that seem to thrive in the presence of inflammation. Since they are found in healthy dogs, cats and swine, a putative zoonotic risk has been assigned to infection with AIEC for development of Crohn's disease.10

References

1.  Thompson RCA, Smith A. Zoonotic enteric protozoa. Vet Parasitol. 2011 Nov 24;182(1):70–78. Available from: www.ncbi.nlm.nih.gov/pubmed/21798668.

2.  Hart CA, Shears P. Manson's tropical infectious diseases. Elsevier. 2014. Available from: www.sciencedirect.com/science/article/pii/B978070205101200025X.

3.  Morse SS, Mazet JAK, Woolhouse M, Parrish CR, Carroll D, Karesh WB, et al. Prediction and prevention of the next pandemic zoonosis. Lancet. 2012 Dec 1;380(9857):1956–1965. Available from: www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3712877&tool=pmc%20entrez&rendertype=abstract.

4.  Wieczorek K, Osek J. Antimicrobial resistance mechanisms among Campylobacter. Biomed Res Int. 2013 Jan;2013:340605. Available from: www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3707206&tool=pmc%20entrez&rendertype=abstract.

5.  Weese JS. Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoonotic potential. Vet Clin North Am Small Anim Pract. 2011 Mar;41(2):287–309. Available from: www.sciencedirect.com/science/article/pii/S0195561610001701.

6.  Hemsworth S, Pizer B. Pet ownership in immunocompromised children - a review of the literature and survey of existing guidelines. Eur J Oncol Nurs. 2006 Apr;10(2):117–127. Available from: www.ncbi.nlm.nih.gov/pubmed/16581294.

7.  Robertson ID, Thompson RC. Enteric parasitic zoonoses of domesticated dogs and cats. Microbes Infect. 2002 Jul;4(8):867–873. Available from: www.ncbi.nlm.nih.gov/pubmed/12270734.

8.  Marks SL, Rankin SC, Byrne BA, Weese JS. Enteropathogenic bacteria in dogs and cats: diagnosis, epidemiology, treatment, and control. J Vet Intern Med. 2011;25(6):1195–1208. Available from: www.ncbi.nlm.nih.gov/pubmed/22092607.

9.  Caprioli A, Morabito S, Brugère H, Oswald E. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res.2005;36(3):289–311. Available from: www.ncbi.nlm.nih.gov/pubmed/15845227.

10. Simpson KW, Dogan B, Rishniw M, Goldstein RE, Klaessig S, McDonough PL, et al. Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun. 2006;74(8):4778–4792. Available from: www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1539603&tool=pmc%20entrez&rendertype=abstract.

  

Speaker Information
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Melanie Craven, BVetMed, PhD, DSAM, DECVIM-CA, MRCVS
USA


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