Immunology & Medic Al Microbiology

MINIREVIEW Helicobacter equorum: prevalence and signi¢cance for horses and humans Hilde Moyaert1, Frank Pasmans2, Annemie Decostere2, Richard Ducatelle2 & Freddy Haesebrouck2

1International Clinical Development, s.a. Alcon-Couvreur n.v., Puurs, Belgium; and 2Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium Downloaded from https://academic.oup.com/femspd/article/57/1/14/481915 by guest on 24 September 2021

Correspondence: Hilde Moyaert, Abstract International Clinical Development, s.a. Alcon-Couvreur n.v., Rijksweg 14, B-2870 Helicobacter equorum colonizes the caecum, colon and rectum of horses. The agent Puurs, Belgium. Tel.: 132 3 890 2146; is highly prevalent in o 6-month-old foals. In adult horses, the prevalence of H. fax: 132 3 890 2815; e-mail: hilde. equorum seems to be rather low, but these animals may harbour low, subdetectable [email protected] numbers of this microorganism in their intestines. So far, no association could be made between the presence of H. equorum and clinical disease or intestinal lesions Received 5 October 2008; accepted 6 July in adult horses. Further research is necessary to elucidate the pathogenic potential 2009. of this bacterial species towards young foals. Helicobacter equorum DNA was not Final version published online 14 August 2009. detected in human faeces, indicating that this microorganism does not commonly spread from horses towards humans. DOI:10.1111/j.1574-695X.2009.00583.x

Editor: Willem van Leeuwen

Keywords Helicobacter equorum; horses; humans. rRNA gene was developed. This tool was used to determine Introduction the presence of H. equorum in different horse populations Barry Marshall and Robin Warren, two Australian researchers (Moyaert et al., 2007c, 2009). Faecal samples of 120 adult, who discovered the bacterium Helicobacter pylori in 1982 healthy privately owned horses, 227 adult, healthy riding- (Marshall & Warren, 1984), have been awarded the Nobel Prize school horses, 239 adult hospitalized horses and sixty-six 3- of 2005 in Physiology or Medicine for proving that stomach day- to 6-month-old foals were screened for H. equorum ulcers are caused by this microorganism. Their finding inspired DNA. The vast majority of the adult hospitalized horses many scientists around the world and made this bacterium one were under treatment with an antimicrobial agent at the of the most investigated bacterial species ever. After Marshall moment of sampling, while the other horses had not been and Warren’s discovery, interest rose in other Helicobacter treated with an antimicrobial agent in the 14 days preceding species that colonize the stomach or the intestines of different the sampling. vertebrate hosts. Applying a genus-specific PCR test on Helicobacter equorum DNA was demonstrated in faeces equine faecal samples demonstrated the presence of Helico- from 0.8% of the adult privately owned horses, 3.1% of the bacter DNA in horse faeces. Subsequent isolation trials adult riding-school horses and 7.9% of the adult hospita- resulted in the discovery of a novel, urease-negative Helico- lized horses. The prevalence of H. equorum was significantly bacter species, Helicobacter equorum (Moyaert et al., 2007b). higher in adult hospitalized than in adult privately owned In this article, the prevalence of this recently described horses (P = 0.02). These results indicate that the prevalence microorganism in horses of different ages and in humans, of H. equorum in adult horses may be influenced by the as well as its interactions with its equine host, are discussed. health status of the investigated horse population and/or by antimicrobial treatment. Several factors that are more Prevalence of H. equorum in adult horses likely to be present in hospitalized animals including anti-

IMMUNOLOGY & MEDICAL MICROBIOLOGY microbial treatment, stress, surgical treatment and dietary and foals changes, have been associated with an altered gastrointest- Following on the description of H. equorum sp. nov., a inal microbiota. Alterations in the equilibrium of the diagnostic H. equorum-speciﬁc PCR assay based on the 23S intestinal microbiota may result in increased numbers of

c 2009 Federation of European Microbiological Societies FEMS Immunol Med Microbiol 57 (2009) 14–16 Published by Blackwell Publishing Ltd. All rights reserved Helicobacter equorum in horses and humans 15 potentially pathogenic organisms (Hawrelak & Myers, with gastrointestinal disease or lesions (Moyaert et al., 2004). 2007a). In this in vivo experiment, adult horses were used The prevalence of H. equorum was significantly that were repeatedly screened beforehand for the presence of (P o 0.001) higher in foals compared with adult horses: H. equorum DNA in their faeces and always tested negative. 63.6% of the foals harboured H. equorum DNA in their In view of the above-mentioned hypothesis, it can, however, faeces. This indicates that the prevalence of this microorgan- not be excluded that these animals had developed immunity ism is additionally influenced by the age of the sampled to H. equorum, preventing a more severe clinical outcome of horses. For H. pylori, it is known that its prevalence increases the experimental infection. As a result, it would be interest- progressively with age. In developed countries, it is uncom- ing to perform similar experiments in naive foals. However, mon for young children to be colonized, whereas approxi- keeping in mind the wide-spread occurrence of H. equorum mately 50% of adults are colonized by the age of 60 (Taylor in foals, it will be difficult to find suitable experimental Downloaded from https://academic.oup.com/femspd/article/57/1/14/481915 by guest on 24 September 2021 & Blaser, 1991). In developing countries, H. pylori infection animals that are free from the agent and passive or active is acquired earlier in life and more frequently than in immunity against it. So far, there are no techniques available developed countries: 70–90% of this population carries for the detection of H. equorum-specific antibodies. Devel- H. pylori and almost all of these acquire the infection before opment of such tests will most probably be hampered due to the age of 10 years. Close person to person contact in cross-reactivity between Helicobacter and Campylobacter childhood – for instance by sharing a bed due to over- species (Faulde et al., 1991). crowding – or unhygienic living conditions may both promote faecal–oral or oral–oral transmission of this micro- Prevalence of H. equorum in humans organism (Mendall & Northfield, 1995; Dunn et al., 1997). Similarly, oral–oral contact between mare and foal and Stool samples of 531 humans suffering from gastrointestinal faecal–oral exposures might explain the high H. equorum disease and 100 clinically healthy humans were tested for the infection rate in young foals. It is known that colts and fillies presence of H. equorum DNA, using a species-specific PCR show coprophagic behaviour during the first months after (Moyaert et al., 2007c). No evidence of H. equorum infection birth, with the greatest frequency during the first 2 months. was found in any of the 631 human samples, indicating that They usually eat the faeces of their mother and this this microorganism does not commonly infect humans. behaviour may provide nutrients and introduce normal Nevertheless, because the human faecal samples in this study bacterial flora to the gut (Crowell-Davis & Houpt, 1985). were anonymized and no information about a possible close Current knowledge implies that, once acquired, H. pylori contact between the sampled humans and horses was infection persists lifelong in most infected subjects (Perez- available, one cannot exclude a possible zoonotic potential Perez et al., 2004). Possibly, adult horses harbour low, of this microorganism. It would therefore be interesting to subdetectable levels of H. equorum in their gut due to the investigate the presence of H. equorum in faecal samples development of a mature immune system. The lower detec- from people who have close contact with horses. tion limit of the H. equorum-specific PCR assay is 130 fg of genomic H. equorum DNA per PCR mixture (Moyaert et al., Conclusions 2007c), corresponding to approximately 26 bacterial cells Helicobacter equorum colonizes the equine lower bowel and 3 per PCR mixture (Germani et al., 1997) or 26 Â 10 bacterial is highly prevalent in 6-month-old foals. In adult horses, À1 o cells g faeces. Therefore, H. equorum bacteria shed in low the prevalence of H. equorum seems to be rather low and, so numbers by adult horses may have been missed. Moreover, far, the organism was not detected in stool samples from the occurrence of H. equorum may be underestimated due to humans. Further research is necessary to elucidate the sampling at one time point and because only 200 mg of pathogenic potential of this bacterial species. faecal material was used for each DNA extraction (Moyaert et al., 2007c). Indeed, we noticed that H. equorum is not homogenously distributed throughout the equine faeces and References intermittent faecal shedding of enterohepatic helicobacters Crowell-Davis SL & Houpt KA (1985) Coprophagy by foals: has been described before (Oxley & McKay, 2004). effects of age and possible functions. Equine Vet J 17: 17–19. Dunn BE, Cohen H & Blaser M (1997) Helicobacter pylori. Clin Interactions of H. equorum with adult Microbiol Rev 10: 720–741. horses Faulde M, Putzker M, Mertes T & Sobe D (1991) Evaluation of an immunofluorescence assay for specific detection of immuno- In an experimental infection study, it was demonstrated that globulin G antibodies against Helicobacter pylori, and antigenic H. equorum is able to colonize the caecum, colon and cross-reactivity between H. pylori and Campylobacter jejuni. rectum of horses, but so far, its presence was not associated J Clin Microbiol 29: 323–327.

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