Isolation and Characterization of a Novel Helicobacter Species, “ Helicobacter macacae ,” from Rhesus Monkeys with and without Chronic Idiopathic Colitis

Abstract

Chronic idiopathic colitis is a common clinical entity in young captive rhesus monkeys. Eight isolates, cultured from five monkeys in colony 1 with endemic diarrhea and three from colony 2 without diarrhea, were grown under microaerobic conditions on selective agar and were classified by full 16S rRNA sequence, biochemical, and phenotypic analysis as a novel helicobacter, "Helicobacter macacae" (proposed name). All eight strains of H. macacae had 99.5% identical 16S rRNA sequences.Chronic idiopathic colitis in young rhesus monkeys (Macaca mulatta) is a common clinical entity in animals maintained in captivity (1). Monkeys with this disease have progressive weight loss and dehydration as a result of chronic diarrhea. The affected colons in these monkeys have severe inflammation characterized by lymphoplasmacytic infiltration, crypt epithelial hyperplasia, goblet cell depletion, the presence of multifocal crypt abscesses, and mucosal erosion and ulceration.In a previous study, we described the presence of two novel Helicobacter spp. Helicobacter sp. strain rhesus monkey 1 was isolated from two monkeys with mild colitis (6). These animals were part of a cohort of monkeys in which chronic idiopathic colitis was endemic (1, 6). To further examine the prevalence of enteric helicobacters in this group of monkeys with endemic chronic diarrhea, as well as in a second established colony of adult macaques used in neurophysiology studies that were without diarrheal disease, we tabulated the prevalence of Helicobacter spp. by Helicobacter genus-specific PCR (5) and the specific presence of a novel (rhesus monkey 1) helicobacter by culturing colonic tissue collected at necropsy or during endoscopic biopsy (colony 1) or by culturing the feces (colony 2). Twenty-six juvenile rhesus monkeys from a colony with endemic idiopathic colitis (colony 1) were necropsied or underwent endoscopic biopsy and had their colonic tissue cultured under microaerobic conditions as previously described (6). A second group of 35 adult rhesus monkeys (colony 2) without a clinical history of endemic diarrhea had their feces cultured for Helicobacter spp.Helicobacter genus-specific primers C97 (5Ј-GCT ATG ACG GGT ATC C-3Ј) and C05 (5Ј-ACT TCA CCC CAG TCG CTG-3Ј) were used to amplify a 1,200-base-pair PCR product from the DNA of bacterial isolates suspected based on colony morphology and Gram stain to be Helicobacter spp. (5, 6). In colony 1, Helicobacter spp. in the colonic contents of 21/26 (81%) of the monkeys were identified by colony morphology and Gram stain and confirmed by the amplification of the 1,200-base-pair Helicobacter genus-specific PCR product (5). Using the same criteria, culture results on fecal samples in colony 2 yielded helicobacter isolates in 20/35 (57%) of the animals.Eight isolates classified as rhesus monkey type 1 by 16S rRNA analysis, five from four monkeys without diarrhea and one monkey with diarrhea from colony 1 and three from three nondiarrheic monkeys from colony 2, were subjected to a detailed biochemical characteriza...

Diversity of zoonotic enterohepatic Helicobacter species and detection of a putative novel gastric Helicobacter species in wild and wild-born captive chimpanzees and western lowland gorillas

“…Other putative species detected in the present study include 'H. macacae', previously isolated from rhesus monkeys with and without chronic idiopathic colitis (Fox et al, 2007), H. pullorum and H. canadensis, as well as several species mainly detected in rodents, such as H. trogontum (only detected in unhabituated animals), H. rodentium, H. ganmani, H. mesocricetorum, H. mastomyrinus and H. typhlonius. In addition to H. cinaedi and H. fennelliae, several of these species (H. rodentium, H. canadensis, H. pullorum) have been associated with diarrhoea, colitis or chronic liver diseases in humans (Fox et al, 2000;Ceelen et al, 2005;Nakonieczna et al, 2010;Hansen et al, 2011).…”

“…Apart from humans, members of the genus Helicobacter have also been detected in a wide variety of other animal species, both domesticated and non-domesticated (Fox et al, 2007;Haesebrouck et al, 2009;Schrenzel et al, 2010;Lertpiriyapong et al, 2014). These include various non-human primates, such as rhesus macaques, mandrills and crab-eating macaques (O'Rourke et al, 2004;Schrenzel et al, 2010).…”

Enterohepatic Helicobacter spp. in cats with non-haematopoietic intestinal carcinoma: a survey of 55 cases

“…Natural EHS infection has also been associated with colitis and intestinal adenocarcinoma in non-human primates. In rhesus macaques, EHS were commonly cultured in rhesus with chronic colitis, with a 81 % prevalence among primates with diarrhoea and 57 % prevalence in a non-diarrheic cohort housed in different institutions (Fox et al, 2007. Subsequent studies have identified persistent infection and 93 % EHS prevalence among rhesus macaques with intestinal adenocarcinoma (IAC) (Marini et al, 2010;Lertpiriyapong et al, 2014).…”

Helicobacter saguini, a Novel Helicobacter Isolated from Cotton-Top Tamarins with Ulcerative Colitis, Has Proinflammatory Properties and Induces Typhlocolitis and Dysplasia in Gnotobiotic IL-10 −/− Mice

“…H. hepaticus, H. bilis, and other EHS infections in immunocompromised mice cause chronic typhlocolitis, high-grade dysplasia, and progression to colitis-associated carcinoma (CAC) (8)(9)(10)(11). Novel Helicobacter spp., including H. macacae, have been cultured from idiopathic colitis and colon adenocarcinomas in rhesus monkeys (12)(13)(14). H. cinaedi and H. fennelliae were first isolated from homosexual men (presumably immunocompromised by HIV infection) with proctitis (15).…”