Elsevier

Veterinary Microbiology

Volume 166, Issues 3–4, 25 October 2013, Pages 681-685
Veterinary Microbiology

Short communication
Fatal atypical O:3 Yersinia pseudotuberculosis infection in cynomolgus macaques

https://doi.org/10.1016/j.vetmic.2013.07.013Get rights and content

Abstract

Fatal Yersinia pseudotuberculosis infection in cynomolgus macaques was diagnosed based upon pathology, microbiology and PCR for this study. Pathological findings included acute, erosive to ulcerative, necrohemorrhagic enterocolitis. Genotyping by PCR showed an O:3 pattern (gmd-fcl+, ddhC-prt+, manB+, ddhA-B+), but an additional gene, wbyK, was detected. This is the second report to identify wbyK+ O:3 genotype as the cause of fatal yersiniosis. The first case was reported in 2008, and involved farm deer in the U.S. As the frequency of wbyK+ O:3 genotype is found more often in different carriers, O:3 genotype is proposed to be divided into two subtypes: O:3a without wbyK and O:3b with wbyK. Virulence gene analysis showed the presence of inv, ypmC, irp1, ybtP-ybtQ, yadA, yopB, yopH, lcrF, and suggested that this O:3b isolate could be a highly pathogenic strain to cynomolgus macaques.

Introduction

Yersinia pseudotuberculosis is a gram-negative coccobacillus Enterobacteriaceae found in soil, water, foods, birds, and mammals. In cynomolgus macaques (Macaca fascicularis), Y. pseudotuberculosis causes various symptoms, ranging from diarrhea, enterocolitis, to fatal disease (Rosenberg et al., 1980).

The pathogenicity of Y. pseudotuberculosis is determined by several virulence factors. O-antigen (O-polysaccharide), a side chain of lipopolysaccharide (LPS) on the bacteria's outer membrane, plays a role in the virulence by causing Y. pseudotuberculosis to invade Peyer's patches and epithelial cells more efficiently (Skurnik and Bengoechea, 2003). Traditionally, immune sera against O-antigen was used to diagnose different serotypes (Tsubokura and Aleksić, 1995). Based on the genetic composition of O-antigen gene clusters between hemH and gsk genes, 21 O-serotypes or O-genotypes have also been identified (Bogdanovich et al., 2003).

Besides O-antigen, virulence factors derived from the chromosome include invasin (Inv), Y. pseudotuberculosis-derived mitogen (3 variants, YPMa, YPMb, and YPMc) and high-pathogenicity island (HPI); plasmid-born virulence factors include Yersinia adhesin A (YadA,), Yersinia outer membrane proteins (Yops), low-Ca2+ response F protein (LcrF), etc. The loss of virulence plasmids will either decrease the pathogenicity or cause the bacteria to become nonpathogenic.

Although the bacteriological, biochemical, and histopathological properties of Y. pseudotuberculosis infections in cynomolgous monkeys have been well studied (Bronson et al., 1972, Rosenberg et al., 1980), little is known about their O-genotyping and virulence genetics. In 2011, a group of our cynomolgus macaques suffered from acute fatal yersinosis. Here we reported the isolation of Y. pseudotuberculosis, the pathological findings, the typing of the O-antigen gene cluster and its virulence gene distribution.

Section snippets

Animals’ history

A group of 40 cynomolgus monkeys of Chinese origin (age: 2 to 4 years) were received into an indoor holding facility on May 25, 2011. Animals were fed a commercial High Protein Monkey Diet (PMI LabDiet) and were supplemented with fresh fruits, vegetables and other enrichment items. On June 12, 201l, one female (animal A) was found dead with no previous signs of illness other than being slightly underweight. A fecal sample from the cage mate (animal B) was submitted to Antech Diagnostics

Pathology

Bacterial-related gross findings were similar in necropsied animals B, C, D and E, which included enlarged mesenteric, colonic and iliac lymph nodes; multiple dark brown foci at various sites of the gastric mucosa; mucoid contents in the stomach and small intestine; edematous and congested cecum and colon wall; multiple raised punctate green-yellow or linear red foci on the mucosa of the cecum, colon, and/or rectum.

Microscopically, all necropsied animals (B–E) had minimal to marked acute,

Discussion

The original source of the Y. pseudotuberculosis infections in our cynomolgus monkeys was unknown. These monkeys were bred outdoors; therefore, contaminated food, water, soil, wild rodent carries, or asymptomatic monkeys kept in the same cage could all be possible vectors of transmission. Also, the animals were fed fresh fruit and vegetables while housed at the quarantine facility. Although, all fruit and vegetables are washed prior to feeding, studies have shown that these types of foods have

Acknowledgements

We thank Claudia Crandall, Kimmi Schrader, Martha Obeso and Dr. Rita Brenden for their assistances with the serotyping experiment in California Department of Public Health. We also thank Patty Srisawangvong for her help in PCR, and Joanne Starkey for her assistance in manuscript preparation. Lastly, we thank the Laboratory Animal Services and the Pathology departments at Novartis Pharmaceuticals for assisting with sample collection and processing. This work was supported by VRL Laboratories and

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Cited by (3)

  • Atypical Yersinia pseudotuberculosis serotype O:3 isolated from hunted wild boars in Italy

    2014, Veterinary Microbiology
    Citation Excerpt :

    Recently, an atypical O:3 serotype, carrying an additional gene, wbyK, has been reported in fatal cases of yersiniosis in farmed deer and cynomolgus macaques in North America. This atypical O:3 serotype carried several virulence genes, in both cases inv, yopB, and yopH were detected; ypmC, irp1, ybtP-ybtQ, yadA and lcrF were found in isolates from cynomolgus macaques, which were also reported as melibiose-negative (Zhang et al., 2008; Zao et al., 2013). To the best of our knowledge, this atypical O:3 strain has never been reported in healthy animals or outside North America.

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