Characterization of a Moraxella species that causes epistaxis in macaques

Abstract

Bacteria of the genus Moraxella have been isolated from a variety of mammalian hosts. In a prior survey of bacteria that colonize the rhesus macaque nasopharynx, performed at the Tulane National Primate Research Center, organisms of the Moraxella genus were isolated from animals with epistaxis, or “bloody nose syndrome.” They were biochemically identified as Moraxella catarrhalis, and cryopreserved. Another isolate was obtained from an epistatic cynomolgus macaque at the U.S. Army Medical Research Institute of Infectious Diseases. Based on differences in colony and cell morphologies between rhesus and human M. catarrhalis isolates, we hypothesized that the nonhuman primate Moraxella might instead be a different species. Despite morphological differences, the rhesus isolates, by several biochemical tests, were indistinguishable from M. catarrhalis. Analysis of the cynomolgus isolate by Vitek 2 Compact indicated that it belonged to a Moraxella group, but could not differentiate among species. However, sequencing of the 16S ribosomal RNA gene from four representative rhesus isolates and the cynomolgus isolate showed closest homology to Moraxella lincolnii, a human respiratory tract inhabitant, with 90.16% identity. To examine rhesus macaques as potential hosts for M. catarrhalis, eight animals were inoculated with human M. catarrhalis isolates. Only one of the animals was colonized and showed disease, whereas four of four macaques became epistatic after inoculation with the rhesus Moraxella isolate. The nasopharyngeal isolates in this study appear uniquely adapted to a macaque host and, though they share many of the phenotypic characteristics of M. catarrhalis, appear to form a genotypically distinct species.

Nonhuman Primates

“…Clinical signs occur most commonly in dry winter months and may also include sneezing and occasionally, periorbital swelling. Sequencing of the 16S ribosomal RNA gene indicated that isolates from macaques were most closely related to M. lincolnii and rhesus macaques were resistant to infection with human strains of M. catarrhalis (Embers et al, 2011). Treatment with long-acting penicillin may be effective (VandeWoude and Luzarraga, 1991), but recurrent infections are possible if low-humidity conditions persist.…”

Genome Sequence of Moraxella macacae 0408225, a Novel Bacterial Species Isolated from a Cynomolgus Macaque with Epistaxis

“…Previous outbreaks of epistaxis among cynomolgus macaques have been attributed to Branhamella ( Moraxella ) catarrhalis (3) or Neisseria ( Moraxella ) catarrhalis (4) based on biochemical testing. While the results of phenotypic and biochemical testing of M. macacae were consistent with those of M. catarrhalis , sequence analysis of the 16S rRNA indicated only 88% identity to M. catarrhalis (2). In fact, the closest 16S sequence match was to M. lincolnii , a human respiratory tract inhabitant, with 90% nucleotide identity (2).…”

“…The most important human-pathogenic species is M. catarrhalis , a major cause of upper and lower respiratory tract infections, sinusitis, and childhood otitis media (1). Moraxella macacae is a recently described species causing epistaxis, or bloody nose syndrome, in both rhesus macaques from the Tulane National Primate Research Center and cynomolgus macaques from the U.S. Army Medical Research Institute of Infectious Diseases (USAMRIID) (2). Previous outbreaks of epistaxis among cynomolgus macaques have been attributed to Branhamella ( Moraxella ) catarrhalis (3) or Neisseria ( Moraxella ) catarrhalis (4) based on biochemical testing.…”

Development of real‐time PCR assays for the detection of Moraxella macacae associated with bloody nose syndrome in rhesus (Macaca mulatta) and cynomolgus (Macaca fascicularis) macaques

“…Detection of M. macacae thus far has been based on traditional microbiological and biochemical methods. Unfortunately, with the exception of beta‐lactamase, M. macacae exhibits identical reactivity in the biochemical tests of the API NH panel (BioMérieux, Durham, NC, USA) as M. catarrhalis , the human pathogenic species . In fact, previous descriptions of bloody nose syndrome in non‐human primates in 1991 and 2002 were attributed to M .…”

“…( Branhamella ) catarrhalis based on colony morphology, Gram stain, and biochemical analysis, but were most likely due to M. macacae . Proper identification of M. macacae was ultimately only made by sequence analysis of its 16S rRNA gene .…”