Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study

Abstract

Summary Background Lyme borreliosis is the most common tick-borne disease in the northern hemisphere. It is a multisystem disease caused by Borrelia burgdorferi sensu lato genospecies and characterised by tissue localisation and low spirochaetaemia. In this study we aimed to describe a novel Borrelia species causing Lyme borreliosis in the USA. Methods At the Mayo clinic, from 2003 to 2014, we tested routine clinical diagnostic specimens from patients in the USA with PCR targeting the oppA1 gene of B burgdorferi sensu lato. We identified positive specimens with an atypical PCR result (melting temperature outside of the expected range) by sequencing, microscopy, or culture. We collected Ixodes scapularis ticks from regions of suspected patient tick exposure and tested them by oppA1 PCR. Findings 100 545 specimens were submitted by physicians for routine PCR from Jan 1, 2003 to Sept 30, 2014. From these samples, six clinical specimens (five blood, one synovial fluid) yielded an atypical oppA1 PCR product, but no atypical results were detected before 2012. Five of the six patients with atypical PCR results had presented with fever, four had diffuse or focal rash, three had symptoms suggestive of neurological inclusion, and two were admitted to hospital. The sixth patient presented with knee pain and swelling. Motile spirochaetes were seen in blood samples from one patient and cultured from blood samples from two patients. Among the five blood specimens, the median oppA1 copy number was 180 times higher than that in 13 specimens that tested positive for B burgdorferi sensu stricto during the same time period. Multigene sequencing identified the spirochaete as a novel B burgdorferi sensu lato genospecies. This same genospecies was detected in ticks collected at a probable patient exposure site. Interpretation We describe a new pathogenic Borrelia burgdorferi sensu lato genospecies (candidatus Borrelia mayonii) in the upper midwestern USA, which causes Lyme borreliosis with unusually high spirochaetaemia. Clinicians should be aware of this new B burgdorferi sensu lato genospecies, its distinct clinical features, and the usefulness of oppA1 PCR for diagnosis.

There is inadequate evidence to support the division of the genus Borrelia

“…Interestingly, infection with the recently described genospecies of the B. burgdorferi s.l. complex, Borrelia mayonii, produced high spirochaetal blood densities, akin to that seen following infection with species of the RF group [6].…”

“…1) underscore our criticism and highlights the uncertainty around the proposed genus split. Presumably this is only the tip of the iceberg, as more RFlike and LB species continue to be detected and described every few years [3,6]. In this context, it is our opinion that it would be prudent to retain the generic name Borrelia for both LB and RF spirochaetes.…”

“…spirochaetes to humans likewise are the principal vectors of B. miyamotoi. Further RF-like and LB spirochaetes are being discovered and described [3,6], and the ecological and genetic differences between these groups will most certainly become even more blurred in the future.…”

The Biological Survey of Canada: A Personal History

“…It is worth noting that many new tick-borne zoonoses are emerging with increasing frequency globally and within North America (Vasconcelos and Calisher 2016). Heartland virus (Savage et al 2013) and Bourbon virus (Kosoy et al 2015) are recently described human pathogens associated with lone star tick, and Borrelia mayonii Pritt et al in blacklegged ticks in the Midwest (Pritt et al 2016) are two examples of this. Clearly readers of this handbook will need to consult the current literature to be aware of new, emerging tick-associated pathogens.…”

A systematic review and meta-analysis for the adverse effects, immunogenicity and efficacy of Lyme disease vaccines: Guiding novel vaccine development

“…In addition to incorporating all major Borrelia species, the new vaccine should also take into consideration the recent identification of the novel pathogenic species causing LB with high spirochaetaemia (B. mayonii). 41 Last, data on cost-effectiveness of monovalent vaccine suggest that the vaccine was not cost effective outside high incidence areas. 42 …”