Globalisation of Lyme borreliosis
Authors: Stephen W Barthold
Journal: The Lancet (1996)

Borrelia burgdorferi, the agent of Lyme disease, belongs to a genospecies complex (B burgdorferisensu lato) genetically divided into B burgdorferisensu stricto, B garinii, B afzelii, B japonica, B andersoni, and other, less distinct subdivisions.1Assous MV Postic D Paul G Nevot P Baranton G Individualisation of two genomic groups among American Borrelia burgdorferisensu lato.FEMS Microbiol Lett. 1994; 121: 93-98Crossref PubMed Scopus (45) Google Scholar In parts of Europe B burgdorferiss, B afzelii, and B gariniiare all represented in the same region, mixed infections being reported in individual patients as well as in ticks.2Demaerschalck I BenMessaoud A DeKesel M Hyois B Lobet Y Hoet P Bigaignon G Bollen A Godfroid E Simultaneous presence of different Borrelia burgdorferigenospecies in biological fluids of Lyme disease patients.J Clin Microbiol. 1995; 33: 602-608PubMed Google Scholar, 3Guttman DS Wang PW Wang IN Bosler EM Luft BJ Dykhuizen DE Multiple infections of Ixodes scapularisticks by Borrelia burgdorferias revealed by single-strand conformation polymorphism analysis.J Clin Microbiol. 1996; 34: 652-656PubMed Google Scholar North American B burgdorferiisolates are also genetically diverse. Despite this heterogeneity, the genus Borreliahas a clonal population structure,5Dykhuizen DE Polin DS Dunn JJ Wilske B PreacMursic V Dattwyler RJ Luft BJ Borrelia burgdorferiis clonal: implications for taxonomy and vaccine development.Proc Natl Acad Sci USA. 1993; 90: 10163-10167Crossref PubMed Scopus (142) Google Scholar which suggests that genetic diversity1Assous MV Postic D Paul G Nevot P Baranton G Individualisation of two genomic groups among American Borrelia burgdorferisensu lato.FEMS Microbiol Lett. 1994; 121: 93-98Crossref PubMed Scopus (45) Google Scholar, 4Zingg BC Brown RN Lane RS LeFebvre RB Genetic diversity among Borrelia burgdorferiisolates from wood rats and kangaroo rats in California.J Clin Microbiol. 1993; 31: 3109-3114PubMed Google Scholar has resulted from evolution within separate ecosystems. A perspective on why there is heterogeneity among B burgdorferiisolates within the same geographic regions can be realised through an understanding of the palaeoarchaeology of Ixodes persulcatuscomplex ticks.6Filippova NA A hypothesis for the paleogenesis of the distribution of the main vectors for Lyme disease.in: Modern acarology. vol 1. Prague and SPB Academic Publishing, The Hague: Academia1991: 109-118Google Scholar The principal vectors of B burgdorferisl are I ricinusin central and western Europe, I persulcatusin the subarctic regions from the Baltic Sea to the Pacific Ocean, I scapularisin the northeast and midwest USA, and I pacificusin western USA. These are the dominant species today but historically the ranges of members of the I persulcatuscomplex differed, and many contemporary I persulcatustick species have only minor geographic ranges because of host selectivity and because the advance and retreat of the last Ice Age critically influenced the environment, flora, and fauna that these species depend upon. In Europe and Asia, only I ricinusand I persulcatus, respectively, have survived as geographically widespread, successful species. These geographic events, occurring over many thousands of years, probably created unique and isolated reservoir habitats conducive to coevolution of genetically distinct tick populations and the B burgdorferithey carried. Even today, B burgdorferiss is generally restricted to I ricinusin western Europe, whereas B afzeliiand B gariniiare associated with I persulcatusin Eurasia. Mixing of B burgdorferi (in which B burgdorferiss, B afzelii, and B garinii)and/or genetic diversity among isolates within each of the genospecies probably took place as the range of these dominant tick species expanded, and their reservoir hosts and enzootic cycles intermixed. The mixing has been favoured by the non-selective host preferences of most B burgdorferiisolates and of I persulcatus, I ricinus, I scapularis, and I pacificus. Several recent reports have described a seabird enzootic cycle of B garinii in Sweden, maintained by I uriaeticks in the absence of traditional terrestrial reservoir hosts and tick vectors. The circumpolar distribution of I uriaeand B gariniicontributes to north-south transhemispheric exchange of spirochaetes among seabirds.7Bunikis J Olsen B Fingerle V Bonnedahl J Wilske B Bergstron S Molecular polymorphism of the Lyme disease agent Borrelia gariniiin Northern Europe is influenced by a novel enzootic Borreliafocus in the North Atlantic.J Clin Microbiol. 1996; 34: 364-368PubMed Google Scholar This enzootic cycle is represented by a genetically homogeneous population of B garinii.By contrast, migratory passerine birds in Sweden are parasitised by I ricinusand I persulcatus, which are infected with genetically diverse B burgdorferiss, B afzelii, and B garinii.The types of ticks and B burgdorferisl isolates obtained from migratory passerine (perching) birds correlated with migration routes of the birds.7Bunikis J Olsen B Fingerle V Bonnedahl J Wilske B Bergstron S Molecular polymorphism of the Lyme disease agent Borrelia gariniiin Northern Europe is influenced by a novel enzootic Borreliafocus in the North Atlantic.J Clin Microbiol. 1996; 34: 364-368PubMed Google Scholar Migratory birds also contribute to the dissemination of mixing of B burgdorferiin North America.8Anderson JF Magnarelli LA Stafford III, KC Bird-feeding ticks transstadially transmit Borrelia burgdorferithat infect Syrian hamsters.J Wildlife Dis. 1990; 26: 1-10Crossref PubMed Scopus (71) Google Scholar Thus birds contribute to terrestrial enzootic cycles of B burgdorferi, either as transporters of infected ticks or as reservoir hosts of B burgdorferi.Even though the seabird/I uriaeenzootic cycle is ecologically isolated from terrestrial B burgdorferienzootic cycles in Europe, there are regions of geographic overlap between I uriaeand I ricinusin the northern Baltic Sea7Bunikis J Olsen B Fingerle V Bonnedahl J Wilske B Bergstron S Molecular polymorphism of the Lyme disease agent Borrelia gariniiin Northern Europe is influenced by a novel enzootic Borreliafocus in the North Atlantic.J Clin Microbiol. 1996; 34: 364-368PubMed Google Scholar allowing “bridging” between these enzootic cycles. Some enzootic cycles, such as the sea bird cycle, remain relatively unaltered, involving homogeneous genetic populations of B burgdorferiwithin ecologically isolated host-tick niches. Such cycles present a glimpse of how B burgdorferimay have evolved into its genetically distinct subdivisions. Other examples of ecologically isolated niches include B burgdorferiinfection in dusky-footed wood rats in California maintained by I neotomae9Brown RN Lane RS Lyme disease in California: a novel epizootic transmission cycle of Borrelia burgdorferi..Science. 1992; 256: 1439-1442Crossref PubMed Scopus (204) Google Scholar and infection of Mexican wood rats in Colorado by I spinipalpis.10Maupin GO Gage KL Piesman J Motenieri J Sviat SL VanderZasnden L Happ CM Dolan M Johnson BJB Discovery of an enzootic cycle of Borrelia burgdorferiin Neotoma mexicanaand Ixodes spinipalpisfrom Northern Colorado, an area where Lyme disease in nonendemic.J Infect Dis. 1996; 170: 636-643Crossref Scopus (84) Google Scholar In California, bridging occurs via I pacificus, whereas in Colorado a bridge vector is not present.4 In Japan, there are at least two enzootic cycles, involving I persulcatusand I ovatus. B burgdorferiisolates from I persulcatusin Japan are genetically diverse, reminiscent of B burgdorferiisolates on the mainland, whereas B burgdorferiisolates from I ovatusare genetically unique (B japonica) and homogeneous.11Nakao M Miyamoto K Uchikawa K Fujita H Characterization of Borrelia burgdorferiisolated from Ixodes persulcatusand Ixodes ovatusticks.Am J Trop Med Hyg. 1992; 47: 505-511PubMed Google Scholar In Connecticut, B andersoniin maintained in cottontail rabbits by I dentatus. Some of the above examples involve ticks (I uriae, neotomae, spinipalpis, ovatus) that do not belong to the I persulcatuscomplex. Quite possibly, these niches are evidence of bridging, in which I persulcatus-derived B burgdorferiinitially infected these hosts, and enzootic cycles subsequently evolved separately within isolated niches following climatic change. Conversely, there may be evidence of a far more archaic association with B burgdorferi, before the I persulcatuscomplex branched from the Ixodesfamily tree. What now exists in Eurasia and North America is a highly distorted amalgamation of ecosystems taken over by dominant reservoir hosts and vectors, and mixed by migratory birds and bridging vectors following retreat of the last Ice Age. Further perturbation of the environment and influence on enzootic cycles has occurred by human habitation. Lyme disease is an outstanding example of the complex natural history of an infectious disease emerging in the modern world.