Distribution of Borrelia burgdorferi sensu lato genomic groups in. Europe, a review. Z. Hubálek & J. Halouzka. Institute of Landscape Ecology, Academy of ...
European Journal of Epidemiology 13: 951–957, 1997. 1997 Kluwer Academic Publishers. Printed in the Netherlands.
Distribution of Borrelia burgdorferi sensu lato genomic groups in Europe, a review Z. Hubálek & J. Halouzka Institute of Landscape Ecology, Academy of Sciences of the Czech Republic, Brno, Czech Republic Accepted in revised form 5 June 1997
Abstract. The survey is based on a total of 1263 records (738 isolations and 525 molecular DNA detections) of five Borrelia burgdorferi s.l. genomic groups available from 26 European countries: B. burgdorferi sensu stricto, B. afzelii, B. garinii, B. valaisiana (= VS116) and B. lusitaniae (= PoTiB2). It shows the geographic distribution, the source (ixodid ticks 802 records, fleas 2 records, mosquitoes 2 records, wild mammals 66 records, human patients 391 records) and the association of the genomic groups with particular clinical manifestations of Lyme borreliosis in humans (B. afzelii significantly
prevails in skin lesions whereas B. garinii is more often associated with neuroborreliosis). The most frequent genomic groups in Europe are B. garinii (501 records) and B. afzelii (469 records). They occur across the continent and islands, whereas the third frequent genomic group, B. burgdorferi s.s. (201 records), has only rarely been isolated in eastern Europe. The remaining genomic groups, i.e. B. valaisiana (85 records) and B. lusitaniae (7 records) have only been isolated from, or detected in, Ixodes ricinus ticks in a few European countries.
Key words: Borrelia genospecies, Clinical manifestations, Distribution, Fleas, Ixodid ticks, Lyme borreliosis, Mammals, Mosquitoes
Introduction After revealing a considerable phenotypic and genomic heterogeneity within European isolates of Borrelia burgdorferi [1–5], several studies resulted in the description of at least 13 genomic groups (‘genomovars’, ‘genomospecies’ or species) of the B. burgdorferi sensu lato spirochetes worldwide. B. burgdorferi sensu stricto, B. garinii, B. afzelii (= VS461), B. valaisiana (= VS116: A.P. van Dam, personal communication 1997) and B. lusitaniae (= PoTiB2: D. Postic, personal communication 1997) groups were described in Europe [4–9]. Additional genomic groups were characterized in the USA (e.g., B. andersoni, DN127, CA55, 25015) and Japan (B. japonica, B. miyamotoi, HK501). It is epidemiologically important that different genomic groups of B. burgdorferi s.l. can cause diverse clinical manifestations of Lyme borreliosis (LB) in humans [10–13] although some controversy still exists on this issue [14–15]. For instance, B. burgdorferi s.s. is the common agent of arthritis, while B. afzelii usually predominates in the skin forms (erythema migrans, EM, and especially acrodermatitis chronica atrophicans, ACA) and B. garinii is often associated with neuroborreliosis (e.g., meningoradiculoneuritis). Because the proportion of particular clinical forms varies in European countries [16–17], it has been of interest to analyze the geo-
graphic distribution of different genomic groups of B. burgdorferi s.l. in Europe. Materials and methods Most published data on the isolation and/or DNA detection (by PCR and various molecular techniques) of B. burgdorferi s.l. in Europe have been recorded and stored in our database [1–15, 18–78]. The records include the strain designation, genomic group identification, source, country and year of isolation, and the reference. Some unpublished data have been obtained through the courtesy of D. Postic (B. lusitaniae), A.P. van Dam and M.M. Wittenbrink (B. valaisiana), S.J. Cutler (the UK strains), K. Schwarzová, B. Pet’ko and S. TylewskaWierzbanowska (Slovak and Polish isolates). The total number of available records has been 738 isolates and 525 DNA detections by molecular techniques without the isolation, that were classified in genomic groups; untypified cases (identified as B. burgdorferi s.l.) have been excluded from the analysis. Results and discussion A total of 1263 records of five borrelial genomic groups have been registered in Europe (Table 1): B.
952 Table 1. Geographic distribution of B. burgdorferi s.l. genomic groups in Europe (number of isolations or DNA detections) Genomic group
B. bur.
B. gar.
B. afz.
B. val.
B. lus.
Total
Austria Belarus Belgium Croatia Czechlanda Denmark Finland France Germany Great Britain Hungary Iceland, Faeroe i. Ireland Italy Lithuania Moldavia Netherlands Poland Portugal Russia (Eur. part) Slovakia Slovenia Spain Sweden Switzerland Ukraine
009 000 011 002 000 001 016 014 021 000 000 000 021 011 000 000 030 001 000 000 001 010 001 007 045 000
022 000 020 005 014 005 033 013 137 001 002 003 026 008 002 000 038 005 000 008 011 026 000 051 070 001
030 000 010 038 017 014 019 021 106 001 000 000 016 007 000 000 081 001 000 010 001 055 000 013 029 000
00 00 00 15 00 00 00 00 03 01 00 00 47 00 00 00 15 00 00 00 00 00 00 00 04 00
0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 3 0 0 0 0 0 0 1
061 001 041 060 032 020 068 048 267 003 002 003 110 026 002 001 164 007 003 018 013 091 001 071 148 002
Total
201
501
469
85
7
1263
a
Czech Republic.
garinii 501 records (39.7% of all records), B. afzelii 469 records (37.1%), B. burgdorferi 201 records (15.9%), B. valaisiana 85 records (6.7%), and B. lusitaniae 7 records (0.6%). Geographic distribution of the five B. burgdorferi s.l. genomic groups detected in Europe includes 26 countries (Table 1, Figures 1–4). The bulk of records covers a few countries (Germany, Switzerland, the Netherlands, Ireland, Slovenia, Sweden, Finland, Croatia, France, Belgium, and Austria), whereas no records on borrelial genomic species have been available from Norway, Estonia, Latvia, Romania, Bulgaria, Yugoslavia, Albania, Greece, and European Turkey. However, the distribution reflects the intensity of investigation in particular countries rather than actual geographic occurrence. In a recent review [71], we have stated that B. burgdorferi s.l. spirochetes were detected virtually in all European populations of Ixodes ricinus ticks examined. Because I. ricinus occurs in every European country (except for Iceland), B. burgdorferi s.l. (and human LB cases as well) should be present in all countries of Europe. The two most frequent European genomic groups, B. garinii and B. afzelii, occur over the whole continent, whereas the third frequent genomic group, B. burgdorferi s.s., has only rarely been isolated or
detected in eastern Europe (Poland, Slovakia). The remaining genomic groups, i.e. B. valaisiana and B. lusitaniae have been isolated from, or detected in, I. ricinus ticks in a few countries. The source of individual genomic groups of B. burgdorferi s.l. is given in Table 2. Most of them were isolated from, or detected in, ixodid ticks (63.5% of records) and human patients (31.0% of records), less often rodents (3.0% of records), other wild mammals (Erinaceus europaeus and Vulpes vulpes, 2.2% of records: 59, 60), fleas (Ctenophthalmus agyrtes collected on forest rodent: 70) and mosquitoes (Aedes vexans: 69). B. garinii has predominated among tick isolates (including six notable records from the seabird tick Ixodes uriae in N. Europe, partially outside the range of I. ricinus: 65), whereas B. afzelii has been more frequently recorded in human patients. However, this result may be greatly affected by the frequency of isolation and detection assays done in particular arthropod and mammalian groups. Table 2 gives some idea about the association of different borrelial genomic groups with human clinical manifestations of LB. B. afzelii significantly predominates (80.7% of particular records) among human skin isolates (EM, and especially ACA cases),
953
Figure 1. European distribution of Borrelia burgdorferi sensu stricto.
Figure 2. European distribution of Borrelia garinii.
Figure 3. European distribution of Borrelia afzelii.
Figure 4. European distribution of Borrelia valaisiana (VS116 – black points) and B. lusitaniae (PoTiB2 – asterisks).
Table 2. Distribution of B. burgdorferi s.l. genomic groups according to the source (host) in Europe (number of isolations or DNA detections) Genomic group
B. bur.
B. gar.
B. afz.
B. val.
B. lus.
Total
Ixodid ticks Mosquitoes Fleas Rodent organs Rodent skin Hedgehog skin Fox skin Human skin Human CSF Other body fluidsa
163 000 000 000 000 000 000 012 006 020
350 000 000 007 000 001 027 038 055 023
197 002 002 015 016 000 000 209 015 013
85 00 00 00 00 00 00 00 00 00
7 0 0 0 0 0 0 0 0 0
802 002 002 022 016 001 027 259 076 056
a
Human blood or synovial fluid.
954 whereas B. garinii in the cerebrospinal fluid (72.4% of particular records) from patients with neuroborreliosis (p < 0.001: χ2 test, Fisher’s exact test), as described previously by a number of investigators [10–13, 15, 68]. The latter species has also been frequent among the blood isolates. Interestingly, the proportion of borrelial genomic groups in ixodid ticks seems to be more similar to that in CSF records than to that in skin records. Different genomic groups of B. burgdorferi s.l. are often present in an I. ricinus population in one area simultaneously [28, 36, 45, 50, 54, 74, 76], and even in individual ticks [51, 61, 72–74, 78]. For instance, B. garinii, B. afzelii and B. burgdorferi s.s. were detected in I. ricinus ticks collected from an area
