Lyme disease is common in North-Western Russia, including the southern areas of the Arkhangelsk province. Two Borrelia genotypes (B. afzelii and B. garinii) are found among ticks in the Arkhangelsk province, and every tenth tick is dually infected by both genotypes. Lower incidences of Lyme disease in the Arkhangelsk province in comparison with other north-western provinces is likely the consequence of differences in climate conditions, but under-diagnosis of Lyme disease may also be of importance.
Lyme disease (Lyme borreliosis) is wide spread in the Russian Federation. Natural foci of this infection have been registered in different geographical zones of Russia; from the western borders to southern Sakhalin . Lyme disease is also prevalent in the north-western region of the country [2-7], although ticks have not been tested for Borrelia burgdorferi sensu lato in large areas of this region.
In the Arkhangelsk province the distribution of ticks, the vector of the Lyme disease agent, differs with geographical zones. Ticks are wide spread in the southern forest areas of the province, but have not been found in the northern tundra zones.
The aim of this study was to investigate the incidence and to analyse epidemiological data on Lyme disease in the Arkhangelsk province, as well as to determine bacterial genotypes.
Material and methods
The Arkhangelsk province is located in the northern part of the Russian Federation. The territory is 587,000 square kilometres, and the population is approximately 1.5 million people (urban population 1.1 million; rural population 0.4 million). The province is characterised by different climatic zones including polar tundra, forest tundra and forest.
The local sanitary-epidemiological institutions are required to register all cases of Lyme disease and tick bites in addition to epidemiological information. Reports are submitted monthly to the Republican Centre for Sanitary-Epidemiological Surveillance. Since persons experiencing tick bites do not seek medical care, the vast majority of tick bites are not registered. Official epidemiological data from cases registered in 1992-2001 in addition to data on tick bites from the same period were analysed in this study.
The polymerase chain reaction (PCR) with primers to gene p66 was used to detect Borrelia burgdorferi sensu lato in 190 ticks collected in nine areas of Arkhangelsk province. Genospecies characteristics of the agents were also determined. An enzyme immunoassay containing recombinant Borrelia antigens (p41, DbpA, OspC, and p66) was used to detect IgG antibodies in 101 serum samples from persons living in the Nenets autonomous district (a tundra zone that is free of ticks) and in 83 serum samples from persons bitten by ticks in the southern areas. To calculate the ratio between tick infectivity and the disease frequency, the number of persons bitten was divided by the average proportion of ticks infected with Borrelia burgdorferi and by the number of Lyme disease cases.
Results and discussion
In the 1990s, the number of Lyme disease cases in the Arkhangelsk province grew steadily, partly due to improvements in clinical and laboratory diagnostics (Figure 1).
Fig 1. Number of patients with Lyme borreliosis in the Arkhangelsk province during 1992-2001
However, the Arkhangelsk province had the lowest incidence and a slower increase in incidence of Lyme disease in the Russian Federation's north-western territories (Figure 2).
Fig 2. Incidence of Lyme borreliosis in the Arkhangelsk and Vologda provinces during 1992-2001 in comparison with the whole country
Nevertheless, 13,638 persons bitten by ticks and 219 patients with Lyme disease were registered in the province during the ten year period 1992-2001, making Lyme disease more common than many other infections with natural foci (leptospirosis, tick-borne encephalitis and haemorrhagic fever with renal syndrome). The average incidence rate was 2.6 cases per 100,000 persons; two times lower than in the whole country and eight times lower than in the neighbouring Vologda province.
The seasonal distribution of cases correlated with tick activity, with over 90 % of the patients registered in the period May to August. The disease was rarely observed among children. Only 5.4 % of the cases were diagnosed in the age group up to 14 years. Half the cases were diagnosed in patients 20-60 years of age, and a substantial number of cases were diagnosed in retired persons.
Between 1999 and 2001, a significant increase in tick bites was noted (Figure 3).
Fig 3. Number of persons bitten by ticks in the Arkhangelsk province during1992-2001.
Close contact with the nature (summer-houses, mushroom- and berry-picking, hunting, fishing etc.) was a risk factor for tick bites. There was, however, no correlation between incidence of Lyme disease and the profession of the patients. Most persons (56.8% of cases) were infected as a result of tick bites contracted when working in their gardens.
Among 53 % of the patients the disease developed within 7 to 14 days after the tick bite. The incubation period was less than 7 days in 30 % of the patients, and in some patients the disease did not develop until 3 to 4 weeks after the tick bite. Two fifth of the patients (42 %) had fever, with temperatures between 38 and 39_C.
Annular erythema at the site of the tick bite was used as diagnostic criteria of Lyme disease in the patients. Since many patients with the disease do not have this typical skin lesion, it can be concluded that many cases of Borrelia infection were not diagnosed in the Arkhangelsk province. This conclusion was supported by data from seroepidemiological studies. In the southern areas, IgG antibodies were detected in 17 of 83 persons with tick bites and a titre increase was registered in nine persons. Clinical signs and symptoms of Lyme disease were registered in 13 of these persons (76% of persons with specific antibodies). The use of enzyme immunoassay allowed the diagnosis of four additional cases of Lyme disease. The specificity of the assay was very good and the analyses yielded no false positive results in samples from 101 patients from the northern areas of Arkhangelsk province where Lyme disease has not been reported.
Twenty-six percent of the ticks investigated (Ixodes persulcatus) were infected with Borrelia burgdorferi sensu lato. The frequency of tick infection varied between the different districts of the province. The overall ratio between tick infectivity and disease frequency in persons bitten by ticks was approximately 16:1 as compared to a ratio of 3:1 in St. Petersburg . This difference may partly be the consequence of better health care provision in St. Petersburg, and the subsequent under-diagnosis of Lyme disease in the Arkhangelsk province.
Two Borrelia genotypes were detected among the collected ticks; Borrelia afzelii (74 % of the ticks) dominated over Borrelia garinii (16 % of the ticks). Ten percent of the ticks were infected with both Borrelia genotypes.
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