Borrelia miyamotoi in Saint Petersburg and Leningrad Oblast, Russia: A Multi-Level Assessment of Ticks, Rodents, and Human Exposure

Background: Borrelia miyamotoi is an emerging tick-borne pathogen causing relapsing fever in humans. Although Saint Petersburg and the surrounding Leningrad Oblast harbor a high abundance of ixodid ticks (I. ricinus, I. persulcatus), no integrated assessment has yet simultaneously addressed pathogen circulation in vectors, reservoir hosts, and human populations in this specific northwestern region of Russia. Methods: During 2022–2024, we collected 1518 questing adult ticks and trapped 516 small mammals in Saint Petersburg and Leningrad Oblast. B. miyamotoi DNA was detected by real-time PCR. Sera from 3743 randomly selected volunteers (1553 from Saint Petersburg, 2190 from Leningrad Oblast) were tested for anti-B. miyamotoi IgG/IgM using a protein microarray (antigens: GlpQ, Vmps, flagellin). Infection rates and seroprevalence with 95% Wilson confidence intervals were compared using chi-square tests. Results: The overall tick infection rate was 3.78% (57/1506). I. ricinus had a significantly higher prevalence (4.94%; 95% CI: 3.67–6.60%) than I. persulcatus (2.29%; 95% CI: 1.39–3.74%; p = 0.011). Ticks from Leningrad Oblast also showed markedly elevated infection rates (4.98%; 95% CI: 3.75–6.58%) compared to those from Saint Petersburg (1.89%; 95% CI: 1.06–3.35%; p = 0.004). Small mammals exhibited substantially higher infection rates in Leningrad Oblast (39.44%; 95% CI: 31.78–47.65%) than in Saint Petersburg (13.90%; 95% CI: 10.76–17.78%; p < 0.001). Bank voles (Myodes glareolus) and yellow-necked mice (Apodemus flavicollis) were the main reservoirs; synanthropic rodents trapped within the city were found to be infected for the first time. No significant organotropism was detected, but positive correlations between infection in the heart, liver, and kidney suggested hematogenous dissemination. The overall human seroprevalence of B. miyamotoi was 1.71% (95% CI: 1.34–2.18%) and was significantly higher in Leningrad Oblast (2.19%; 95% CI: 1.66–2.89%) than in Saint Petersburg (1.03%; 95% CI: 0.64–1.67%; p = 0.010). In contrast, the seroprevalence of B. burgdorferi s. l. did not differ between the two regions (approximately 5.1%). Conclusions: This first comprehensive, multi-level investigation in Saint Petersburg and Leningrad Oblast reveals a stable epidemiological gradient: natural foci in Leningrad Oblast sustain higher B. miyamotoi circulation in ticks and rodents, which translates into a two-fold higher exposure of the rural population. The findings highlight the need to include B. miyamotoi in regional tick-borne infection surveillance programs and to adopt differentiated risk assessment strategies for urban and rural settings.