Rickettsiales Occurrence and Co-occurrence in Ixodes ricinus Ticks in Natural and Urban Areas

Abstract

Bacteria of Rickettsiaceae and Anaplasmataceae families include disease agents spread by Ixodes ricinus ticks, the most common tick vector in Europe. The aim of the study was to compare the prevalence and co-infection prevalence of particular tick-transmitted Rickettsiales members: Rickettsia spp. (further referred as Rs), Anaplasma phagocytophilum (Ap), and "Candidatus Neoehrlichia mikurensis" (CNM) in I. ricinus ticks in two types of areas, different in terms of human impact: natural and urban. Using additional data, we aimed at investigating co-occurrence of these Rickettsiales with Borreliella spp. A total of 4189 tick specimens, 2363 from the urban area (Warsaw park and forests) and 1826 from the natural area (forests and park in the vicinity of National Parks), were tested for the presence of Rickettsiales DNA by PCRs. The prevalence of selected Rickettsiales was twice higher in urban than natural areas (13.2% vs. 6.9%, respectively). In total ticks, the prevalence of Rs, Ap, and CNM was 6.5%, 5.3%, and 3.6% in urban areas vs. 4.4%, 1.1%, and 2.1% in natural areas, respectively. Co-infections of Rickettsiales were also more prevalent in urban areas (2.6% vs. 0.3%, respectively). The most common Rs was R. helvetica; also R. monacensis and novel "Candidatus Rickettsia mendelii" were detected. Positive association between Ap and CNM infections was discovered. Rickettsiales bacteria occurrence was not associated with Borreliella occurrence, but co-infections with these two groups were more common in ticks in urban areas. In conclusion, three groups of Rickettsiales constituted the important part of the tick pathogen community in Poland, especially in the urbanized central Poland (Mazovia). In the Warsaw agglomeration, there is a greater risk of encountering the I. ricinus tick infected with Rickettsiales and co-infected with Lyme spirochaetes, in comparison to natural areas. This finding raises the question whether cities might in fact be the hot spots for TBDs.

Keywords: Anaplasma phagocytophilum; City; Co-infection; Ixodes ricinus; Natural; Neoehrlichia mikurensis; Rickettsia helvetica; Rickettsiales; Urban.

Fig. 1

Prevalence of infections and co-infections of selected Rickettsiales in Ixodes ricinus ticks in urban and natural areas. a Prevalence of Rickettsiales in urban and natural areas. b Prevalence of Rickettsiales co-infections in urban and natural areas. c Prevalence of Ap and CNM in urban and natural areas in a group uninfected and infected with a second pathogen (CNM or Ap, respectively). d Prevalence of Rickettsiales and Borreliella spirochaetes (Bs) co-infection in urban and natural areas. Abbreviations: Ap Anaplasma phagocytophilum, CNM “Candidatus Neoehrlichia mikurensis,” Rs Rickettsia spp., Bs Borreliella spp. Asterisk (*) marks the significant differences in observed prevalence values or observed and expected values (Type of area in a, b, and d or infection status in c)

Fig. 2

Seasonal changes of the Rickettsiales prevalence in total ticks (nymphs and adults) during 2012–2015 period. 1 spring-summer season. 2 summer-autumn season. Abbreviations: Ap Anaplasma phagocytophilum, CNM “Candidatus Neoehrlichia mikurensis,” Rs Rickettsia spp.