Expanding range of Ixodes scapularis Say (Acari: Ixodidae) and Borrelia burgdorferi infection in North Carolina counties, 2018-2023

Abstract

North Carolina (NC) has been experiencing a recent surge in human Lyme disease (LD) cases. Understanding the distribution of tick-borne diseases necessitates understanding the distribution of the ticks that transmit their causative pathogens. Unfortunately, in NC, knowledge on tick distribution is outdated. In this manuscript, we report the results of a state-wide entomologic survey conducted in 42 NC counties by flagging/dragging from spring 2018 to summer 2023. Ixodes scapularis nymphs and adults were screened for Borrelia burgdorferi (the causative agent of LD) and four other tick-borne bacterial pathogens (Anaplasma phagocytophilum, B. mayonii, B. miyamotoi, and Babesia microti) by the Centers for Disease Control and Prevention (CDC). Consistent with current data on human LD cases incidence and distribution, results of this study indicated a range expansion of I. scapularis with higher tick densities and B. burgdorferi infection prevalence now occurring in the Blue Ridge Mountains province of western NC. Temporal analysis of I. scapularis presence data indicated that this shift is fairly recent (about 10 years). Finally, in the Blue Ridge Mountains we detected a northeast-to-southwest gradient in I. scapularis tick and B. burgdorferi infection prevalence suggesting that this trend is driven by a spread of the northern clade I. scapularis ticks into NC from southwestern Virginia, along the Appalachian Mountains. Other pathogenic bacteria detected in I. scapularis ticks included B. miyamotoi and A. phagocytophilum, that were limited to the Blue Ridge Mountains. These results have important public health implications, including the need for enhanced tick surveillance, updated clinical awareness, and targeted public education in newly affected areas.

Fig 1. Statewide distribution and regional comparison of Ixodes scapularis nymph density and Borrelia burgdorferi infection prevalence in North Carolina.

(A) County-level distribution of I. scapularis nymph densities (number per 100 m transect). Bold lines separate the three major physiogeographic provinces of North Carolina: Mountains, Piedmont, and Coastal Plain (going from west to east, respectively). (B) Comparison of mean nymph density (±95% CI) across the three major physiogeographic provinces of North Carolina. N represents the total number of transects surveyed. Z and P values are from a negative binomial GLMM. (C) County-level distribution of B. burgdorferi infection prevalence in I. scapularis nymphs (for counties with > 6 nymphs) (D) Comparison of B. burgdorferi infection prevalence (±95% binomial CI) in nymphs across the three physiogeographic provinces. N denotes the number of nymphs tested. Z and P values are derived from a weighted logistic regression. Different letters indicate statistically significant differences among regions.

Fig 2. Statewide distribution and regional comparison of Ixodes scapularis adult tick density and Borrelia burgdorferi infection prevalence in North Carolina.

(A) County-level distribution of I. scapularis adult densities (number per 100 m transect). Bold lines separate the three major physiogeographic provinces of North Carolina: Mountains, Piedmont, and Coastal Plain (going from from west to east, respectively). (B) Comparison of mean adult tick density (±95% CI) across the three major physiogeographic provinces of North Carolina. N represents the total number of transects surveyed. Z and P values are from a negative binomial GLMM. (C) County-level distribution of B. burgdorferi infection prevalence in I. scapularis adults (for counties with > 6 adult ticks). (D) Comparison of B. burgdorferi infection prevalence (±95% binomial CI) in adults across the three physiogeographic provinces. N denotes the number of nymphs tested. Z and P values are derived from a weighted logistic regression. Different letters indicate statistically significant differences among regions.

Fig 3. Change in presence status of blacklegged ticks (Ixodes scapularis) in North Carolina counties.

(A) Presence status for 1907-1996 (Source: Dennis et al. [26]). (B) Cumulative presence status for 1907-2015 (Source: Eisen et al. [27]). (C.) Cumulative presence status for 1907-2023 (this study). The color of the counties indicates the ‘presence category’ status of I. scapularis: white for ‘not detected or not surveyed’, green for ‘reported’ (defined as < 6 individuals of a single life stage), and red for ‘established’ (defined as at least 6 individuals of the same life stage or at least a single individual of at least two different life stages collected in one year). Bold lines separate the map into the three physiographic provinces of NC: Blue Ridge Mountains (left or west), Piedmont (middle or central), and Coastal Plain (right or east).

Fig 4. The effect of latitude (of sampling site) on I. scapularis density and Bb infection prevalence.

Panels A and B, depict these patterns for nymphs and panels C and D, present these data for adult ticks. Regression equation, P-value, and R² are derived from respective GLMM models (negative binomial for tick density and logistic regression for prevalence). The bands around the lines-of-best-fit are standard error margins.