High Diversity and Prevalence of Borrelia burgdorferi sensu lato in Wildlife Hosts, Domestic Animals, and Ticks in Yunnan Province, Southwestern China

Zhihai He; Baogui Jiang; Lin Huang; Zongti Shao; Yun Zhang; Yuqiong Li; Ennian Pu; Xingde Duan; Hang Jiang; Jian Wang; Mingguo Yao; Fan Wang; Shuangshuang Bie; Michael E von Fricken; Yi Sun; Yi Dong; Jiafu Jiang; Chunhong Du

doi:10.3389/fmicb.2022.876079

High Diversity and Prevalence of Borrelia burgdorferi sensu lato in Wildlife Hosts, Domestic Animals, and Ticks in Yunnan Province, Southwestern China

Front Microbiol. 2022 May 4:13:876079. doi: 10.3389/fmicb.2022.876079. eCollection 2022.

Authors

Zhihai He^{1

2}, Baogui Jiang³, Lin Huang^{3

4}, Zongti Shao¹, Yun Zhang¹, Yuqiong Li¹, Ennian Pu¹, Xingde Duan¹, Hang Jiang¹, Jian Wang¹, Mingguo Yao¹, Fan Wang¹, Shuangshuang Bie¹, Michael E von Fricken⁵, Yi Sun³, Yi Dong¹, Jiafu Jiang³, Chunhong Du¹

Affiliations

¹ Yunnan Institute of Endemic Diseases Control and Prevention, Yunnan, China.
² Longgang Center for Disease Control and Prevention of Shenzhen, Guangdong, China.
³ State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.
⁴ Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, Hefei, China.
⁵ Department of Global and Community Health, George Mason University, Fairfax, VA, United States.

Abstract

Borrelia burgdorferi sensu lato (BBSL), the causative agent of Lyme disease, is commonly found in wild and domestic mammals and ticks worldwide. In China, human cases of Borrelia burgdorferi infections have been identified across a wide geographic range including Yunnan Province, but few studies have examined BBSL in reservoirs and vectors in southwestern China. Here we conducted a thorough and broad-range investigation of BBSL in small mammals, domestic mammals, and ticks collected from 159 sample sites across 42 counties in Yunnan Province. DNA was extracted from spleen tissue of small mammals, blood from domestic mammals, and homogenized ticks. Nested PCR targeting the 5S-23S rRNA intergenic spacer gene of BBSL was used for screening, with amplicons sequenced directly and analyzed using a BLAST algorithm. A total of 8,478 samples were collected, which were composed of 5,044 mammals belonging to 68 species, 1,927 livestock belonging to five species, and 1, 507 ticks belonging to 14 species. BBSL was detected in 147 mammals (2.9%) from 30 different species, 20 of which represent the first reported detection in that species. A total of 52 (2.7%) livestock samples were positive for BBSL, with dogs having the highest detection rate (6.3%, 43/687), and 103 ticks (6.8%) tested positive with high prevalence in Ixodes granulatus (44.2%, 23/52), Haemaphysalis nepalensi (33.3%, 3/9) and Haemaphysalis kolonini (19.0%, 31/163). Sequence analysis revealed six genospecies of BBSL including B. afzelii, B. burgdorferi sensu stricto, B. japonica, B. garinii, B. sinica, and B. valaisiana. Significant differences in prevalence rates of BBSL were observed by species, landscape types, altitude, and season. Our findings indicate a wide distribution of multiple endemic BBSL genospecies based on a large-scale survey within Yunnan, which underline the need to expand surveillance efforts for human in southwestern China.

Keywords: Borrelia burgdorferi sensu lato; China; domestic mammals; lyme disease; small mammals; ticks.