Tick Exposure Patterns and Associated Risk Factors in Northeastern China

Abstract

Background: In northeastern China, tick-borne diseases pose a major public health challenge, which is exacerbated by environmental and anthropogenic changes. This study was aimed at assessing the risk of tick bites and the effectiveness of protective measures in an endemic region, and investigating the influences of socio-demographic, behavioral, and landscape factors.

Methods: A comprehensive online survey was conducted among 3000 participants from Heilongjiang, Liaoning, and Jilin provinces between July and August 2022. Data on self-reported tick bites, protective measures, and associated socio-demographic characteristics were gathered. Landscape analysis was conducted with satellite imagery, and the Shannon diversity index (SHDI) and forest patch density (PD) were selected to quantify landscape factors. Factors influencing tick bite incidence were identified with a logistic regression model, and linkages between landscape characteristics and exposure risk were assessed with spatial statistics.

Results: Twenty-one percent of respondents reported experiencing tick bites, primarily during the active tick season (May to October). The self-reported incidence of tick-borne diseases (e.g., tick-borne encephalitis (TBE), Lyme disease (LD), and severe fever with thrombocytopenia syndrome (SFTS)) varied across provinces, and notable socio-demographic factors (e.g., age, gender, occupation, and lifestyle) associated with tick exposure were identified. Adoption of protective measures was high (80.3%) among the surveyed population, particularly among those who had previously experienced tick bites. Landscape analysis revealed an inverse relationship between land use diversity and tick bite incidence, thus suggesting that areas with lower land use diversity might have higher tick bite risk.

Conclusions: The study highlights the multifaceted nature of tick-borne disease risk in northeastern China and the importance of integrated strategies encompassing awareness, behavioral change, and environmental management to decrease tick exposure and prevent disease transmission. These insights might assist public health authorities in developing targeted interventions to combat the spread of tick-borne diseases in the region.

Keywords

Tick Exposure / Protective Measures / Northeastern China / Land Use Diversity / Socio-Demographic Factors

References

[1] Men X, Du H, Cai X, Fu L, Zhu Y. Meta analysis of TBEV prevalence in ticks and human populations in China. Chin J Zoonoses. 2021; 37: 631-638.

[2] Parola P, Raoult D. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis. 2001; 32(6): 897-928.

[3] Liu G, Ren QM, He SX, Wang F, Yang J. Distribution and medical importance of ticks in three provinces of northeast China. Chin J Hyg Insectic Equip. 2008; 14(1): 39-42.

[4] Bogovic P, Strle F. Tick-borne encephalitis: a review of epidemiology, clinical characteristics, and management. World J Clin Cases. 2015; 3(5): 430-441.

[5] Yin D, Liu R. Review on the control of forest encephalitis in the forest areas of north-east China. Chin J Epidemiol. 2000; 21: 387-389.

[6] Wu XB, Na RH, Wei SS, Zhu JS, Peng HJ. Distribution of tick-borne diseases in China. Parasit Vectors. 2013; 6: 119.

[7] Li J, Chang J, Wang F, Liang G. The seminar on prevention and control of forest encephalitis in China was held in Changchun. Chin J Zoonoses. 2020; 36: 964.

[8] Yang Y, Du YD. Progress in research of tick-borne encephalitis. Chin J Epidemiol. 2016; 37(10): 1435-1438.

[9] Zhang Z, Zhang J, Zhu G, Tian D, Zhang Z, Wan K, et al. Investigation of Lyme disease in northeast of China. Chin J Epidemiol. 1989; 10(5): 261-264.

[10] Deng B, Zhou B, Zhang S, Zhu Y, Han L, Geng Y, et al. Clinical features and factors associated with severity and fatality among patients with severe fever with thrombocytopenia syndrome Bunyavirus infection in northeast China. PLoS One. 2013; 8(11): e80802.

[11] Liu Z, Li L, Xu W, Yuan Y, Liang X, Zhang L, et al. Extensive diversity of RNA viruses in ticks revealed by metagenomics in northeastern China. PLoS Negl Trop Dis. 2022; 16(12): e0011017.

[12] Zhang G, Zheng D, Tian Y, Li S. A dataset of distribution and diversity of ticks in China. Sci Data. 2019; 6(1): 105.

[13] Sormunen JJ, Kulha N, Klemola T, Mäkelä S, Vesilahti EM, Vesterinen EJ. Enhanced threat of tick-borne infections within cities? Assessing public health risks due to ticks in urban green spaces in Helsinki, Finland. Zoonoses Public Health. 2020; 67(7): 823-839.

[14] Hansford KM, Fonville M, Gillingham EL, Coipan EC, Pietzsch ME, Krawczyk AI, et al. Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks Tick Borne Dis. 2017; 8(3): 353-361.

[15] Heylen D, Lasters R, Adriaensen F, Fonville M, Sprong H, Matthysen E. Ticks and tick-borne diseases in the city: role of landscape connectivity and green space characteristics in a metropolitan area. Sci Total Environ. 2019; 670: 941-949.

[16] Li S, Juhász-Horváth L, Trájer A, Pintér L, Rounsevell MDA, Harrison PA. Lifestyle, habitat and farmers’ risk of exposure to tick bites in an endemic area of tick-borne diseases in Hungary. Zoonoses Public Health. 2018; 65(1): e248-e253.

[17] Vanwambeke SO, Lambin EF, Meyfroidt P, Asaaga FA, Millins C, Purse BV. Land system governance shapes tick-related public and animal health risks. J Land Use Sci. 2024; 19(1): 78-96.

[18] Garcia-Martí I, Zurita-Milla R, Swart A, van den Wijngaard KC, van Vliet AJH, Bennema S, et al. Identifying environmental and human factors associated with tick bites using volunteered reports and frequent pattern mining. Trans GIS. 2016; 21(2): 277-299.

[19] Ghane Kisomi M, Wong LP, Tay ST, Bulgiba A, Nizam QNH. A qualitative study to explore farmworkers’ knowledge, beliefs and preventive practices toward ticks and tick-borne diseases. J Infect Dev Ctries. 2019; 13(12): 1117-1126.

[20] Li P, Yao C, Wang T, Wu T, Yi W, Zheng Y, et al. Recovery of a Far-Eastern strain of tick-borne encephalitis virus with a full-length infectious cDNA clone. Virol Sin. 2021; 36(6): 1375-1386.

[21] Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a one health perspective. Trends Parasitol. 2012; 28(10): 437-446.

[22] Piesman J, Eisen L. Prevention of tick-borne diseases. Annu Rev Entomol. 2008; 53: 323-343.

[23] Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012; 379(9814): 461-473.

[24] Vázquez M, Muehlenbein C, Cartter M, Hayes EB, Ertel S, Shapiro ED. Effectiveness of personal protective measures to prevent Lyme disease. Emerg Infect Dis. 2008; 14(2): 210-216.

[25] Connally NP, Durante AJ, Yousey-Hindes KM, Meek JI, Nelson RS, Heimer R. Peridomestic Lyme disease prevention: results of a population-based case-control study. Am J Prev Med. 2009; 37(3): 201-206.

[26] Ghane Kisomi M, Wong LP, Tay ST, Bulgiba A, Zandi K, Kho KL, et al. Factors associated with tick bite preventive practices among farmworkers in Malaysia. PLoS One. 2016; 11(6): e0157987.

[27] Eisen L. Personal protection measures to prevent tick bites in the United States: knowledge gaps, challenges, and opportunities. Ticks Tick Borne Dis. 2022; 13(4): 101944.

[28] Sun RX, Lai SJ, Yang Y, Li XL, Liu K, Yao HW, et al. Mapping the distribution of tick-borne encephalitis in mainland China. Ticks Tick Borne Dis. 2017; 8(4): 631-639.

[29] Wu Y, Zhou Q, Mao M, Chen H, Qi R. Diversity of species and geographic distribution of tick-borne viruses in China. Front Microbiol. 2024; 15: 1309698.

[30] Concepción ED, Díaz M, Baquero RA. Effects of landscape complexity on the ecological effectiveness of agri-environment schemes. Landscape Ecol. 2007; 23(2): 135-148.

[31] Liu J, Coomes DA, Gibson L, Hu G, Liu J, Luo Y, et al. Forest fragmentation in China and its effect on biodiversity. Biol Rev Camb Philos Soc. 2019; 94(5): 1636-1657.

[32] Su N, Jarvie S, Yan Y, Gong X, Li F, Han P, et al. Landscape context determines soil fungal diversity in a fragmented habitat. Catena. 2022; 213: 106163.

[33] Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996; 49(12): 1373-1379.

[34] Zhou H, Long L. Statistical remedies for common methods biases. Adv Psychol Sci. 2004; 12(6): 942-950.

[35] Salmerón Gómez R, García Pérez J, López Martín MDM, García CG. Collinearity diagnostic applied in ridge estimation through the variance inflation factor. J Appl Stat. 2016; 43(10): 1831-1849.

[36] Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982; 143(1): 29-36.

[37] Nahm FS. Receiver operating characteristic curve: overview and practical use for clinicians. Korean J Anesthesiol. 2022; 75(1): 25-36.

[38] Liu Y, Chen L, Li M, Ren G, Yan D, Zhu J, et al. Investigation on the first natural focus of forest encephalitis in the Greater Khingan Mountains forest area. Chin Prim Health Care. 1996; 10(12): 42-43.

[39] Septfons A, Figoni J, Gautier A, Soullier N, de Valk H, Desenclos JC. Increased awareness and knowledge of Lyme Borreliosis and tick bite prevention among the general population in France: 2016 and 2019 health barometer survey. BMC Public Health. 2021; 21(1): 1808.

[40] Zajc V, Sroka J, Wójcik-Fatla A . Knowledge, protection behaviours and seroprevalence of Lyme borreliosis in inhabitants of Lublin Province, eastern Poland - evaluation of a prophylaxis programme. Ann Agric Environ Med. 2023; 30(3): 413-424.

[41] Beck A, Solomon J, Hinckley AF, Nelson CA. Tick bite frequency, prevention practices and Lyme disease diagnoses among U.S. Hispanic survey respondents. Zoonoses Public Health. 2021; 68(6): 658-665.

[42] Cuadera MKQ, Mader EM, Safi AG, Harrington LC. Knowledge, attitudes, and practices for tick bite prevention and tick control among residents of Long Island, New York, USA. Ticks Tick Borne Dis. 2023; 14(3): 102124.

[43] Zöldi V, Turunen T, Lyytikäinen O, Sane J. Knowledge, attitudes, and practices regarding ticks and tick-borne diseases, Finland. Ticks Tick Borne Dis. 2017; 8(6): 872-877.

[44] Narita T, Abeywickrama HM, Sato MO, Watanabe K, Arai R, Tamura T, et al. Knowledge, attitudes, and practices regarding tick-borne diseases among an at-risk population living in Niigata prefecture, Japan. PLoS One. 2022; 17(6): e0270411.

[45] Kianersi S, Luetke M, Wolfe CG, Clark WA, Omodior O. Associations between personal protective measures and self-reported tick-borne disease diagnosis in indiana residents. J Community Health. 2020; 45(4): 739-750.

[46] Schwartz AM, Mackeprang JM, Mead PS, Hinckley AF. Effectiveness of personal protection measures against Lyme disease: a review of epidemiologic studies from the United States. Zoonoses Public Health. 2022; 69(7): 777-791.

[47] Gupta S, Eggers P, Arana A, Kresse B, Rios K, Brown L, et al. Knowledge and preventive behaviors towards tick-borne diseases in Delaware. Ticks Tick Borne Dis. 2018; 9(3): 615-622.

[48] Aenishaenslin C, Michel P, Ravel A, Gern L, Milord F, Waaub JP, et al. Factors associated with preventive behaviors regarding Lyme disease in Canada and Switzerland: a comparative study. BMC Public Health. 2015; 15: 185.

[49] Aenishaenslin C, Bouchard C, Koffi JK, Ogden NH. Exposure and preventive behaviours toward ticks and Lyme disease in Canada: results from a first national survey. Ticks Tick Borne Dis. 2017; 8(1): 112-118.

[50] Stufano A, Iatta R, Sgroi G, Jahantigh HR, Cagnazzo F, Flöel A, et al. Seroprevalence of vector-borne pathogens in outdoor workers from southern Italy and associated occupational risk factors. Parasit Vectors. 2022; 15(1): 264.

[51] Jones TF, Garman RL, LaFleur B, Stephan SJ, Schaffner W. Risk factors for tick exposure and suboptimal adherence to preventive recommendations. Am J Prev Med. 2002; 23(1): 47-50.

[52] Jore S, Vanwambeke SO, Slunge D, Boman A, Krogfelt KA, Jepsen MT, et al. Spatial tick bite exposure and associated risk factors in Scandinavia. Infect Ecol Epidemiol. 2020; 10(1): 1764693.

[53] Aenishaenslin C, Charland K, Bowser N, Perez-Trejo E, Baron G, Milord F, et al. Behavioral risk factors associated with reported tick exposure in a Lyme disease high incidence region in Canada. BMC Public Health. 2022; 22(1): 807.

[54] Václavík T, Balážová A, Baláž V, Tkadlec E, Schichor M, Zechmeisterová K, et al. Landscape epidemiology of neglected tick-borne pathogens in central Europe. Transbound Emerg Dis. 2021; 68(3): 1685-1696.

[55] De Keukeleire M, Vanwambeke SO, Somassè E, Kabamba B, Luyasu V, Robert A. Scouts, forests, and ticks: impact of landscapes on human-tick contacts. Ticks Tick Borne Dis. 2015; 6(5): 636-644.

[56] Ehrmann S, Liira J, Gärtner S, Hansen K, Brunet J, Cousins SAO, et al. Environmental drivers of Ixodes ricinus abundance in forest fragments of rural European landscapes. BMC Ecol. 2017; 17(1): 31.

[57] Allan BF, Keesing F, Ostfeld RS . Effect of forest fragmentation on Lyme disease risk. Conserv Biol. 2003; 17(1): 267-272.

[58] Brownstein JS, Skelly DK, Holford TR, Fish D. Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia. 2005; 146(3): 469-475.

[59] Diuk-Wasser MA, VanAcker MC, Fernandez MP. Impact of land use changes and habitat fragmentation on the eco-epidemiology of tick-borne diseases. J Med Entomol. 2021; 58(4): 1546-1564.

[60] Estrada-Peña A. Understanding the relationships between landscape connectivity and abundance of Ixodes ricinus ticks. Exp Appl Acarol. 2002; 28(1-4): 239-248.

[61] Butler AD, Sedghi T, Petrini JR, Ahmadi R. Tick-borne disease preventive practices and perceptions in an endemic area. Ticks Tick Borne Dis. 2016; 7(2): 331-337.