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The prevalence and clinical characteristics of tick-borne diseases at One Sentinel Hospital in Northeastern China

Published online by Cambridge University Press:  01 August 2018

Hong-Bo Liu
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Ran Wei
Affiliation:
The Affiliated Hospital of Shandong University of Traditional Chinese Medicine, Jinan 250014, P.R. China
Xue-Bing Ni
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Yuan-Chun Zheng
Affiliation:
Mudanjiang Forestry Central Hospital, Mudanjiang 157000, P.R. China
Qiu-Bo Huo
Affiliation:
Mudanjiang Forestry Central Hospital, Mudanjiang 157000, P.R. China
Bao-Gui Jiang
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Lan Ma
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Rui-Ruo Jiang
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Jin Lv
Affiliation:
The Second Artillery Corps General Hospital, Beijing 100088, China
Yun-Xi Liu
Affiliation:
Chinese PLA General Hospital, 28 Fu-Xing Road, Hai-Dian District, Beijing 10853, P.R. China
Fang Yang
Affiliation:
Mudangjiang Entry-Exit Inspection and Quarantine Bureau of the People's Republic of China, Mudanjiang 157000, P.R. China
Yun-Huan Zhang
Affiliation:
Mudangjiang Entry-Exit Inspection and Quarantine Bureau of the People's Republic of China, Mudanjiang 157000, P.R. China
Jia-Fu Jiang*
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Na Jia*
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
Wu-Chun Cao*
Affiliation:
State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, P.R. China
*
Author for correspondence: Wu-Chun Cao, Na-Jia, and Jia-Fu Jiang, E-mail: caowc@bmi.ac.cn; na2002043@126.com; jiangjf2008@gmail.com
Author for correspondence: Wu-Chun Cao, Na-Jia, and Jia-Fu Jiang, E-mail: caowc@bmi.ac.cn; na2002043@126.com; jiangjf2008@gmail.com
Author for correspondence: Wu-Chun Cao, Na-Jia, and Jia-Fu Jiang, E-mail: caowc@bmi.ac.cn; na2002043@126.com; jiangjf2008@gmail.com

Abstract

Northeastern China is a region of high tick abundance, multiple tick-borne pathogens and likely human infections. The spectrum of diseases caused by tick-borne pathogens has not been objectively evaluated in this region for clinical management and for comparison with other regions globally where tick-transmitted diseases are common. Based on clinical symptoms, PCR, indirect immunofluorescent assay and (or) blood smear, we identified and described tick-borne diseases from patients with recent tick bite seen at Mudanjiang Forestry Central Hospital. From May 2010 to September 2011, 42% (75/180) of patients were diagnosed with a specific tick-borne disease, including Lyme borreliosis, tick-borne encephalitis, human granulocytic anaplasmosis, human babesiosis and spotted fever group rickettsiosis. When we compared clinical and laboratory features to identify factors that might discriminate tick-transmitted infections from those lacking that evidence, we revealed that erythema migrans and neurological manifestations were statistically significantly differently presented between those with and without documented aetiologies (P < 0.001, P = 0.003). Twelve patients (6.7%, 12/180) were co-infected with two tick-borne pathogens. We demonstrated the poor ability of clinicians to identify the specific tick-borne disease. In addition, it is necessary to develop specific laboratory assays for optimal diagnosis of tick-borne diseases.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Belongia, EA (2002) Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector Borne and Zoonotic Diseases 2, 265273.CrossRefGoogle ScholarPubMed
Belongia, EA, Reed, KD, Mitchell, PD, Chyou, PH, Mueller-Rizner, N, Finkel, MF and Schriefer, ME (1999) Clinical and epidemiological features of early Lyme disease and human granulocytic ehrlichiosis in Wisconsin. Clinical infectious Diseases 29, 14721477.CrossRefGoogle ScholarPubMed
Belongia, EA, Reed, KD, Mitchell, PD, Mueller-Rizner, N, Vandermause, M, Finkel, MF and Kazmierczak, JJ (2001) Tickborne infections as a cause of nonspecific febrile illness in Wisconsin. Clinical Infectious Diseases 32, 14341439.CrossRefGoogle ScholarPubMed
Brouqui, P, Bacellar, F, Baranton, G, Birtles, RJ, Bjoersdorff, A, Blanco, JR, Caruso, G, Cinco, M, Fournier, PE, Francavilla, E, Jensenius, M, Kazar, J, Laferl, H, Lakos, A, Lotric Furlan, S, Maurin, M, Oteo, JA, Parola, P, Perez-Eid, C, Peter, O, Postic, D, Raoult, D, Tellez, A, Tselentis, Y, Wilske, B and Escmid Study Group on Coxiella Anaplasma, Rickettsia, Bartonella and European Network for Surveillance of Tick-Borne Diseases (2004) Guidelines for the diagnosis of tick-borne bacterial diseases in Europe. Clinical Microbiology and Infection 10, 11081132.CrossRefGoogle Scholar
Cao, WC, Zhao, QM, Zhang, PH, Dumler, JS, Zhang, XT, Fang, LQ and Yang, H (2000) Granulocytic ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic. Journal of Clinical Microbiology 38, 42084210.Google ScholarPubMed
Cao, WC, Zhao, QM, Zhang, PH, Yang, H, Wu, XM, Wen, BH, Zhang, XT and Habbema, JD (2003) Prevalence of Anaplasma phagocytophila and Borrelia burgdorferi in Ixodes persulcatus ticks from northeastern China. The American Journal of Tropical Medicine and Hygiene 68, 547550.CrossRefGoogle ScholarPubMed
Cao, WC, Zhan, L, He, J, Foley, JE, SJ, DEV, Wu, XM, Yang, H, Richardus, JH and Habbema, JD (2006) Natural Anaplasma phagocytophilum infection of ticks and rodents from a forest area of Jilin Province, China. The American Journal of Tropical Medicine and Hygiene 75, 664668.CrossRefGoogle ScholarPubMed
Cao, WC, Zhan, L, De Vlas, SJ, Wen, BH, Yang, H, Richardus, JH and Habbema, JD (2008) Molecular detection of spotted fever group Rickettsia in Dermacentor silvarum from a forest area of northeastern China. Journal of Medical Entomology 45, 741744.Google ScholarPubMed
Centers for Disease, Control and Prevention (2004) Fatal cases of Rocky Mountain spotted fever in family clusters – three states, 2003. MMWR. Morbidity and Mortality Weekly Report 53, 407410.Google Scholar
Chu, CY, Jiang, BG, He, J, Gao, Y, Zhang, PH, Wu, XM, Zhang, WY, Shi, H, Gaowa, HS, Wang, JB, Foley, JE, Liu, W and Cao, WC (2011) Genetic diversity of Borrelia burgdorferi sensu lato isolates from Northeastern China. Vector Borne and Zoonotic Diseases 11, 877882.CrossRefGoogle ScholarPubMed
Cimperman, J, Maraspin, V, Lotric-Furlan, S, Ruzic-Sabljic, E, Avsic-Zupanc, T and Strle, F (2002) Double infection with tick borne encephalitis virus and Borrelia burgdorferi sensu lato. Wiener Klinische Wochenschrift 114, 620622.Google ScholarPubMed
Duan, C, Tong, Y, Huang, Y, Wang, X, Xiong, X and Wen, B (2011) Complete genome sequence of Rickettsia heilongjiangensis, an emerging tick-transmitted human pathogen. Journal of Bacteriology 193, 55645565.CrossRefGoogle ScholarPubMed
Duffy, J, Pittlekow, MR, Kolbert, CP, Rutledge, BJ and Persing, DH (1997) Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis. The Lancet 349, 399.CrossRefGoogle ScholarPubMed
Hilton, E, DeVoti, J, Benach, JL, Halluska, ML, White, DJ, Paxton, H and Dumler, JS (1999) Seroprevalence and seroconversion for tick-borne diseases in a high-risk population in the northeast United States. The American Journal of Medicine 106, 404409.CrossRefGoogle Scholar
Horowitz, HW, Aguero-Rosenfeld, ME, Holmgren, D, McKenna, D, Schwartz, I, Cox, ME and Wormser, GP (2013) Lyme disease and human granulocytic anaplasmosis coinfection: impact of case definition on coinfection rates and illness severity. Journal of Biochemistry and Molecular Biology 56, 9399.Google ScholarPubMed
Jia, N, Jiang, JF, Huo, QB, Jiang, BG and Cao, WC (2013 a) Rickettsia sibirica subspecies sibirica BJ-90 as a cause of human disease. New England Journal of Medicine 369, 11761178.CrossRefGoogle ScholarPubMed
Jia, N, Zheng, YC, Jiang, JF, Ma, L and Cao, WC (2013 b) Human infection with Candidatus Rickettsia tarasevichiae. New England Journal of Medicine 369, 11781180.CrossRefGoogle ScholarPubMed
Jia, N, Zheng, YC, Ma, L, Huo, QB, Ni, XB, Jiang, BG, Chu, YL, Jiang, RR, Jiang, JF and Cao, WC (2014) Human infections with Rickettsia raoultii, China. Emerging Infectious Dieseases 20, 866868.CrossRefGoogle ScholarPubMed
Jiang, JF, Jiang, BG, Yu, JH, Zhang, WY, Gao, HW, Zhan, L, Sun, Y, Zhang, XA, Zhang, PH, Liu, W, Wu, XM, Xu, RM and Cao, WC (2011) Anaplasma phagocytophilum infection in ticks, China-Russia border. Emerging Infectious Diseases 17, 932934.CrossRefGoogle ScholarPubMed
Jiang, JF, Zheng, YC, Jiang, RR, Li, H, Huo, QB, Jiang, BG, Sun, Y, Jia, N, Wang, YW, Ma, L, Liu, HB, Chu, YL, Ni, XB, Liu, K, Song, YD, Yao, NN, Wang, H, Sun, T and Cao, WC (2015) Epidemiological, clinical, and laboratory characteristics of 48 cases of ‘Babesia venatorum’ infection in China: a descriptive study. The Lancet Infectious Diseases 15, 196203.CrossRefGoogle ScholarPubMed
Krause, PJ, Telford, SR III, Spielman, A, Sikand, V, Ryan, R, Christianson, D, Burke, G, Brassard, P, Pollack, R, Peck, J and Persing, DH (1996) Concurrent Lyme disease and babesiosis. Evidence for increased severity and duration of illness. JAMA 275, 16571660.CrossRefGoogle ScholarPubMed
Krause, PJ, McKay, K, Thompson, CA, Sikand, VK, Lentz, R, Lepore, T, Closter, L, Christianson, D, Telford, SR, Persing, D, Radolf, JD, Spielman, A and Deer-Associated Infection Study Group (2002) Disease-specific diagnosis of coinfecting tickborne zoonoses: babesiosis, human granulocytic ehrlichiosis, and Lyme disease. Journal of Biochemistry and Molecular Biology 34, 11841191.Google ScholarPubMed
Li, H, Jiang, JF, Liu, W, Zheng, YC, Huo, QB, Tang, K, Zuo, SY, Liu, K, Jiang, BG, Yang, H and Cao, WC (2012) Human infection with Candidatus Neoehrlichia mikurensis, China. Emerging Infectious Dieseases 18, 16361639.CrossRefGoogle ScholarPubMed
Li, H, Zheng, YC, Ma, L, Jia, N, Jiang, BG, Jiang, RR, Huo, QB, Wang, YW, Liu, HB, Chu, YL, Song, YD, Yao, NN, Sun, T, Zeng, FY, Dumler, JS, Jiang, JF and Cao, WC (2015) Human infection with a novel tick-borne Anaplasma species in China: a surveillance study. The Lancet Infectious Diseases 15, 663670.CrossRefGoogle ScholarPubMed
Lu, Z, Broker, M and Liang, G (2008) Tick-borne encephalitis in mainland China. Vector Borne and Zoonotic Diseases 8, 713720.CrossRefGoogle ScholarPubMed
Magnarelli, LA, Dumler, JS, Anderson, JF, Johnson, RC and Fikrig, E (1995) Coexistence of antibodies to tick-borne pathogens of babesiosis, ehrlichiosis, and Lyme borreliosis in human sera. Journal of Clinical Microbiology 33, 30543057.Google ScholarPubMed
Magnarelli, LA, Ijdo, JW, Anderson, JF, Padula, SJ, Flavell, RA and Fikrig, E (1998) Human exposure to a granulocytic Ehrlichia and other tick-borne agents in Connecticut. Journal of Clinical Microbiology 36, 28232827.Google ScholarPubMed
Moniuszko, A, Dunaj, J, Swiecicka, I, Zambrowski, G, Chmielewska-Badora, J, Zukiewicz-Sobczak, W, Zajkowska, J, Czupryna, P, Kondrusik, M, Grygorczuk, S, Swierzbinska, R and Pancewicz, S (2014) Co-infections with Borrelia species, Anaplasma phagocytophilum and Babesia spp. in patients with tick-borne encephalitis. European Journal of Clinical Microbiology & Infectious Diseases, 33, 18351841.CrossRefGoogle ScholarPubMed
Ni, XB, Jia, N, Jiang, BG, Sun, T, Zheng, YC, Huo, QB, Liu, K, Ma, L, Zhao, QM, Yang, H, Wang, X, Jiang, JF and Cao, WC (2014) Lyme borreliosis caused by diverse genospecies of Borrelia burgdorferi sensu lato in northeastern China. Clinical Microbiology And infection 20, 808814.CrossRefGoogle ScholarPubMed
Parola, P, Paddock, CD and Raoult, D (2005) Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Reviews 18, 719756.CrossRefGoogle ScholarPubMed
Steere, AC, McHugh, G, Suarez, C, Hoitt, J, Damle, N and Sikand, VK (2003) Prospective study of coinfection in patients with erythema migrans. Clinical infectious Diseases 36, 10781081.CrossRefGoogle ScholarPubMed
Sun, J, Liu, Q, Lu, L, Ding, G, Guo, J, Fu, G, Zhang, J, Meng, F, Wu, H, Song, X, Ren, D, Li, D, Guo, Y, Wang, J, Li, G, Liu, J and Lin, H (2008 a) Coinfection with four genera of bacteria (Borrelia, Bartonella, Anaplasma, and Ehrlichia) in Haemaphysalis longicornis and Ixodes sinensis ticks from China. Vector Borne and Zoonotic Diseases 8, 791795.CrossRefGoogle ScholarPubMed
Sun, Y, Liu, G, Yang, L, Xu, R and Cao, W (2008 b) Babesia microti-like rodent parasites isolated from Ixodes persulcatus (Acari: Ixodidae) in Heilongjiang Province, China. Veterinary Parasitology 156, 333339.CrossRefGoogle ScholarPubMed
Swanson, SJ, Neitzel, D, Reed, KD and Belongia, EA (2006) Coinfections acquired from ixodes ticks. Clinical Microbiology Reviews 19, 708727.CrossRefGoogle ScholarPubMed
Tijsse-Klasen, E, Jacobs, JJ, Swart, A, Fonville, M, Reimerink, JH, Brandenburg, AH, van der Giessen, JW, Hofhuis, A and Sprong, H (2011) Small risk of developing symptomatic tick-borne diseases following a tick bite in The Netherlands. Parasites & Vectors 4, 17.CrossRefGoogle ScholarPubMed
Trevejo, RT, Krause, PJ, Sikand, VK, Schriefer, ME, Ryan, R, Lepore, T, Porter, W and Dennis, DT (1999) Evaluation of two-test serodiagnostic method for early Lyme disease in clinical practice. Journal of Infectious Disease 179, 931938.CrossRefGoogle ScholarPubMed
Wang, TJ, Liang, MH, Sangha, O, Phillips, CB, Lew, RA, Wright, EA, Berardi, V, Fossel, AH and Shadick, NA (2000) Coexposure to Borrelia burgdorferi and Babesia microti does not worsen the long-term outcome of Lyme disease. Clinical infectious Diseases 31, 11491154.CrossRefGoogle Scholar
Wen, B, Cao, W and Pan, H (2003) Ehrlichiae and ehrlichial diseases in China. Annals of the New York Academy of Sciences 990, 4553.CrossRefGoogle Scholar
Wormser, GP, Dattwyler, RJ, Shapiro, ED, Halperin, JJ, Steere, AC, Klempner, MS, Krause, PJ, Bakken, JS, Strle, F, Stanek, G, Bockenstedt, L, Fish, D, Dumler, JS and Nadelman, RB (2006) The clinical assessment, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clinical Infectious Diseases 43, 10891134.CrossRefGoogle ScholarPubMed
Yu, XJ, Liang, MF, Zhang, SY, Liu, Y, Li, JD, Sun, YL, Zhang, L, Zhang, QF, Popov, VL, Li, C, Qu, J, Li, Q, Zhang, YP, Hai, R, Wu, W, Wang, Q, Zhan, FX, Wang, XJ, Kan, B, Wang, SW, Wan, KL, Jing, HQ, Lu, JX, Yin, WW, Zhou, H, Guan, XH, Liu, JF, Bi, ZQ, Liu, GH, Ren, J, Wang, H, Zhao, Z, Song, JD, He, JR, Wan, T, Zhang, JS, Fu, XP, Sun, LN, Dong, XP, Feng, ZJ, Yang, WZ, Hong, T, Zhang, Y, Walker, DH, Wang, Y and Li, DX (2011) Fever with thrombocytopenia associated with a novel bunyavirus in China. The New England Journal of Medicine 364, 15231532.CrossRefGoogle Scholar
Zhan, L, Cao, WC, Jiang, JF, Zhang, XA, Liu, YX, Wu, XM, Zhang, WY, Zhang, PH, Bian, CL, Dumler, JS, Yang, H, Zuo, SQ, Chu, CY, Liu, W, Richardus, JH and Habbema, JD (2010) Anaplasma phagocytophilum from rodents and sheep, China. Emerging Infectious Dieseases 16, 764768.CrossRefGoogle ScholarPubMed
Zhang, Y, Si, BY, Liu, BH, Chang, GH, Yang, YH, Huo, QB, Zheng, YC and Zhu, QY (2012) Complete genomic characterization of two tick-borne encephalitis viruses isolated from China. Virus Research 167, 310313.CrossRefGoogle ScholarPubMed
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