Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T11:00:45.207Z Has data issue: false hasContentIssue false
  • English
  • Français

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 Open the ORCID record for Hong-Bo Liu [Opens in a new window] ,
Ran Wei ,
Xue-Bing Ni ,
Yuan-Chun Zheng ,
Qiu-Bo Huo ,
Bao-Gui Jiang ,
Lan Ma ,
Rui-Ruo Jiang ,
Jin Lv  and
Yun-Xi Liu
...Show all authors
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
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Chinaco-infectionetiologytick bitetick-borne infectious disease
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 161 - 167
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Belongia, EA (2002) Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector Borne and Zoonotic Diseases 2, 265–273.Google Scholar
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, 1472–1477.Google Scholar
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, 1434–1439.Google Scholar
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, 1108–1132.Google 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, 4208–4210.Google Scholar
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, 547–550.Google Scholar
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, 664–668.Google Scholar
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, 741–744.Google Scholar
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, 407–410.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, 877–882.Google Scholar
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, 620–622.Google Scholar
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, 5564–5565.Google Scholar
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.Google Scholar
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, 404–409.Google 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, 93–99.Google Scholar
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, 1176–1178.Google Scholar
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, 1178–1180.Google Scholar
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, 866–868.Google Scholar
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, 932–934.Google Scholar
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, 196–203.Google Scholar
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, 1657–1660.Google Scholar
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, 1184–1191.Google Scholar
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, 1636–1639.Google Scholar
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, 663–670.Google Scholar
Lu, Z, Broker, M and Liang, G (2008) Tick-borne encephalitis in mainland China. Vector Borne and Zoonotic Diseases 8, 713–720.Google Scholar
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, 3054–3057.Google Scholar
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, 2823–2827.Google Scholar
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, 1835–1841.Google Scholar
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, 808–814.Google Scholar
Parola, P, Paddock, CD and Raoult, D (2005) Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Reviews 18, 719–756.Google Scholar
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, 1078–1081.Google Scholar
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, 791–795.Google Scholar
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, 333–339.Google Scholar
Swanson, SJ, Neitzel, D, Reed, KD and Belongia, EA (2006) Coinfections acquired from ixodes ticks. Clinical Microbiology Reviews 19, 708–727.Google Scholar
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.Google Scholar
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, 931–938.Google Scholar
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, 1149–1154.Google Scholar
Wen, B, Cao, W and Pan, H (2003) Ehrlichiae and ehrlichial diseases in China. Annals of the New York Academy of Sciences 990, 45–53.Google 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, 1089–1134.Google Scholar
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, 1523–1532.Google 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, 764–768.Google Scholar
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, 310–313.Google Scholar
Supplementary material: PDF

Liu et al. supplementary material

Table S1

Download Liu et al. supplementary material(PDF)
PDF 102.3 KB
Supplementary material: PDF

Liu et al. supplementary material

Table S2

Download Liu et al. supplementary material(PDF)
PDF 33 KB