• 1

    Chen SM, Dumler JS, Bakken JS, Walker DH, 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32 :589–595.

    • Search Google Scholar
    • Export Citation
  • 2

    Centers for Disease Control and Prevention, 2008. Tickborne Rickettsial Diseases. Available at: http://www.cdc.gov/ticks/index.html. Accessed December 20, 2008.

  • 3

    Petrovec M, Lotric FS, Zupanc TA, Strle F, Brouqui P, Roux V, Dumler JS, 1997. Human disease in Europe caused by a granulocytic Ehrlichia species. J Clin Microbiol 35 :1556–1559.

    • Search Google Scholar
    • Export Citation
  • 4

    Keysary A, Massung RF, Inbar M, Wallach AD, Shanas U, Mumcuoglu KY, Waner T, 2007. Molecular evidence for Anaplasma phagocytophilum in Israel. Emerg Infect Dis 13 :1411–1412.

    • Search Google Scholar
    • Export Citation
  • 5

    Ohashi N, Inayoshi M, Kitamura K, Kawamori F, Kawaguchi D, Nishimura Y, Naitou H, Hiroi M, Masuzawa T, 2005. Anaplasma phagocytophilum-infected ticks, Japan. Emerg Infect Dis 11 :1780–1783.

    • Search Google Scholar
    • Export Citation
  • 6

    Cao WC, Zhao QM, Zhang PH, Dumler JS, Zhang XT, Fang LQ, Yang H, 2000. Granulocytic Ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic. J Clin Microbiol 38 :4208–4210.

    • Search Google Scholar
    • Export Citation
  • 7

    Zhang L, Liu Y, Ni D, Li Q, Yu Y, Yu XJ, Wan K, Li D, Liang G, Jiang X, Jing H, Run J, Luan M, Fu X, Zhang J, Yang W, Wang Y, Dumler JS, Feng Z, Ren J, Xu J, 2008. Nosocomial transmission of human granulocytic anaplasmosis in China. JAMA 300 :2263–2270.

    • Search Google Scholar
    • Export Citation
  • 8

    Schauber EM, Gertz SJ, Maple WT, Ostfeld RS, 1998. Coinfection of blacklegged ticks (Acari: Ixodidae) in Dutchess County, New York, with the agents of Lyme disease and human granulocytic ehrlichiosis. J Med Entomol 35 :901–903.

    • Search Google Scholar
    • Export Citation
  • 9

    Stanczak J, Gabre RM, Kruminis-Lozowska W, Racewicz M, Kubica-Biernat B, 2004. Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Ann Agric Environ Med 11 :109–114.

    • Search Google Scholar
    • Export Citation
  • 10

    Liu M, Che D, Huang K, 1996. Tick species and the key for identification of Ixodoidea tick in Shanxi. J Shanxi Normal Univ 10 :35–38.

  • 11

    Liu M, Wu Y, 1995. Investigation of ticks and tick-bites in Pangquangou natural reservation. J Changzhi Medical College 9 :199–200.

  • 12

    Liu M, Wu Y, Zhao Z, 2006. Preliminary investigation of Lyme disease serology of patients in Changzhi, Shanxi Province. J Changzhi Medical College 20 :17–18.

    • Search Google Scholar
    • Export Citation
  • 13

    Chen Z, Pan L, Song X, Bi D, Wang H, 1997. An investigation of vector and host animal of SFG and Lyme disease in Ninghua County of Fujian Provice. Chin J Vector Biol Control 8 :215.

    • Search Google Scholar
    • Export Citation
  • 14

    Luo HL, Pan L, and Yu SC, 1994. The report of four cases of Lyme disease in Wuyi Mountain area. Chin J Zoonoses 10 :40.

  • 15

    Liu MS, Wu YY, Zhao ZF, 2006. Seroepidemiologic study of Lyme disease in Shanxi Province. J Changzhi Medical College 20 :17–18.

  • 16

    Zhan L, He J, Saren GW, Wu XM, Wang JB, Zhao QM, Zhang PH, Huang HN, Jiang BG, Jiang JF, Zhang JB, Chu CY, Gao Y, Yang H, Cao WC, 2007. Investigation on Anaplasma phagocytophilum infection in rodents from forest areas in northeastern China. Chin J Epidemiol 28 :157–159.

    • Search Google Scholar
    • Export Citation
  • 17

    Zhang L, Shan A, Mathew B, Yin J, Fu X, Zhang J, Lu J, Xu J, Dumler JS, 2008. Rickettsial seroepidemiology among farm workers, Tianjin, People’s Republic of China. Emerg Infect Dis 14 :938–940.

    • Search Google Scholar
    • Export Citation
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Seroprevalence of Human Granulocytotropic Anaplasmosis in Central and Southeastern China

Shouyin ZhangState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Rong HaiState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Wenyuan LiState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Guohua LiState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Guangyu LinState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Jinrong HeState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Xiuping FuState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Jingshan ZhangState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Hong CaiState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Fengqin MaState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Jianhua ZhangState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Dongzheng YuState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Xue-jie YuState Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, China; Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, China; Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, China; Department of Pathology, University of Texas Medical Branch, Galveston, Texas

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Human granulocytic anaplasmosis (HGA) is an emerging tick-borne infectious disease. To determine the prevalence of HGA in central and southeastern China, a total of 323 human sera were collected from individuals at high risk for exposure to ticks and animals. The IgG antibody against the etiologic agent of HGA, Anaplasma phagocytophilum was detected with indirect immunofluorescence assay. The results showed that 20% of the tested individuals (64/323) were positive to A. phagocytophilum and that the incidence was higher in male (22%) than female (16%). We concluded that A. phagocytophilum infection was prevalent in central and southeastern China.

INTRODUCTION

Human granulocytic anaplasmosis (HGA) is a tick-borne disease caused by an obligatory intracellular bacterium Anaplasma phagocytophilum. It was previously known as human granulocytic ehrlichiosis (HGE). The HGA was first identified in the United States of America in 1994 from a patient with febrile illness.1 Since then the annual incidence of the disease gradually increased in the United States and in average more than 600 cases were reported annually from 2004 to 2006 by the Centers for Disease Control and Prevention (CDC).2 The disease has also been reported in Europe.3 Anaplasma phagocytophilum DNA has been detected from ticks in Israel, Japan, and China.46 The HGA was first reported in China in 2008 and the first HGA outbreak in China was noteworthy because it caused nosocomial infection.7 Because HGA only emerged recently in China, the pathogen of HGA has not yet been isolated and the epidemic data is incomplete. To determine the epidemiology of HGA in China, we studied the seroprevalence of HGA in risk populations from two areas in China, one forestry mountain area in southeastern China and one hilly area in central China. These areas were chosen because they are endemic for Lyme disease, and the pathogens of Lyme and HGA share the same tick vectors in the United States and Europe. 8,9

MATERIALS AND METHODS

Geographic characteristics of sample collection sites.

Two areas that had been reported for Lyme disease were selected: Wuyi Mountain area including Guangzhe and Jianyang counties that are located in Fujian Province of southeastern China; and a hilly area including Jiaocheng, Yicheng, Quwo, and Yuncheng counties that are located in Shanxi Province of central China (Figure 1). Both areas have a mild climate where several species of tick have been identified. Tick species identified in Shanxi including Ixodes persulcatus, Haemaphysalis concinna, H. japonica, H. campanulata, H. longicornis, H. verticalis, Dermacentor reticulatus, D. silvarum, D. sinicus, Hyalomma ditritum, Rhipicephalus sanguineus, and Boophilus microplus and tick species identified in Fujian including Ornithodoros papillipes, Haemaphysalis yeni, H. formosensis, H. longicornis, Ixodes granulatus, and B. microplus.1013

Sample collection.

Three hundred three human sera were collected from May to July in 2007 from forestry workers, shepherds, or hunters that were at high risk for exposure to ticks. The other 20 serum samples collected from March to August in 2006 were combined with the 2007 samples for testing of HGA antibody. A 5 mL sample of blood was collected from each individual by venipuncture. The serum samples were obtained after centrifugation of whole blood and were stored at −20°C until use. Epidemiologic data were collected for each sampled individual including age, gender, job type, living place, medical history, and history of animal contact and tick bite.

Indirect immunofluorescence assay (IFA).

An IFA kit from Focus Diagnostics (Cypress, CA) was used to detect human serum IgG antibodies against A. phagocytophilum in collected samples following the protocols of the manufacturer. A serum titer of ≥ 1:64 was considered as positive to A. phagocytophilum according to the definition of the manufacturer.

RESULTS AND DISCUSSION

To evaluate the prevalence of A. phagocytophilum infection among population in regions where cases of Lyme disease had been reported, 14,15 we performed IFA tests on sera from individuals at high risk for exposure to ticks in the Fujian and Shanxi provinces. Sixty-four of 323 sera (20%) were found positive to A. phagocytophilum. The A. phagocytophilum seroprevalence rate in samples from Fujian and Shanxi were 18% (39 out of 221) and 25% (25 out of 102), respectively (Table 1). Comparison of A. phagocytophilum seroprevalence by age group revealed the highest incidence of A. phagocytophilum infection in the age group of 41 to 60 years (21%), followed by the age group of 22 to 40 years (17%), and the age group of over 60 years (18%, Table 2). Anaplasma phagocytophilum seroprevalence rate was higher in male (22%) than in female (16%, Table 3).

Little is known about the epidemiology of human infection caused by A. phagocytophilum in China. Polymerase chain reaction (PCR) detection of 16S rRNA gene showed that A. phagocytophilum existed in ticks and rodents from northern China. 6,16 Very recently a death case was confirmed as a result of A. phagocytophilum infection. This case also caused a cluster of 9 cases of nosocomial infection among health care workers and family members after exposure to the index patient.7 Our serologic survey revealed a seroprevalence rate of 20% for A. phagocytophilum, indicating the existence of infection by A. phagocytophilum with a relatively high frequency among population at high risk for exposure to ticks in central and southeastern China. The seroprevalence rates in our study were higher than those reported in a recent study from North China. 17 This may be explained by the fact that we studied serum samples from high-risk population, which may not reflect that of the general population of the same country. Nevertheless, these studies indicated the urgency and necessity for large-scale serologic survey of high-risk population for A. phagocytophilum infection in China. Study of HGA was initiated only a few years ago and HGA is still not recognized by most doctors in China. The first HGA outbreak in China was mistakenly diagnosed as hemorrhagic fever. It is most likely that in the past and even right now the HGA cases in China were mistaken as hemorrhagic fever or other viral infections because clinical manifestations and laboratory test results of HGA are similar to viral infections. However, the treatment of HGA is very different from viral infection because HGA is sensitive to tetracycline. Thus, serologic studies of A. phagocytophilum infection among high-risk populations would provide valuable insights for developing public health strategies to prevent and control HGA. We hope this study can serve as an indicator to our clinicians that A. phagocytophilum infection was present among the population in the area studied. Patients in the endemic areas who present with nonspecific febrile illness after exposure to ticks should be evaluated for HGA.

Table 1

Results of Anaplasma phagocytophilum IgG antibody in human serum samples from Shanxi and Fujian

Table 1
Table 2

Distribution of Anaplasma phagocytophilum IgG antibody in serum samples among different age groups

Table 2
Table 3

Distribution of Anaplasma phagocytophilum IgG antibody in serum samples among different sexes

Table 3
Figure 1.
Figure 1.

The areas where the serum samples were collected.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 81, 2; 10.4269/ajtmh.2009.81.293

*

Address correspondence to Dongzheng Yu, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, 102206, China. E-mail: yudongzheng@icdc.cn

Authors’ addresses: Shouyin Zhang, Rong Hai, Jinrong He, Xiuping Fu, Jingshan Zhang, Hong Cai, Fengqin Ma, and Jianhua Zhang, State Key Lab for Infectious Diseases Prevention and Control, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, 102206, China. Wenyuan Li and Guohua Li, Shanxi Provincial Centers for Disease Control and Prevention, Taiyuan, 030012, China. Guangyu Lin, Nanping City Centers for Disease Control and Prevention of Fujian Province, Nanping, 353000, China. Dongzheng Yu, National Institute for Communicable Diseases Prevention and Control, Chinese Centers for Disease Control and Prevention, Beijing, 102206, China, Tel: 8610-61739444, Fax: 8610-61731691, E-mail: yudongzheng@icdc.cn. Xue-jie Yu, Department of Pathology, University of Texas Medical Branch, Galveston, TX 77555-0609.

REFERENCES

  • 1

    Chen SM, Dumler JS, Bakken JS, Walker DH, 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32 :589–595.

    • Search Google Scholar
    • Export Citation
  • 2

    Centers for Disease Control and Prevention, 2008. Tickborne Rickettsial Diseases. Available at: http://www.cdc.gov/ticks/index.html. Accessed December 20, 2008.

  • 3

    Petrovec M, Lotric FS, Zupanc TA, Strle F, Brouqui P, Roux V, Dumler JS, 1997. Human disease in Europe caused by a granulocytic Ehrlichia species. J Clin Microbiol 35 :1556–1559.

    • Search Google Scholar
    • Export Citation
  • 4

    Keysary A, Massung RF, Inbar M, Wallach AD, Shanas U, Mumcuoglu KY, Waner T, 2007. Molecular evidence for Anaplasma phagocytophilum in Israel. Emerg Infect Dis 13 :1411–1412.

    • Search Google Scholar
    • Export Citation
  • 5

    Ohashi N, Inayoshi M, Kitamura K, Kawamori F, Kawaguchi D, Nishimura Y, Naitou H, Hiroi M, Masuzawa T, 2005. Anaplasma phagocytophilum-infected ticks, Japan. Emerg Infect Dis 11 :1780–1783.

    • Search Google Scholar
    • Export Citation
  • 6

    Cao WC, Zhao QM, Zhang PH, Dumler JS, Zhang XT, Fang LQ, Yang H, 2000. Granulocytic Ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic. J Clin Microbiol 38 :4208–4210.

    • Search Google Scholar
    • Export Citation
  • 7

    Zhang L, Liu Y, Ni D, Li Q, Yu Y, Yu XJ, Wan K, Li D, Liang G, Jiang X, Jing H, Run J, Luan M, Fu X, Zhang J, Yang W, Wang Y, Dumler JS, Feng Z, Ren J, Xu J, 2008. Nosocomial transmission of human granulocytic anaplasmosis in China. JAMA 300 :2263–2270.

    • Search Google Scholar
    • Export Citation
  • 8

    Schauber EM, Gertz SJ, Maple WT, Ostfeld RS, 1998. Coinfection of blacklegged ticks (Acari: Ixodidae) in Dutchess County, New York, with the agents of Lyme disease and human granulocytic ehrlichiosis. J Med Entomol 35 :901–903.

    • Search Google Scholar
    • Export Citation
  • 9

    Stanczak J, Gabre RM, Kruminis-Lozowska W, Racewicz M, Kubica-Biernat B, 2004. Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Ann Agric Environ Med 11 :109–114.

    • Search Google Scholar
    • Export Citation
  • 10

    Liu M, Che D, Huang K, 1996. Tick species and the key for identification of Ixodoidea tick in Shanxi. J Shanxi Normal Univ 10 :35–38.

  • 11

    Liu M, Wu Y, 1995. Investigation of ticks and tick-bites in Pangquangou natural reservation. J Changzhi Medical College 9 :199–200.

  • 12

    Liu M, Wu Y, Zhao Z, 2006. Preliminary investigation of Lyme disease serology of patients in Changzhi, Shanxi Province. J Changzhi Medical College 20 :17–18.

    • Search Google Scholar
    • Export Citation
  • 13

    Chen Z, Pan L, Song X, Bi D, Wang H, 1997. An investigation of vector and host animal of SFG and Lyme disease in Ninghua County of Fujian Provice. Chin J Vector Biol Control 8 :215.

    • Search Google Scholar
    • Export Citation
  • 14

    Luo HL, Pan L, and Yu SC, 1994. The report of four cases of Lyme disease in Wuyi Mountain area. Chin J Zoonoses 10 :40.

  • 15

    Liu MS, Wu YY, Zhao ZF, 2006. Seroepidemiologic study of Lyme disease in Shanxi Province. J Changzhi Medical College 20 :17–18.

  • 16

    Zhan L, He J, Saren GW, Wu XM, Wang JB, Zhao QM, Zhang PH, Huang HN, Jiang BG, Jiang JF, Zhang JB, Chu CY, Gao Y, Yang H, Cao WC, 2007. Investigation on Anaplasma phagocytophilum infection in rodents from forest areas in northeastern China. Chin J Epidemiol 28 :157–159.

    • Search Google Scholar
    • Export Citation
  • 17

    Zhang L, Shan A, Mathew B, Yin J, Fu X, Zhang J, Lu J, Xu J, Dumler JS, 2008. Rickettsial seroepidemiology among farm workers, Tianjin, People’s Republic of China. Emerg Infect Dis 14 :938–940.

    • Search Google Scholar
    • Export Citation
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