Use of Ultrasonography to Evaluate Schistosoma japonicum-Related Morbidity in Children, Sichuan Province, China, 2000–2007

Michelle S. Hsiang Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Elizabeth J. Carlton Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Yi Zhang Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Bo Zhong Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Qiu Dongchuan Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Pierre-Alain Cohen Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Christopher C. Stewart Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Robert C. Spear Global Health Sciences, University of California, San Francisco, California; School of Public Health, University of California, Berkeley, California; Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China; Department of Radiology, University of California, San Francisco, California; Department of Pediatrics, University of California, San Francisco, California

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Liver ultrasonography is a convenient way to evaluate Schistosoma japonicum-related morbidity; however, no consensus standards exist, and data on use in Chinese children are scant. We describe 7 years of ultrasound findings in a prospective cohort of 151 children from an endemic area in Sichuan Province, China and evaluate technical aspects of the ultrasound methodology. Although prevalence of infection decreased over time, prevalence of hepatomegaly increased, which was likely caused by re-infections. The prevalence of late findings such as parenchymal fibrosis and splenomegaly were rare and did not increase over time; however, when present, they were associated with stunting. The use of adult thresholds versus height-adjusted standards underestimated pathology in children. Reliability of all measures except parenchymal grade was poor to fair. Our findings highlight the importance of early intervention and screening. We also suggest methodological refinements to improve reliability of ultrasonography for large-scale assessment of S. japonicum-related subclinical morbidity in children.

Author Notes

*Address correspondence to Michelle S. Hsiang, Global Health Sciences, University of California, 50 Beale Street, 12th Floor, San Francisco, CA 94105. E-mail: hsiangm@globalhealth.ucsf.edu

Financial Support: This study was funded in part by a grant from the National Institutes of Health (R01 AI-50612-5) and support from Sichuan Centers for Disease Control and Prevention.

Authors' addresses: Michelle S. Hsiang, Global Health Sciences, University of California, San Francisco, CA, E-mail: hsiangm@globalhealth.ucsf.edu. Elizabeth J. Carlton, School of Public Health, University of California, Berkeley, CA, E-mail: ejcarlton@berkeley.edu. Yi Zhang, Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China, E-mail: zhangxxcdept@163.com. Bo Zhong, Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China, E-mail: zhongbo1968@163.com. Qiu Dongchuan, Institute of Parasitic Disease, Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan, People's Republic of China, E-mail: qiudongchuan@163.com. Pierre-Alain Cohen, Department of Radiology, University of California, San Francisco General Hospital, San Francisco, CA, E-mail: PCohen@sfghrad.ucsf.edu. Christopher C. Stewart, Department of Pediatrics, University of California, San Francisco General Hospital, San Francisco, CA, E-mail: CStewart@sfghpeds.ucsf.edu. Robert C. Spear, School of Public Health, University of California, Berkeley, CA, E-mail: spear@berkeley.edu.

Reprint requests: Michelle S. Hsiang, Global Health Sciences, University of California, 50 Beale Street, 12th Floor, San Francisco, CA 94105, Tel: 415-597-8180, Fax: 415-597-8299, E-mail: hsiangm@globalhealth.ucsf.edu.

  • 1.

    Chitsulo L, Engels D, Montresor A, Savioli L, 2000. The global status of schistosomiasis and its control. Acta Trop 77: 4151.

  • 2.

    Zhou XN, Guo JG, Wu XH, Jiang QW, Zheng J, Dang H, Wang XH, Xu J, Zhu HQ, Wu GL, Li YS, Xu XJ, Chen HG, Wang TP, Zhu YC, Qiu DC, Dong XQ, Zhao GM, Zhang SJ, Zhao NQ, Xia G, Wang LY, Zhang SQ, Lin DD, Chen MG, Hao Y, 2007. Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerg Infect Dis 13: 14701476.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Leenstra T, Acosta LP, Langdon GC, Manalo DL, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines 1. Am J Clin Nutr 83: 371379.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    McGarvey ST, Wu G, Zhang S, Wang Y, Peters P, Olds GR, Wiest PM, 1993. Child growth, nutritional status, and schistosomiasis japonica in Jiangxi, People's Republic of China. Am J Trop Med Hyg 48: 547553.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Li YS, Li Y, Yu BD, Hu Q, Xiang Y, Zhong ZN, 1993. A multivariate analysis of the relationship between work ability and S. japonicum infection in Dongting Lake region, in China. Rev Inst Med Trop Sao Paulo 35: 347353.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Nokes C, McGarvey ST, Shiue L, Wu G, Wu H, Bundy DA, Olds GR, 1999. Evidence for an improvement in cognitive function following treatment of Schistosoma japonicum infection in Chinese primary school children. Am J Trop Med Hyg 60: 556565.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Hatz CF, 2001. The use of ultrasound in schistosomiasis. Adv Parasitol 48: 225284.

  • 8.

    Jenkins JM, Hatz C, The Cairo Working Group, 1992. The use of diagnostic ultrasound in schistosomiasis—attempts at standardization of methodology. Acta Trop 51: 4563.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Richter J, Naimey Working Group, 2000. Ultrasound in Schistosomiais: A Practical Guide to the Standard Use of Ultrasonography for the Assessment of Schistosomiasis-Related Morbidity. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J, 2005. The public health significance and control of schistosomiasis in China—then and now. Acta Trop 96: 97105.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Spear RC, Seto E, Liang S, Birkner M, Hubbard A, Qiu D, Yang C, Zhong B, Xu F, Gu X, Davis GM, 2004. Factors influencing the transmission of Schistosoma japonicum in the mountains of Sichuan Province of China. Am J Trop Med Hyg 70: 4856.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Liang S, Yang C, Zhong B, Qiu D, 2006. Re-emerging schistosomiasis in hilly and mountainous areas of Sichuan, China. Bull World Health Organ 84: 139144.

  • 13.

    Doehring E, 1988. Schistosomiasis in childhood. European Journal of Pediatrics 147: 29.

  • 14.

    Wiest PM, Wu G, Zhong S, McGarvey ST, Tan E, Yuan J, Peters P, Olveda RM, Olds GR, 1993. Schistosomiasis japonica on Jishan Island, Jiangxi Province, People's Republic of China: persistence of hepatic fibrosis after reduction of the prevalence of infection with age. Trans R Soc Trop Med Hyg 87: 290294.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Wiest PM, Wu G, Zhong S, McGarvey ST, Yuan J, Olveda RM, Peters PA, Olds GR, 1994. Impact of annual screening and chemotherapy with praziquantel on Schistosomiasis japonica on Jishan Island, People's Republic of China. Am J Trop Med Hyg 51: 162169.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Gibson R, 1990. Principles of Nutritional Assessment. New York: Oxford University Press.

  • 17.

    World Health Organization, 1995. Physical Status: The Use of an Interpretation of Anthropometry. Geneva: World Health Organization.

  • 18.

    World Health Organization, 2006. WHO Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight-for-Height and Body Mass Index-for-Age. Methods and Development. Geneva: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Butte NF, Garza C, de Onis M, 2007. Evaluation of the feasibility of international growth standards for school-aged children and adolescents. J Nutr 137: 153157.

  • 20.

    Chinese National Survey on Students Constitution and Health, 2000. Report on the Physical Fitness and Health Surveillance of the Chinese School Students. Beijing, China: High Education Publishing.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Cai WM, 2000. Ultrasound diagnostic in schistosomiasis. Public Relations of China, eds. Handbook of Schistosomiasis Control. Diagnosis of Schistosomiasis. Disease Control Department Ministry of Health, Beijing, China, 97103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Li YS, Kardorff R, Richter J, Sun KY, Zhou H, McManus DP, Hatz C, 2004. Ultrasound organometry: the importance of body height adjusted normal ranges in assessing liver and spleen parameters among Chinese subjects with Schistosoma japonicum infection. Acta Trop 92: 133138.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Landis JR, Koch GG, 1977. The measurement of observer agrevement for categorical data. Biometrics 33: 159174.

  • 24.

    Shrout PE, Fleiss JL, 1979. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86: 420428.

  • 25.

    Olveda RM, Daniel BL, Ramirez BD, Aligui GD, Acosta LP, Fevidal P, Tiu E, de Veyra F, Peters PA, Romulo R, Domingo E, Wiest PM, Olds GR, 1996. Schistosomiasis japonica in the Philippines: the long-term impact of population-based chemotherapy on infection, transmission, and morbidity. J Infect Dis 174: 163172.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Li YS, Sleigh AC, Li Y, Tanner M, Dessein A, Williams GM, McManus DP, 2002. Five-year impact of repeated praziquantel treatment on subclinical morbidity due to Schistosoma japonicum in China. Trans R Soc Trop Med Hyg 96: 438443.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Balen J, Zhao ZY, Williams GM, McManus DP, Raso G, Utzinger J, Zhou J, Li YS, 2007. Prevalence, intensity and associated morbidity of Schistosoma japonicum infection in the Dongting Lake region, China. Bull World Health Organ 85: 519526.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Lin DD, Liu JX, Liu YM, Hu F, Zhang YY, Xu JM, Li JY, Ji MJ, Bergquist R, Wu GL, Wu HW, 2008. Routine Kato-Katz technique underestimates the prevalence of Schistosoma japonicum: a case study in an endemic area of the People's Republic of China. Parasitol Int 57: 281286.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Liang S, Seto EY, Remais JV, Zhong B, Yang C, Hubbard A, Davis GM, Gu X, Qiu D, Spear RC, 2007. Environmental effects on parasitic disease transmission exemplified by schistosomiasis in western China. Proc Natl Acad Sci USA 104: 71107115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Carlton EJ, Hsiang MS, Zhang Y, Johnson S, Hubbard A, Spear RC, 2009. The Impact of Schistosoma japonicum Infection on Ultrasound-Detectable Liver and Spleen Pathology: Results From a Five-Year Longitudinal Cohort in Southwest China. [submitted].

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Manzella A, Ohtomo K, Monzawa S, Lim JH, 2008. Schistosomiasis of the liver. Abdom Imaging 33: 144150.

  • 32.

    Koukounari A, Sacko M, Keita AD, Gabrielli AF, Landoure A, Dembele R, Clements AC, Whawell S, Donnelly CA, Fenwick A, Traore M, Webster JP, 2006. Assessment of ultrasound morbidity indicators of schistosomiasis in the context of large-scale programs illustrated with experiences from Malian children. Am J Trop Med Hyg 75: 10421052.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192: 528536.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Coutinho HM, Acosta LP, Wu HW, McGarvey ST, Su L, Langdon GC, Jiz MA, Jarilla B, Olveda RM, Friedman JF, Kurtis JD, 2007. Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. J Infect Dis 195: 288295.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    King CH, Magak P, Salam EA, Ouma JH, Kariuki HC, Blanton RE, 2003. Measuring morbidity in Schistosomiasis mansoni: relationship between image pattern, portal vein diameter and portal branch thickness in large-scale surveys using new WHO coding guidelines for ultrasound in schistosomiasis. Trop Med Int Health 8: 109117.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Doehring-Schwerdtfeger E, Kaiser C, Franke D, Kardorff R, Ali QM, Abdel-Rahim IM, 1992. Inter-observer variance in ultrasonographical assessment of Schistosoma mansoni-related morbidity in young schoolchildren. Acta Trop 51: 8588.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Kratzer W, Fritz V, Mason RA, Haenle MM, Kaechele V, 2003. Factors affecting liver size: a sonographic survey of 2080 subjects. J Ultrasound Med 22: 11551161.

  • 38.

    Li T, Yu BG, Dai YH, 2000. Impact and counter measures on acute schistosomiasis transmission by Yangtze River flood. Chinese Journal of Schistosomiasis Control 12: 268272.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Xia GL, Liu CB, Cao HL, Bi SL, Zhan MY, Su CA, Nan JH, Qi XQ, 1996. Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemologic study of hepatitis A, B, C, D, and E virus infections in China, 1992. International Hepatology Communications 5: 6273.

    • PubMed
    • Search Google Scholar
    • Export Citation
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