Factors Influencing the Serological Response in Hepatic Echinococcus granulosus Infection

Raffaella Lissandrin Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Francesca Tamarozzi Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Luca Piccoli Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Carmine Tinelli Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Annalisa De Silvestri Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Mara Mariconti Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Valeria Meroni Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Francesca Genco Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Enrico Brunetti Department of Infectious Diseases, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; World Health Organization Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy; Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Italy; Clinical Epidemiology and Biometry Unit, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Microbiology and Virology, Istituto Di Ricovero e Cura a Carattere Scientifico San Matteo Hospital Foundation, Pavia, Italy; Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy

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Knowledge of variables influencing serology is crucial to evaluate serology results for the diagnosis and clinical management of cystic echinococcosis (CE). We analyzed retrospectively a cohort of patients with hepatic CE followed in our clinic in 2000–2012 to evaluate the influence of several variables on the results of commercial enzyme-linked immunosorbent assay (ELISA) and indirect hemagglutination (IHA) tests. Sera from 171 patients with ≥ 1 hepatic CE cyst, and 90 patients with nonparasitic cysts were analyzed. CE cysts were staged according to the WHO-IWGE classification and grouped by activity. A significant difference in ELISA optical density (OD) values and percentage of positivity was found among CE activity groups and with controls (P < 0.001). The serological response was also influenced by age (P < 0.001) and cyst number (P = 0.003). OD values and cyst size were positively correlated in active cysts (P = 0.001). IHA test showed comparable results. When we analyzed the results of 151 patients followed over time, we found that serology results were significantly influenced by cyst activity, size, number, and treatment ≤ 12 months before serum collection. In conclusion, serological responses as assessed by commercial tests depend on CE cyst activity, size and number, and time from treatment. Clinical studies and clinicians in their practice should take this into account.

Author Notes

* Address correspondence to Francesca Tamarozzi, Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Via Brambilla 74, Pavia 27100, Italy. E-mail: f_tamarozzi@yahoo.com
† These authors contributed equally to this work.

Financial support: The research leading to these results has been partly funded from the European Union Seventh Framework Programme (FP7/2007-2013) under the project HERACLES (grant agreement no. 602051) to Enrico Brunetti.

Authors' addresses: Raffaella Lissandrin and Enrico Brunetti, Department of Infectious Diseases, IRCCS San Matteo Hospital Foundation, Pavia, Italy, WHO Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy, and Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy, E-mails: raffaella.lissandrin@unipv.it and enrico.brunetti@unipv.it. Francesca Tamarozzi, WHO Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy, and Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy, E-mail: f_tamarozzi@yahoo.com. Luca Piccoli, Department of Infectious Diseases, IRCCS san Matteo Hospital Foundation, Pavia, Italy, Current address: Institute for Research in Biomedicine, Bellinzona, Switzerland, E-mail: luca.piccoli@irb.usi.ch. Carmine Tinelli and Annalisa De Silvestri, Clinical Epidemiology and Biometry Unit, IRCCS San Matteo Hospital Foundation, Pavia, Italy, E-mails: ctinelli@smatteo.pv.it and a.desilvestri@smatteo.pv.it. Mara Mariconti, Department of Infectious Diseases, IRCCS San Matteo Hospital Foundation, Pavia, Italy, and WHO Collaborating Centre for Clinical Management of Cystic Echinococcosis, Pavia, Italy, E-mail: mara.mariconti@guest.unimi.it. Francesca Genco, Department of Microbiology and Virology, IRCCS San Matteo Hospital Foundation, Pavia, Italy, E-mail: francesca.genco@unipv.it. Valeria Meroni, Department of Microbiology and Virology, IRCCS San matteo Hospital Foundation, Department of Internal Medicine and Clinical Therapy, University of Pavia, Italy, E-mail: v.meroni@smatteo.pv.it.

  • 1.

    Budke CM, 2006. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12: 296303.

  • 2.

    Craig PS, Budke CM, Schantz P, Li T, Qiu J, Yang JY, Zeyhle E, Rogan MT, Ito A, 2007. Human echinococcosis: a neglected disease? Trop Med Health 35: 283292.

  • 3.

    Polat P, Kantarci M, Alper F, Suma S, Koruyucu MB, Okur A, 2003. Hydatid disease from head to toe. Radiographics 23: 475494, quiz 536–537.

  • 4.

    Pedrosa I, Saiz A, Arrazola J, Ferreiros J, Pedrosa CS, 2000. Hydatid disease: radiologic and pathologic features and complications. Radiographics 20: 795817.

  • 5.

    Brunetti E, Kern P, Vuitton DA, 2010. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114: 116.

  • 6.

    WHO Informal Working Group, 2003. International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Trop 85: 253261.

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

    Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E, 2008. Clinical management of cystic echinococcosis: state of the art, problems, and perspectives. Am J Trop Med Hyg 79: 301311.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Hosch W, Junghanss T, Stojkovic M, Brunetti E, Heye T, Kauffmann GW, Hull WE, 2008. Metabolic viability assessment of cystic echinococcosis using high-field 1H MRS of cyst contents. NMR Biomed 21: 734754.

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

    Carmena D, Benito A, Eraso E, 2006. Antigens for the immunodiagnosis of Echinococcus granulosus infection: an update. Acta Trop 98: 7486.

  • 10.

    Hernandez-Gonzalez A, Santivanez S, Garcia HH, Rodriguez S, Munoz S, Ramos G, Orduna A, Siles-Lucas M, 2012. Improved serodiagnosis of cystic echinococcosis using the new recombinant 2B2t antigen. PLoS Negl Trop Dis 6: e1714.

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

    Ben Nouir N, Nunez S, Gianinazzi C, Gorcii M, Muller N, Nouri A, Babba H, Gottstein B, 2008. Assessment of Echinococcus granulosus somatic protoscolex antigens for serological follow-up of young patients surgically treated for cystic echinococcosis. J Clin Microbiol 46: 16311640.

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

    Li T, Ito A, Chen X, Sako Y, Qiu J, Xiao N, Qiu D, Nakao M, Yanagida T, Craig PS, 2010. Specific IgG responses to recombinant antigen B and em18 in cystic and alveolar echinococcosis in China. Clin Vaccine Immunol 17: 470475.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Li T, Ito A, Pengcuo R, Sako Y, Chen X, Qiu D, Xiao N, Craig PS, 2011. Post-treatment follow-up study of abdominal cystic echinococcosis in Tibetan communities of northwest Sichuan Province, China. PLoS Negl Trop Dis 5: e1364.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Yang YR, Craig PS, Ito A, Vuitton DA, Giraudoux P, Sun T, Williams GM, Huang Z, Li Z, Wang Y, Teng J, Li Y, Huang L, Wen H, Jones MK, McManus DP, 2007. A correlative study of ultrasound with serology in an area in China co-endemic for human alveolar and cystic echinococcosis. Trop Med Int Health 12: 637646.

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

    Santivanez SJ, Arias P, Portocarrero M, Rodriguez S, Gonzalez AE, Gilman RH, Gavidia CM, Garcia HH, 2012. Serological diagnosis of lung cystic hydatid disease using the synthetic p176 peptide. Clin Vaccine Immunol 19: 944947.

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

    Hernandez-Gonzalez A, Muro A, Barrera I, Ramos G, Orduna A, Siles-Lucas M, 2008. Usefulness of four different Echinococcus granulosus recombinant antigens for serodiagnosis of unilocular hydatid disease (UHD) and postsurgical follow-up of patients treated for UHD. Clin Vaccine Immunol 15: 147153.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Galitza Z, Bazarsky E, Sneier R, Peiser J, El-On J, 2006. Repeated treatment of cystic echinococcosis in patients with a long-term immunological response after successful surgical cyst removal. Trans R Soc Trop Med Hyg 100: 126133.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Rigano R, Ioppolo S, Ortona E, Margutti P, Profumo E, Ali MD, Di Vico B, Teggi A, Siracusano A, 2002. Long-term serological evaluation of patients with cystic echinococcosis treated with benzimidazole carbamates. Clin Exp Immunol 129: 485492.

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

    Piccoli L, Tamarozzi F, Cattaneo F, Mariconti M, Filice C, Bruno A, Brunetti E, 2014. Long-term sonographic and serological follow-up of inactive echinococcal cysts of the liver: hints for a “watch-and-wait” approach. PLoS Negl Trop Dis 8: e3057.

    • PubMed
    • Search Google Scholar
    • Export Citation
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