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Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience

Year 2025, Volume: 78 Issue: 1, 69 - 75, 31.03.2025

Abstract

Objectives: The purpose of this study is to reveal the epidemiological data of cystic echinococcosis (CE) patients who applied to our hospital and to determine the diagnostic performance of the indirect hemagglutination test (IHAT).

Materials and Methods: The patients whose serum samples were routinely sent to Ankara University İbni Sina Research and Application Hospital, Central Laboratory for CE IHAT between 01.01.2023 and 01.09.2024 were evaluated. The patient’s IHAT results were interpreted with clinical and laboratory findings and radiological imaging results. In the evaluation of the IHAT, the serological titer, which is 1/320 and above, is declared positive, and 1/80 and 1/160 are declared as suspicious.

Results: Serology results of 636 patients were evaluated. The positivity rate was found to be 5.97%. The age group of 0-19 had the greatest positivity percentage (19%). Age-group differences in CE seropositivity were statistically significant (p=0.011). The patient group with cystic lesions apparent in radiological imaging had the greatest seropositivity rate (11.9%). The seropositivity rate of IHAT in patients with CE-specific findings identified on radiological imaging was calculated as 39.6% when the threshold value was taken as 1/80. The seronegativity rate was found to be 95.7% in patients with no cysts detected on radiological imaging
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Conclusion: The positivity rate of IHAT was found to be low in patients with CE lesions identified on radiological imaging. Therefore, it is thought that it would be beneficial to utilize a second serological test together with IHAT to increase analytical sensitivity in routine laboratory tests.

Keywords: Cystic echinococcosis, indirect hemagglutination test, seropositivity rates, radiological imaging

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Thanks

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References

  • 1. Torgerson PR, Robertson LJ, Enemark HL, et al. Source attribution of human echinococcosis: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14:e0008382.
  • 2. Hogea MO, Ciomaga BF, Muntean MM, et al. Cystic Echinococcosis in the Early 2020s: a review. Trop Med Infect Dis. 2024;9:36.
  • 3. World Health Organization. Echinococcosis. Available from: https://www.who.int/news-room/fact-sheets/detail/echinococcosis. Accessed on 10 November, 2024.
  • 4. Morar R, Feldman C. Pulmonary echinococcosis. Eur Respir J. 2003;21:1069-1077.
  • 5. Alshaikhli A, Al-Hillan A. Liver Cystic Disease. [Updated 2023 Apr 24]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2025. Available from:https://www.ncbi.nlm.nih.gov/books/NBK567739/
  • 6. Brunetti E, Kern P, Vuitton DA; Writing Panel for the WHO-IWGE. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114:1-16.
  • 7. Devi M, Venumadhav T, Sukanya B, et al. Role of ımaging in diagnosis, predicting biological activity and in treatment plan of hydatid disease. Open J. Intern. Med. 2018;8:177-195.
  • 7. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al. Serological diagnosis and follow-up of human cystic echinococcosis: a new hope for the future? Biomed Res Int. 2015;2015:428205.
  • 8. Derbel F, Zidi MK, Mtimet A, et al. Hydatid cyst of the pancreas: a report on seven cases. Arab J Gastroenterol. 2010;11:219-22.
  • 9. Vola A, Manciulli T, De Silvestri A, et al. Diagnostic performances of commercial ELISA, ındirect hemagglutination, and western blot in differentiation of hepatic echinococcal and non-echinococcal lesions: a retrospective analysis of data from a single referral centre. Am J Trop Med Hyg. 2019;101:1345-1349.
  • 10. Siles-Lucas M, Uchiumi L, Tamarozzi F. ‘No cyst, no echinococcosis’: a scoping review update on the diagnosis of cystic echinococcosis after the issue of the WHO-IWGE Expert Consensus and current perspectives. Curr Opin Infect Dis. 2023;36:333-340.
  • 11. Yılmaz A, Uslu H, Aktaş F. 2009-2013 yılları arasında Erzurum Bölge Hastanesindeki kistik ekinokokkozis şüpheli hastaların indirekt hemaglütinasyon (İHA) metoduyla değerlendirilmesi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2016;5:23- 32.
  • 12. Ertabaklar H, Yıldız İ, Malatyalı E, et al. Retrospective analysis of cystic echinococcosis results in Aydın Adnan Menderes University Training and Research Hospital Parasitology Laboratory between 2005 and 2017. Turkiye Parazitol Derg. 2019;43:118-122.
  • 13. Başer S, Ismayıl A, Maçin S. Evaluation of the seropositivity of patients with cystic echinococcosis in Konya, Turkey. J Contemp Med. 2021;11:139-141.
  • 14. Ulusan Bağcı Ö, Pektaş B, Aksoy Gökmen A, et al. Use of ındirect hemagglutination test in the diagnosis of cystic echinococcosis: two years of retrospective laboratory experience. Turk Mikrobiyol Cem Derg. 2022;52: 223-231.
  • 15. Özkeklikçi A, Cirit OS. Investigation of the prevalence of cystic echinococcosis in Gaziantep-Türkiye by ELI.H.A Echinococcus ELITech between 2015-2022. Trakya Univ J Nat Sci. 2024;25:91-96.
  • 16. Karadağ A, Yanık K, Ünal N, et al. Kistik ekinokokkozis şüphesi ile 2005-2011 yılları arasında Ondokuz Mayıs Üniversitesi Tıp Fakültesi Parazitoloji Laboratuvarına gönderilen örneklerin değerlendirilmesi. Turkiye Parazitol Derg. 2013;37:28-31.
  • 17. Karaman U, Mıman O, Kara M, et al. Kars bölgesinde hidatik kist prevalansı [Hydatid cyst prevalence in the region of Kars.]. Turkiye Parazitol Derg. 2005;29:238-240.
  • 18. Taşbent FE, Yağcı B, Kadıyoran C, et al. Comparative evaluation of the efficacy of ındirect hemagglutination test and radiological methods in thepre-diagnosis of cystic echinococcosis. Turkiye Parazitol Derg. 2021;45:22-27.
  • 19. Vázquez-Pérez Á, Santos-Pérez JL. Cystic echinococcosis in a Moroccan boy: a silent and neglected disease among refugee and migrant children. BMJ Case Rep. 2022;15:e246399.
  • 20. Lees EA, Ives A, Fowler D, et al. Pulmonary cystic echinococcosis in a child presenting in the United Kingdom with fever and chest pain: a brief report and discussion on management. Pediatr Infect Dis J. 2023;42:e343-e345.
  • 21. Kern P, Da Silva AM, Akhan O, et al. The echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol. 2017;96:259-369.
  • 22. Balci AE, Eren N, Eren Ş, et al. Ruptured hydatid cysts of the lung in children: clinical review and results of surgery. Ann Thorac Surg. 2002;74:889-892.
  • 23. Ulusal Mikrobiyoloji Standartları. Bulaşıcı Hastalıklar Laboratuvar Tanı Rehberi. Cilt 3. T.C. Sağlık Bakanlığı Türkiye Halk Sağlığı Kurumu Başkanlığı Mikrobiyoloji Referans Laboratuvarları Daire Başkanlığı; 2014; Ankara.
  • 24. Sako Y, Nakao M, Nakaya K, et al. Alveolar echinococcosis: characterization of diagnostic antigen Em18 and serological evaluation of recombinant Em18. J Clin Microbiol. 2002;40:2760-2765.
  • 25. Gottstein B, Tschudi K, Eckert J, et al. Em2-ELISA for the follow-up of alveolar echinococcosis after complete surgical resection of liver lesions. Trans R Soc Trop Med Hyg. 1989;83:389-393.

Kistik Ekinokokkoz Ayırıcı Tanısında İndirekt Hemaglütinasyon Testinin Tanısal Performansının Değerlendirilmesi: Tek Merkez Deneyimi

Year 2025, Volume: 78 Issue: 1, 69 - 75, 31.03.2025

Abstract

Amaç: Çalışmamızın amacı hastanemize başvuran hastaların kistik ekinokokkoz (KE) epidemiyolojik verilerini ortaya koymak ve indirekt hemaglütinasyon testinin (IHAT) tanısal performansını değerlendirmektir.

Gereç ve Yöntem: Çalışma kapsamında 01.01.2023 ile 01.09.2024 tarihleri arasında KE IHAT istemi ile Ankara Üniversitesi İbni Sina Araştırma ve Uygulama Hastanesi Merkez Laboratuvarı’na rutin olarak serum örnekleri gönderilen hastalar değerlendirildi. Hastaların IHAT sonuçları, klinik ve laboratuvar bulguları ve radyolojik görüntüleme sonuçlarıyla birlikte değerlendirildi. Antikor titresi 1/320 ve üzerindeki değerler pozitif, 1/80 ve 1/160 ise şüpheli olarak belirtildi.

Bulgular: Altı yüz otuz altı hastanın seroloji sonuçları değerlendirildi. Pozitiflik oranı %5,97 olarak belirlendi. 0-19 yaş grubu en yüksek pozitiflik yüzdesine (%19) sahipti. Yaş gruplarının seropozitiflik oranları istatistiksel olarak anlamlı derecede farklı bulundu (p=0,011). Radyolojik görüntülemede kistik lezyonları görülen hasta grubu en yüksek seropozitiflik oranına (%11,9) sahipti. Radyolojik görüntülemelerde KE açısından spesifik bulguları olan hastalarda IHAT’ın seropozitiflik oranı eşik değer 1/80 olarak alındığında %39,6 olarak hesaplandı. Radyolojik görüntülemelerde kist saptanmayan hastalarda ise seronegatiflik oranı %95,7 olarak tespit edildi.

Sonuç: Radyolojik görüntülemelerde KE lezyonları tanımlanan hastalarda IHAT’ın pozitiflik oranı düşük bulunmuştur. Bu nedenle rutin laboratuvar testlerinde analitik duyarlılığı artırmak için IHAT ile birlikte ikinci bir serolojik testin kullanılmasının faydalı olacağı düşünülmektedir.

Anahtar Kelimeler: Kistik ekinokokkoz, indirekt hemaglütinasyon testi, seropozitiflik oranları, radyolojik görüntüleme

Project Number

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References

  • 1. Torgerson PR, Robertson LJ, Enemark HL, et al. Source attribution of human echinococcosis: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14:e0008382.
  • 2. Hogea MO, Ciomaga BF, Muntean MM, et al. Cystic Echinococcosis in the Early 2020s: a review. Trop Med Infect Dis. 2024;9:36.
  • 3. World Health Organization. Echinococcosis. Available from: https://www.who.int/news-room/fact-sheets/detail/echinococcosis. Accessed on 10 November, 2024.
  • 4. Morar R, Feldman C. Pulmonary echinococcosis. Eur Respir J. 2003;21:1069-1077.
  • 5. Alshaikhli A, Al-Hillan A. Liver Cystic Disease. [Updated 2023 Apr 24]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2025. Available from:https://www.ncbi.nlm.nih.gov/books/NBK567739/
  • 6. Brunetti E, Kern P, Vuitton DA; Writing Panel for the WHO-IWGE. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114:1-16.
  • 7. Devi M, Venumadhav T, Sukanya B, et al. Role of ımaging in diagnosis, predicting biological activity and in treatment plan of hydatid disease. Open J. Intern. Med. 2018;8:177-195.
  • 7. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al. Serological diagnosis and follow-up of human cystic echinococcosis: a new hope for the future? Biomed Res Int. 2015;2015:428205.
  • 8. Derbel F, Zidi MK, Mtimet A, et al. Hydatid cyst of the pancreas: a report on seven cases. Arab J Gastroenterol. 2010;11:219-22.
  • 9. Vola A, Manciulli T, De Silvestri A, et al. Diagnostic performances of commercial ELISA, ındirect hemagglutination, and western blot in differentiation of hepatic echinococcal and non-echinococcal lesions: a retrospective analysis of data from a single referral centre. Am J Trop Med Hyg. 2019;101:1345-1349.
  • 10. Siles-Lucas M, Uchiumi L, Tamarozzi F. ‘No cyst, no echinococcosis’: a scoping review update on the diagnosis of cystic echinococcosis after the issue of the WHO-IWGE Expert Consensus and current perspectives. Curr Opin Infect Dis. 2023;36:333-340.
  • 11. Yılmaz A, Uslu H, Aktaş F. 2009-2013 yılları arasında Erzurum Bölge Hastanesindeki kistik ekinokokkozis şüpheli hastaların indirekt hemaglütinasyon (İHA) metoduyla değerlendirilmesi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2016;5:23- 32.
  • 12. Ertabaklar H, Yıldız İ, Malatyalı E, et al. Retrospective analysis of cystic echinococcosis results in Aydın Adnan Menderes University Training and Research Hospital Parasitology Laboratory between 2005 and 2017. Turkiye Parazitol Derg. 2019;43:118-122.
  • 13. Başer S, Ismayıl A, Maçin S. Evaluation of the seropositivity of patients with cystic echinococcosis in Konya, Turkey. J Contemp Med. 2021;11:139-141.
  • 14. Ulusan Bağcı Ö, Pektaş B, Aksoy Gökmen A, et al. Use of ındirect hemagglutination test in the diagnosis of cystic echinococcosis: two years of retrospective laboratory experience. Turk Mikrobiyol Cem Derg. 2022;52: 223-231.
  • 15. Özkeklikçi A, Cirit OS. Investigation of the prevalence of cystic echinococcosis in Gaziantep-Türkiye by ELI.H.A Echinococcus ELITech between 2015-2022. Trakya Univ J Nat Sci. 2024;25:91-96.
  • 16. Karadağ A, Yanık K, Ünal N, et al. Kistik ekinokokkozis şüphesi ile 2005-2011 yılları arasında Ondokuz Mayıs Üniversitesi Tıp Fakültesi Parazitoloji Laboratuvarına gönderilen örneklerin değerlendirilmesi. Turkiye Parazitol Derg. 2013;37:28-31.
  • 17. Karaman U, Mıman O, Kara M, et al. Kars bölgesinde hidatik kist prevalansı [Hydatid cyst prevalence in the region of Kars.]. Turkiye Parazitol Derg. 2005;29:238-240.
  • 18. Taşbent FE, Yağcı B, Kadıyoran C, et al. Comparative evaluation of the efficacy of ındirect hemagglutination test and radiological methods in thepre-diagnosis of cystic echinococcosis. Turkiye Parazitol Derg. 2021;45:22-27.
  • 19. Vázquez-Pérez Á, Santos-Pérez JL. Cystic echinococcosis in a Moroccan boy: a silent and neglected disease among refugee and migrant children. BMJ Case Rep. 2022;15:e246399.
  • 20. Lees EA, Ives A, Fowler D, et al. Pulmonary cystic echinococcosis in a child presenting in the United Kingdom with fever and chest pain: a brief report and discussion on management. Pediatr Infect Dis J. 2023;42:e343-e345.
  • 21. Kern P, Da Silva AM, Akhan O, et al. The echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol. 2017;96:259-369.
  • 22. Balci AE, Eren N, Eren Ş, et al. Ruptured hydatid cysts of the lung in children: clinical review and results of surgery. Ann Thorac Surg. 2002;74:889-892.
  • 23. Ulusal Mikrobiyoloji Standartları. Bulaşıcı Hastalıklar Laboratuvar Tanı Rehberi. Cilt 3. T.C. Sağlık Bakanlığı Türkiye Halk Sağlığı Kurumu Başkanlığı Mikrobiyoloji Referans Laboratuvarları Daire Başkanlığı; 2014; Ankara.
  • 24. Sako Y, Nakao M, Nakaya K, et al. Alveolar echinococcosis: characterization of diagnostic antigen Em18 and serological evaluation of recombinant Em18. J Clin Microbiol. 2002;40:2760-2765.
  • 25. Gottstein B, Tschudi K, Eckert J, et al. Em2-ELISA for the follow-up of alveolar echinococcosis after complete surgical resection of liver lesions. Trans R Soc Trop Med Hyg. 1989;83:389-393.
There are 26 citations in total.

Details

Primary Language English
Subjects Medical Parasitology
Journal Section Research Article
Authors

Özlem Ulusan Bağcı This is me 0000-0002-9695-5703

Gülay Akarsu 0000-0003-0007-9006

Project Number -
Submission Date December 23, 2024
Acceptance Date March 3, 2025
Publication Date March 31, 2025
Published in Issue Year 2025 Volume: 78 Issue: 1

Cite

APA Ulusan Bağcı, Ö., & Akarsu, G. (2025). Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience. Ankara Üniversitesi Tıp Fakültesi Mecmuası, 78(1), 69-75. https://doi.org/10.4274/atfm.galenos.2025.27048
AMA Ulusan Bağcı Ö, Akarsu G. Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience. Ankara Üniversitesi Tıp Fakültesi Mecmuası. March 2025;78(1):69-75. doi:10.4274/atfm.galenos.2025.27048
Chicago Ulusan Bağcı, Özlem, and Gülay Akarsu. “Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience”. Ankara Üniversitesi Tıp Fakültesi Mecmuası 78, no. 1 (March 2025): 69-75. https://doi.org/10.4274/atfm.galenos.2025.27048.
EndNote Ulusan Bağcı Ö, Akarsu G (March 1, 2025) Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience. Ankara Üniversitesi Tıp Fakültesi Mecmuası 78 1 69–75.
IEEE Ö. Ulusan Bağcı and G. Akarsu, “Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience”, Ankara Üniversitesi Tıp Fakültesi Mecmuası, vol. 78, no. 1, pp. 69–75, 2025, doi: 10.4274/atfm.galenos.2025.27048.
ISNAD Ulusan Bağcı, Özlem - Akarsu, Gülay. “Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience”. Ankara Üniversitesi Tıp Fakültesi Mecmuası 78/1 (March2025), 69-75. https://doi.org/10.4274/atfm.galenos.2025.27048.
JAMA Ulusan Bağcı Ö, Akarsu G. Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience. Ankara Üniversitesi Tıp Fakültesi Mecmuası. 2025;78:69–75.
MLA Ulusan Bağcı, Özlem and Gülay Akarsu. “Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience”. Ankara Üniversitesi Tıp Fakültesi Mecmuası, vol. 78, no. 1, 2025, pp. 69-75, doi:10.4274/atfm.galenos.2025.27048.
Vancouver Ulusan Bağcı Ö, Akarsu G. Evaluation of the Diagnostic Performance of the Indirect Hemagglutination Test in the Differential Diagnosis of Cystic Echinococcosis: Single Center Experience. Ankara Üniversitesi Tıp Fakültesi Mecmuası. 2025;78(1):69-75.