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Original Article

Open Access Gateway

Outcomes of Different Methods for Analysis of Biliary Brush Cytology and of Factors Associated with Positive Diagnosis in an Age-Dependent Retrospective Review

Costa M.a · Canena J.a,d · Mascarenhas-Lemos L.b · Loureiro R.a · Silva M.a · Carvalho D.a · Capela T.a · Russo P.a · Ramos G.a · Mateus-Dias A.a · Ferraz-Oliveira M.b · Veiga P.M.c · Coimbra J.a

Author affiliations

aDepartment of Gastroenterology, Santo António dos Capuchos Hospital do Centro Hospitalar Lisboa Central, Nova Medical School/Faculty of Medical Sciences, Lisbon, Portugal
bDepartment of Pathology, São José Hospital do Centro Hospitalar Lisboa Central, Lisbon, Portugal
cCurva de Gauss – Research, Training and Consulting, Canas de Senhorim, Portugal
dCINTESIS – Center for Health Technology and Services Research, Porto, Portugal

Corresponding Author

Prof. Jorge Canena

Department of Gastroenterology, Santo António dos Capuchos Hospital do Centro

Hospitalar Lisboa Central, Nova Medical School/Faculty of Medical Sciences

Alameda Santo António dos Capuchos, PT–1169-050 Lisbon (Portugal)

E-Mail jmtcanena@live.com.pt

Keywords: Biliary cytologyAgeERCPPredictors of outcome

Related Articles for ""
GE Port J Gastroenterol 2019;26:5–13
https://doi.org/10.1159/000487153

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Abstract

Background and Aims: Brush cytology during endoscopic retrograde cholangiopancreatography (ERCP) is the most frequently used strategy for obtaining a tissue sample from an indeterminate biliary stricture. A recent study reported that age is a factor associated with positive yields, but further analysis of how age influences the results was lacking. We aimed to evaluate clinical effectiveness of biliary cytology and prognostic factors for a positive outcome, especially age. Methods: This study was a single-center, retrospective, clinical study of 77 consecutive patients who underwent brush cytology during ERCP to obtain a diagnosis of an indeterminate biliary stricture. We compared 2 routine cytology techniques: A (smear); B (centrifugation of the cytological material collected and the cut-off brush + cell block when sufficient amount of material was available). The data were collected aiming to compare the accuracy of the different techniques used and the prognostic factors affecting the outcome, with a particular focus on age. The yield for brush cytology was compared with the gold standard defined as either definitive histology or the long-term clinical course. Results: The overall accuracy of the 2 used methods was 75.3%. Sensitivity was 52.5%, specificity was 100%, positive predictive value was 100%, and negative predictive value was 66.1%. Although not statistically significant, there was a trend toward accuracy for method B compared with method A (80.4 vs. 65.4%; p = 0.153). Multiple logistic regression analysis showed that younger age was the only independent prognostic factor associated with a positive diagnosis (OR 0.95; 95% CI 0.90–0.99; p = 0.039). Receiver operating characteristic curves for age yielded an area under the curve value of 68.2%. On the basis of the Youden index, 69 years was found to be the optimal cutoff for age. Conclusions: In this series, the accuracy of routine biliary brush cytology was not equal for all methods and ages; in particular, younger patients (below 69 years) tended to have a higher probability of a correct diagnosis.

© 2018 Sociedade Portuguesa de Gastrenterologia Published by S. Karger AG, Basel

Eficácia de Diferentes Métodos de Avaliação da Citologia Biliar e dos Factores Associados a um Diagnóstico Positivo após Análise Retrospectiva Focada na Idade

Palavras Chave

Citologia biliar · Idade · CPRE · Fatores preditivos ·

Resumo

Introdução: a citologia biliar é a técnica mais utilizada durante a CPRE para o diagnóstico de uma estenose indeterminada. Um artigo recente refere a importância da idade como fator preditivo de um resultado positivo, embora sem analisar este dado. Pretendemos avaliar a acuidade da citologia biliar e dos factores associados para a obtenção de um resultado positivo com especial interesse na idade. Métodos: análise retrospectiva de um único centro de 77 doentes consecutivos submetidos, durante CPRE a citologia biliar para esclarecer a etiologia de uma estenose biliar. A análise comparou 2 técnicas de rotina: A (esfregaço); B (centrifugação do material colectado e da escova+cell block quando existia material suficiente). Pretendeu-se comparar a acuidade diagnóstica dos 2 diferentes métodos e dos factores de prognóstico associados ao resultado em especial a idade. A acuidade da citologia foi comparada com o “gold standard” definido como a histologia definitiva ou o curso clínico a longo prazo. Resultados: a acuidade global dos diferentes métodos foi 75.3%. A sensibilidade foi 52.5%, a especificidade foi 100%, VPP foi 100% e o VPN foi 66.1%. Apesar de não ser estatisticamente definitivo existiu maior acuidade do método B, em comparação com o A (80.4 vs. 65.4%; p = 0.153). A análise multivariada por regressão logística mostrou que a menor idade é o único fator de prognóstico independente associado a um resultado positivo (OR: 0.95; 95% CI: 0.90–0.99; p = 0.039). As curvas ROC para a idade apresentaram um valor para a AUC de 68.2%. O índice de Youden, determinou que os 69 anos seriam o “cutoff” ideal para a idade. Conclusões: nesta população a acuidade de citologia biliar não foi idêntica para todos os métodos e idades; em particular doentes com idade inferior a 69 anos apresentam maior probabilidade de obter um diagnóstico correto.



Related Articles:

References

  1. Mahmoudi N, Enns R, Amar J, AlAli J, Lam E, Telford J: Biliary brush cytology: factors associated with positive yields on biliary brush cytology. World J Gastroenterol 2008; 14: 569–573.
    External Resources
  2. Canena J, Coimbra J, Carvalho D, et al: Endoscopic bilio-duodenal bypass: outcomes of primary and revision efficacy of combined metallic stents in malignant duodenal and biliary obstruction. Dig Dis Sci 2014; 59: 2779–2789.
    External Resources
  3. Draganov P, Chauhan S, Wagh M, et al: Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study. Gastrointest Endosc 2012; 75: 347–353.
    External Resources
  4. Navaneethan U, Hasan MK, Lourdusamy V, Njei B, Varadarajulu S, Hawes RH: Single-operator cholangioscopy and targeted biopsies in the diagnosis of indeterminate biliary strictures: a systematic review. Gastrointest Endosc 2015; 82: 608–614.
    External Resources
  5. Woo YS, Lee JK, Oh SH, et al: Role of SpyGlass peroral cholangioscopy in the evaluation of indeterminate biliary lesions. Dig Dis Sci 2014; 59: 2565–2570.
    External Resources
  6. Nishikawa T, Tsuyuguchi T, Sakai Y, Sugiyama H, Miyazaki M, Yokosuka O: Comparison of the diagnostic accuracy of peroral video-cholangioscopic visual findings and cholangioscopy-guided forceps biopsy findings for indeterminate biliary lesions: a prospective study. Gastrointest Endosc 2013; 77: 219–226.
    External Resources
  7. Khashab MA, Fockens P, Al-Haddad MA: Utility of EUS in patients with indeterminate biliary strictures and suspected extrahepatic cholangiocarcinoma (with videos). Gastrointest Endosc 2012; 76: 1024–1033.
    External Resources
  8. Weilert F, Bhat YM, Binmoeller KF, et al: EUS-FNA is superior to ERCP-based tissue sampling in suspected malignant biliary obstruction: results of a prospective, single-blind, comparative study. Gastrointest Endosc 2014; 80: 97–104.
    External Resources
  9. De Moura DT, Moura EG, Bernardo WM, et al: Endoscopic retrograde cholangiopancreatography versus endoscopic ultrasound for tissue diagnosis of malignant biliary stricture: systematic review and meta-analysis. Endosc Ultrasound 2016, DOI: 10.4103/2303-9027.193597.
    External Resources
  10. Temiño López-Jurado R, Cacho Acosta G, Argüelles Pintos M, et al: Diagnostic yield of brush cytology for biliary stenosis during ERCP. Rev Esp Enferm Dig 2009; 101: 385–394.
    External Resources
  11. Shieh FK, Luong-Player A, Khara HS, et al: Improved endoscopic retrograde cholangiopancreatography brush increases diagnostic yield of malignant biliary strictures. World J Gastrointest Endosc 2014; 6: 312–317.
    External Resources
  12. Navaneethan U, Njei B, Lourdusamy V, Konjeti R, Vargo JJ, Parsi MA: Comparative effectiveness of biliary brush cytology and intraductal biopsy for detection of malignant biliary strictures: a systematic review and meta-analysis. Gastrointest Endosc 2015; 81: 168–176.
    External Resources
  13. Sasaki Y, Okabe Y, Ishida Y, et al: Evaluation of endoscopic transpapillary brushing cytology for the diagnosis of bile duct cancer based on the histopathologic findings. Dig Dis Sci 2014; 59: 2314–2319.
    External Resources
  14. Mohammad Alizadeh AH, Mousavi M, et al: Biliary brush cytology in the assessment of biliary strictures at a tertiary center in Iran. Asian Pac J Cancer Prev 2011; 12: 2793–2796.
    External Resources
  15. Nishikawa T, Tsuyuguchi T, Sakai Y, et al: Factors affecting the accuracy of endoscopic transpapillary sampling methods for bile duct cancer. Dig Endosc 2014; 26: 276–281.
    External Resources
  16. Ponchon T, Gagnon P, Berger F, et al: Value of endobiliary brush cytology and biopsies for the diagnosis of malignant bile duct stenosis: results of a prospective study. Gastrointest Endosc 1995; 42: 565–572.
    External Resources
  17. Pugliese V, Conlo M, Nicolo G, Saccomanno S, Gatteschi B: Endoscopic retrograde forceps biopsy and brush cytology of biliary strictures: a prospective study. Gastrointest Endosc 1995; 42: 520–526.
    External Resources
  18. Harewood GC, Baron TH, Stadheim LM, Kipp BR, Sebo TJ, Salomao DR: Prospective, blinded assessment of factors influencing the accuracy of biliary cytology interpretation. Am J Gastroenterol 2004; 99: 1464–1469.
    External Resources
  19. Urbano M, Rosa A, Gomes D, Camacho E, Calhau CA, Leitão M: Team approach to ERCP-directed single-brush cytology for the diagnosis of malignancy. Rev Esp Enferm Dig 2008; 100: 462–465.
    External Resources
  20. Arvanitakis M, Hookey L, Tessier G, et al: Intraductal optical coherence tomography during endoscopic retrograde cholangiopancreatography for investigation of biliary strictures. Endoscopy 2009; 41: 696–701.
    External Resources
  21. Burnett AS, Calvert TJ, Chokshi RJ: Sensitivity of endoscopic retrograde cholangiopancreatography standard cytology: 10-y review of the literature. J Surg Res 2013; 184: 304–311.
    External Resources
  22. Mehmood S, Loya A, Yusuf MA: Biliary brush cytology revisited. Acta Cytol 2016; 60: 167–172.
    External Resources
  23. Dumonceau J, Macias Gomez C, Casco C, et al: Grasp or brush for biliary sampling at endoscopic retrograde cholangiography? A blinded randomized controlled trial. Am J Gastroenterol 2008; 108: 333–340.
    External Resources
  24. Bang KB, Kim HJ, Park JH, et al: Comparison of brush and basket cytology in differential diagnosis of bile duct stricture at endoscopic retrograde cholangiopancreatography. Hepatobiliary Pancreat Dis Int 2014; 13: 622–627.
    External Resources
  25. Shieh FK, Luong-Player A, Khara HS, et al: Improved endoscopic retrograde cholangiopancreatography brush increases diagnostic yield of malignant biliary strictures. World J Gastrointest Endosc 2014; 6: 312–317.
    External Resources
  26. Salomao M, Gonda TA, Margolskee E, et al: Strategies for improving diagnostic accuracy of biliary strictures. Cancer Cytopathol 2015; 123: 244–252.
    External Resources
  27. Levy MJ, Baron TH, Clayton AC, et al: Prospective evaluation of advanced molecular markers and imaging techniques in patients with indeterminate bile duct strictures. Am J Gastroenterol 2008; 103: 1263–1273.
    External Resources
  28. Farrell RJ, Jain AK, Brandwein SL, Wang H, Chuttani R, Pleskow DK: The combination of stricture dilation, endoscopic needle aspiration, and biliary brushings significantly improves diagnostic yield from malignant bile duct strictures. Gastrointest Endosc 2001; 54: 587–594.
    External Resources
  29. Boldorini R, Paganotti A, Andorno S, et al: A multistep cytological approach for patients with jaundice and biliary strictures of indeterminate origin. J Clin Pathol 2015; 68: 283–287.
    External Resources
  30. De Bellis M, Fogel EL, Sherman S, et al: Influence of stricture dilation and repeat brushing on the cancer detection rate of brush cytology in the evaluation of malignant biliary obstruction. Gastrointest Endosc 2003; 58: 176–182.
    External Resources
  31. Slivka A, Gan I, Jamidar P, et al: Validation of the diagnostic accuracy of probe-based confocal laser endomicroscopy for the characterization of indeterminate biliary strictures: results of a prospective multicenter international study. Gastrointest Endosc 2015; 81: 282–290.
    External Resources
  32. Nathan NA, Narayan E, Smith MM, Horn MJ: Cell block cytology. Improved preparation and its efficacy in diagnostic cytology. Am J Clin Pathol 2000; 114: 599–606.
    External Resources
  33. McGuire DE, Venu RP, Brown RD, Etzkorn KP, Glaws WR, Abu-Hammour A: Brush cytology for pancreatic carcinoma: an analysis of factors influencing results. Gastrointest Endosc 1996; 44: 300–304.
    External Resources
  34. De Bellis M, Fogel EL, Sherman S, et al: Influence of stricture dilation and repeat brushing on the cancer detection rate of brush cytology in the evaluation of malignant biliary obstruction. Gastrointest Endosc 2003; 58: 176–182.
    External Resources
  35. Meining A, Chen Y, Pleskow D, et al: Direct visualization of indeterminate pancreaticobiliary strictures with probe-based confocal laser endomicroscopy: a multicenter experience. Gastrointest Endosc 2011; 74: 961–968.
    External Resources
  36. Baillie J: Distinguishing malignant from benign biliary strictures: can confocal laser endomicroscopy close the gap? Gastrointest Endosc 2015; 81: 291–293.
    External Resources
  37. Yang JF, Sharaiha RZ, Francis G, et al: Diagnostic accuracy of directed cholangioscopic biopsies and confocal laser endomicroscopy in cytology-negative indeterminate bile duct stricture: a multicenter comparison trial. Minerva Gastroenterol Dietol 2016; 62: 227–233.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Original Article

Received: November 27, 2017
Accepted: January 18, 2018
Published online: February 28, 2018
Issue release date: January - February

Number of Print Pages: 9
Number of Figures: 1
Number of Tables: 5

ISSN: 2341-4545 (Print)
eISSN: 2387-1954 (Online)

For additional information: https://www.karger.com/PJG

References

  1. Mahmoudi N, Enns R, Amar J, AlAli J, Lam E, Telford J: Biliary brush cytology: factors associated with positive yields on biliary brush cytology. World J Gastroenterol 2008; 14: 569–573.
    External Resources
  2. Canena J, Coimbra J, Carvalho D, et al: Endoscopic bilio-duodenal bypass: outcomes of primary and revision efficacy of combined metallic stents in malignant duodenal and biliary obstruction. Dig Dis Sci 2014; 59: 2779–2789.
    External Resources
  3. Draganov P, Chauhan S, Wagh M, et al: Diagnostic accuracy of conventional and cholangioscopy-guided sampling of indeterminate biliary lesions at the time of ERCP: a prospective, long-term follow-up study. Gastrointest Endosc 2012; 75: 347–353.
    External Resources
  4. Navaneethan U, Hasan MK, Lourdusamy V, Njei B, Varadarajulu S, Hawes RH: Single-operator cholangioscopy and targeted biopsies in the diagnosis of indeterminate biliary strictures: a systematic review. Gastrointest Endosc 2015; 82: 608–614.
    External Resources
  5. Woo YS, Lee JK, Oh SH, et al: Role of SpyGlass peroral cholangioscopy in the evaluation of indeterminate biliary lesions. Dig Dis Sci 2014; 59: 2565–2570.
    External Resources
  6. Nishikawa T, Tsuyuguchi T, Sakai Y, Sugiyama H, Miyazaki M, Yokosuka O: Comparison of the diagnostic accuracy of peroral video-cholangioscopic visual findings and cholangioscopy-guided forceps biopsy findings for indeterminate biliary lesions: a prospective study. Gastrointest Endosc 2013; 77: 219–226.
    External Resources
  7. Khashab MA, Fockens P, Al-Haddad MA: Utility of EUS in patients with indeterminate biliary strictures and suspected extrahepatic cholangiocarcinoma (with videos). Gastrointest Endosc 2012; 76: 1024–1033.
    External Resources
  8. Weilert F, Bhat YM, Binmoeller KF, et al: EUS-FNA is superior to ERCP-based tissue sampling in suspected malignant biliary obstruction: results of a prospective, single-blind, comparative study. Gastrointest Endosc 2014; 80: 97–104.
    External Resources
  9. De Moura DT, Moura EG, Bernardo WM, et al: Endoscopic retrograde cholangiopancreatography versus endoscopic ultrasound for tissue diagnosis of malignant biliary stricture: systematic review and meta-analysis. Endosc Ultrasound 2016, DOI: 10.4103/2303-9027.193597.
    External Resources
  10. Temiño López-Jurado R, Cacho Acosta G, Argüelles Pintos M, et al: Diagnostic yield of brush cytology for biliary stenosis during ERCP. Rev Esp Enferm Dig 2009; 101: 385–394.
    External Resources
  11. Shieh FK, Luong-Player A, Khara HS, et al: Improved endoscopic retrograde cholangiopancreatography brush increases diagnostic yield of malignant biliary strictures. World J Gastrointest Endosc 2014; 6: 312–317.
    External Resources
  12. Navaneethan U, Njei B, Lourdusamy V, Konjeti R, Vargo JJ, Parsi MA: Comparative effectiveness of biliary brush cytology and intraductal biopsy for detection of malignant biliary strictures: a systematic review and meta-analysis. Gastrointest Endosc 2015; 81: 168–176.
    External Resources
  13. Sasaki Y, Okabe Y, Ishida Y, et al: Evaluation of endoscopic transpapillary brushing cytology for the diagnosis of bile duct cancer based on the histopathologic findings. Dig Dis Sci 2014; 59: 2314–2319.
    External Resources
  14. Mohammad Alizadeh AH, Mousavi M, et al: Biliary brush cytology in the assessment of biliary strictures at a tertiary center in Iran. Asian Pac J Cancer Prev 2011; 12: 2793–2796.
    External Resources
  15. Nishikawa T, Tsuyuguchi T, Sakai Y, et al: Factors affecting the accuracy of endoscopic transpapillary sampling methods for bile duct cancer. Dig Endosc 2014; 26: 276–281.
    External Resources
  16. Ponchon T, Gagnon P, Berger F, et al: Value of endobiliary brush cytology and biopsies for the diagnosis of malignant bile duct stenosis: results of a prospective study. Gastrointest Endosc 1995; 42: 565–572.
    External Resources
  17. Pugliese V, Conlo M, Nicolo G, Saccomanno S, Gatteschi B: Endoscopic retrograde forceps biopsy and brush cytology of biliary strictures: a prospective study. Gastrointest Endosc 1995; 42: 520–526.
    External Resources
  18. Harewood GC, Baron TH, Stadheim LM, Kipp BR, Sebo TJ, Salomao DR: Prospective, blinded assessment of factors influencing the accuracy of biliary cytology interpretation. Am J Gastroenterol 2004; 99: 1464–1469.
    External Resources
  19. Urbano M, Rosa A, Gomes D, Camacho E, Calhau CA, Leitão M: Team approach to ERCP-directed single-brush cytology for the diagnosis of malignancy. Rev Esp Enferm Dig 2008; 100: 462–465.
    External Resources
  20. Arvanitakis M, Hookey L, Tessier G, et al: Intraductal optical coherence tomography during endoscopic retrograde cholangiopancreatography for investigation of biliary strictures. Endoscopy 2009; 41: 696–701.
    External Resources
  21. Burnett AS, Calvert TJ, Chokshi RJ: Sensitivity of endoscopic retrograde cholangiopancreatography standard cytology: 10-y review of the literature. J Surg Res 2013; 184: 304–311.
    External Resources
  22. Mehmood S, Loya A, Yusuf MA: Biliary brush cytology revisited. Acta Cytol 2016; 60: 167–172.
    External Resources
  23. Dumonceau J, Macias Gomez C, Casco C, et al: Grasp or brush for biliary sampling at endoscopic retrograde cholangiography? A blinded randomized controlled trial. Am J Gastroenterol 2008; 108: 333–340.
    External Resources
  24. Bang KB, Kim HJ, Park JH, et al: Comparison of brush and basket cytology in differential diagnosis of bile duct stricture at endoscopic retrograde cholangiopancreatography. Hepatobiliary Pancreat Dis Int 2014; 13: 622–627.
    External Resources
  25. Shieh FK, Luong-Player A, Khara HS, et al: Improved endoscopic retrograde cholangiopancreatography brush increases diagnostic yield of malignant biliary strictures. World J Gastrointest Endosc 2014; 6: 312–317.
    External Resources
  26. Salomao M, Gonda TA, Margolskee E, et al: Strategies for improving diagnostic accuracy of biliary strictures. Cancer Cytopathol 2015; 123: 244–252.
    External Resources
  27. Levy MJ, Baron TH, Clayton AC, et al: Prospective evaluation of advanced molecular markers and imaging techniques in patients with indeterminate bile duct strictures. Am J Gastroenterol 2008; 103: 1263–1273.
    External Resources
  28. Farrell RJ, Jain AK, Brandwein SL, Wang H, Chuttani R, Pleskow DK: The combination of stricture dilation, endoscopic needle aspiration, and biliary brushings significantly improves diagnostic yield from malignant bile duct strictures. Gastrointest Endosc 2001; 54: 587–594.
    External Resources
  29. Boldorini R, Paganotti A, Andorno S, et al: A multistep cytological approach for patients with jaundice and biliary strictures of indeterminate origin. J Clin Pathol 2015; 68: 283–287.
    External Resources
  30. De Bellis M, Fogel EL, Sherman S, et al: Influence of stricture dilation and repeat brushing on the cancer detection rate of brush cytology in the evaluation of malignant biliary obstruction. Gastrointest Endosc 2003; 58: 176–182.
    External Resources
  31. Slivka A, Gan I, Jamidar P, et al: Validation of the diagnostic accuracy of probe-based confocal laser endomicroscopy for the characterization of indeterminate biliary strictures: results of a prospective multicenter international study. Gastrointest Endosc 2015; 81: 282–290.
    External Resources
  32. Nathan NA, Narayan E, Smith MM, Horn MJ: Cell block cytology. Improved preparation and its efficacy in diagnostic cytology. Am J Clin Pathol 2000; 114: 599–606.
    External Resources
  33. McGuire DE, Venu RP, Brown RD, Etzkorn KP, Glaws WR, Abu-Hammour A: Brush cytology for pancreatic carcinoma: an analysis of factors influencing results. Gastrointest Endosc 1996; 44: 300–304.
    External Resources
  34. De Bellis M, Fogel EL, Sherman S, et al: Influence of stricture dilation and repeat brushing on the cancer detection rate of brush cytology in the evaluation of malignant biliary obstruction. Gastrointest Endosc 2003; 58: 176–182.
    External Resources
  35. Meining A, Chen Y, Pleskow D, et al: Direct visualization of indeterminate pancreaticobiliary strictures with probe-based confocal laser endomicroscopy: a multicenter experience. Gastrointest Endosc 2011; 74: 961–968.
    External Resources
  36. Baillie J: Distinguishing malignant from benign biliary strictures: can confocal laser endomicroscopy close the gap? Gastrointest Endosc 2015; 81: 291–293.
    External Resources
  37. Yang JF, Sharaiha RZ, Francis G, et al: Diagnostic accuracy of directed cholangioscopic biopsies and confocal laser endomicroscopy in cytology-negative indeterminate bile duct stricture: a multicenter comparison trial. Minerva Gastroenterol Dietol 2016; 62: 227–233.
    External Resources
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Mariana Costa and Jorge Canena contributed equally to this article.