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High predictive ability of apparent diffusion coefficient value for wall-invasion pattern of advanced gallbladder carcinoma

  • Hepatobiliary
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Abdominal Radiology Aims and scope Submit manuscript

Abstract

Purpose

The wall-invasion pattern classification of advanced gallbladder carcinoma (GBC) has been reported. However, its association with clinical findings remains unclear. We aimed to clarify relationships between clinicopathological characteristics, prognosis, and apparent diffusion coefficient (ADC) values of advanced GBC based on the wall-invasion pattern.

Methods

We reviewed the data of 37 patients who had undergone advanced GBC cholecystectomy at our institution between 2009 and 2021. Clinicopathological findings, prognosis, and ADC values were retrospectively analyzed.

Results

Based on the wall-invasion pattern, patients were classified into infiltrative growth (IG) type (n = 22) and destructive growth (DG) type (n = 15). In the DG-type, the incidence of venous invasion (P = 0.027), neural invasion (P = 0.008), and lymph node metastasis (P = 0.047) was significantly higher than in the IG-type, and recurrent-free survival (RFS) was significantly shorter (P = 0.015); the median RFS was 11.4 months (95% confidence interval, 6.3–16.5 months) in the DG-type and not reached in the IG-type. The ADC value in the DG-type was significantly lower than in the IG-type (median, 1.19 × 10−3 mm2/s vs. 1.86 × 10−3 mm2/s, P < 0.001). The area under the receiver operating characteristic curve for the ADC values to differentiate wall-invasion patterns was 0.95 (95% confidence interval, 0.87–1.00). The optimal cutoff ADC value was 1.45 × 10–3 mm2/s (sensitivity, 92.9%; specificity, 90.9%).

Conclusions

The wall-invasion pattern of advanced GBC is associated with its aggressiveness and prognosis, and can be predicted by ADC values with high accuracy.

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References

  1. Kayahara M, Nagakawa T, Nakagawara H, Kitagawa H, Ohta T. Prognostic factors for gallbladder cancer in Japan. Ann Surg. 2008; 248: 807-14.

    Article  PubMed  Google Scholar 

  2. Ishihara S, Horiguchi A, Miyakawa S, Endo I, Miyazaki M, Takada T. Biliary tract cancer registry in Japan from 2008 to 2013. J Hepatobiliary Pancreat Sci. 2016; 23: 149-57.

    Article  PubMed  Google Scholar 

  3. Okada K, Kijima H, Imaizumi T, Hirabayashi K, Matsuyama M, Yazawa N, Oida Y, Dowaki S, Tobita K, Ohtani Y, Tanaka M, Inokuchi S, Makuuchi H. Wall-invasion pattern correlates with survival of patients with gallbladder adenocarcinoma. Anticancer Res. 2009; 29: 685-91.

    PubMed  Google Scholar 

  4. Okada K, Kijima H, Imaizumi T, Hirabayashi K, Matsuyama M, Yazawa N, Dowaki S, Tobita K, Ohtani Y, Tanaka M, Inokuchi S, Makuuchi H.. Clinical significance of wall invasion pattern of subserosa-invasive gallbladder carcinoma. Oncol Rep. 2012; 28: 1531-6.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kijima H, Wu Y, Yosizawa T, Suzuki T, Tsugeno Y, Haga T, Seino H, Morohashi S, Hakamada K. Pathological characteristics of early to advanced gallbladder carcinoma and extrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Sci. 2014; 21: 453-8.

    Article  PubMed  Google Scholar 

  6. Toba T, Kijima H, Hakamada K, Igarashi Y. Histological phenotype is correlated with the wall-invasion pattern of gallbladder adenocarcinoma. Biomed Res. 2014; 35: 295-302.

    Article  CAS  PubMed  Google Scholar 

  7. Lyng H, Haraldseth O, Rofstad EK. Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging. Magn Reson Med. 2000; 43: 828-36.

    Article  CAS  PubMed  Google Scholar 

  8. Yoshikawa T, Kawamitsu H, Mitchell DG, Ohno Y, Ku Y, Seo Y, Fujii M, Sugimura K. ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol. 2006; 187: 1521-30.

    Article  PubMed  Google Scholar 

  9. Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG. Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging. 2012; 35: 1365-71.

    Article  PubMed  Google Scholar 

  10. Lee NK, Kim S, Kim GH, Kim DU, Seo HI, Kim TU, Kang DH, Jang HJ. Diffusion-weighted imaging of biliopancreatic disorders: correlation with conventional magnetic resonance imaging. World J Gastroenterol. 2012; 18: 4102-17.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kang TW, Kim SH, Jang KM, Choi D, Ha SY, Kim KM, Kang WK, Kim MJ. Gastrointestinal stromal tumours: correlation of modified NIH risk stratification with diffusion-weighted MR imaging as an imaging biomarker. Eur J Radiol. 2015; 84: 33-40.

    Article  PubMed  Google Scholar 

  12. Kim M, Kang TW, Kim YK, Kim SH, Kwon W, Ha SY, Ji SA. Pancreatic neuroendocrine tumour: Correlation of apparent diffusion coefficient or WHO classification with recurrence-free survival. Eur J Radiol. 2016; 85: 680-7.

    Article  PubMed  Google Scholar 

  13. Sugita R, Yamazaki T, Furuta A, Itoh K, Fujita N, Takahashi S. High b-value diffusion-weighted MRI for detecting gallbladder carcinoma: preliminary study and results. Eur Radiol. 2009; 19: 1794-8.

    Article  PubMed  Google Scholar 

  14. Ogawa T, Horaguchi J, Fujita N, Noda T, Kobayashi G, Ito K, Koshita S, Kanno Y, Masu K, Sugita R. High b-value diffusion-weighted magnetic resonance imaging for gallbladder lesions: differentiation between benignity and malignancy. J Gastroenterol. 2012; 47: 1352-60.

    Article  PubMed  Google Scholar 

  15. Kim SJ, Lee JM, Kim H, Yoon JH, Han JK, Choi BI. Role of diffusion-weighted magnetic resonance imaging in the diagnosis of gallbladder cancer. J Magn Reson Imaging. 2013; 38: 127-37.

    Article  PubMed  Google Scholar 

  16. Kitazume Y, Taura S, Nakaminato S, Noguchi O, Masaki Y, Kasahara I, Kishino M, Tateishi U. Diffusion-weighted magnetic resonance imaging to differentiate malignant from benign gallbladder disorders. Eur J Radiol. 2016; 85: 864-73.

    Article  PubMed  Google Scholar 

  17. Lee NK, Kim S, Moon JI, Shin N, Kim DU, Seo HI, Kim HS, Han GJ, Kim JY, Lee JW. Diffusion-weighted magnetic resonance imaging of gallbladder adenocarcinoma: analysis with emphasis on histologic grade. Clin Imaging. 2016; 40: 345-51.

    Article  PubMed  Google Scholar 

  18. Min JH, Kang TW, Cha DI, Kim SH, Shin KS, Lee JE, Jang KT, Ahn SH. Apparent diffusion coefficient as a potential marker for tumour differentiation, staging and long-term clinical outcomes in gallbladder cancer. Eur Radiol. 2019; 29: 411-21.

    Article  PubMed  Google Scholar 

  19. Nakata T, Kobayashi A, Miwa S, Soeda J, Uehara T, Miyagawa S. Clinical and pathological features of primary carcinoma of the cystic duct. J Hepatobiliary Pancreat Surg. 2009; 16: 75-82.

    Article  PubMed  Google Scholar 

  20. Nan L, Wang C, Dai Y, Wang J, Bo X, Zhang S, Zhang D, Liu H, Wang Y. Cystic Duct Carcinoma: A New Classification System and the Clinicopathological Features of 62 Patients. Front Oncol. 2021; 11: 696714.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Brierley J, Gospodarowics M, Wittekind C. TNM classification of malignant tumours. 8th Edition. Wiley-Blacwell, Oxford. 2017.

    Google Scholar 

  22. Miyazaki M, Ohtsuka M, Miyakawa S, Nagino M, Yamamoto M, Kokudo N, Sano K, Endo I, Unno M, Chijiiwa K, Horiguchi A, Kinoshita H, Oka M, Kubota K, Sugiyama M, Uemoto S, Shimada M, Suzuki Y, Inui K, Tazuma S, Furuse J, Yanagisawa A, Nakanuma Y, Kijima, H, Takada T. Classification of biliary tract cancers established by the Japanese Society of Hepato-Biliary-Pancreatic Surgery: 3(rd) English edition. J Hepatobiliary Pancreat Sci. 2015; 22: 181–96.

  23. Shirai Y, Sakata J, Wakai T, Ohashi T, Hatakeyama K. "Extended" radical cholecystectomy for gallbladder cancer: long-term outcomes, indications and limitations. World J Gastroenterol. 2012; 18: 4736-43.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Fluss R, Faraggi D, Reiser B. Estimation of the Youden Index and its associated cutoff point. Biom J. 2005; 47: 458-72.

    Article  PubMed  Google Scholar 

  25. Kashiwagi H, Kijima H, Dowaki S, Ohtani Y, Tobita K, Yamazaki H, Nakamura M, Ueyama Y, Tanaka M, Inokuchi S, Makuuchi H. MUC1 and MUC2 expression in human gallbladder carcinoma: a clinicopathological study and relationship with prognosis. Oncol Rep. 2001; 8: 485-9.

    CAS  PubMed  Google Scholar 

  26. Kawamoto T, Shoda J, Irimura T, Miyahara N, Furukawa M, Ueda T, Asano T, Kano M, Koike N, Fukao K, Tanaka N, Todoroki T. Expression of MUC1 mucins in the subserosal layer correlates with postsurgical prognosis of pathological tumor stage 2 carcinoma of the gallbladder. Clin Cancer Res. 2001; 7: 1333-42.

    CAS  PubMed  Google Scholar 

  27. Chang HJ, Kim SW, Lee BL, Hong EK, Kim WH. Phenotypic alterations of mucins and cytokeratins during gallbladder carcinogenesis. Pathol Int. 2004; 54: 576-84.

    Article  CAS  PubMed  Google Scholar 

  28. Hiraki T, Yamada S, Higashi M, Hatanaka K, Yokoyama S, Kitanozo I, Goto Y, Kirishima M, Batra SK, Yonezawa S, Tanimoto A. Immunohistochemical expression of mucin antigens in gallbladder adenocarcinoma: MUC1-positive and MUC2-negative expression Is associated with vessel invasion and shortened survival. Histol Histopathol. 2017; 32: 585-96.

    CAS  PubMed  Google Scholar 

  29. Carrasco C, Tittarelli A, Paillaleve N, Pozo MD, Rojas-Sepúlveda D, Barría O, Fluxá P, Hott M, Martin C, Quezada C, Salazar-Onfray F. The Evaluation of 17 Gastrointestinal Tumor Markers Reveals Prognosis Value for MUC6, CK17, and CD10 in Gallbladder-Cancer Patients. Diagnostics (Basel). 2021; 11.

  30. Lee H, Kwon W, Han Y, Kim JR, Kim SW, Jang JY. Optimal extent of surgery for early gallbladder cancer with regard to long-term survival: a meta-analysis. J Hepatobiliary Pancreat Sci. 2018; 25: 131-41.

    Article  PubMed  Google Scholar 

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Acknowledgements

We are deeply grateful to Kengo Yoshimitsu, Shigeki Nagamachi, and Suguru Hasegawa for providing advice on this study. The authors are also grateful to Yasushi Yamauchi, Takamitsu Sasaki, Daisuke Kato for their engagement in the patient care and follow-up.

Funding

The authors did not receive support from any organization for the submitted work.

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Authors and Affiliations

  1. Department of Gastroenterology and Medicine, Faculty of Medicine, Fukuoka University, 7-45-1 Nanakuma, Jonan-Ku, Fukuoka, 814-0180, Japan

    Takehiko Koga, Yusuke Ishida, Naoaki Tsuchiya, Takanori Kitaguchi, Keisuke Matsumoto & Fumihito Hirai

  2. Department of Pathology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

    Yoshihiro Hamada

  3. Department of Radiology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

    Yukihisa Takayama

  4. Department of Gastroenterological Surgery, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

    Masatoshi Kajiwara, Shigetoshi Naito, Fuminori Ishii, Ryo Nakashima & Takahide Sasaki

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  1. Takehiko Koga
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  2. Yusuke Ishida
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by TK, YH, YT, YI, and NT. The first draft of the manuscript was written by TK and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yusuke Ishida.

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Koga, T., Ishida, Y., Hamada, Y. et al. High predictive ability of apparent diffusion coefficient value for wall-invasion pattern of advanced gallbladder carcinoma. Abdom Radiol 48, 902–912 (2023). https://doi.org/10.1007/s00261-023-03805-4

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