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Association of the primary tumor’s SUVmax with survival after surgery for clinical stage IA esophageal cancer: a single-center retrospective study

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Abstract

Background

Compared to other esophageal cancers, clinical stage IA esophageal cancer generally has a good prognosis, although a subgroup of patients has a poor prognosis. Unfortunately, clinical diagnoses of invasion depth or lymph node metastasis are not always accurate, which make it difficult to identify patients with a high risk of postoperative recurrence using the tumor-node-metastasis staging system. Fluorodeoxyglucose-positron emission tomography may help guide the identification of malignant tumors and the evaluation of their malignant grade based on glucose metabolism. We aimed to evaluate the association between pre-operative fluorodeoxyglucose-positron emission tomography findings and the postoperative prognosis of patients with clinical stage IA esophageal cancer.

Methods

This single-center retrospective study evaluated pre-esophagectomy fluorodeoxyglucose-positron emission tomography findings from 38 patients with clinical stage IA esophageal cancer. Receiver operating characteristic curve analysis was performed to evaluate the prognostic significance of the primary tumor having low and high SUVmax values (cut-off: 3.56).

Results

Overall survival (log-rank p = 0.034) and progression-free survival (log-rank p = 0.008) were significantly different between the groups with low SUVmax values (n = 18) and high SUVmax values (n = 20). Furthermore, the primary tumor’s SUVmax value was related to pathological vascular invasion (p = 0.045) and distant metastasis (p = 0.042).

Conclusion

The SUVmax of the primary tumor is a predictor of postoperative survival for clinical stage IA esophageal cancer. Thus, using fluorodeoxyglucose-positron emission tomography to evaluate the primary tumor’s glucose metabolism may reflect the tumor’s grade and potentially compensate for inaccuracies in tumor-node-metastasis staging.

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References

  1. Kitagawa Y, Uno T, Oyama T et al (2019) Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal society: part 1. Esophagus 16:1–24

    Article  Google Scholar 

  2. Endo M, Kawano T (1997) Detection and classification of early squamous cell esophageal cancer. Dis Esophagus 10:155–158

    Article  CAS  Google Scholar 

  3. Muto M, Minashi K, Yano T et al (2010) Early detection of superficial squamous cell carcinoma in the head and neck region and esophagus by narrow band imaging: a multicenter randomized controlled trial. J Clin Oncol 28:1566–1572

    Article  Google Scholar 

  4. Ishihara R, Iishi H, Uedo N et al (2008) Comparison of EMR and endoscopic submucosal dissection for en bloc resection of early esophageal cancers in Japan. Gastrointest Endosc 68:1066–1072

    Article  Google Scholar 

  5. Katada C, Tanabe S, Wada T et al (2019) Retrospective assessment of the diagnostic accuracy of the depth of invasion by narrow band imaging magnifying endoscopy in patients with superficial esophageal squamous cell carcinoma. J Gastrointest Cancer 50:292–297

    Article  Google Scholar 

  6. Mizumoto T, Hiyama T, Oka S et al (2018) Diagnosis of superficial esophageal squamous cell carcinoma invasion depth before endoscopic submucosal dissection. Dis Esophagus. https://doi.org/10.1093/dote/dox142

    Article  PubMed  Google Scholar 

  7. McGuill MJ, Byrne P, Ravi N et al (2008) The prognostic impact of occult lymph node metastasis in cancer of the esophagus or esophago-gastric junction: systematic review and meta-analysis. Dis Esophagus 21:236–240

    Article  CAS  Google Scholar 

  8. Aoyama J, Kawakubo H, Mayanagi S et al (2019) Discrepancy between the clinical and final pathological findings of lymph node metastasis in superficial esophageal cancer. Ann Surg Oncol 26:2874–2881

    Article  Google Scholar 

  9. Rigo P, Paulus P, Kaschten BJ et al (1996) Oncological applications of positron emission tomography with fluorine-18 fluorodeoxyglucose. Eur J Nucl Med 23:1641–1674

    Article  CAS  Google Scholar 

  10. Kato H, Kuwano H, Nakajima M et al (2002) Comparison between positron emission tomography and computed tomography in the use of the assessment of esophageal carcinoma. Cancer 94:921–928

    Article  Google Scholar 

  11. Guo H, Zhu H, Xi Y et al (2007) Diagnostic and prognostic value of 18F-FDG PET/CT for patients with suspected recurrence from squamous cell carcinoma of the esophagus. J Nucl Med 48:1251–1258

    Article  Google Scholar 

  12. Brücher BL, Weber W, Bauer M et al (2001) Neoadjuvant therapy of esophageal squamous cell carcinoma: response evaluation by positron emission tomography. Ann Surg 233:300–309

    Article  Google Scholar 

  13. Downey RJ, Akhrust T, Ilson D et al (2003) Whole body 18FDGPET and the response of esophageal cancer to induction therapy: results of a prospective trial. J Clin Oncol 21:428–432

    Article  Google Scholar 

  14. Miyata H, Yamasaki M, Takahashi T et al (2014) Determinants of response to neoadjuvant chemotherapy for esophageal cancer using 18F-fluorodeoxiglucose positron emission tomography (18F-FDG-PET). Ann Surg Oncol 21:575–582

    Article  Google Scholar 

  15. Miyata H, Doki Y, Yasuda T et al (2008) Evaluation of clinical significance of 18F-fluorodeoxyglucose positron emission tomography in superficial squamous cell carcinomas of the thoracic esophagus. Dis Esophagus 21:144–150

    Article  CAS  Google Scholar 

  16. Kita Y, Okumura H, Uchikado Y et al (2013) Clinical significance of 18F-fluorodeoxyglucose positron emission tomography in superficial esophageal squamous cell carcinoma. Ann Surg Oncol 20:1646–1652

    Article  Google Scholar 

  17. Nakajima M, Muroi H, Yokoyama H et al (2018) 18 F-Fluorodeoxyglucose positron emission tomography can be used to determine the indication for endoscopic resection of superficial esophageal cancer. Cancer Med 7:3604–3610

    Article  CAS  Google Scholar 

  18. Rice TW, Gress DM, Patil DT et al (2017) Cancer of the esophagus and esophagogastric junction-major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin 67:304–317

  19. Japan Esophageal Society (2017) Japanese Classification of Esophageal Cancer, 11th edition: part I. Esophagus 14:1–36

    Article  Google Scholar 

  20. Brown C, Howes B, Jamieson GG et al (2012) Accuracy of PET-CT in predicting survival in patients with esophageal cancer. World J Surg 36:1089–1095

    Article  Google Scholar 

  21. Yasuda T, Yano M, Miyata H et al (2015) Prognostic significance of (18)F-fluorodeoxyglucose positron emission tomography (FDG-PET)-positive lymph nodes following neoadjuvant chemotherapy and surgery for resectable thoracic esophageal squamous cell carcinoma. Ann Surg Oncol 22:2599–2607

    Article  Google Scholar 

  22. Hamai Y, Hihara J, Emi M et al (2016) Ability of fluorine-18 fluorodeoxyglucose positron emission tomography to predict outcomes of neoadjuvant chemoradiotherapy followed by surgical treatment for esophageal squamous cell carcinoma. Ann Thorac Surg 102:1132–1139

    Article  Google Scholar 

  23. Izumi D, Yoshida N, Watanabe M et al (2016) Tumor/normal esophagus ratio in (18)F-fluorodeoxyglucose positron emission tomography/computed tomography for response and prognosis stratification after neoadjuvant chemotherapy for esophageal squamous cell carcinoma. J Gastroenterol 51:788–795

    Article  CAS  Google Scholar 

  24. Furukawa T, Hamai Y, Hihara J et al (2016) Clinical significance of FDG-PET to predict pathologic tumor invasion and lymph node metastasis of superficial esophageal squamous cell carcinoma. Ann Surg Oncol 23:4086–4092

    Article  Google Scholar 

  25. Nakajima Y, Nagai K, Miyake S et al (2002) Evaluation of an indicator for lymph node metastasis of esophageal squamous cell carcinoma invading the submucosal layer. Jpn J Cancer Res. 93(3):305–312

    Article  CAS  Google Scholar 

  26. Shimada H, Nabeya Y, Matsubara H et al (2006) Prediction of lymph node status in patients with superficial esophageal carcinoma: analysis of 160 surgically resected cancers. Am J Surg. 191(2):250–254

    Article  Google Scholar 

  27. Stein HJ, Feith M, Bruecher BL et al (20015) Early esophageal cancer: pattern of lymphatic spread and prognostic factors for long-term survival after surgical resection. Ann Surg 242(4):566–573 (discussion 573–5)

  28. Altorki NK, Lee PC, Liss Y et al (2008) Multifocal neoplasia and nodal metastases in T1 esophageal carcinoma: implications for endoscopic treatment. Ann Surg. 247(3):434–439. https://doi.org/10.1097/SLA.0b013e318163a2ff

    Article  PubMed  Google Scholar 

  29. Ancona E, Rampado S, Cassaro M et al (2008) Prediction of lymph node status in superficial esophageal carcinoma. Ann Surg Oncol. 15(11):3278–3288. https://doi.org/10.1245/s10434-008-0065-1(Epub 2008 Aug 26)

    Article  PubMed  Google Scholar 

  30. Tomita N, Matsumoto T, Hayashi T et al (2008) Lymphatic invasion according to D2–40 immunostaining is a strong predictor of nodal metastasis in superficial squamous cell carcinoma of the esophagus: algorithm for risk of nodal metastasis based on lymphatic invasion. Pathol Int. 58(5):282–287. https://doi.org/10.1111/j.1440-1827.2008.02224.x

    Article  PubMed  Google Scholar 

  31. Tachibana M, Hirahara N, Kinugasa S et al (2008) Clinicopathologic features of superficial esophageal cancer: results of consecutive 100 patients. Ann Surg Oncol. 15(1):104–116 (Epub 2007 Sep 22)

    Article  Google Scholar 

  32. Chiba T, Kawachi H, Kawano T et al (2010) Independent histological risk factors for lymph node metastasis of superficial esophageal squamous cell carcinoma; implication of claudin-5 immunohistochemistry for expanding the indications of endoscopic resection. Dis Esophagus. 23(5):398–407. https://doi.org/10.1111/j.1442-2050.2009.01023.x(Epub 2009 Nov 9)

    Article  CAS  PubMed  Google Scholar 

  33. Zhuge L, Wang S, Xie J et al (2018) A model based on endoscopic morphology of submucosal esophageal squamous cell carcinoma for determining risk of metastasis on lymph nodes. J Thorac Dis. 10(12):6846–6853. https://doi.org/10.21037/jtd.2018.11.77

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kato H, Miyazaki T, Nakajima M et al (2005) The incremental effect of positron emission tomography on diagnostic accuracy in the initial staging of esophageal carcinoma. Cancer 103(1):148–156

    Article  Google Scholar 

  35. Akutsu Y, Kato K, Igaki H et al (2016) The prevalence of overall and initial lymph node metastases in clinical T1N0 thoracic esophageal cancer: from the results of JCOG0502, a prospective multicenter study. Ann Surg 264:1009–1015

    Article  Google Scholar 

  36. Yamashina T, Ishihara R, Nagai K et al (2013) Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol 108:544–551

    Article  Google Scholar 

  37. Kurokawa Y, Muto M, Minashi K et al (2009) A phase II trial of combined treatment of endoscopic mucosal resection and chemoradiotherapy for clinical stage I esophageal carcinoma: Japan Clinical Oncology Group Study JCOG0508. Jpn J Clin Oncol 39:686–689

    Article  Google Scholar 

  38. Ando N, Kato H, Igaki H et al (2012) A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol. 19(1):68–74. https://doi.org/10.1245/s10434-011-2049-9(Epub 2011 Aug 31)

    Article  PubMed  Google Scholar 

  39. Jingu K, Umezawa R, Yamamoto T et al (2019) FDG-PET might not contribute to improving survival in patients with locally advanced inoperable esophageal cancer. Int J Clin Oncol 24:927–933

    Article  Google Scholar 

  40. Makino T, Yamasaki M, Tanaka K et al (2019) (2018) Metabolic tumor volume change predicts long-term survival and histological response to preoperative chemotherapy in locally advanced esophageal cancer. Ann Surg 270(6):1090–1095. https://doi.org/10.1097/SLA.0000000000002808

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Yukihiro Watanabe (a biostatistician) for advice on statistical methods.

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Authors and Affiliations

  1. Department of Gastroenterological Surgery, Saitama Medical University International Medical Center, 1397-1 Yamane, Hidaka-shi, Saitama, 350-1298, Japan

    Yutaka Miyawaki, Hiroshi Sato, Naoto Fujiwara, Shuichiro Oya, Hirofumi Sugita, Yasumitsu Hirano, Shinichi Sakuramoto, Kojun Okamoto, Shigeki Yamaguchi & Isamu Koyama

  2. Department of Nuclear Medicine, Saitama Medical University International Medical Center, 1397-1 Yamane, Hidaka-shi, Saitama, 350-1298, Japan

    Tomohiko Yamane

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  1. Yutaka Miyawaki
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Contributions

YM: Study conception and design, collecting, analyzing, and interpreting the data, and writing the manuscript. HS: Study conception and design. NF: Collecting the data. SO: Collecting the data. HS: Collecting the data. YH: Collecting the data. TY: Analyzing and interpreting the data. SS: Critical intellectual contributions. KO: Critical intellectual contributions. SY: Critical intellectual contributions. IK: Study supervision.

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Correspondence to Yutaka Miyawaki.

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All procedures were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Miyawaki, Y., Sato, H., Fujiwara, N. et al. Association of the primary tumor’s SUVmax with survival after surgery for clinical stage IA esophageal cancer: a single-center retrospective study. Int J Clin Oncol 25, 561–569 (2020). https://doi.org/10.1007/s10147-019-01606-8

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  • DOI: https://doi.org/10.1007/s10147-019-01606-8

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