Skip to main content
Top
Published in: Annals of Nuclear Medicine 3/2023

20-12-2022 | Pneumonia | Original Article

Invasive mucinous adenocarcinoma of the lung: clinicopathological features, 18F-FDG PET/CT findings, and survival outcomes

Authors: Xiaolin Sun, Baozhen Zeng, Xiaoyue Tan, Zhijian Chen, Xiaoqiang Pan, Lei Jiang

Published in: Annals of Nuclear Medicine | Issue 3/2023

Login to get access

Abstract

Objective

Invasive mucinous adenocarcinoma (IMA) is a rare subtype of lung adenocarcinoma. This study aimed to retrospectively evaluate the clinicopathological features, 18F-FDG PET/CT findings, and prognosis of IMA of the lung, as well as to investigate the associations among these variables, to improve the management of such patients.

Methods

Clinicopathological and 18F-FDG PET/CT characteristics of 72 patients with pathologically confirmed IMA of the lung were retrospectively collected and investigated, and their predictive efficacy on progression-free survival (PFS) was evaluated.

Results

The median age of the enrolled 72 patients was 61 years (range, 26–79 years), and the male-to-female ratio was 1:1.25. According to the radiological morphology of IMA, solidary nodule/mass type (n = 59, 81.9%) was the most common, followed by GGO type (n = 8, 11.1%) and pneumonia type (n = 5, 6.9%). Lobulated or spiculated margin and pleural traction were the most common radiological signs. The median SUVmax of IMA lesions was 3.0, ranging from 0.5 to 23.1. Higher SUVmax was observed in IMA with non-GGO type, clinical symptom, advanced stage, lobulated margin, pleural traction or spread through air spaces (STAS) (P < 0.05). Moreover, higher SUVmax was related to larger tumor size in non-pneumonia-type IMA (r = 0.708, P < 0.001). The median PFS was 21.3 months, and the 12-, 24- and 36-month PFS rates were 89.8%, 83.3% and 75.5%, respectively. A poorer PFS was significantly associated with SUVmax ≥ 3, advanced stage and STAS.

Conclusion

18F-FDG PET/CT combined with clinicopathological characteristics can aid the diagnosis and prognostic evaluation of lung IMA, which could provide guidance for the appropriate management of such patients.
Literature
1.
go back to reference Suzuki S, Aokage K, Hishida T, Yoshida J, Kuwata T, Yamauchi C, et al. Interstitial growth as an aggressive growth pattern in primary lung cancer. J Cancer Res Clin Oncol. 2016;142(7):1591–8.CrossRefPubMed Suzuki S, Aokage K, Hishida T, Yoshida J, Kuwata T, Yamauchi C, et al. Interstitial growth as an aggressive growth pattern in primary lung cancer. J Cancer Res Clin Oncol. 2016;142(7):1591–8.CrossRefPubMed
2.
go back to reference Masai K, Sakurai H, Sukeda A, Suzuki S, Asakura K, Nakagawa K, et al. Prognostic Impact of Margin Distance and Tumor Spread Through Air Spaces in Limited Resection for Primary Lung Cancer. J Thorac Oncol. 2017;12(12):1788–97.CrossRefPubMed Masai K, Sakurai H, Sukeda A, Suzuki S, Asakura K, Nakagawa K, et al. Prognostic Impact of Margin Distance and Tumor Spread Through Air Spaces in Limited Resection for Primary Lung Cancer. J Thorac Oncol. 2017;12(12):1788–97.CrossRefPubMed
3.
go back to reference Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244–85.CrossRefPubMedPubMedCentral Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244–85.CrossRefPubMedPubMedCentral
4.
go back to reference Kish JK, Ro JY, Ayala AG, McMurtrey MJ. Primary mucinous adenocarcinoma of the lung with signet-ring cells: a histochemical comparison with signet-ring cell carcinomas of other sites. Hum Pathol. 1989;20(11):1097–102.CrossRefPubMed Kish JK, Ro JY, Ayala AG, McMurtrey MJ. Primary mucinous adenocarcinoma of the lung with signet-ring cells: a histochemical comparison with signet-ring cell carcinomas of other sites. Hum Pathol. 1989;20(11):1097–102.CrossRefPubMed
5.
go back to reference Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to The 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. J Thorac Oncol. 2015;10(9):1240–2.CrossRefPubMed Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to The 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. J Thorac Oncol. 2015;10(9):1240–2.CrossRefPubMed
6.
go back to reference Nie K, Nie W, Zhang YX, Yu H. Comparing clinicopathological features and prognosis of primary pulmonary invasive mucinous adenocarcinoma based on computed tomography findings. Cancer Imaging. 2019;19(1):47.CrossRefPubMedPubMedCentral Nie K, Nie W, Zhang YX, Yu H. Comparing clinicopathological features and prognosis of primary pulmonary invasive mucinous adenocarcinoma based on computed tomography findings. Cancer Imaging. 2019;19(1):47.CrossRefPubMedPubMedCentral
7.
go back to reference Watanabe H, Saito H, Yokose T, Sakuma Y, Murakami S, Kondo T, et al. Relation between thin-section computed tomography and clinical findings of mucinous adenocarcinoma. Ann Thorac Surg. 2015;99(3):975–81.CrossRefPubMed Watanabe H, Saito H, Yokose T, Sakuma Y, Murakami S, Kondo T, et al. Relation between thin-section computed tomography and clinical findings of mucinous adenocarcinoma. Ann Thorac Surg. 2015;99(3):975–81.CrossRefPubMed
8.
go back to reference Beyer T, Townsend DW, Brun T, Kinahan PE, Charron M, Roddy R, et al. A combined PET/CT scanner for clinical oncology. J Nucl Med. 2000;41(8):1369–79.PubMed Beyer T, Townsend DW, Brun T, Kinahan PE, Charron M, Roddy R, et al. A combined PET/CT scanner for clinical oncology. J Nucl Med. 2000;41(8):1369–79.PubMed
9.
go back to reference Wang T, Yang Y, Liu X, Deng J, Wu J, Hou L, et al. Primary invasive mucinous adenocarcinoma of the lung: prognostic value of CT imaging features combined with clinical factors. Korean J Radiol. 2021;22(4):652–62.CrossRefPubMed Wang T, Yang Y, Liu X, Deng J, Wu J, Hou L, et al. Primary invasive mucinous adenocarcinoma of the lung: prognostic value of CT imaging features combined with clinical factors. Korean J Radiol. 2021;22(4):652–62.CrossRefPubMed
10.
go back to reference Han Y, Luo Y. Primary lung invasive adenocarcinoma misdiagnosed as infectious pneumonia in (18)F-FDG PET/CT: A case report. Radiol Case Rep. 2022;17(3):808–11.CrossRefPubMed Han Y, Luo Y. Primary lung invasive adenocarcinoma misdiagnosed as infectious pneumonia in (18)F-FDG PET/CT: A case report. Radiol Case Rep. 2022;17(3):808–11.CrossRefPubMed
12.
go back to reference Lee HY, Choi YL, Lee KS, Han J, Zo JI, Shim YM, et al. Pure ground-glass opacity neoplastic lung nodules: histopathology, imaging, and management. AJR Am J Roentgenol. 2014;202(3):W224–33.CrossRefPubMed Lee HY, Choi YL, Lee KS, Han J, Zo JI, Shim YM, et al. Pure ground-glass opacity neoplastic lung nodules: histopathology, imaging, and management. AJR Am J Roentgenol. 2014;202(3):W224–33.CrossRefPubMed
13.
go back to reference Wislez M, Massiani MA, Milleron B, Souidi A, Carette MF, Antoine M, et al. Clinical characteristics of pneumonic-type adenocarcinoma of the lung. Chest. 2003;123(6):1868–77.CrossRefPubMed Wislez M, Massiani MA, Milleron B, Souidi A, Carette MF, Antoine M, et al. Clinical characteristics of pneumonic-type adenocarcinoma of the lung. Chest. 2003;123(6):1868–77.CrossRefPubMed
14.
go back to reference Duruisseaux M, Antoine M, Rabbe N, Poulot V, Fleury-Feith J, Vieira T, et al. The impact of intracytoplasmic mucin in lung adenocarcinoma with pneumonic radiological presentation. Lung Cancer. 2014;83(3):334–40.CrossRefPubMed Duruisseaux M, Antoine M, Rabbe N, Poulot V, Fleury-Feith J, Vieira T, et al. The impact of intracytoplasmic mucin in lung adenocarcinoma with pneumonic radiological presentation. Lung Cancer. 2014;83(3):334–40.CrossRefPubMed
15.
go back to reference Boland JM, Maleszewski JJ, Wampfler JA, Voss JS, Kipp BR, Yang P, et al. Pulmonary invasive mucinous adenocarcinoma and mixed invasive mucinous/nonmucinous adenocarcinoma-a clinicopathological and molecular genetic study with survival analysis. Hum Pathol. 2018;71:8–19.CrossRefPubMed Boland JM, Maleszewski JJ, Wampfler JA, Voss JS, Kipp BR, Yang P, et al. Pulmonary invasive mucinous adenocarcinoma and mixed invasive mucinous/nonmucinous adenocarcinoma-a clinicopathological and molecular genetic study with survival analysis. Hum Pathol. 2018;71:8–19.CrossRefPubMed
16.
go back to reference Dirican N, Baysak A, Cok G, Goksel T, Aysan T. Clinical characteristics of patients with bronchioloalveolar carcinoma: a retrospective study of 44 cases. Asian Pac J Cancer Prev. 2013;14(7):4365–8.CrossRefPubMed Dirican N, Baysak A, Cok G, Goksel T, Aysan T. Clinical characteristics of patients with bronchioloalveolar carcinoma: a retrospective study of 44 cases. Asian Pac J Cancer Prev. 2013;14(7):4365–8.CrossRefPubMed
17.
go back to reference Casali C, Rossi G, Marchioni A, Sartori G, Maselli F, Longo L, et al. A single institution-based retrospective study of surgically treated bronchioloalveolar adenocarcinoma of the lung: clinicopathologic analysis, molecular features, and possible pitfalls in routine practice. J Thorac Oncol. 2010;5(6):830–6.CrossRefPubMed Casali C, Rossi G, Marchioni A, Sartori G, Maselli F, Longo L, et al. A single institution-based retrospective study of surgically treated bronchioloalveolar adenocarcinoma of the lung: clinicopathologic analysis, molecular features, and possible pitfalls in routine practice. J Thorac Oncol. 2010;5(6):830–6.CrossRefPubMed
18.
go back to reference Kandathil A, Sibley RC III, Subramaniam RM. Lung Cancer Recurrence: (18)F-FDG PET/CT in Clinical Practice. AJR Am J Roentgenol. 2019;213(5):1136–44.CrossRefPubMed Kandathil A, Sibley RC III, Subramaniam RM. Lung Cancer Recurrence: (18)F-FDG PET/CT in Clinical Practice. AJR Am J Roentgenol. 2019;213(5):1136–44.CrossRefPubMed
19.
go back to reference Chang JM, Lee HJ, Goo JM, Lee HY, Lee JJ, Chung JK, et al. False positive and false negative FDG-PET scans in various thoracic diseases. Korean J Radiol. 2006;7(1):57–69.CrossRefPubMedPubMedCentral Chang JM, Lee HJ, Goo JM, Lee HY, Lee JJ, Chung JK, et al. False positive and false negative FDG-PET scans in various thoracic diseases. Korean J Radiol. 2006;7(1):57–69.CrossRefPubMedPubMedCentral
20.
go back to reference Cha MJ, Lee KS, Kim TJ, Kim HS, Kim TS, Chung MJ, et al. Solitary nodular invasive mucinous adenocarcinoma of the lung: imaging diagnosis using the morphologic-metabolic dissociation sign. Korean J Radiol. 2019;20(3):513–21.CrossRefPubMedPubMedCentral Cha MJ, Lee KS, Kim TJ, Kim HS, Kim TS, Chung MJ, et al. Solitary nodular invasive mucinous adenocarcinoma of the lung: imaging diagnosis using the morphologic-metabolic dissociation sign. Korean J Radiol. 2019;20(3):513–21.CrossRefPubMedPubMedCentral
21.
go back to reference Lee H, Lee K, Han J, Kim B, Cho Y, Shim Y, et al. Mucinous versus nonmucinous solitary pulmonary nodular bronchioloalveolar carcinoma: CT and FDG PET findings and pathologic comparisons. Lung Cancer (Amsterdam, Netherlands). 2009;65(2):170–5.CrossRefPubMed Lee H, Lee K, Han J, Kim B, Cho Y, Shim Y, et al. Mucinous versus nonmucinous solitary pulmonary nodular bronchioloalveolar carcinoma: CT and FDG PET findings and pathologic comparisons. Lung Cancer (Amsterdam, Netherlands). 2009;65(2):170–5.CrossRefPubMed
22.
go back to reference Murakami S, Saito H, Karino F, Kondo T, Oshita F, Ito H, et al. 18F-fluorodeoxyglucose uptake on positron emission tomography in mucinous adenocarcinoma. Eur J Radiol. 2013;82(11):e721–5.CrossRefPubMed Murakami S, Saito H, Karino F, Kondo T, Oshita F, Ito H, et al. 18F-fluorodeoxyglucose uptake on positron emission tomography in mucinous adenocarcinoma. Eur J Radiol. 2013;82(11):e721–5.CrossRefPubMed
23.
go back to reference Lee HY, Cha MJ, Lee KS, Lee HY, Kwon OJ, Choi JY, et al. Prognosis in resected invasive mucinous adenocarcinomas of the lung: related factors and comparison with resected nonmucinous adenocarcinomas. J Thorac Oncol. 2016;11(7):1064–73.CrossRefPubMed Lee HY, Cha MJ, Lee KS, Lee HY, Kwon OJ, Choi JY, et al. Prognosis in resected invasive mucinous adenocarcinomas of the lung: related factors and comparison with resected nonmucinous adenocarcinomas. J Thorac Oncol. 2016;11(7):1064–73.CrossRefPubMed
24.
go back to reference Kadota K, Nitadori JI, Sima CS, Ujiie H, Rizk NP, Jones DR, et al. Tumor spread through air spaces is an important pattern of invasion and impacts the frequency and location of recurrences after limited resection for small Stage I lung adenocarcinomas. J Thorac Oncol. 2015;10(5):806–14.CrossRefPubMedPubMedCentral Kadota K, Nitadori JI, Sima CS, Ujiie H, Rizk NP, Jones DR, et al. Tumor spread through air spaces is an important pattern of invasion and impacts the frequency and location of recurrences after limited resection for small Stage I lung adenocarcinomas. J Thorac Oncol. 2015;10(5):806–14.CrossRefPubMedPubMedCentral
25.
go back to reference Warth A, Muley T, Kossakowski CA, Goeppert B, Schirmacher P, Dienemann H, et al. Prognostic impact of intra-alveolar tumor spread in pulmonary adenocarcinoma. Am J Surg Pathol. 2015;39(6):793–801.CrossRefPubMed Warth A, Muley T, Kossakowski CA, Goeppert B, Schirmacher P, Dienemann H, et al. Prognostic impact of intra-alveolar tumor spread in pulmonary adenocarcinoma. Am J Surg Pathol. 2015;39(6):793–801.CrossRefPubMed
26.
go back to reference Nishimori M, Iwasa H, Miyatake K, Nitta N, Nakaji K, Matsumoto T, et al. 18F FDG-PET/CT analysis of spread through air spaces (STAS) in clinical stage I lung adenocarcinoma. Ann Nucl Med. 2022;36(10):897–903.CrossRefPubMed Nishimori M, Iwasa H, Miyatake K, Nitta N, Nakaji K, Matsumoto T, et al. 18F FDG-PET/CT analysis of spread through air spaces (STAS) in clinical stage I lung adenocarcinoma. Ann Nucl Med. 2022;36(10):897–903.CrossRefPubMed
27.
go back to reference Yoshizawa A, Motoi N, Riely GJ, Sima CS, Gerald WL, Kris MG, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol. 2011;24(5):653–64.CrossRefPubMed Yoshizawa A, Motoi N, Riely GJ, Sima CS, Gerald WL, Kris MG, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol. 2011;24(5):653–64.CrossRefPubMed
28.
go back to reference Russell PA, Wainer Z, Wright GM, Daniels M, Conron M, Williams RA. Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol. 2011;6(9):1496–504.CrossRefPubMed Russell PA, Wainer Z, Wright GM, Daniels M, Conron M, Williams RA. Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol. 2011;6(9):1496–504.CrossRefPubMed
29.
go back to reference Warth A, Muley T, Meister M, Stenzinger A, Thomas M, Schirmacher P, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol. 2012;30(13):1438–46.CrossRefPubMed Warth A, Muley T, Meister M, Stenzinger A, Thomas M, Schirmacher P, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol. 2012;30(13):1438–46.CrossRefPubMed
30.
go back to reference Yoshizawa A, Sumiyoshi S, Sonobe M, Kobayashi M, Fujimoto M, Kawakami F, et al. Validation of the IASLC/ATS/ERS lung adenocarcinoma classification for prognosis and association with EGFR and KRAS gene mutations: analysis of 440 Japanese patients. J Thorac Oncol. 2013;8(1):52–61.CrossRefPubMed Yoshizawa A, Sumiyoshi S, Sonobe M, Kobayashi M, Fujimoto M, Kawakami F, et al. Validation of the IASLC/ATS/ERS lung adenocarcinoma classification for prognosis and association with EGFR and KRAS gene mutations: analysis of 440 Japanese patients. J Thorac Oncol. 2013;8(1):52–61.CrossRefPubMed
31.
go back to reference Groheux D, Quere G, Blanc E, Lemarignier C, Vercellino L, de Margerie-Mellon C, et al. FDG PET-CT for solitary pulmonary nodule and lung cancer: Literature review. Diagn Interv Imaging. 2016;97(10):1003–17.CrossRefPubMed Groheux D, Quere G, Blanc E, Lemarignier C, Vercellino L, de Margerie-Mellon C, et al. FDG PET-CT for solitary pulmonary nodule and lung cancer: Literature review. Diagn Interv Imaging. 2016;97(10):1003–17.CrossRefPubMed
32.
go back to reference Tosi D, Pieropan S, Cattoni M, Bonitta G, Franzi S, Mendogni P, et al. Prognostic value of 18F-FDG PET/CT metabolic parameters in surgically treated stage I lung adenocarcinoma patients. Clin Nucl Med. 2021;46(8):621–6.CrossRefPubMedPubMedCentral Tosi D, Pieropan S, Cattoni M, Bonitta G, Franzi S, Mendogni P, et al. Prognostic value of 18F-FDG PET/CT metabolic parameters in surgically treated stage I lung adenocarcinoma patients. Clin Nucl Med. 2021;46(8):621–6.CrossRefPubMedPubMedCentral
33.
go back to reference Khiewvan B, Ziai P, Houshmand S, Salavati A, Ziai P, Alavi A. The role of PET/CT as a prognosticator and outcome predictor in lung cancer. Expert Rev Respir Med. 2016;10(3):317–30.CrossRefPubMed Khiewvan B, Ziai P, Houshmand S, Salavati A, Ziai P, Alavi A. The role of PET/CT as a prognosticator and outcome predictor in lung cancer. Expert Rev Respir Med. 2016;10(3):317–30.CrossRefPubMed
34.
go back to reference Shimizu K, Okita R, Saisho S, Maeda A, Nojima Y, Nakata M. Clinicopathological and immunohistochemical features of lung invasive mucinous adenocarcinoma based on computed tomography findings. Onco Targets Ther. 2017;10:153–63.CrossRefPubMed Shimizu K, Okita R, Saisho S, Maeda A, Nojima Y, Nakata M. Clinicopathological and immunohistochemical features of lung invasive mucinous adenocarcinoma based on computed tomography findings. Onco Targets Ther. 2017;10:153–63.CrossRefPubMed
35.
go back to reference Uruga H, Fujii T, Fujimori S, Kohno T, Kishi K. Semiquantitative assessment of tumor spread through air spaces (STAS) in early-stage lung adenocarcinomas. J Thorac Oncol. 2017;12(7):1046–51.CrossRefPubMed Uruga H, Fujii T, Fujimori S, Kohno T, Kishi K. Semiquantitative assessment of tumor spread through air spaces (STAS) in early-stage lung adenocarcinomas. J Thorac Oncol. 2017;12(7):1046–51.CrossRefPubMed
36.
go back to reference Lu S, Tan KS, Kadota K, Eguchi T, Bains S, Rekhtman N, et al. Spread through air spaces (STAS) is an independent predictor of recurrence and lung cancer-specific death in squamous cell carcinoma. J Thorac Oncol. 2017;12(2):223–34.CrossRefPubMed Lu S, Tan KS, Kadota K, Eguchi T, Bains S, Rekhtman N, et al. Spread through air spaces (STAS) is an independent predictor of recurrence and lung cancer-specific death in squamous cell carcinoma. J Thorac Oncol. 2017;12(2):223–34.CrossRefPubMed
Metadata
Title
Invasive mucinous adenocarcinoma of the lung: clinicopathological features, 18F-FDG PET/CT findings, and survival outcomes
Authors
Xiaolin Sun
Baozhen Zeng
Xiaoyue Tan
Zhijian Chen
Xiaoqiang Pan
Lei Jiang
Publication date
20-12-2022
Publisher
Springer Nature Singapore
Keyword
Pneumonia
Published in
Annals of Nuclear Medicine / Issue 3/2023
Print ISSN: 0914-7187
Electronic ISSN: 1864-6433
DOI
https://doi.org/10.1007/s12149-022-01816-7

Other articles of this Issue 3/2023

Annals of Nuclear Medicine 3/2023 Go to the issue