Molecular Imaging in Esophagus Malignancies
PDF
Cite
Share
Request
Review
P: 141-150
July 2024

Molecular Imaging in Esophagus Malignancies

Nucl Med Semin 2024;10(2):141-150
No information available.
No information available
Online Date: 31.07.2024
Publish Date: 31.07.2024
PDF
Cite
Share
Request

Abstract

Upper gastrointestinal tract cancers arising from the esophagus and gastroesophageal junction are a global health problem. The most common histological subtypes are adenocarcinoma and squamous cell carcinoma, and their etiologies, locations, treatments, and prognoses differ from each other. F-18 fluorodeoxyglucose (FDG) positron emission tomography/computed tomography (PET/CT) is a valuable imaging method that is frequently used in the diagnosis, staging, and restaging of many malignancies. Although its clinical use in the diagnosis of esophageal cancer is limited, it provides important information to the clinician in staging, restaging, and evaluating the response to treatment. However, hypermetabolism secondary to inflammation caused by gastroesophageal reflux, inflammation-related hypermetabolism in the early post-treatment period, and missing metastatic lymph nodes located close to the primary lesion may lead to false negative or positive interpretations in this area. As a result, patient management could be planned incorrectly. Therefore, the Nuclear Medicine physician should be aware of the pearls and pitfalls in these cases. In esophageal cancer, locoregional disease staging is performed by CT (thorax and abdomen, if necessary, pelvic area with oral and intravenous contrast agent) and endoscopic ultrasonography (EUS). The most accurate staging in patients with possible metastasis is performed with F-18 FDG PET/CT. While CT and EUS provide anatomical information, PET provides information about blood flow, metabolism, or receptor status depending on the chosen radiopharmaceuticals.

Keywords:
Esophageal cancer, staging, FDG, PET

References

1
World Health Organization. Oesophagus. Accessed January 13, 2023. Available at:http://gco.iarc.fr/today/data/factsheets/cancers/6-Oesophagus-fact-sheet.pdf
2
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394-424.
3
Corley DA, Buffler PA. Oesophageal and gastric cardia adenocarcinomas: analysis of regional variation using the Cancer Incidence in Five Continents database. Int J Epidemiol. 2001;30:1415-1425.
4
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7-30.
5
Torre LA, Siegel RL, Ward EM, Jemal A. Global Cancer Incidence and Mortality Rates and Trends--An Update. Cancer Epidemiol Biomarkers Prev. 2016;25:16-27.
6
Cossentino MJ, Wong RK. Barrett’s esophagus and risk of esophageal adenocarcinoma. Semin Gastrointest Dis. 2003;14:128-135.
7
Stahl A, Ott K, Weber WA, et al. FDG-PET imag- ing of locally advanced gastric carcinomas: cor- relation with endoscopic and histopathological findings. Eur J Nucl Med Mol Imaging. 2003;30:288-295.
8
Kim TJ, Kim HY, Lee KW, et al. Multimodality assessment of esophageal cancer: preoperative staging and monitoring of response to therapy. Radiographics. 2009;29:403-421.
9
Choi J, Kim SG, Kim JS, et al. Comparison of endoscopic ultrasonography (EUS), positron emission tomography (PET), and computed tomography (CT) in the preoperative locoregional staging of resectable esophageal cancer. Surg Endosc. 2010;24:1380-1386.
10
Rösch T. Endosonographic staging of esophageal cancer: A review of literature results. Gastrointest Endosc Clin N Am. 1995;5:537-547.
11
Munden RF, Macapinlac HA, Erasmus JJ. Esophageal cancer: the role of integrated CT-PET in initial staging and response assessment after preoperative therapy. J Thorac Imaging. 2006;21:137-145.
12
Cuellar SL, Carter BW, Macapinlac HA, et al. Clinical staging of patients with early esophageal adenocarcinoma: does FDG-PET/CT have a role? J Thorac Oncol. 2014;9:1202-1206.
13
Little SG, Rice TW, Bybel B, et al. Is FDG-PET indicated for superficialesophageal cancer? Eur J Cardiothorac Surg. 2007;31:791-796.
14
Amin MB, Edge SB, Greene FL, et al, eds. AJCC Cancer Staging Manual. 8th ed. Springer; 2017.
15
Tirumani H, Rosenthal MH, Tirumani SH, et al. Esophageal carcinoma: current concepts in the role of imaging in staging and management. Can Assoc Radiol J. 2015;66:130-139.
16
Lin E, Alavi A. PET and PET/CT- A Clinical Guide. 3rd Edition. New York:Thieme; 2019.
17
Cerfolio RJ, Bryant AS. Maximum standardized uptake values on positron emission tomography of esophageal cancer predicts stage, tumor biology, and survival. Ann Thorac Surg. 2006;82:391-4; discussion 394-5.
18
Betancourt-Cuellar SL, Palacio DP, Benveniste MFK, Mawlawi Y, Erasmus JJ. Pitfalls and Pearls in Esophageal Carcinoma. Semin Ultrasound CT MR. 2021;42:535-541.
19
Lerut T, Coosemans W, Decker G, et al. Cancer of the esophagus and gastro-esophageal junc- tion: potentially curative therapies. Surg Oncol. 2001;10:113-122.
20
van Vliet EP, Heijenbrok-Kal MH, Hunink MG, et al. Staging investigations for oesophageal cancer: a meta-analysis. Br J Cancer. 2008;98:547-557.
21
Puli SR, Reddy JB, Bechtold ML, et al. Staging accuracy of esophageal cancer by endoscopic ultrasound: a meta-analysis and systematic review. World J Gastroenterol. 2008;14:1479-1490.
22
Vazquez-Sequeiros E, Norton ID, Clain JE, et al. Impact of EUS-guided fine-needle aspiration on lymph node staging in patients with esophageal carcinoma. Gastrointest Endosc. 2001;53:751-757.
23
Liberman M, Hanna N, Duranceau A, et al. Endobronchial ultrasonography added to endoscopic ultrasonography improves staging in esophageal cancer. Ann Thorac Surg. 2013;96:232-236.
24
Keswani RN, Early DS, Edmundowicz SA, et al. Routine positron emission tomography does not alter nodal staging in patients undergoing EUS-guided FNA for esophageal cancer. Gastrointest Endosc. 2009;69:1210-1217.
25
Deng J, Chu X, Ren Z, Wang B. Relationship between T stage and survival in distantly metastatic esophageal cancer: A STROBE-compliant study. Medicine (Baltimore). 2020;99:e20064.
26
Nguyen NC, Chaar BT, Osman MM. Prevalence and patterns of soft tissue metastasis: Detection with true whole-body F-18 FDG PET/CT. BMC Med Imaging. 2007;7:8
27
Bruzzi JF, Truong MT, Macapinlac H, et al. Integrated CT-PET imaging of esophageal cancer: Unexpected and unusual distribution of distant organ metastases. Curr Probl Diagn Radiol. 2007;36:21-29.
28
Flamen P, Lerut A, Van Cutsem E, et al. Utility of positron emission tomography for the staging of patients with potentially operable esophageal carcinoma. J Clin Oncol. 2000;18:3202-3210.
29
Chatterton BE, Ho Shon I, Baldey A, et al. Positron emission tomography changes management and prognostic stratification in patients with oesophageal cancer: results of a multicentre prospective study. Eur J Nucl Med Mol Imaging. 2009;36:354-361.
30
Shmidt E, Nehra V, Lowe V, Oxentenko AS. Clinical significance of incidental [18 F]FDG uptake in the gastrointestinal tract on PET/CT imaging: a retrospective cohort study. BMC Gastroenterol. 2016;16:125.
31
Nakagawa S, Kanda T, Kosugi S, Ohashi M, Suzuki T, Hatakeyama K. Recurrence pattern of squamous cell carcinoma of the thoracic esophagus after extended radical esophagectomy with three-field lymphadenectomy. J Am Coll Surg. 2004;198:205-211.
32
Betancourt Cuellar SL, Palacio DP, Wu CC, et al.FDG-PET/CT is useful in the follow-up of surgically treated patients with oesophageal adenocarcinoma. Br J Radiol. 2018;91:20170341.
33
Goense L, van Rossum PS, Reitsma JB, et al. Diagnostic performance of (1)(8)F-FDG PET and PET/CT for the detection of recurrent esophageal cancer after treatment with curative intent: A systematic review and meta-analysis. J Nucl Med. 2015;56:995-1002.
34
Sun L, Su XH, Guan YS, et al. Clinical usefulness of 18F-FDG PET/CT in the restaging of esophageal cancer after surgical resection and radiotherapy. World J Gastroenterol. 2009;15:1836-1842.
35
Kamaya A, Federle MP, Desser TS. Imaging manifestations of abdominal fat necrosis and its mimics. Radiographics. 2011;31:2021-2034.
36
Flamen P, Lerut A, Van Cutsem E, et al. Utility of positron emission tomography for the staging of patients with potentially operable esophageal carcinoma. J Clin Oncol. 2000;18:3202-3210.
37
Levine EA, Farmer MR, Clark P, et al. Predictive value of 18-fluoro-deoxy-glucose-positron emission tomography (18F-FDG-PET) in the identification of responders to chemoradiation therapy for the treatment of locally advanced esophageal cancer. Ann Surg. 2006;243:472-478.
38
Chirieac LR, Swisher SG, Ajani JA, et al. Posttherapy pathologic stage predicts survival in patients with esophageal carcinoma receiving preoperative chemoradiation. Cancer. 2005;103:1347-1355.
39
Ancona E, Ruol A, Santi S, et al. Only pathologic complete response to neoadjuvant chemotherapy improves significantly the long term survival of patients with resectable esophageal squamous cell carcinoma: final report of a randomized, controlled trial of preoperative chemotherapy versus surgery alone. Cancer. 2001;91:2165-2174.
40
Rohatgi PR, Swisher SG, Correa AM, et al. Failure patterns correlate with the proportion of residual carcinoma after preoperative chemoradiotherapy for carcinoma of the esophagus. Cancer. 2005;104:1349-1355.
41
Jones DR, Parker LA Jr, Detterbeck FC, et al. Inadequacy of computed tomography in assess- ing patients with esophageal carcinoma after induction chemoradiotherapy. Cancer. 1999;85:1026-1032.
42
Swisher SG, Maish M, Erasmus JJ, et al. Utility of PET, CT, and EUS to identify pathologic responders in esophageal cancer. Ann Thorac Surg. 2004;78:1152-1160.
43
Westerterp M, van Westreenen HL, Reitsma JB, et al. Esophageal cancer: CT, endoscopic US, and FDG PET for assessment of response to neoadjuvant therapy — systematic review. Radiology. 2005;236:841-851.
44
Guo H, Zhu H, Xi Y, et al. Diagnostic and prognostic value of 18F-FDG PET/CT for patients with suspected recurrence from squamous cell carcinoma of the esophagus. J Nucl Med. 2007;48:1251-1258.
45
Vollenbrock SE, Voncken FEM, van Dieren JM, et al. Diagnostic performance of MRI for assessment of response to neoadjuvant chemoradiotherapy in oesophageal cancer. Br J Surg. 2019;106:596-605.
46
Erasmus JJ, Munden RF, Truong MT, et al. Preoperative chemo-radiation- induced ulceration in patients with esophageal cancer: a confounding factor in tumor response assessment in integrated computed tomographic-positron emission tomographic imaging. J Thorac Oncol. 2006;1:478-486.
47
Kumar P, Damle NA, Bal C. Role of F18-FDG PET/CT in the staging and restaging of esophageal cancer: A comparison with CECT. Indian J Surg Oncol. 2011;2:343-350.
48
Grant MJ, Didier RA, Stevens JS, et al. Radiation-induced liver disease as a mimic of liver metastases at serial PET/CT during neoadjuvant chemoradiation of distal esophageal cancer. Abdom Imaging. 2014;39:963-968.
49
Voncken FEM, Aleman BMP, van Dieren JM, et al. Radiation-induced liver injury mimicking liver metastases on FDG-PET-CT after chemoradiotherapy for esophageal cancer: A retrospective study and literatüre review. Strahlenther Onkol. 2018;194:156-163.
50
Weber WA, Ott K, Becker K, et al. Prediction of response to preoperative chemotherapy in ade- nocarcinomas of esophagogastric junction by metabolic imaging. J Clin Oncol. 2001;19:3058-3065.
51
Brücher BL, Weber W, Bauer M, et al. Neoad- juvant therapy of esophageal squamous cell carcinoma: response evaluation by positron emission tomography. Ann Surg. 2001;233:300-309.
52
Zeisel SH. Dietary choline: biochemistry, physiology, and pharmacology. Annu Rev Nutr. 1981;1:95-121.
53
Zeisel SH. Choline: an essential nutrient for humans. Nutrition. 2000;16:669-671.
54
Suttie S, McAteer D, Sheehan M, et al. F-18-FDG and C-11-Choline Positron Emission Tomography in Human Esophago-Gastric Cancer: Prediction of Response to Therapy. World J Oncol. 2010;1:66-67.
55
Jager PL, Que TH, Vaalburg W, Pruim J, Elsinga P, Plukker JT. Carbon-11 choline or FDG-PET for staging of oesophageal cancer? Eur J Nucl Med. 2001;28:1845-1849.
56
Kobori O, Kirihara Y, Kosaka N, Hara T. Positron emission tomography of esophageal carcinoma using (11)C-choline and (18)F-fluorodeoxyglucose: a novel method of preoperative lymph node staging. Cancer. 1999;86:1638-1648.
57
Kratochwil C, Flechsig P, Lindner T, et al. (68)Ga-FAPI PET/CT: Tracer Uptake in 28 Different Kinds of Cancer. J Nucl Med. 2019;60:801-805.
58
Hamson EJ, Keane FM, Tholen S, Schilling O, Gorrell MD. Understanding Fibroblast Activation Protein (FAP): Substrates, Activities, Expression and Targeting for Cancer Therapy. Proteomics Clin Appl. 2014;8:454-463.
59
Tanswell P, Garin-Chesa P, Rettig WJ, et al. Population pharmacokinetics of an- tifibroblast activation protein monoclonal antibody F19 in cancer patients. Br J Clin Pharmacol. 2001;51:177-180.
60
Laverman P, van der Geest T, Terry SY, et al. Immuno-PET and immuno-SPECT of rheumatoid arthritis with radiolabeled anti-fibroblast activation protein an- tibody correlates with severity of arthritis. J Nucl Med. 2015;56:778-783.
61
Meletta R, Müller Herde A, Chiotellis A, et al. Evaluation of the radiolabeled boronic acid-based FAP inhibitor MIP-1232 for atherosclerotic plaque imaging. Molecules. 2015;20:2081-2099.
62
Lindner T, Loktev A, Altmann A, et al. Development of quinoline-based ther- anostic ligands for the targeting of fibroblast activation protein. J Nucl Med. 2018;59:1415-1422.
63
Loktev A, Lindner T, Burger EM, et al. Development of fibroblast activation protein-targeted radiotracers with improved tumour retention. J Nucl Med. 2019;60:1421-1429.
64
Jansen K, Heirbaut L, Cheng JD, et al. Selective inhibitors of fibroblast acti- vation protein (FAP) with a (4-Quinolinoyl)-glycyl-2-cyanopyrrolidine Scaffold. ACS Med Chem Lett. 2013;4:491.
65
Guo W, Pang Y, Yao L, et al. Imaging fibroblast activation protein in liver cancer: a single-center post hoc retrospective analysis to compare [(68)Ga]Ga-FAPI-04 PET/CT versus MRI and [(18)F]-FDG PET/CT. Eur J Nucl Med Mol Imaging. 2020;48:1604-1617.
66
Liu H, Hu Z, Yang X, Dai T, Chen Y. Comparison of [Ga]Ga-DOTA-FAPI-04 and [F]FDG Uptake in Esophageal Cancer. Front Oncol. 2022;12:875081.
67
Zhao L, Chen S, Lin L, et al. [(68)Ga]Ga-DOTA-FAPI-04 improves tumor stag- ing and monitors early response to chemoradiotherapy in a patient with esophageal cancer. Eur J Nucl Med Mol Imaging. 2020;47:3188-3189.
68
Zhao L, Chen S, Chen S, et al. (68)Ga-fibroblast activation protein inhibitor PET/CT on gross tumour volume delineation for radiotherapy planning of esophageal cancer. Radiother Oncol. 2021;158:55-61.
69
Peng D, He J, Liu H, Cao J, Wang Y, Chen Y. FAPI PET/CT research progress in digestive system tumours. Dig Liver Dis. 2022;54:164-169.