REVIEW ARTICLE
Current and future imaging modalities in gastric cancer
Elwin Tham MD,
Michael Sestito MD,
Brian Markovich MD,
Mary Garland-Kledzik MD,
Elwin Tham MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorMichael Sestito MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorBrian Markovich MD
Department of Diagnostic Radiology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorCorresponding Author
Mary Garland-Kledzik MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Correspondence Mary Garland-Kledzik, MD, Department of Surgical Oncology, West Virginia University School of Medicine, PO Box 9238, 7300 HSS, Morgantown, WV 26506-9238, USA.
Email: [email protected]
Search for more papers by this authorElwin Tham MD,
Michael Sestito MD,
Brian Markovich MD,
Mary Garland-Kledzik MD,
Elwin Tham MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorMichael Sestito MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorBrian Markovich MD
Department of Diagnostic Radiology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Search for more papers by this authorCorresponding Author
Mary Garland-Kledzik MD
Department of Surgical Oncology, West Virginia University School of Medicine, Morgantown, West Virginia, USA
Correspondence Mary Garland-Kledzik, MD, Department of Surgical Oncology, West Virginia University School of Medicine, PO Box 9238, 7300 HSS, Morgantown, WV 26506-9238, USA.
Email: [email protected]
Search for more papers by this authorAbstract
Gastric adenocarcinoma treatment can include endoscopic mucosal resection, surgery, chemotherapy, radiation, and palliative measures depending on staging. Both invasive and noninvasive staging techniques have been used to dictate the best treatment pathway. Here, we review the current imaging modalities used in gastric cancer as well as novel techniques to accurately stage and screen these patients.
CONFLICTS OF INTEREST
The authors declare no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
REFERENCES
- 1Bray 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.
- 2Joshi SS, Badgwell BD. Current treatment and recent progress in gastric cancer. CA Cancer J Clin. 2021; 71: 264-79.
- 3Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017; 67: 93-99.
- 4Network NCC. Gastric Cancer Version 5.2021. Accessed January 10, 2021. https://www.nccn.org/professionals/physician_gls/pdf/gastric.pdf
- 5Gertsen EC, Brenkman HJF, van Hillegersberg R, et al. 18F-fludeoxyglucose-positron emission tomography/computed tomography and laparoscopy for staging of locally advanced gastric cancer: a multicenter prospective Dutch Cohort Study (PLASTIC). JAMA Surg. 2021; 156:e215340.
- 6Seevaratnam R, Cardoso R, Fau - McGregor C, et al. How useful is preoperative imaging for tumor, node, metastasis (TNM) staging of gastric cancer? A meta-analysis. Gastric Cancer. 2012; 15(Suppl 1): S3-S18.
- 7Hwang SW, Lee DH, Lee SH, et al. Preoperative staging of gastric cancer by endoscopic ultrasonography and multidetector-row computed tomography. J Gastroenterol Hepatol. 2010; 25: 512-518.
- 8Isomoto H, Shikuwa S, Yamaguchi N, et al. Endoscopic submucosal dissection for early gastric cancer: a large-scale feasibility study. Gut. 2009; 58: 331-336.
- 9Smyth EC, Nilsson M, Grabsch HI, van Grieken NC, Lordick F. Gastric cancer. Lancet. 2020; 396: 635-648.
- 10Borggreve AS, Goense L, Brenkman HJF, et al. Imaging strategies in the management of gastric cancer: current role and future potential of MRI. Br J Radiol. 2019; 92:20181044.
- 11Shimada H, Fukagawa T, Haga Y, Okazumi SI, Oba K. Clinical TNM staging for esophageal, gastric, and colorectal cancers in the era of neoadjuvant therapy: a systematic review of the literature. Ann Gastroenterol Surg. 2021; 5: 404-418.
- 12Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006; 355: 11-20.
- 13Kang YK, Yook JH, Park YK, et al. PRODIGY: a phase III study of neoadjuvant docetaxel, oxaliplatin, and S-1 plus surgery and adjuvant S-1 versus surgery and adjuvant S-1 for resectable advanced gastric cancer. J Clin Oncol. 2021; 39: 2903-2913.
- 14Kwee RM, Kwee TC. Imaging in local staging of gastric cancer: a systematic review. J Clin Oncol. 2007; 25: 2107-2116.
- 15Huang Z, Xie DH, Guo L, et al. The utility of MRI for pre-operative T and N staging of gastric carcinoma: a systematic review and meta-analysis. Br J Radiol. 2015; 88(1050):20140552.
- 16Kaneko Y, Murray WK, Link E, Hicks RJ, Duong C. Improving patient selection for 18F-FDG PET scanning in the staging of gastric cancer. J Nucl Med. 2015; 56: 523-529.
- 17Kostrubiak DE, DeHay PW, Ali N, et al. Body MRI subspecialty reinterpretations at a tertiary care center: discrepancy rates and error types. Am J Roentgenol. 2020; 215(6): 1384-1388.
- 18Dassen AE, Lips DJ, Hoekstra CJ, Pruijt JF, Bosscha K. FDG-PET has no definite role in preoperative imaging in gastric cancer. Eur J Surg Oncol. 2009; 35(5): 449-455.
- 19Fukagawa T, Katai H, Mizusawa J, et al. A prospective multi-institutional validity study to evaluate the accuracy of clinical diagnosis of pathological stage III gastric cancer (JCOG1302A). Gastric Cancer. 2018; 21: 68-73.
- 20Mocellin S, Pasquali S. Diagnostic accuracy of endoscopic ultrasonography (EUS) for the preoperative locoregional staging of primary gastric cancer. Cochrane Database Syst Rev. 2015:CD009944.
- 21Mocellin S, Marchet A, Nitti D. EUS for the staging of gastric cancer: a meta-analysis. Gastrointest Endosc. 2011; 73: 1122-1134.
- 22Nie R-C, Yuan S-Q, Chen X-J, et al. Endoscopic ultrasonography compared with multidetector computed tomography for the preoperative staging of gastric cancer: a meta-analysis. World J Surg Oncol. 2017; 15: 113.
- 23van Rossum PSN, van Hillegersberg R, Lever FM, et al. Imaging strategies in the management of oesophageal cancer: what's the role of MRI? Eur Radiol. 2013; 23: 1753-1765.
- 24Kim JH, Song KS, Youn YH, et al. Clinicopathologic factors influence accurate endosonographic assessment for early gastric cancer. Gastrointest Endosc. 2007; 66: 901-908.
- 25Akashi K, Yanai H, Nishikawa J, et al. Ulcerous change decreases the accuracy of endoscopic ultrasonography diagnosis for the invasive depth of early gastric cancer. Int J Gastrointest Cancer. 2006; 37: 133-138.
- 26Chen CY, Wu CW, Lo SS, Hsieh MC, Lui WY, Shen KH. Peritoneal carcinomatosis and lymph node metastasis are prognostic indicators in patients with Borrmann type IV gastric carcinoma. Hepatogastroenterology. 2002; 49: 874-877.
- 27Nakamura K, Morisaki T, Sugitani A, et al. An early gastric carcinoma treatment strategy based on analysis of lymph node metastasis. Cancer. 1999; 85: 1500-1505.
10.1002/(SICI)1097-0142(19990401)85:7<1500::AID-CNCR10>3.0.CO;2-8 CAS PubMed Web of Science® Google Scholar
- 28Kodera Y, Yamamura Y, Shimizu Y, et al. Lymph node status assessment for gastric carcinoma: is the number of metastatic lymph nodes really practical as a parameter for N categories in the TNM Classification? Tumor Node Metastasis. 1998; 69: 15-20.
- 29Deng JY, Liang H. Clinical significance of lymph node metastasis in gastric cancer. World J Gastroenterol. 2014; 20: 3967-3975.
- 30Siewert JR, Böttcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg. 1998; 228: 449-461.
- 31Takagane A, Terashima M, Abe K, et al. Evaluation of the ratio of lymph node metastasis as a prognostic factor in patients with gastric cancer. Gastric Cancer. 1999; 2(2): 122-128.
- 32Yokota T, Kunii Y, Teshima S, et al. Significant prognostic factors in patients with early gastric cancer. Int Surg. 2000; 85: 286-290.
- 33Deng J, Liang H, Sun D, Pan Y. The prognostic analysis of lymph node-positive gastric cancer patients following curative resection. J Surg Res. 2010; 161: 47-53.
- 34Roviello F, Rossi S, Marrelli D, et al. Number of lymph node metastases and its prognostic significance in early gastric cancer: a multicenter Italian study. J Surg Oncol. 2006; 94: 275-280. Discussion 4.
- 35Vergadis C, Schizas D. Is accurate N – staging for gastric cancer possible? Front Surg. 2018; 5: 41.
- 36Zhang XF, Huang CM, Lu HS, et al. Surgical treatment and prognosis of gastric cancer in 2,613 patients. World J Gastroenterol. 2004; 10: 3405-3408.
- 37Mönig SP, Zirbes TK, Schröder W, et al. Staging of gastric cancer: correlation of lymph node size and metastatic infiltration. Am J Roentgenol. 1999; 173: 365-367.
- 38Noda N, Sasako M, Yamaguchi N, Nakanishi Y. Ignoring small lymph nodes can be a major cause of staging error in gastric cancer. Br J Surg. 1998; 85(6): 831-834.
- 39Kwee RM, Kwee TC. Imaging in assessing lymph node status in gastric cancer. Gastric Cancer. 2009; 12: 6-22.
- 40Altini C, Niccoli Asabella A, Di Palo A, et al. 18F-FDG PET/CT role in staging of gastric carcinomas: comparison with conventional contrast enhancement computed tomography. Medicine. 2015; 94:e864.
- 41Kawanaka Y, Kitajima K, Fukushima K, et al. Added value of pretreatment (18)F-FDG PET/CT for staging of advanced gastric cancer: comparison with contrast-enhanced MDCT. Eur J Radiol. 2016; 85: 989-995.
- 42Kim EY, Lee WJ, Choi D, et al. The value of PET/CT for preoperative staging of advanced gastric cancer: comparison with contrast-enhanced CT. Eur J Radiol. 2011; 79: 183-188.
- 43Joo I, Lee JM, Kim JH, Shin CI, Han JK, Choi BI. Prospective comparison of 3T MRI with diffusion-weighted imaging and MDCT for the preoperative TNM staging of gastric cancer. J Magn Reson Imaging. 2015; 41: 814-821.
- 44Caivano R, Rabasco P, Lotumolo A, et al. Gastric cancer: the role of diffusion weighted imaging in the preoperative staging. Cancer Invest. 2014; 32: 184-190.
- 45Cheng J, Wang Y, Deng J, et al. Discrimination of metastatic lymph nodes in patients with gastric carcinoma using diffusion-weighted imaging. J Magn Reson Imaging. 2013; 37: 1436-1444.
- 46Zhong J, Zhao W, Ren F, et al. Lymph node metastasis in patients with gastric cancer: a multi-modality, morphologic and functional imaging study. Am J Transl Res. 2016; 8(12): 5601-5609.
- 47Hasbahceci M, Akcakaya A, Memmi N, et al. Diffusion MRI on lymph node staging of gastric adenocarcinoma. Quant Imaging Med Surg. 2015; 5: 392-400.
- 48Tokuhara T, Tanigawa N, Matsuki M, et al. Evaluation of lymph node metastases in gastric cancer using magnetic resonance imaging with ultrasmall superparamagnetic iron oxide (USPIO): diagnostic performance in post-contrast images using new diagnostic criteria. Gastric Cancer. 2008; 11(4): 194-200.
- 49Tatsumi Y, Tanigawa N, Nishimura H, et al. Preoperative diagnosis of lymph node metastases in gastric cancer by magnetic resonance imaging with ferumoxtran-10. Gastric Cancer. 2006; 9: 120-128.
- 50Vasanawala SS, Nguyen KL, Hope MD, et al. Safety and technique of ferumoxytol administration for MRI. Magn Reson Med. 2016; 75: 2107-2111.
- 51Kim KH, Lee KW, Baek SK, et al. Survival benefit of gastrectomy ± metastasectomy in patients with metastatic gastric cancer receiving chemotherapy. Gastric Cancer. 2011; 14(2): 130-138.
- 52Dixon M, Mahar AL, Helyer LK, Vasilevska-Ristovska J, Law C, Coburn NG. Prognostic factors in metastatic gastric cancer: results of a population-based, retrospective cohort study in Ontario. Gastric Cancer. 2016; 19: 150-159.
- 53Sarela AI, Yelluri S, Leeds Upper Gastrointestinal Cancer Multidisciplinary Team. Gastric adenocarcinoma with distant metastasis: is gastrectomy necessary? Arch Surg. 2007; 142(2): 143-149.
- 54Sarela AI, Miner TJ, Karpeh MS, Coit DG, Jaques DP, Brennan MF. Clinical outcomes with laparoscopic stage M1, unresected gastric adenocarcinoma. Ann Surg. 2006; 243: 189-195.
- 55 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 208 (5th edition). Gastric Cancer. 2021; 24: 1-21.
- 56Smyth EC, Verheij M, Allum W, et al. Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016; 27: v38-v49.
- 57De Manzoni G, Marrelli D, Baiocchi GL, et al. The Italian Research Group for Gastric Cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer. 2017; 20: 20-30.
- 58Kwee RM, Kwee TC. Modern imaging techniques for preoperative detection of distant metastases in gastric cancer. World J Gastroenterol. 2015; 21: 10502-10509.
- 59Wang Z, Chen JQ. Imaging in assessing hepatic and peritoneal metastases of gastric cancer: a systematic review. BMC Gastroenterol. 2011; 11: 19.
- 60Smyth E, Schöder H, Strong VE, et al. A prospective evaluation of the utility of 2-deoxy-2-[(18) F]fluoro-D-glucose positron emission tomography and computed tomography in staging locally advanced gastric cancer. Cancer. 2012; 118: 5481-5488.
- 61Chu KM, Kwok KF, Law S, Wong KH. A prospective evaluation of catheter probe EUS for the detection of ascites in patients with gastric carcinoma. Gastrointest Endosc. 2004; 59: 471-474.
- 62Lee YT, Ng EK, Hung LC, et al. Accuracy of endoscopic ultrasonography in diagnosing ascites and predicting peritoneal metastases in gastric cancer patients. Gut. 2005; 54: 1541-1545.
- 63Leake PA, Cardoso R, Seevaratnam R, et al. A systematic review of the accuracy and indications for diagnostic laparoscopy prior to curative-intent resection of gastric cancer. Gastric Cancer. 2012; 15(Suppl 1): S38-S47.
- 64Soussan M, Des Guetz G, Barrau V, et al. Comparison of FDG-PET/CT and MR with diffusion-weighted imaging for assessing peritoneal carcinomatosis from gastrointestinal malignancy. Eur Radiol. 2012; 22: 1479-1487.
- 65Maegerlein C, Fingerle AA, Souvatzoglou M, Rummeny EJ, Holzapfel K. Detection of liver metastases in patients with adenocarcinomas of the gastrointestinal tract: comparison of (18)F-FDG PET/CT and MR imaging. Abdom Imaging. 2015; 40: 1213-1222.
- 66Han NY, Park BJ, Sung DJ, et al. Chemotherapy-induced focal hepatopathy in patients with gastrointestinal malignancy: gadoxetic acid–enhanced and diffusion-weighted MR imaging with clinical-pathologic correlation. Radiology. 2014; 271: 416-425.
- 67Zheng DX, Meng SC, Liu QJ, et al. Predicting liver metastasis of gastrointestinal tract cancer by diffusion-weighted imaging of apparent diffusion coefficient values. World J Gastroenterol. 2016; 22: 3031-3037.
- 68Lee DH, Kim SH, Joo I, Hur BY, Han JK. Comparison between 18F-FDG PET/MRI and MDCT for the assessment of preoperative staging and resectability of gastric cancer. Eur J Radiol. 2016; 85(6): 1085-1091.
- 69Buchbender C, Heusner TA, Lauenstein TC, Bockisch A, Antoch G. Oncologic PET/MRI, part 1: tumors of the brain, head and neck, chest, abdomen, and pelvis. J Nucl Med. 2012; 53: 928-938.
- 70Galea N, Cantisani V, Taouli B. Liver lesion detection and characterization: role of diffusion-weighted imaging. J Magn Reson Imaging. 2013; 37: 1260-1276.
- 71Al-Batran SE, Homann N, Pauligk C, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet. 2019; 393: 1948-1957.
- 72Rausei S, Bali CD, Lianos GD. Neoadjuvant chemotherapy for gastric cancer. Has the time to decelerate the enthusiasm passed us by? Semin Oncol. 2020; 47(6): 355-360.
- 73Reddavid R, Sofia S, Chiaro P, et al. Neoadjuvant chemotherapy for gastric cancer. Is it a must or a fake? World J Gastroenterol. 2018; 24(2): 274-289.
- 74Redondo-Cerezo E, Martínez-Cara JG, Jiménez-Rosales R, et al. Endoscopic ultrasound in gastric cancer staging before and after neoadjuvant chemotherapy. A comparison with PET-CT in a clinical series. United Eur Gastroenterol J. 2017; 5: 641-647.
- 75Ott K, Herrmann K, Schuster T, et al. Molecular imaging of proliferation and glucose utilization: utility for monitoring response and prognosis after neoadjuvant therapy in locally advanced gastric cancer. Ann Surg Oncol. 2011; 18: 3316-3323.
- 76Park SR, Lee JS, Kim CG, et al. Endoscopic ultrasound and computed tomography in restaging and predicting prognosis after neoadjuvant chemotherapy in patients with locally advanced gastric cancer. Cancer. 2008; 112: 2368-2376.
- 77Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009; 45: 228-247.
- 78Kwee RM, Kwee TC. Role of imaging in predicting response to neoadjuvant chemotherapy in gastric cancer. World J Gastroenterol. 2014; 20: 1650-1656.
- 79Wang ZL, Li YL, Li XT, Tang L, Li ZY, Sun YS. Role of CT in the prediction of pathological complete response in gastric cancer after neoadjuvant chemotherapy. Abdom Radiol. 2021; 46: 3011-3018.
- 80Jang GS, Kim MJ, Ha HI, et al. Comparison of RECIST version 1.0 and 1.1 in assessment of tumor response by computed tomography in advanced gastric cancer. Chin J Cancer Res. 2013; 25: 689-694.
- 81De Cobelli F, Giganti F, Orsenigo E. Apparent diffusion coefficient modifications in assessing gastro-oesophageal cancer response to neoadjuvant treatment: comparison with tumour regression grade at histology. Eur Radiol. 2013; 23(8): 2165-2174.
- 82Zhong J, Zhao W, Ma W, et al. DWI as a quantitative biomarker in predicting chemotherapeutic efficacy at multitime points on gastric cancer lymph nodes metastases. Medicine. 2016; 95:e3236.
- 83Lee DH, Kim SH, Im SA, Oh DY, Kim TY, Han JK. Multiparametric fully-integrated 18-FDG PET/MRI of advanced gastric cancer for prediction of chemotherapy response: a preliminary study. Eur Radiol. 2016; 26: 2771-2778.
- 84Lagendijk JJ, Raaymakers BW, Raaijmakers AJ, et al. MRI/linac integration. Radiother Oncol. 2008; 86: 25-29.
- 85Fuse N, Nagahisa-Oku E, Doi T, et al. Effect of RECIST revision on classification of target lesions and overall response in advanced gastric cancer patients. Gastric Cancer. 2013; 16(3): 324-328.
- 86Kurokawa Y, Shibata T, Sasako M, et al. Validity of response assessment criteria in neoadjuvant chemotherapy for gastric cancer (JCOG0507-A). Gastric Cancer. 2014; 17: 514-521.
- 87Xu X, Zheng G, Zhang T, Zhao Y, Zheng Z. Is pathologic tumor regression grade after neo-adjuvant chemotherapy a promising prognostic indicator for patients with locally advanced gastric cancer? A cohort study evaluating tumor regression response. Cancer Chemother Pharmacol. 2019; 84(3): 635-646.
- 88Gao J, Zhang X, Meng Q, et al. Linked color imaging can improve detection rate of early gastric cancer in a high-risk population: a multi-center randomized controlled clinical trial. Dig Dis Sci. 2021; 66(4): 1212-1219.
- 89Ono S, Kawada K, Dohi O, et al. Linked color imaging focused on neoplasm detection in the upper gastrointestinal tract: a randomized trial. Ann Intern Med. 2021; 174: 18-24.
- 90van Timmeren JE, Cester D, Tanadini-Lang S, Alkadhi H, Baessler B. Radiomics in medical imaging—“how-to” guide and critical reflection. Insights Imaging. 2020; 11: 91.
- 91Feng QX, Liu C, Qi L, et al. An intelligent clinical decision support system for preoperative prediction of lymph node metastasis in gastric cancer. J Am Coll Radiol. 2019; 16: 952-960.
- 92Wang Y, Liu W, Yu Y, et al. CT radiomics nomogram for the preoperative prediction of lymph node metastasis in gastric cancer. Eur Radiol. 2020; 30: 976-986.
- 93Li J, Dong D, Fang M, et al. Dual-energy CT-based deep learning radiomics can improve lymph node metastasis risk prediction for gastric cancer. Eur Radiol. 2020; 30(4): 2324-2333.
- 94Jiang Y, Liang X, Wang W, et al. Noninvasive prediction of occult peritoneal metastasis in gastric cancer using deep learning. JAMA Network Open. 2021; 4:e2032269.
- 95Jiang Y, Jin C, Yu H, et al. Development and validation of a deep learning CT signature to predict survival and chemotherapy benefit in gastric cancer: a multicenter, retrospective study. Ann Surg. 2021; 274: e1153-e1161.
- 96Jiang Y, Chen C, Xie J, et al. Radiomics signature of computed tomography imaging for prediction of survival and chemotherapeutic benefits in gastric cancer. EBioMedicine. 2018; 36: 171-182.
- 97Li W, Zhang L, Tian C, et al. Prognostic value of computed tomography radiomics features in patients with gastric cancer following curative resection. Eur Radiol. 2019; 29: 3079-3089.
Citing Literature
