SJS0010.1177/1457496915571400Gastric cancer and staging protocolsC. S. Chong, et al.


Scandinavian Journal of Surgery  0:  1­–4,  2015

Computed tomography of the thorax for gastric cancer staging: is it necessary? C. S. Chong, Celene Wei-Qi Ng, A. Shabbir, K. Kono, J. B. Y. So

University Surgical Cluster, National University Hospital and National University of Singapore, Singapore


Background: The utility of computed tomography scans of the thorax, abdomen, and pelvis for gastric cancer staging has been recommended in many countries. However, the validity of the use of computed tomography thorax in gastric cancer staging has not been challenged. Methods: A retrospective review was conducted on our gastric cancer registry from 1998 till 2012 in the National University Hospital, Singapore. We performed computed tomography thorax only in selected cases. We defined isolated lung metastasis as the presence of suspicious findings on computed tomography thorax in the absence of metastasis elsewhere. Results: A total of 808 gastric cancer cases were reviewed. The mean age of the patients was 66 years (standard deviation 13.53), and 67% were male. In all, 238 patients (30%) had metastatic disease at presentation, and 1 (0.42%) had isolated lung metastasis. The most common site of metastasis was intra-abdominal (73.8%). Among the patients who underwent surgery, the overall distant recurrence rate was 30%, of which only 83 (30%) patients had lung metastasis and all had concurrent metastasis in an intra-abdominal site. Conclusion: The rarity of isolated lung metastasis in gastric cancer suggests the limited value of computed tomography thorax as a routine staging tool for gastric cancers. Key words: Guidelines; stomach cancer; lung metastasis

Background Accurate staging is essential for effective treatment of any cancer. The current published guidelines from Correspondence: Jimmy B. Y. So Associate Professor University Surgical Cluster National University Hospital and National University of Singapore Tower Block Level 8 1E Kent Ridge Road Singapore 119228 Email: [email protected]

various countries have recommended the routine use of computed tomography (CT) thorax, abdomen, and pelvis for gastric cancer staging (1–5). However, the validity of the use of CT thorax for routine gastric cancer staging has not been challenged in recent literature. Gastric cancer is the fourth most common cancer in the world (6–8). Interestingly, there is an obvious geographical variation, with distal gastric cancers being more prevalent in Asia, Singapore included, in contrast to proximal gastric cancers in the West (6, 8–12). In our hospital, CT scans of the abdomen and pelvis are routinely performed for gastric cancer staging, while CT thorax is reserved for proximal gastric tumors extending toward the lower esophagus. We aim to review and evaluate the necessity of CT thorax in routine gastric cancer staging in our population.


C. S. Chong, et al.

Methods Study population

All patients with gastric cancer from 1998 to 2011 in our Gastric Cancer Registry at the National University Hospital, Singapore were reviewed. Hospital protocol for gastric cancer

The current protocol in our unit for the staging of gastric cancer consists of a complete clinical assessment, chest radiograph (CXR), and CT abdomen and pelvis. The CT scan of the abdomen is performed with a gastric distension technique in which the stomach is filled with either gas or water prior to the scan (13). CT thorax is performed only in patients with proximal gastric cancers, suspicious findings on the CXR, or where chest symptoms such as chest pain and breathlessness are present. All scans are performed with intravenous contrast using a high-resolution 64-slice CT scanner. Staging laparoscopy is routinely performed in advanced gastric cancers. Endoscopic ultrasound (EUS) was not used routinely. All gastric cancer patients in our institution are discussed at the weekly multidisciplinary team (MDT) meeting attended by surgeons, radiologists, pathologists, oncologists, and care coordinators. All cancers were staged according to the American Joint Committee on Cancer (AJCC) Gastric Cancer Staging version 7 (9). The standard of care in our centre is D2 gastrectomy for curative intent. Surgical therapies were planned in accordance to the recommendations made in Japanese Gastric Cancer Treatment Guidelines (1–5). Follow-up

All patients are routinely followed up at the specialist outpatient clinic at 3-monthly intervals for the first year, 6-monthly intervals for the next 3 years, and yearly thereafter. Radiological imaging and endoscopy are performed only if clinically indicated, such as in cases of suspected recurrence. Study definitions

For this study, isolated lung metastasis was defined as the presence of lung metastasis without any other sites of metastasis on CT scan. Recurrence was defined as the radiological evidence of metastasis after 3 months from surgery. Histological confirmation was performed only if clinically indicated. All patients are on lifelong follow-up after surgery. Those who defaulted routine follow-up and had no recorded demise in the National Death Registry of Singapore are deemed as loss to follow-up. Admissions to other hospitals recorded in the National Electronic Healthcare Systems are also reviewed in our study for any significant event following gastric cancer surgery. Statistical analysis

Patient characteristics, staging information, histology, and follow-up data were extracted from the

database and patients’ clinical notes. All cases of incomplete data were excluded from the analysis. Chi-square test was used for categorized variables. Data were analyzed using SPSS v17.0 and reviewed with a statistician. Results At presentation

A total of 808 of the 839 patients in the Gastric Cancer Registry at the National University Hospital were analyzed. In all, 17 (0.02%) patients were excluded due to incomplete follow-up data. There were 538 (66.58%) male patients and 270 (33.42%) female patients. The predominant race was Chinese (81.73%), and the mean age was 66 years, ranging from 20 to 98 years. The pathological characteristics of patients at presentation are shown in Table 1. At initial presentation, 238 (29.5%) gastric cancer patients had distant metastasis. Lung involvement was present only in 17 (7.14%) patients. Only 1 patient (0.42%) had isolated lung metastasis, while the other patients had synchronous metastasis in the liver and bone. Out of the 238 patients with distant metastases, majority (55%) had liver and peritoneal metastasis. The other sites of metastasis were mainly intra-abdominal (5%), involving organs such as spleen, adrenal gland, and the bladder. None of our patients had concurrent lung pathology that directly influenced the treatment for gastric cancer. We reviewed the locations of primary gastric cancer in 238 patients who presented with metastatic disease and found that majority (58.82%) of the patients with lung metastasis had gastric cancers located in the upper one-third of the stomach. This is in contrast to the patients who had no metastatic lung involvement where cancers were predominantly (46.20%) located in the distal one-third of the stomach (Table 2). However, the difference was not statistically significant (p = 0.09). The single patient with isolated lung metastasis had a proximal gastric adenocarcinoma without esophageal extension diagnosed on upper endoscopy and biopsy. A CT thorax was performed after suspicious findings of pleural thickening on routine staging CXR. Due to multiple comorbidities, the patient received palliative care, and his demise 3 months later was related to metastatic gastric cancer. At recurrence

A total of 273 patients underwent surgery with curative intent. The median follow-up period was 25 months (range: 7–54 months). The overall recurrence rate is 30.4%. Lung metastasis was detected in four patients (4.82%), all of whom had concurrent metastasis in intra-abdominal sites detected on CT scan of the abdomen and pelvis. There were no cases of isolated lung recurrence in the follow-up of these patients. In all, 78.3% of patients had recurrence at a single site, with the most common site being the gastric bed. Distribution of recurrence sites is described in Fig. 1.


Gastric cancer and staging protocols Table 1 Pathological characteristics of patients.

Single Site    2 Sites      3 Sites

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808 (100.0)

92 (11.4) 57 (7.1) 55 (6.8) 62 (7.7) 71 (8.8) 106 (13.1) 109 (13.5) 238 (29.5) 18 (2.2)

Table 2 Correlation of sites of gastric cancer with metastatic lung involvement. Number of gastric cancer patients who presented with metastasis = 238 Lung involvement in 17 patients (7.1%)

No lung involvement in 221 patients (92.9%)

Upper 1/3 Middle 1/3 Distal 1/3

Upper 1/3 Middle 1/3 Distal 1/3

74 (33.3) 45 (20.3) 102 (46.2)

Values are presented as number (%).

Discussion Following the advances in CT imaging, the use of CT for staging has become a standard for many cancers. The inclusion of CT thorax for gastric cancer staging has been recommended by guidelines based in United States and Europe. These include National Comprehensive Cancer Network (NCCN) guidelines (3, 4), European Society for Medical Oncology (ESMO) (2), Association of Upper Gastrointestinal Surgeons of Great Britain and Ireland (AUGIS) (14), and Scottish Intercollegiate Guidelines Network (SIGN) (1). The incidence of lung involvement in gastric cancers reported in the literature is low and is similar to that reported in our current study (6, 8). From our study, the inclusion of CT thorax as an initial staging tool for all gastric cancers will only detect seven posi-

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26 (3.2) 192 (23.4) 471 (57.3) 6 (0.7) 113 (15.5)



182 (22.5) 283 (35.0) 64 (7.9) 279 (34.5)

AJCC: American Joint Committee on Cancer. Values are presented as number (%).

10 (58.8) 3 (17.6) 4 (23.5)

65 (78.3)         17 (20.5)      1 (1.2)


194 (24.0) 196 (24.3) 418 (51.7)

Number of Patients

Location and histology of tumor  Upper 1/3   Middle 1/3   Lower 1/3 Histology  Adenocarcinoma Laurens Classification  Diffuse  Intestinal  Mixed  Not otherwise specified Tumor differentiation  Well  Moderate  Poor  Undifferentiated  Not otherwise specified Final pathological staging (AJCC 7th Edition)  Ia  Ib  IIa  IIb  IIIa  IIIb  IIIc  IV   Incomplete staging

Patients with recurrence after curative surgery = 83

Fig. 1. Recurrence pattern. LN: lymph node.

tive findings out of every 100 patients staged. More importantly, most, if not all, will have concurrent metastases in the abdominal cavity. Hence, even if there is a positive finding in the chest, it does not change the management of the patient. Conversely, routine inclusion of CT thorax underpins rising healthcare cost and potentially unwarranted radiation. Furthermore, the detection of non-specific findings that mimic metastasis may aggravate the anxiety with further investigations and follow-up scans. The clinical impact of detection of lung metastasis is further diminished when we examine our data on metastatic cases alone. From our data, only 7.14% of metastatic cases will have involvement of lung parenchyma. Only in the 1 patient (0.42%) with isolated lung metastasis can this be potentially beneficial where a non-therapeutic surgery may be averted. This can be argued as a diagnostic laparoscopy, which might have revealed peritoneal metastasis, that was not detected on CT imaging. Proximal gastric cancers were postulated to have a higher incidence of lung metastasis given the increased likelihood of mediastinal lymph node involvement in proximal gastric cancers. This was however not statistically significant in our cohort. Given the overall low incidence of lung metastasis, we are unable to conclude the utility CT thorax for this specific subgroup of patients in our current review. To the authors’ knowledge, there is no further similar analysis done for gastric cancers in the literature. Hence, with the current evidence, the authors recommend that CT abdomen and CXR should suffice for gastric cancer staging especially in Asian countries where proximal cancers remain relatively uncommon (15). CT thorax should be recommended only in selected patients with chest symptoms or abnormal CXR as the incidence of isolated lung metastasis is exceedingly rare from our data. In patients with stage 4 disease and evidence of intra-abdominal metastasis, CT thorax should be included only for patients


C. S. Chong, et al.

with optimal response to chemotherapy, therefore making the patient a suitable candidate for therapeutic surgery. Conclusion Isolated lung metastasis in gastric cancer has not been reported before. Given the rarity of such occurrence in gastric cancer and minimal impact on treatment strategy, the risks outweigh the benefit for routine inclusion of CT thorax for staging. We recommend selective use of CT thorax as a staging tool for gastric cancer, and further research can focus on delineating specific subgroups with higher risk of lung metastasis. References 1. Scottish Intercollegiate Guidelines Network: SIGN 87-Management of oesophageal and gastric cancer. A National Clinical Guideline, SIGN, Edinburgh, 2006. 2. Okines A, Allum W, Verheij M et al: Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010;21(Suppl. 5):v50–v54. 3. Ajani J, Bekaii-Saab T, D’Amico TA et al: Gastric cancer, NCCN practice guidelines in oncology v22010. National Comprehensive Cancer Network, Fort Washington, MD, 2010. 4. Ajani J, Bekaii-Saab T, D’Amico TA et al: Esophageal and esophagogastric junction cancers, NCCN practice guidelines in oncology v12010. National Comprehensive Cancer Network, Fort Washington, MD, 2010.

5. Japanese Gastric Cancer Association: Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 2010;2011(14): 113–123. 6. Jemal A, Bray F, Center MM et al: Global cancer statistics. CA Cancer J Clin 2011;61(2):69–90. 7. Wynder EL, Kmet J, Dungal N et al: An epidemiological investigation of gastric cancer. Cancer 1963;16:1416–1496. 8. Correa P, Haenszel W, Tannenbaum S: Epidemiology of gastric carcinoma: Review and future prospects. Natl Cancer Inst Monogr 1982;62:129–134. 9. Edge SB, Byrd DR, Compton et al: American Joint Committee on Cancer Staging Manual, 7th ed. Springer, New York, 2010, p. 117. 10. Chia KS, Seow A, Lee HP et al: Cancer incidence in Singapore 1993–1997. Singapore Cancer RegistryReport no. 5, 2000. 11. Seow A, Koh WP, Chia KS et al: Trends in cancer incidence in Singapore 1968–2002. Singapore Cancer RegistryReport no. 6, 2004. 12. Wong CS, Chow KY, Lim GH et  al: Cancer survival in Singapore 1968–2002. Singapore Cancer Registry, 2008. 13. Gore RM: Upper gastrointestinal tract tumors: Diagnosis staging strategies. Cancer Imaging 2005;5(1):95–98. 14. Allum WH Blazeby JM, Griffin SM et  al: Guidelines for the management of oesophageal and gastric cancer. Gut 2011;60:1449–1472. 15. Deans C, Yeo MS, Soe MY et  al: Cancer of the gastric cardia is rising in incidence in an Asian population and is associated with adverse outcome. World J Surg 2011;35:617–624.

Received: July 28, 2014 Accepted: December 18, 2014

Computed tomography of the thorax for gastric cancer staging: Is it necessary?

The utility of computed tomography scans of the thorax, abdomen, and pelvis for gastric cancer staging has been recommended in many countries. However...
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