Indian Journal of Cancer
Home  ICS  Feedback Subscribe Top cited articles Login 
Users Online :734
Small font sizeDefault font sizeIncrease font size
Navigate here
  Search
 
  
Resource links
 »  Similar in PUBMED
 »Related articles
 »  Article in PDF (244 KB)
 »  Citation Manager
 »  Access Statistics
 »  Reader Comments
 »  Email Alert *
 »  Add to My List *
* Registration required (free)  

 
  In this article
 »  Abstract
 »  Background and I...
 »  Materials and Me...
 » Results
 » Discussion
 » Conclusion
 »  References
 »  Article Tables

 Article Access Statistics
    Viewed219    
    Printed7    
    Emailed0    
    PDF Downloaded89    
    Comments [Add]    

Recommend this journal

 

  Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 56  |  Issue : 4  |  Page : 297-301
 

Management of colon cancer at a tertiary referral center in India - Patterns of presentation, treatment, and survival outcomes


Department of GI and HPB Oncology, Tata Memorial Hospital and Homi Bhabha National Institute, Parel, Mumbai, Maharashtra, India

Date of Web Publication11-Oct-2019

Correspondence Address:
Ashwin deSouza
Department of GI and HPB Oncology, Tata Memorial Hospital and Homi Bhabha National Institute, Parel, Mumbai, Maharashtra
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijc.IJC_379_18

Rights and Permissions

 » Abstract 


AIM: To define the patterns of disease presentation, treatment strategies, and outcomes for patients with colon cancer at a tertiary referral center in India over 1 year period.
MATERIALS AND METHODS: This is a retrospective analysis of a prospectively maintained database. All consecutive patients with proven or suspected colonic adenocarcinoma between July 2013 and July 2014 were evaluated in a dedicated analysed multidisciplinary clinic at the Tata Memorial Hospital, Mumbai. The demography, treatment plan, pathology, stage, and survival data were examined.
RESULTS: The median age of presentation was 49 years with 60.1% male patients. In total, 151 cases (57.4%) underwent treatment with curative intent consisting of surgery with adjuvant chemotherapy as indicated. The rest were offered either palliative chemotherapy (36.9%) or best supportive care (5.7%). Approximately, 70% patients had advanced stage disease (Stage III/IV) at presentation and 41.8% presented with metastatic disease with the liver being the most common site of disease dissemination. With a median follow-up of 29 months, the estimated 3-year disease free survival for patients treated with curative intent was 67.1%. The median progression free survival was 12.3 months for patients treated with palliative intent. The estimated 3-year overall survival was 89.7%, 65.5%, and 22.8% for Stage I/II, Stage III, and Stage IV, respectively.
CONCLUSION: Indian patients with colon cancer, at a tertiary referral center, tend to present at more advanced stages of the disease as compared to the West. However, curative treatment with surgery and chemotherapy offers similar survival outcomes when compared stage for stage.


Keywords: Cancer, colon, India, survival


How to cite this article:
Noronha J, deSouza A, Patil P, Mehta S, Engineer R, Ostwal V, Ramaswamy A, Ankathi SK, Ramadwar M, Saklani A. Management of colon cancer at a tertiary referral center in India - Patterns of presentation, treatment, and survival outcomes. Indian J Cancer 2019;56:297-301

How to cite this URL:
Noronha J, deSouza A, Patil P, Mehta S, Engineer R, Ostwal V, Ramaswamy A, Ankathi SK, Ramadwar M, Saklani A. Management of colon cancer at a tertiary referral center in India - Patterns of presentation, treatment, and survival outcomes. Indian J Cancer [serial online] 2019 [cited 2019 Nov 18];56:297-301. Available from: http://www.indianjcancer.com/text.asp?2019/56/4/297/268959





 » Background and Introduction Top


In India, the annual incidence rate of colon cancer in men and women is 4.4 and 3.9 per 100,000.[1] It is the eight most common cancer in men, whereas for women, colon cancer ranks ninth. Western literature reports colorectal cancer to be the third most commonly occurring cancer in men and second most commonly occurring cancer in women.[2] The higher frequency of colorectal cancer in America, Europe, and Oceania in comparison to Africa and Asia has been attributed to higher indices of development and/or income. By virtue of a population of over one billion and underreporting of the disease, the absolute number of colorectal cancer patients in India still remains high despite its low incidence. An increased frequency of colon cancer in the urban Indian population as well as Indian migrants abroad is known.[3],[4],[5] The rapid increase in urbanization of the subcontinent with accompanying diet and lifestyle changes will, in all probability, increase the incidence of colon cancer in India in the coming decade.

There is a dearth of Indian data in reported literature on the patterns of presentation and treatment outcomes for colon cancer. We could come across a single published article [6] with similar data, but the cohort consisted of right colon cancer cases alone. This audit aims to define the patterns of disease presentation, treatment strategies, and outcomes for patients with colon cancer at a tertiary referral center in India. Such studies provide a foundation on which to draw comparisons with internationally reported data, which aid in the development and improvement of treatment strategies in the management of colon cancer.


 » Materials and Methods Top


This is a retrospective analysis of a prospectively maintained database of colon cancer patients treated in a dedicated multidisciplinary colorectal cancer clinic between July 2013 and July 2014, at the Tata Memorial Hospital, a tertiary referral center for cancer in India. The aim of this study was to evaluate the demography, stage at presentation, and survival outcomes of colon cancer patients registered at our center over a one-year period. Only tumors of the abdominal colon i.e., with the lower limit above the sacral promontory as determined on imaging/endoscopy were included in this analysis. Tumors with rectosigmoid involvement were excluded, as the management of these lesions is influenced by the location of the epicenter of the mass. Neoadjuvant chemoradiation can be considered for lesions extending into the upper and mid rectum, especially if the circumferential resection margin is involved/threatened, however, this is not suitable for tumors with the epicenter in the sigmoid colon with involvement of the rectosigmoid. In view of the heterogeneity in the management of this patient group, they were excluded from this study. Right colon cancers were defined as tumours proximal to the splenic flexure. Tumors with involvement of the splenic flexure, descending, or sigmoid colon were labeled as left sided tumors. All patients with suspected or proven colon cancer were assessed and treated as per standard prevailing guidelines by a multidisciplinary team (MDT) consisting of at least one surgical oncologist, medical oncologist, radiation oncologist, medical gastroenterologist, and dedicated colorectal radiologist. Patients were staged according to the 8th edition American Joint Committee on Cancer, TNM classification.[7] Surgery for tumors with evidence of intestinal obstruction, perforation, or intraluminal bleeding requiring blood transfusion were labeled as emergency procedures. Such patients were not scheduled on the routine operating list but rather accommodated on the next operating list or operated out of routine hours, each case being decided on an individual basis. Anastomotic leak was defined as feculant drainage in the intraoperatively placed surgical drains or presence of contrast extravasation or perianastomotic collection (with or without contrast extravasation) on post-operative imaging. After completing treatment, patients were followed up with an annual Contrast Enhanced Computed Tomography (CECT) scan of the thorax, abdomen, and pelvis till 5 years, and a complete physical examination and serum Carcinoembryonic antigen (CEA) every 3 months for the first 2 years and then 6 monthly till 5 years. Surveillance colonoscopy was performed at 1 year, and if normal, repeated after 3 years and then 5 yearly. Patients who were symptomatic in the interim were discussed in MDT and treated accordingly. Survival data were collected from follow-up hospital visits and telephonic interviews when possible. Survival time was calculated from the date of surgery and date of registration for patient treated with curative and palliative intent, respectively. Survival analysis was done using Kaplan Meir method. Data were analyzed using SPSS Version 20.0 for Windows. Institutional Ethics Committee approval was obtained for this study.


 » Results Top


Patterns of presentation

From July 2013 to July 2014, 263 treatment-naïve and previously treated patients with colon adenocarcinoma were evaluated at our dedicated colorectal MDT. At presentation, 223 patients had primary disease (metachronous second primary in 4 patients), whereas 40 patients had recurrent disease after treatment of their primary cancer. Among patients with primary cancers, 68 (30.5%) had prior cancer directed treatment. In total, 80% of these previously treated patients had surgery for the primary cancer before being referred to our institute.

Overall, 158 (60.1%) were male with the median age of presentation in men and women being 50 years and 47 years, respectively. Totally, 133 patients (50.57%) were <50 years, with a third of the patients presenting at <40 years of age [Table 1]. A little more than half of the patients (57.8%) had right sided tumors i.e., in the caecum, appendix, ascending, and transverse colon. The rest (39.9%) had tumors in the left colon with only 6 patients (2.3%) presenting with synchronous colonic cancers [Table 2].
Table 1: Age distribution of all patients at presentation (n=263)

Click here to view
Table 2: Sub site distribution of all patients at presentation (n=263)

Click here to view


Adenocarcinoma was diagnosed in all patients on endoscopic biopsy. However, tumor differentiation was reported in 72.6% of patients. Moderately differentiated adenocarcinoma formed the bulk of tumours in this series [Table 3]. There were 37 (14.1%) patients with signet ring morphology and 51 (19%) cases reported to have mucinous adenocarcinoma.
Table 3: Histology on colonoscopic biopsy (n=263)

Click here to view


The stage grouping is listed in [Table 4], with 30.4% early colon cancer (Stage I/II) and 27.8% loco-regional disease (Stage III). The majority of patients in this study (41.8%) had distant metastases at presentation. Stage IV disease at presentation was seen in 35.9% of patients with primary colon cancer (n = 223). In total, 75% of patients with recurrent disease had distant metastasis with only 10 of these patients (25%) presenting with isolated locoregional recurrence [Table 5]. Of the 110 patients with metastatic disease, at the time of registration 37 (33.63%) had liver metastases making it the most common site of disease dissemination followed by the peritoneum (25.45%). The majority of patients with metastatic disease had more than one site of disease spread (58.1%). Isolated lung metastasis in the absence of other systemic metastasis was seen in just 2 patients (1.8%) at presentation [Table 6].
Table 4: Clinico-radiological stage distribution at presentation (n=263)

Click here to view
Table 5: Primary Vs Recurrent Cancers

Click here to view
Table 6: Stage IV patients at presentation - Site of metastasis (n=110)

Click here to view


Treatment modalities

After MDT evaluation, 151 patients (57.4%) were offered curative treatment with surgery and adjuvant chemotherapy as indicated, 97 patients (36.9%) underwent palliative treatment, and 15 patients (5.7%) were offered best supportive care. Treatment with curative intent was offered to 62.8% of patients with primary cancer but to only 11 patients (27.5%) presenting with recurrent disease [Table 5]. In total, 192 operations were performed for staging, curative, and palliative purposes [Table 7]. Totally, 52 surgical procedures (27.08%) were performed as emergency surgeries for obstruction, perforated, or bleeding tumors. Of the 178 radical colonic resections, 32 patients underwent palliative tumor resections for symptom control. An anastomosis was fashioned for all patients undergoing radical resection, and a covering ileostomy was performed in one of these patients on account of intraoperative hemodynamic instability. Six patients (6/178 anastomoses, 3.4%) had an anastomotic dehiscence that required a return to operation theater. There was no 30-day mortality, and postoperative complications are as listed in [Table 8]. There was no difference in the 30-day morbidity associated with patients undergoing radical colonic resections either with curative or palliative intent (P = 0.106).
Table 7: Surgical procedure distribution (Staging/curative/palliative; n=192)

Click here to view
Table 8: Clavien-Dindo complications of patients undergoing surgery (n=192)

Click here to view


Outcomes

Follow-up data were available for 70% of patients in this study, with a median follow-up duration of 29 months. The estimated 3-year disease free survival (DFS) and overall survival (OS) for patients treated with curative intent was 67.1% and 79.1%, respectively. For patients treated with palliative intent, the median progression free survival and estimated 3-year overall survival was 12.3 months and 19.9%, respectively. When analyzed by stage, the estimated 3-year overall survival was 89.7%, 65.5%, and 22.8% for Stage I/II, Stage III, and Stage IV, respectively. The recurrence patterns have been listed in [Table 9].
Table 9: Recurrence patterns in patients treated with curative intent (n=151)

Click here to view


The estimated 3-year OS and DFS for patients with right colon lesions treated with curative intent was 74.8% and 64.5%, respectively. Similarly, for left colon lesions, these values were 81.2% and 59.6%, respectively. There was no statistical difference in the OS (P = 0.29) and DFS (P = 0.87) when the survival outcomes of right and left sided tumors were compared.


 » Discussion Top


The incidence of colon cancer in India, like other developing nations, is lower than that reported in the West but is steadily increasing.[2],[8] The median age in our cohort was 49 years with 77 patients (28.5%) presenting with colon cancer under the age of 40. Other Indian studies have reported the incidence in the same age group to range between 12% and 37% that is higher than the 10% observed in the West.[9],[10],[11] In the United States of America, >90% colorectal cancers are diagnosed in people above the age of 50.[12]

Patients with early colon cancer (Stage I/II) comprised 30.4% of our cohort, with 41.8% of patients presenting with metastatic disease at registration. Even in patients with primary colon cancer, Stage IV disease at presentation formed the single largest patient group (35.9%). This contrasts with data from the American SEER database, which reports corresponding figures of 39% (Stage I/II) and 21% (Stage IV).[13] Our center serves as a tertiary referral center for cancer for India. This could partly explain the greater proportion of patients with advanced and metastatic disease in our study.

Of the patients presenting with stage IV disease, 19.1% had metastases confined to the peritoneal cavity that is similar to the 25% reported in literature.[14] Isolated liver metastases has been reported to range between 10% to 25%; we observed 15.4% of such patients in our series.[15] However, 2.3% patients had synchronous lesions which are similar to the overall prevalence of 3.5% published from 39 pooled studies.[16]

Signet ring colon cancer is reported to have a female predominance, a predilection for patients younger than 40 years of age, present with higher stage, have lower survival and higher disease recurrence.[17] There were 38 (14.1%) patients with signet ring morphology in our series. Although most Western series report this as a rare histopathological entity with an incidence of less than 2%, one series from Lebanon found the incidence of more than 10%.[18],[19]

Mucinous adenocarcinoma is reported to have lower survival after correction for stage.[20] There were 18.1% patients with mucinous histology in our series, which is higher than 5–15% in Western literature.[21],[22] An environmental or genetic basis are possible etiologies for this finding. Further research is required to ascertain the cause of the higher incidence of these specific tumor types in our study population.

Surgical intervention as an emergency procedure is required in 25%–36% of procedures for colon cancer.[23],[24] We performed 52 (27.08%) such emergency procedures in the curative and palliative setting for bowel obstruction, perforation, and bleeding tumors. Radical colectomy is indispensable when offering treatment with curative intent for colon cancer. However, polyagent chemotherapy with or without targeted therapy offers a median survival of 20–30 months even with metastatic disease.[25] A few studies have shown than radical surgery in the presence of metastatic disease may offer a survival advantage though it may be argued that these studies are limited by selection bias.[26],[27] Additionally, surgery may offer excellent palliation for a symptomatic colon primary.[28] There was no statistical difference in the postoperative morbidity for both curative and palliative resections in our study (P = 0.106), suggesting that palliative colonic resection is a feasible option for symptomatic tumors in the metastatic setting, in a select group of patients.

We have adopted a standardized technique both for stapled and hand-sewn anastomoses, the selection of which was dependent on surgeon preference, condition of the bowel wall, clinical presentation of the patient, and competing comorbid factors. However, 3.4% patients had a leak after abdominal colectomy with primary anastomosis, which compares well with reported leak rates of 0.5%–13% for primary anastomoses in large bowel resection for cancer.[29]

Isolated locoregional recurrence following radical colectomy with curative intent was 5.3% in our study, which compares with other contemporary series that report locoregional recurrence rates of 4.4%.[30] While curative treatment could be offered to a large proportion of patients with primary disease (62.8%), 72.5% of patients presenting with recurrent disease could only be offered palliative treatment after discussion in MDT.

Literature on outcomes of right and left colon cancer treated with curative intent shows conflicting results. Survival outcomes favor left colon cancer in the majority of reports.[31],[32],[33],[34],[35],[36] However, some reports demonstrate a more favorable outcome for right colon lesions.[37],[38] We did observe a marginally better estimated 3-year OS for left vs. right colon cancers (81.2% vs. 74.8%). However, this did not reach statistical significance.

The population based 5-year survival for colon cancer according to the Mumbai Cancer Registry reported in 2001 was 61.2% for localized colon cancer, 31.9% for regional, and 9.0% for distant metastatic disease, while the 5-year survival reported from the American SEER database was 89.9% for localized colon cancer, 71.3% for regional, and 13.9% for distant metastatic disease.[13],[39] We observed comparable estimated 3-year overall survival rates of 89.7%, 65.5%, and 22.8% for Stage I/II, Stage III, and Stage IV, respectively.

The main drawbacks of this study are its retrospective nature, short follow-up duration, and missing follow-up data. Additionally, the pattern of disease presentation as seen in this study, is probably not representative of the nationwide pattern of colon cancer presentation, as Tata Memorial Hospital serves as a tertiary referral center for cancer in India.


 » Conclusion Top


Indian patients with colon cancer, at a tertiary referral center, tend to present at more advanced stages of the disease with higher proportions of signet ring and mucinous histology as compared to the West. However, curative treatment with surgery and chemotherapy offers similar survival outcomes when compared stage for stage. Palliative surgery for the symptomatic primary in the metastatic setting is a viable treatment option in a select group of patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

1.
Indian Council Of Medical Research. Consenses document for management of colorectal cancer. 2014. Available from: http://www.icmr.nic.in/guide/cancer/Colorectal/Colorectal%20Cancer.pdf. [Last cited on 2018 Nov 01].  Back to cited text no. 1
    
2.
Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut 2017;66:683-91.  Back to cited text no. 2
    
3.
Grulich AE, McCredie M, Coates M. Cancer incidence in Asian migrants to New South Wales, Australia. Br J Cancer 1995;71:400-8.  Back to cited text no. 3
    
4.
Ali R, Barnes I, Kan SW, Beral V. Cancer incidence in British Indians and British whites in Leicester, 2001–2006. Br J Cancer 2010;103:143-8.  Back to cited text no. 4
    
5.
Mohandas KM, Desai DC. Epidemiology of digestive tract cancers in India. V. Large and small bowel. Indian J Gastroenterol 1999;18:118-21.  Back to cited text no. 5
    
6.
Franklyn J, Mittal R, Sebastian T, Perakath B. Demographics and outcomes of surgically treated right sided colon cancer in India: A 9-year single institution experience. Trop Gastroenterol 2016;37:46-52.  Back to cited text no. 6
    
7.
AJCC. In: AMin MB, editor. AJCC Cancer Staging Manual. 8th ed. Springer; 2017.  Back to cited text no. 7
    
8.
Yeole BB. Trends in cancer incidence in esophagus, stomach, colon, rectum and liver in males in India. Asian Pac J Cancer Prev 2008;9:97-100.  Back to cited text no. 8
    
9.
Gupta S, Bhattacharya D, Acharya AN, Majumdar S, Ranjan P, Das S. Colorectal carcinoma in young adults: A retrospective study on Indian patients: 2000-2008. Colorectal Dis 2010;12:e182-9.  Back to cited text no. 9
    
10.
Sudarshan V, Hussain N, Gahine R, Mourya J. Colorectal cancer in young adults in a tertiary care hospital in Chhattisgarh, Raipur. Indian J Cancer 2013;50:337-40.  Back to cited text no. 10
[PUBMED]  [Full text]  
11.
Peedikayil MC, Nair P, Seena SM, Radhakrishnan L, Sadasivan S, Naryanan VA, et al. Colorectal cancer distribution in 220 Indian patients undergoing colonoscopy. Indian J Gastroenterol 2009;28:212-5.  Back to cited text no. 11
    
12.
Haggar FA, Boushey RP. Colorectal cancer epidemiology: Incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg 2009;22:191-7.  Back to cited text no. 12
    
13.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin 2017;67:7-30.  Back to cited text no. 13
    
14.
Yan TD, Black D, Savady R, Sugarbaker PH. Systematic review on the efficacy of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for peritoneal carcinomatosis from colorectal carcinoma. J Clin Oncol 2006;24:4011-9.  Back to cited text no. 14
    
15.
Sheth KR, Clary BM. Management of hepatic metastases from colorectal cancer. Clin Colon Rectal Surg 2005;18:215-23.  Back to cited text no. 15
    
16.
Lam AKY, Chan SSY, Leung M. Synchronous colorectal cancer: Clinical, pathological and molecular implications. World J Gastroenterol 2014;20:6815-20.  Back to cited text no. 16
    
17.
Park PY, Goldin T, Chang J, Markman M, Kundranda MN. Signet-ring cell carcinoma of the colon: A case report and review of the literature. Case Rep Oncol 2015;8:466-71.  Back to cited text no. 17
    
18.
Sasaki S, Masaki T, Umetani N, Futakawa N, Ando H, Muto T. Characteristics in primary signet-ring cell carcinoma of the colorectum, from clinicopathological observations. Jpn J Clin Oncol 1998;28:202-6.  Back to cited text no. 18
    
19.
Ibrahim NK, Abdul-Karim FW. Colorectal adenocarcinoma in young Lebanese adults. The American University of Beirut-Medical Center experience with 32 patients. Cancer 1986;58:816-20.  Back to cited text no. 19
    
20.
Verhulst J, Ferdinande L, Demetter P, Ceelen W. Mucinous subtype as prognostic factor in colorectal cancer: A systematic review and meta-analysis. J Clin Pathol 2012;65:381-8.  Back to cited text no. 20
    
21.
Hyngstrom JR, Hu CY, Xing Y, You YN, Feig BW, Skibber JM, et al. Clinicopathology and outcomes for mucinous and signet ring colorectal adenocarcinoma: Analysis from the National Cancer Data Base. Ann Surg Oncol 2012;19:2814-21.  Back to cited text no. 21
    
22.
Sung CO, Seo JW, Kim K-M, Do I-G, Kim SW, Park C-K. Clinical significance of signet-ring cells in colorectal mucinous adenocarcinoma. Mod Pathol 2008;21:1533-41.  Back to cited text no. 22
    
23.
Sjo OH, Larsen S, Lunde OC, Nesbakken A. Short term outcome after emergency and elective surgery for colon cancer. Colorectal Disease. 2009;11:733-9.  Back to cited text no. 23
    
24.
Anderson JH, Hole D, McArdle CS. Elective versus emergency surgery for patients with colorectal cancer. Br J Surg 1992;79:706-9.  Back to cited text no. 24
    
25.
Meulenbeld HJ, van Steenbergen LN, Janssen-Heijnen MLG, Lemmens VEPP, Creemers GJ. Significant improvement in survival of patients presenting with metastatic colon cancer in the south of The Netherlands from 1990 to 2004. Ann Oncol 2008;19:1600-4.  Back to cited text no. 25
    
26.
de Mestier L, Manceau G, Neuzillet C, Bachet JB, Spano JP, Kianmanesh R, et al. Primary tumor resection in colorectal cancer with unresectable synchronous metastases: A review. World J Gastrointest Oncol 2014;6:156-69.  Back to cited text no. 26
    
27.
Liu SK, Church JM, Lavery IC, Fazio VW. Operation in patients with incurable colon cancer--is it worthwhile? Dis Colon Rectum 1997;40:11-4.  Back to cited text no. 27
    
28.
Dixon MR, Stamos MJ. Strategies for palliative care in advanced colorectal cancer. Digestive Surgery 2004;21:344-51.  Back to cited text no. 28
    
29.
Fielding LP, Stewart-Brown S, Blesovsky L, Kearney G. Anastomotic integrity after operations for large-bowel cancer: A multicentre study. Br Med J 1980;281:411-4.  Back to cited text no. 29
    
30.
Liska D, Stocchi L, Karagkounis G, Elagili F, Dietz DW, Kalady MF, et al. Incidence, patterns, and predictors of locoregional recurrence in colon cancer. Ann Surg Oncol 2017;24:1093-9.  Back to cited text no. 30
    
31.
Benedix F, Kube R, Meyer F, Schmidt U, GastingerI, Lippert H, et al. Comparison of 17,641 patients with right and left sided colon cancer: Differences in epidermilogy, perioperative course, histology, and survival. Dis Colon Rectum 2010;53:57-64.  Back to cited text no. 31
    
32.
Suttie SA, Shaikh I, Mullen R, Amin AI, Daniel T, Yalamarthi S. Outcome of right- and left-sided colonic and rectal cancer following surgical resection. Colorectal Dis 2011;13:884-9.  Back to cited text no. 32
    
33.
Huang CW, Tsai HL, Huang MY, Huang CM, Yeh YS, Ma CJ, et al. Different clinicopathologic features and favorable outcomes of patients with stage III left-sided colon cancer. World J Surg Oncol 2015;13:257.  Back to cited text no. 33
    
34.
Meguid RA, Slidell MB, Wolfgang CL, Chang DC, Ahuja N. Is there a difference in survival between right- versus left-sided colon cancers? Ann Surg Oncol 2008;15:2388-94.  Back to cited text no. 34
    
35.
Jess P, Hansen IO, Gamborg M, Jess T, Danish Colorectal Cancer Group. A nationwide Danish cohort study challenging the categorization into right-sided and left-sided colon cancer. BMJ Open 2013;3:pii: e002608.  Back to cited text no. 35
    
36.
Lim DR, Kuk JK, Kim T, Shin EJ. Comparison of oncological outcomes of right-sided colon cancer versus left-sided colon cancer after curative resection: Which side is better outcome? Medicine (Baltimore) 2017;96:e8241.  Back to cited text no. 36
    
37.
Warschkow R, Sulz MC, Marti L, Tarantino I, Schmied BM, Cerny T, et al. Better survival in right-sided versus left-sided stage I-III colon cancer patients. BMC Cancer 2016;16:554.  Back to cited text no. 37
    
38.
Moritani K, Hasegawa H, Okabayashi K, Ishii Y, Endo T, Kitagaw Y. Difference in the recurrence rate between right- and left-sided colon cancer: A 17-year experience at a single institution. Surg Today 2014;44:1685-91.  Back to cited text no. 38
    
39.
Yeole BB, Sunny L, Swaminathan R, Sankaranarayanan R, Parkin DM. Population-based survival from colorectal cancer in Mumbai, (Bombay) India. Eur J Cancer 2001;37:1402-8.  Back to cited text no. 39
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

Top
Print this article  Email this article
 

    

  Site Map | What's new | Copyright and Disclaimer
  Online since 1st April '07
  © 2007 - Indian Journal of Cancer | Published by Wolters Kluwer - Medknow