Oncotarget, Vol. 6, No. 36
www.impactjournals.com/oncotarget/
Pattern of distant metastases in colorectal cancer: a SEER based study Miaozhen Qiu1,2,*, Jianming Hu3,*, Dajun Yang4,*, David Peter Cosgrove2 and Ruihua Xu1 1
Department of Medical Oncology, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China 2
Department of Oncology, The Sidney Kimmel Comprehensive Cancer Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA 3
Department of Medical Imaging Department, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China 4
Department of Experimental Research, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China *
These authors have contributed equally to this work
Correspondence to: Ruihua Xu, email: [email protected] Keywords: incidence, metastases, colon cancer, rectal cancer, SEER Received: August 13, 2015
Accepted: September 24, 2015
Published: October 15, 2015
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
ABSTRACT More and more evidences suggest that primary colon and rectum tumors should not be considered as a single disease entity. In this manuscript, we evaluate the metastatic patterns of colon and rectum cancers and analyze the potential distribution of metastatic disease in these two malignancies. Data queried for this analysis include colorectal adenocarcinoma (2010-2011) from the Surveillance, Epidemiology, and End Results Program (SEER) database. Metastatic distribution information was provided for liver, lung, bone and brain. All of statistical analyses were performed using the Intercooled Stata 13.0 (Stata Corporation, College Station, TX). All statistical tests were two-sided. Totally, there were 46,027 eligible patients for analysis. We found that colon cancer had a higher incident rate of liver metastasis than rectum cancer (13.8% vs 12.3%), while rectum cancer had a higher incident rate of lung (5.6% vs 3.7%) and bone (1.2% vs 0.8%) metastasis than colon cancer, P”.
Outcome variables The anatomic sub-sites of the left colon, right colon and rectum were categorized according to the International Classification of Diseases for Oncology, third edition (ICD-0-3) topography codes. Right-sided colon cancers were identified with the following SEER cancer site codes: cecum (ICD-0-3 code C18.0), ascending colon (Code C18.2), hepatic flexure (Code C18.3) and transverse colon (Code C18.4). Left-sided colon cancers were identified with codes: splenic flexure (Code C18.5), descending colon (code C18.6), sigmoid colon (code C18.7) and rectosigmoid (code C19.9). Rectal cancer was identified as code C20.9. 38664
Oncotarget
CONFLICTS OF INTEREST
For the purposes of this manuscript, only the adenocarcinoma pathologic type (SEER histology codes 8140 to 8147, 8210 to 8211, 8220 to 8221, 8260 to 8263, 8480 to 8481 and 8490) is included. We excluded cases without follow-up records and those who had multiple tumors and CRC was not the first tumor. According to the Collaborative stage data collection system, user documentation and coding instructions, the output of metastasis to lung, bone, brain and liver will present with 4 different codes. 0 means no metastasis to the site; 1 means confirmed metastasis to the site; 8 means not applicable; and 9 means whether this site is involved is unknown and there is no supportive documentation in patient record. We focused on the code 0 and code 1.
All authors declared that there is no conflict of interest.
REFERENCES 1.
2. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2010; 19: 1893-1907. 3. Lee YC, Lee YL, Chuang JP, Lee JC. Differences in survival between colon and rectal cancer from SEER data. PLoS One. 2013; 8: e78709.
Statistical analysis
4. Disibio G, French SW. Metastatic patterns of cancers: results from a large autopsy study. Arch Pathol Lab Med. 2008; 132: 931-939.
The patients’ demographic and tumor characteristics were summarized with descriptive statistics. Comparisons of categorical variables among different groups of patients were performed using the Chi square test, and continuous variables were compared using Student’s t test. CSS was calculated from the date of diagnosis to the date of cancer specific death. Deaths attributed to CRC were treated as events and deaths from other causes were treated as censored observations. Survival function estimation and comparison among different variables were performed using Kaplan-Meier estimates and the log-rank test. All of statistical analyses were performed using the Intercooled Stata 13.0 (Stata Corporation, College Station, TX). Statistical significance was set at two-sided P < 0.05. This study was deemed exempt from institutional review board approval by Sun Yat-sen University Cancer Center and informed consent was waived.
5. Hugen N, van de Velde CJ, de Wilt JH, Nagtegaal ID. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014; 25: 651-657. 6. Cook AD, Single R, McCahill LE. Surgical resection of primary tumors in patients who present with stage IV colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000. Ann Surg Oncol. 2005; 12: 637-645. 7. Hess KR, Varadhachary GR, Taylor SH, Wei W, Raber MN, Lenzi R, Abbruzzese JL. Metastatic patterns in adenocarcinoma. Cancer. 2006; 106: 1624-1633. 8. Weiss L, Grundmann E, Torhorst J, Hartveit F, Moberg I, Eder M, Fenoglio-Preiser CM, Napier J, Horne CH, Lopez MJ, et al. Haematogenous metastatic patterns in colonic carcinoma: an analysis of 1541 necropsies. J Pathol. 1986; 150: 195-203.
ACKNOWLEDGMENTS
9. Van Cutsem E, Nordlinger B, Adam R, Kohne CH, Pozzo C, Poston G, Ychou M, Rougier P. Towards a pan-European consensus on the treatment of patients with colorectal liver metastases. Eur J Cancer. 2006; 42: 2212-2221.
We would like to thank the staff members of the National Cancer Institute and their colleagues across the United States and at Information Management Services, Inc., who have been involved with the Surveillance, Epidemiology and End Results (SEER) Program.
10. Altendorf-Hofmann A, Scheele J. A critical review of the major indicators of prognosis after resection of hepatic metastases from colorectal carcinoma. Surg Oncol Clin N Am. 2003; 12: 165-192, xi.
FUNDING
11. Pawlik TM, Schulick RD, Choti MA. Expanding criteria for resectability of colorectal liver metastases. Oncologist. 2008; 13: 51-64.
This work was supported by: 1. The third outstanding young talents training plan of Sun Yat-sen University cancer center. 2. Medical Scientific Research of Guangdong province B2014161. 3. Scientific and Technological projects Guangdong Esophageal Cancer Institute Q201408
www.impactjournals.com/oncotarget
Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64: 9-29.
12. Pozzo C, Basso M, Cassano A, Quirino M, Schinzari G, Trigila N, Vellone M, Giuliante F, Nuzzo G, Barone C. Neoadjuvant treatment of unresectable liver disease with irinotecan and 5-fluorouracil plus folinic acid in colorectal cancer patients. Ann Oncol. 2004; 15: 933-939. 13. Schouten LJ, Rutten J, Huveneers HA, Twijnstra A. Incidence of brain metastases in a cohort of patients with carcinoma of the breast, colon, kidney, and lung and melanoma. Cancer. 2002; 94: 2698-2705. 38665
Oncotarget
14. Sundermeyer ML, Meropol NJ, Rogatko A, Wang H, Cohen SJ. Changing patterns of bone and brain metastases in patients with colorectal cancer. Clin Colorectal Cancer. 2005; 5: 108-113.
28. Roato I. Bone metastases: When and how lung cancer interacts with bone. World J Clin Oncol. 2014; 5: 149-155.
15. Gomez Raposo C, Mora Rillo M, Gomez Senent S, Robles Maruhenda A, Montoya F, Garcia Puig J, Gonzalez Baron M. Brain metastases as the first sign of colon cancer. Clin Transl Oncol. 2007; 9: 742-743. 16. Succi L, Urrico GS, Prumeri S, Politi A, Latteri F. Brain metastasis: first sign of colorectal carcinoma. Chir Ital. 2000; 52: 419-420. 17. Hansen IO, Jess P. Possible better long-term survival in left versus right-sided colon cancer - a systematic review. Dan Med J. 2012; 59: A4444. 18. Yamauchi M, Lochhead P, Morikawa T, Huttenhower C, Chan AT, Giovannucci E, Fuchs C, Ogino S. Colorectal cancer: a tale of two sides or a continuum? Gut. 2012; 61: 794-797. 19. Lee GH, Malietzis G, Askari A, Bernardo D, Al-Hassi HO, Clark SK. Is right-sided colon cancer different to left-sided colorectal cancer? - A systematic review. Eur J Surg Oncol. 2014. 20. Benedix F, Kube R, Meyer F, Schmidt U, Gastinger I, Lippert H. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. 2010; 53: 57-64. 21. Phatak UR, Kao LS, Millas SG, Wiatrek RL, Ko TC, Wray CJ. Interaction between age and race alters predicted survival in colorectal cancer. Ann Surg Oncol. 2013; 20: 3363-3369. 22. Aizer AA, Paly JJ, Zietman AL, Nguyen PL, Beard CJ, Rao SK, Kaplan ID, Niemierko A, Hirsch MS, Wu CL, Olumi AF, Michaelson MD, D’Amico AV et al. Multidisciplinary care and pursuit of active surveillance in low-risk prostate cancer. J Clin Oncol. 2012; 30: 3071-3076. 23. Cohen SD, Sharma T, Acquaviva K, Peterson RA, Patel SS, Kimmel PL. Social support and chronic kidney disease: an update. Adv Chronic Kidney Dis. 2007; 14: 335-344. 24. Coello MC, Luketich JD, Litle VR, Godfrey TE. Prognostic significance of micrometastasis in non-small-cell lung cancer. Clin Lung Cancer. 2004; 5: 214-225. 25. Lagerwaard FJ, Levendag PC, Nowak PJ, Eijkenboom WM, Hanssens PE, Schmitz PI. Identification of prognostic factors in patients with brain metastases: a review of 1292 patients. Int J Radiat Oncol Biol Phys. 1999; 43: 795-803. 26. Sorensen JB, Hansen HH, Hansen M, Dombernowsky P. Brain metastases in adenocarcinoma of the lung: frequency, risk groups, and prognosis. J Clin Oncol. 1988; 6: 14741480. 27. Rodrigus P, de Brouwer P, Raaymakers E. Brain metastases and non-small cell lung cancer. Prognostic factors and correlation with survival after irradiation. Lung Cancer. 2001; 32: 129-136. www.impactjournals.com/oncotarget
38666
Oncotarget
www.impactjournals.com/oncotarget/
Pattern of distant metastases in colorectal cancer: a SEER based study Miaozhen Qiu1,2,*, Jianming Hu3,*, Dajun Yang4,*, David Peter Cosgrove2 and Ruihua Xu1 1
Department of Medical Oncology, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China 2
Department of Oncology, The Sidney Kimmel Comprehensive Cancer Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA 3
Department of Medical Imaging Department, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China 4
Department of Experimental Research, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China *
These authors have contributed equally to this work
Correspondence to: Ruihua Xu, email: [email protected] Keywords: incidence, metastases, colon cancer, rectal cancer, SEER Received: August 13, 2015
Accepted: September 24, 2015
Published: October 15, 2015
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
ABSTRACT More and more evidences suggest that primary colon and rectum tumors should not be considered as a single disease entity. In this manuscript, we evaluate the metastatic patterns of colon and rectum cancers and analyze the potential distribution of metastatic disease in these two malignancies. Data queried for this analysis include colorectal adenocarcinoma (2010-2011) from the Surveillance, Epidemiology, and End Results Program (SEER) database. Metastatic distribution information was provided for liver, lung, bone and brain. All of statistical analyses were performed using the Intercooled Stata 13.0 (Stata Corporation, College Station, TX). All statistical tests were two-sided. Totally, there were 46,027 eligible patients for analysis. We found that colon cancer had a higher incident rate of liver metastasis than rectum cancer (13.8% vs 12.3%), while rectum cancer had a higher incident rate of lung (5.6% vs 3.7%) and bone (1.2% vs 0.8%) metastasis than colon cancer, P”.
Outcome variables The anatomic sub-sites of the left colon, right colon and rectum were categorized according to the International Classification of Diseases for Oncology, third edition (ICD-0-3) topography codes. Right-sided colon cancers were identified with the following SEER cancer site codes: cecum (ICD-0-3 code C18.0), ascending colon (Code C18.2), hepatic flexure (Code C18.3) and transverse colon (Code C18.4). Left-sided colon cancers were identified with codes: splenic flexure (Code C18.5), descending colon (code C18.6), sigmoid colon (code C18.7) and rectosigmoid (code C19.9). Rectal cancer was identified as code C20.9. 38664
Oncotarget
CONFLICTS OF INTEREST
For the purposes of this manuscript, only the adenocarcinoma pathologic type (SEER histology codes 8140 to 8147, 8210 to 8211, 8220 to 8221, 8260 to 8263, 8480 to 8481 and 8490) is included. We excluded cases without follow-up records and those who had multiple tumors and CRC was not the first tumor. According to the Collaborative stage data collection system, user documentation and coding instructions, the output of metastasis to lung, bone, brain and liver will present with 4 different codes. 0 means no metastasis to the site; 1 means confirmed metastasis to the site; 8 means not applicable; and 9 means whether this site is involved is unknown and there is no supportive documentation in patient record. We focused on the code 0 and code 1.
All authors declared that there is no conflict of interest.
REFERENCES 1.
2. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2010; 19: 1893-1907. 3. Lee YC, Lee YL, Chuang JP, Lee JC. Differences in survival between colon and rectal cancer from SEER data. PLoS One. 2013; 8: e78709.
Statistical analysis
4. Disibio G, French SW. Metastatic patterns of cancers: results from a large autopsy study. Arch Pathol Lab Med. 2008; 132: 931-939.
The patients’ demographic and tumor characteristics were summarized with descriptive statistics. Comparisons of categorical variables among different groups of patients were performed using the Chi square test, and continuous variables were compared using Student’s t test. CSS was calculated from the date of diagnosis to the date of cancer specific death. Deaths attributed to CRC were treated as events and deaths from other causes were treated as censored observations. Survival function estimation and comparison among different variables were performed using Kaplan-Meier estimates and the log-rank test. All of statistical analyses were performed using the Intercooled Stata 13.0 (Stata Corporation, College Station, TX). Statistical significance was set at two-sided P < 0.05. This study was deemed exempt from institutional review board approval by Sun Yat-sen University Cancer Center and informed consent was waived.
5. Hugen N, van de Velde CJ, de Wilt JH, Nagtegaal ID. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014; 25: 651-657. 6. Cook AD, Single R, McCahill LE. Surgical resection of primary tumors in patients who present with stage IV colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000. Ann Surg Oncol. 2005; 12: 637-645. 7. Hess KR, Varadhachary GR, Taylor SH, Wei W, Raber MN, Lenzi R, Abbruzzese JL. Metastatic patterns in adenocarcinoma. Cancer. 2006; 106: 1624-1633. 8. Weiss L, Grundmann E, Torhorst J, Hartveit F, Moberg I, Eder M, Fenoglio-Preiser CM, Napier J, Horne CH, Lopez MJ, et al. Haematogenous metastatic patterns in colonic carcinoma: an analysis of 1541 necropsies. J Pathol. 1986; 150: 195-203.
ACKNOWLEDGMENTS
9. Van Cutsem E, Nordlinger B, Adam R, Kohne CH, Pozzo C, Poston G, Ychou M, Rougier P. Towards a pan-European consensus on the treatment of patients with colorectal liver metastases. Eur J Cancer. 2006; 42: 2212-2221.
We would like to thank the staff members of the National Cancer Institute and their colleagues across the United States and at Information Management Services, Inc., who have been involved with the Surveillance, Epidemiology and End Results (SEER) Program.
10. Altendorf-Hofmann A, Scheele J. A critical review of the major indicators of prognosis after resection of hepatic metastases from colorectal carcinoma. Surg Oncol Clin N Am. 2003; 12: 165-192, xi.
FUNDING
11. Pawlik TM, Schulick RD, Choti MA. Expanding criteria for resectability of colorectal liver metastases. Oncologist. 2008; 13: 51-64.
This work was supported by: 1. The third outstanding young talents training plan of Sun Yat-sen University cancer center. 2. Medical Scientific Research of Guangdong province B2014161. 3. Scientific and Technological projects Guangdong Esophageal Cancer Institute Q201408
www.impactjournals.com/oncotarget
Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64: 9-29.
12. Pozzo C, Basso M, Cassano A, Quirino M, Schinzari G, Trigila N, Vellone M, Giuliante F, Nuzzo G, Barone C. Neoadjuvant treatment of unresectable liver disease with irinotecan and 5-fluorouracil plus folinic acid in colorectal cancer patients. Ann Oncol. 2004; 15: 933-939. 13. Schouten LJ, Rutten J, Huveneers HA, Twijnstra A. Incidence of brain metastases in a cohort of patients with carcinoma of the breast, colon, kidney, and lung and melanoma. Cancer. 2002; 94: 2698-2705. 38665
Oncotarget
14. Sundermeyer ML, Meropol NJ, Rogatko A, Wang H, Cohen SJ. Changing patterns of bone and brain metastases in patients with colorectal cancer. Clin Colorectal Cancer. 2005; 5: 108-113.
28. Roato I. Bone metastases: When and how lung cancer interacts with bone. World J Clin Oncol. 2014; 5: 149-155.
15. Gomez Raposo C, Mora Rillo M, Gomez Senent S, Robles Maruhenda A, Montoya F, Garcia Puig J, Gonzalez Baron M. Brain metastases as the first sign of colon cancer. Clin Transl Oncol. 2007; 9: 742-743. 16. Succi L, Urrico GS, Prumeri S, Politi A, Latteri F. Brain metastasis: first sign of colorectal carcinoma. Chir Ital. 2000; 52: 419-420. 17. Hansen IO, Jess P. Possible better long-term survival in left versus right-sided colon cancer - a systematic review. Dan Med J. 2012; 59: A4444. 18. Yamauchi M, Lochhead P, Morikawa T, Huttenhower C, Chan AT, Giovannucci E, Fuchs C, Ogino S. Colorectal cancer: a tale of two sides or a continuum? Gut. 2012; 61: 794-797. 19. Lee GH, Malietzis G, Askari A, Bernardo D, Al-Hassi HO, Clark SK. Is right-sided colon cancer different to left-sided colorectal cancer? - A systematic review. Eur J Surg Oncol. 2014. 20. Benedix F, Kube R, Meyer F, Schmidt U, Gastinger I, Lippert H. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. 2010; 53: 57-64. 21. Phatak UR, Kao LS, Millas SG, Wiatrek RL, Ko TC, Wray CJ. Interaction between age and race alters predicted survival in colorectal cancer. Ann Surg Oncol. 2013; 20: 3363-3369. 22. Aizer AA, Paly JJ, Zietman AL, Nguyen PL, Beard CJ, Rao SK, Kaplan ID, Niemierko A, Hirsch MS, Wu CL, Olumi AF, Michaelson MD, D’Amico AV et al. Multidisciplinary care and pursuit of active surveillance in low-risk prostate cancer. J Clin Oncol. 2012; 30: 3071-3076. 23. Cohen SD, Sharma T, Acquaviva K, Peterson RA, Patel SS, Kimmel PL. Social support and chronic kidney disease: an update. Adv Chronic Kidney Dis. 2007; 14: 335-344. 24. Coello MC, Luketich JD, Litle VR, Godfrey TE. Prognostic significance of micrometastasis in non-small-cell lung cancer. Clin Lung Cancer. 2004; 5: 214-225. 25. Lagerwaard FJ, Levendag PC, Nowak PJ, Eijkenboom WM, Hanssens PE, Schmitz PI. Identification of prognostic factors in patients with brain metastases: a review of 1292 patients. Int J Radiat Oncol Biol Phys. 1999; 43: 795-803. 26. Sorensen JB, Hansen HH, Hansen M, Dombernowsky P. Brain metastases in adenocarcinoma of the lung: frequency, risk groups, and prognosis. J Clin Oncol. 1988; 6: 14741480. 27. Rodrigus P, de Brouwer P, Raaymakers E. Brain metastases and non-small cell lung cancer. Prognostic factors and correlation with survival after irradiation. Lung Cancer. 2001; 32: 129-136. www.impactjournals.com/oncotarget
38666
Oncotarget
