Abstract
Colorectal cancer is the third most common cancer in the United States in both men and women, and the second leading cause of cancer-related deaths. Whereas the overall incidence of colon and rectal cancer has been decreasing over the past two decades, due in large part to improved colorectal screening and surveillance of patients who are at risk, incidence rates of colorectal cancer in young adults ages 20 to 50 have actually been increasing. Recently, the American Cancer Society updated their guidelines with recommendations that everyone, not just African Americans or those with a strong family history of colon cancer, should begin colorectal screening at age 45 rather than age 50. However, the United States Multi-Society Task Force on Colorectal Cancer, which is comprised of the American College of Gastroenterology, the American Gastroenterological Association, and the American Society for Gastrointestinal Endoscopy, felt that there is still insufficient evidence to support early screening in the absence of known risk factors. Previous authors have examined the epidemiology and natural history of early onset colorectal cancer but none of these studies are specific to the state of Hawai‘i, which has a unique ethnic profile. The purpose of this article is to review the most recently reported incidence rate and demographics of early onset colorectal cancer in Hawai‘i and to discuss our own experience with colon cancer in patients younger than age 50. If we can determine specific characteristics of young patients with early onset colorectal cancer in Hawai‘i, we can better identify those patients who would benefit most from earlier screening.
Keywords: Early onset colorectal cancer, colorectal screening, American Cancer Society, United States Multi-Society Task Force on Colorectal Cancer
Introduction
Colorectal cancer is the third most common cancer in both men and women, and the second leading cause of cancer-related deaths.1 The Centers for Disease Control and Prevention (CDC) reports that in 2015, the incidence rate for the state of Hawai‘i was 41.3 per 100,000 people, slightly higher than that of the entire United States (US), which was 38. The mortality rates for Hawai‘i and the US were 10.5 and 14 respectively.1 Colorectal cancer incidence in Hawai‘i is highest for Japanese males and females, but the majority of late stage colorectal cancers are diagnosed in Native Hawaiian and other Pacific Islanders, who also have the highest mortality from this disease.2
The United States Multi-Society Task Force on Colorectal Cancer (MSTF) recommends colorectal screening for all average risk individuals after the age of 50.3 Patients at increased risk before age 50 include African Americans, individuals with first-degree relatives diagnosed with colorectal cancer or advanced adenoma before the age of 60, patients with polyposis syndromes such as Lynch Syndrome, and those with a long history of inflammatory bowel disease.3 These patients are advised by the MSTF to undergo screening at an earlier age.3 Modifiable risk factors for the development of colorectal cancer include smoking, alcohol, obesity, and a diet low in fiber, and high in red meats, processed meats, and greasy foods.3
Screening can be done with fecal immunochemical or DNA testing, flexible sigmoidoscopy, as well as virtual/CT colonography, but the gold standard is colonoscopy. Colonoscopy is the only method available to identify and remove pre-cancerous polyps throughout the colon. The Affordable Care Act requires both private insurers and Medicare to cover the costs of all colorectal screening tests recommended by the United States Preventive Services Task Force. Despite this, the colorectal cancer screening rate in 2016 for patients 50 years of age and older in the state of Hawai‘i was only 71.9% according to the American Cancer Society (ACS), which is a little above the national average of 68.9%.4 The goal of the National Colorectal Cancer Roundtable remains a rate of 80% by the end of 2018, which would prevent 277,000 new cases of colorectal cancer by 2030.5
Whereas the overall incidence of colon and rectal cancer in the United States has been decreasing by 1% each year over the past decade, due in large part to improved colorectal screening and surveillance of patients at risk, studies have shown that incidence of colorectal cancer has actually been increasing in youngadults age20to 50.6 This increaseof earlyonsetcolorectalcancer (EOCRC) is largely of tumors in the distal colon and rectum.7
Recently, the ACS updated their guidelines with recommendations that colorectal screening for everyone, not just those at increased risk for colon cancer, should begin at age 45 rather than age 50. They based their recommendation on a decision-analysis which demonstrated an increase in life-years gained when beginning screening at an earlier age.8 Most Gastrointestinal (GI) societies including the American College of Gastroenterology, the American Gastroenterological Association, and the American Society for Gastrointestinal Endoscopy, have not changed their recommendations however, citing insufficient evidence to support early screening in the absence of family history or other risk factors such as Lynch syndrome.9 Furthermore, health insurance companies have yet to approve of early screening for average risk individuals.
We have encountered several cases of EOCRC in our own practice in Honolulu, Hawai‘i over the past 5 years. We will review here the previously reported incidence rate and demographics of colorectal cancer in patients younger than age 50 in Hawai‘i. We will also present a case series of our patients with EOCRC, examining their demographics, family history and other potential risk factors, clinical presentation, and clinical course, and comparing our current findings with those of prior studies on EOCRC.
Results
Incidence rate of EOCRC in Hawai‘i
Data from the National Cancer Institute and the CDC indicates that across all of Hawai‘i, as with the rest of the US, the incidence rate of colorectal cancer in patients younger than age 50 went up from 2011 to 2015, though the overall rate still remains low (Table 1). There were 9.1 cases per 100,000 people in 2015 compared with 6.4 in 2011.10 More recent data from the Hawai‘i Department of Health is not yet available,.
Demographics of EOCRC in Hawai‘i
Between 2009 and 2013, Filipino and Japanese patients had the highest incidence rates of colon cancer before the age of 50, at 10.6 and 10.5 per 100,000 people respectively, according to datafrom the Hawai‘i Tumor Registry of the University of Hawai‘i Cancer Center (Table 2). These incidence rates correlate in part with the overall ethnic makeup of Hawai‘i. The US Census Bureau reports that between 2009 and 2013, Filipinos and Japanese made up two of the largest racial groups in Hawai‘i.11 Males had a higher incidence of colon cancer than females. Data from 2013 to 2015 is still being updated to the Registry.
Case Series
Between 2013 and 2018, we diagnosed nine patients under the age of 50 with colon cancer (Table 3). The median age of our patients was 41, with a range between 27 and 47. Filipinos made up the largest ethnic group. Approximately half were males.
One patient reported a family history of colon cancer and another patient was diagnosed with Lynch syndrome after microsatellite instability (MSI) testing was done on her tumor. Two patients were active smokers. Only one patient had a body mass index (BMI) greater than 40 on presentation and none of the patients were diabetic.
The majority of our patients presented with rectal bleeding and were found to have obstructing tumors of the sigmoid colon or rectum. Only two patients had tumors proximal to the splenic flexure and both presented with iron deficiency anemia. Seven of the nine patients already had stage III or IV colorectal cancer on presentation. Interestingly, carcinoembryonic (CEA) levels were elevated at baseline in only four patients, two of whom were smokers.
All of the patients received segmental resection, and patients with stage III or IVdisease also received postoperative adjuvant chemotherapy. One patientwith stageIVtransverse colon cancermoved to the mainland and his current status is unknown. To our knowledge, at the time of this publication, all of the remaining patients are currently doing well up to four years after their initial diagnosis except for one patient with stage IV disease who unfortunately expired soon after being placed on hospice.
Discussion
Demographics
The median age of our patients was 41 on presentation, which correlates with the median age range of 42-44 noted on previous studies on EOCRC.12 The majority of our patients were Filipino. EOCRC appears to be more prevalent in Black and Hispanic patients across the US, while in Hawai‘i, Filipino and Japanese patients have the highest incidence of colon cancer before the age of 50.2,13–14 In Hawai‘i, the overall incidence rate of EOCRC is higher in males than females, 9.8 versus 7.5, and 11% of all new cases of colorectal cancer in men and 10% in females occur in patients younger than age 50.2,4 In our series, there were approximately equal numbers of males and females, though this was a very small sample size.
Family History and Genetics
One of our patients reported a family history of colon cancer and one patient with a proximal tumor was diagnosed with Lynch Syndrome. One expert pointed out that the majority of EOCRC, up to 75% of patients, are in fact sporadic with no known family history while Lynch syndrome accounts for 17%.15–16 Studies suggest that for a subset of EOCRC, there may be a distinct molecular signature very different from late onset colorectal cancer. This includes progression through the micro-satellite and chromosomal stable (MACS) pathway as well as LINE-1 hypomethylation, which appears to be correlated with chromosomal instability and poor prognosis.12,17–18 In one study however, no change in tumor gene expression was noted among 22,052 patients across various ages upon interpretation of their Oncotype DX.19 The underlying genetics is still being evaluated.
Other Risk Factors
Environmental factors thought to be contributing to EOCRC in patients without a family history include increased prevalence of excess body weight, as well as changes in lifestyle patterns including unhealthy dietary patterns and a sedentary lifestyle.6 Diabetes appear to be another risk factor. In fact, large increases in the incidence rates of obesity and diabetes in young adults during the past three decades parallel the increasing incidence of colorectal cancer (CRC) in this age group.20 Only one of our patients had a BMI greater than 40 and none were diabetic however, suggesting that there are likely also other factors in play. An increase in the consumption of sugar sweetened beverages and a decrease in the consumption of milk, which contains CRC-protective calcium, also parallels increases in CRC incidence rate.20 Current research is exploring other potential associations with CRC including variations in the gut microbiome, exposure to environmental toxins, and changing patterns in the use of statins and antibiotics during the past several decades.6
Clinical Presentation
Almost all of our patients had either sigmoid or rectal tumors. Nonhereditary early-onset cancers largely comprise tumors on the left side of the colon and rectum whereas Lynch syndrome is predominantly characterized by tumors on the right side of the colon.15,21 In one study, 83% of tumors in patients younger than age 50 were in the left colon.22 The authors suggested screening of the left colon by flexible sigmoidoscopy beginning at age 40, however this strategy would have missed proximal tumors in two of our patients.
Compared with older patients with colon cancer, younger patients tend to present with more advanced disease. These patients are more likely to have lymphovascular invasion, T3/T4 tumors, and LN positive disease at diagnosis.23 CEA levels, however, are relatively normal.24 These results correlate with our own patients, the majority of which had stage III or IV disease on presentation but normal CEAlevels. It is still unclear whetherthese patients present at a later stage because their disease is more aggressive or because their symptoms are dismissed until they develop advanced disease and they are then diagnosed at a later stage. In one study, patients with young-onset CRC had a significantly longer median time to diagnosis, up to 1.4 times longer than for older patients, with longer symptom duration and longer time of evaluation.25
Clinical Course
All of our patients underwent segmental resection rather than extended colonic resection (subtotal, total, orproctocolectomy). According to the National Comprehensive Cancer Network (NCCN), extensive colectomy should be considered in patients with colon cancer younger than 50 due to the risk of metachronous lesions, particularly in patients with inflammatory bowel disease (IBD) and polyposis syndromes. Studies have shown that extended colectomy for sporadic CRC in patients younger than 50 does not improve disease-free or overall survival however, and thus segmental resection appears to be sufficient. In a study examining resection extent in sporadic CRC patients, 3.3% of patients undergoing segmental resection developed metachronous CRC vs 0% undergoing extended resection, which was not statistically significant.26
The majority of our stage III or IV patients have already received or are currently receiving chemotherapy and are doing well at the time of submission. Patients with advanced stage EOCRC tend to do better with chemotherapy than older patients, possibly due to a better ability to tolerate chemotherapy or because their disease is more responsive, and thus they have improved outcomes compared with older patients.23 The 5-year survival rate for stage IV cancer in early onset versus late onset colon cancer was 18.1% versus 6.2% in one study, and 25.5% versus 14.8% in another study.18
Conclusion
There has been a definite rise in incidence of EOCRC in Hawai‘i over the past decade and this trend will likely continue through to at least the next decade. Hawai‘i is unique in the variety of its ethnic groups, and the demographics of EOCRC here is very different from the rest of the US. The majority of these patients have no family history of colon cancer or other high risk conditions, as evidenced in our own practice, and there may be a distinct molecular profile. Poor dietary habits and the increasing incidence of obesity in Hawai‘i parallel the increase of EOCRC but other factors are also likely playing a role.
Previous data on EOCRC and our own experience in Hawai‘i support previous findings that most patients with early onset colon cancer tend to have left-sided tumors and are symptomatic on presentation. They also often have advanced disease, requiring postoperative adjuvant chemotherapy after surgical resection, but tend to do better per stage than patients with late onset CRC.
Some experts have recommended colorectal screening of all patients as early as age 40 rather than age 50. Further long-term studies are needed to help identify potential risk factors and target specific populations in Hawai‘i who will benefit most from earlier screening. Endoscopic evaluation must be considered even in the absence of family history or other risk factors for CRC for all young individuals with rectal bleeding or other worrisome features.
Table 1.
Incidence Rate Report for Hawai‘i, Colon & Rectal Cancer, 2011-2015, All Races (Includes Hispanic), Both Sexes, Ages <50
| Geography | Average Annual Count | Age-Adjusted Incidence Rate per 100,000 (95% Confidence Interval) |
Recent 5-Year Trend in Incidence Rates (95% Confidence Interval) |
Recent Trend |
|---|---|---|---|---|
| Hawai‘i | 78 | 9.1 (8.2, 10.0) | + 2.7 (1.6, 3.7) | Rising ↑ |
| US (NPCR + SEER) | 14,970 | 7.6 (7.5, 7.6) | + 3.7 (2.0, 5.5) | Rising ↑ |
Source: CDC’s National Program of Cancer Registries (NPCR) November 2017 data submission, National Institutes of Health (NIH)’s Surveillance, Epidemiology, and End
Results Program (SEER) November 2017 data submission, State Cancer Registries.
Table 2.
Demographics for Hawai‘i, Colon and Rectal Cancer, 2009-2013, All Races (Includes Hispanic), Both Sexes, Ages <50
| Age | Sex | Race | Total Population from 2009-2013 |
Total New Cases from 2009-2013 |
Age-Adjusted Incidence Rate per 100,000 (95% Confidence Interval) |
|---|---|---|---|---|---|
| <50 | Male and Female | All Races | 4,503,859 | 375 | 8.7 (7.8, 9.6) |
| Chinese | 278,321 | 15 | 5.1 (2.8, 8.4) | ||
| Filipino | 806,705 | 86 | 10.6 (8.5, 13.1) | ||
| Hawaiian | 1,167,932 | 70 | 8.2 (6.3, 10.3) | ||
| Japanese | 495,125 | 67 | 10.5 (8.1, 13.5) | ||
| White | 901,432 | 78 | 7.8 (6.2, 9.8) | ||
| Other Races | 854,344 | 50 | 6.9 (5.1, 9.1) | ||
| Male | All Races | 2,333,045 | 215 | 9.8 (8.6, 11.2) | |
| Female | All Races | 2,170,814 | 160 | 7.5 (6.3, 8.7) |
Source: Hawai‘i Tumor Registry, University of Hawai‘i Cancer Center
Table 3.
Patients Younger than Age 50 Diagnosed with Colorectal Cancer in our Gastroenterology Clinic in Honolulu, Hawai‘i from 2013-2018
| Age Race Sex |
Family history of colon cancer? Lynch Syndrome present? |
BMI Smoker? Diabetic? |
Presentation | Location of tumor Stage of tumor on presentation |
Baseline CEA level (Normal up to 4.7) |
Type of surgery Chemotherapy received? |
Last known outcome |
|---|---|---|---|---|---|---|---|
| 47 Filipino Male |
No No |
24 No No |
Right lower quadrant pain, Rectal bleeding, Abnormal imaging | Rectum (obstructing) IV |
50.8 H | Low anterior resection Yes |
Diagnosed in 2014 Expired 2015 |
| 42 Filipina Female |
No No |
21 No No |
Left lower quadrant pain, Diarrhea, Rectal bleeding | Sigmoid colon (obstructing) IIIB (pT3, N1a, M0) |
1.7 | Sigmoid colectomy Yes |
Diagnosed in 2015 Currently doing well |
| 41 Latino Male |
No No |
41 No No |
Iron deficiency anemia, No symptoms | Transverse colon (obstructing) IV |
0.9 | Right hemicolectomy Yes |
Diagnosed in 2015 Current status unknown |
| 47 Japanese Male |
No No |
24 Yes No |
Abdominal pain, Change in bowel habits, Rectal bleeding, Weight loss | Rectum (obstructing) IIIB (pT3, N1a, M0) |
15.5 H | Low anterior resection Yes |
Diagnosed in 2015 Currently doing well |
| 41 Caucasian Female |
No Yes |
21 No No |
Epigastric pain, Iron deficiency anemia | Ascending colon IIIB (pT3, N1a, M0) |
<3 | Right hemicolectomy Yes |
Diagnosed in 2015 Currently doing well |
| 41 Chinese Female |
No No |
20 No No |
Rectal bleeding | Rectum I (pT1, N0,M0) |
<3 | Local (wide) excision No |
Diagnosed in 2016 Currently doing well |
| 39 Filipino Male |
Yes (mother age 48) No |
28 Yes No |
Abdominal pain, Bloating, Rectal bleeding | Sigmoid colon I (pT1,N0,M0) |
3.5 H | Sigmoid colectomy No |
Diagnosed in 2016 Currently doing well |
| 37 Filipina Female |
No No |
27 No No |
Left lower quadrant pain, Change in bowel habits | Sigmoid colon (obstructing) IV |
166.4 H | Low anterior resection Yes |
Diagnosed in 2018 Currently doing well |
| 27 Japanese Female |
No No |
26 No No |
Constipation, Rectal bleeding | Sigmoid colon (obstructing) IIIC-IV (pT3, N2b, Mx) |
1.0 | Low anterior resection Pending |
Diagnosed in 2018 Currently doing well |
DEFINITIONS Presentation: Iron deficiency anemia - low iron and blood counts
| Colon Cancer Staging Systems | |||
|---|---|---|---|
| SEER summary stage | Description | AJCC Stage | TNM stage |
| Localized | Invasive tumor is confined to colon, including tumors extending through muscularis propria and subserosal tissue, but not serosal surface. | I and IIA | T1-3,N0,M0 |
| Regional | Tumor extends outside colon and/or invades regional lymph nodes, including local tumors extending into serosal surface, pericolic, or mesenteric fat. | IIB IIIA-C | T4,N0,M0 Any T,N1-2,M0 |
| Distant | Tumor has spread to distant organs or lymph nodes. | IV | Any T,Any N,M1 |
SEER = Surveillance, Epidemiology, and End Results Program. AJCC = American Joint Committee on Cancer. TNM – Tumor (T) extent, Nodes (N) present, Metastasis (M) present
Types of surgery: Local excision - removal of tumor without cutting through abdominal wall; Low anterior resection - removal of rectum; Sigmoid colectomy - removal of sigmoid colon; Right hemicolectomy - removal of cecum, ascending colon, and part of transverse colon.
Acknowledgments
Dr. Brenda Hernandez (Associate Professor, University of Hawai‘i Cancer Center) and Florlyn Taflinger (Cancer Program Coordinator, State of Hawai‘i Department of Health, Chronic Disease Management Branch).
Glossary
Abbreviations and Acronyms
- ACS
American Cancer Society
- BMI
body mass index
- CDC
Centers for Disease Control and Prevention
- CEA
carcinoembryonic antigen
- CRC
colorectal cancer
- EOCRC
early onset colorectal cancer
- GI
gastrointestinal
- IBD
inflammatory bowel disease
- MSI
microsatellite instability
- MSTF
United States Multi-Society Task Force on Colorectal Cancer
- NIH
National Institutes of Health
- NPCR
National Program of Cancer Registries
- SEER
Surveillance, Epidemiology, and End Results Program)
- US
United States
Conflict of Interest
None of the authors identify any conflict of interest.
References
- 1.Colorectal Cancer Statistics. Division of Cancer Prevention and Control, Centers for Disease Control and Prevention Web Site. https://www.cdc.gov/cancer/colorectal/statistics. Updated June 12, 2018. Accessed September 10, 2018.
- 2.University of Hawai'i Cancer Center, Research Highlights/Reports, 2009-2013. [Accessed September 10, 2018]. University of Hawai'i at Manoa Web Site. http://www.uhcancercenter.org/images/pdf/HTR_cancer_booklet.pdf. Updated December 2016.
- 3.Rex D, Boland CR, Dominitz JA, et al. Colorectal Cancer Screening: Recommendations for Physicians and Patients from the U.S. Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol. 2017;112:1016–1030. doi: 10.1038/ajg.2017.174. [DOI] [PubMed] [Google Scholar]
- 4.Cancer Statistics Center. [Accessed September 10, 2018]. American Cancer Society Web Site. https://cancerstatisticscenter.cancer.org/#!/state/Hawaii. Updated September 1, 2018.
- 5.National Colorectal Cancer Roundtable. [Accessed September 10, 2018]. American Cancer Society Web Site. http://nccrt.org/ beyond-2018-frequently-asked-questions. Updated April 5, 2018.
- 6.Siegel RL, Fedewa SA, Anderson WF, et al. Colorectal Cancer Incidence Patterns in the United States, 1974-2013. J Natl Cancer Inst. 2017;109:djw322–djw327. doi: 10.1093/jnci/djw322. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Siegel RL, Miller KD, Fedewa SA, et al. Colorectal Cancer Statistics, 2017. CA Cancer J Clin. 2017;67:177–193. doi: 10.3322/caac.21395. [DOI] [PubMed] [Google Scholar]
- 8.Peterse EFP, Meester RGS, Siegel RL, et al. The impact of the rising colorectal cancer incidence in young adults on the optimal age to start screening: Microsimulation analysis I to inform the American Cancer Society colorectal cancer screening guideline. Cancer. 2018;124:2964–2973. doi: 10.1002/cncr.31543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Statement from the U.S. Multisociety Task Force on Colorectal Cancer. [Accessed September 11, 2018]. American Gastroenterological Association Web Site. https://www.gastro.org/press-release/statement-from-the-us-multisociety-task-force-on-colorectal-cancer. Updated June 14, 2018.
- 10.National Cancer Institute and Center for Disease Control and Prevention, State Cancer Profiles. [Accessed September 11, 2018]. National Institutes of Health Web Site. https://www.statecancerprofiles.cancer.gov/incidencerates/index.php?stateFIPS=15&cancer=020&race=00&sex=0&age=009&type=incd&sortVaria bleName=rate&sortOrder=default. Updated July 1, 2018.
- 11.United States Census Bureau, American FactFinder. [Accessed September 11, 2018]. United States Census Bureau Web Site. https://factfinder.census.gov/faces/tableservices/jsf/pages/productview.xhtml?pid=ACS_13_5YR_DP05&prodType=table. Updated September 6, 2018.
- 12.Cavestro GM, Mannucci A, Zuppardo RA, Di Leo M, Stoffel E, Tonon G. Early onset sporadic colorectal cancer: Worrisome trends and oncogenic features. Dig Liver Dis. 2018;50:521–532. doi: 10.1016/j.dld.2018.02.009. [DOI] [PubMed] [Google Scholar]
- 13.Yeo H, Betel D, Abelson JS, Zheng XE, Yantiss R, Shah MA. Early-onset Colorectal Cancer is Distinct From Traditional Colorectal Cancer. Clin Colorectal Cancer. 2017;16:293–299. doi: 10.1016/j.clcc.2017.06.002. [DOI] [PubMed] [Google Scholar]
- 14.Rahman R, Schmaltz C, Jackson CS, Simoes EJ, Jackson-Thompson J, Ibdah JA. Increased risk for colorectal cancer under age 50 in racial and ethnic minorities living in the United States. Cancer Med. 2015;4:1863–70. doi: 10.1002/cam4.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Gordon C. Why is Colorectal Cancer Targeting the Young? [Accessed September 12, 2018]. Medscape Web Site. https://www. medscape.com/viewarticle/857294. Updated January 20, 2016.
- 16.Stigliano V, Sanchez-Mete L, Martayan A, Anti M. Early-onset colorectal cancer: A sporadic or inherited disease? World J Gastroenterol. 2014;20:12420–12430. doi: 10.3748/wjg.v20.i35.12420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Connell LC, Mota JM, Braghiroli MI, Hoff PM. The rising incidence of younger patients with colorectal cancer: questions above screening, biology, and treatment: Questions About Screening, Biology, and Treatment. Curr Treat Options Oncol. 2017;18(4):23. doi: 10.1007/s11864-017-0463-3. [DOI] [PubMed] [Google Scholar]
- 18.Patel SG, Ahnen DJ. Colorectal Cancer in the Young. Curr Gastroenterol Rep. 2018;20(4):15. doi: 10.1007/s11894-018-0618-9. [DOI] [PubMed] [Google Scholar]
- 19.Hochster H, Lau A, Turner M, Russell CA. Age Distribution of tumor gene expression in patients with stage II/II colon cancer [2018 GI Cancers Symposium abstract 552] J Clin Oncol. 2018;36(suppl):S552. [Google Scholar]
- 20.Siegel RL, Jemal A, Ward EM. Increase in incidence of colorectal cancer among young men and women in the United States. Cancer Epidemiol Biomarkers Prev. 2009;18:1695–1698. doi: 10.1158/1055-9965.EPI-09-0186. [DOI] [PubMed] [Google Scholar]
- 21.Dozois EJ, Boardman LA, Suwanthanma W, et al. Young-onset colorectal cancer in patients with no known genetic predisposition: can we increase early recognition and improve outcome? Medicine (Baltimore) 2008;87:259–263. doi: 10.1097/MD.0b013e3181881354. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Segev L, Kalady MF, Church JM. Left-Sided Dominance of Early-Onset Cancers: A Rationale for Screening Flexible Sigmoidoscopy in the Young. Dis Colon Rectum. 2018;61:897–902. doi: 10.1097/DCR.0000000000001062. [DOI] [PubMed] [Google Scholar]
- 23.Rodriguez L, Brennan K, Karim S, Nanji S, Patel SV, Booth CM. Disease Characteristics, Clinical Management, and Outcomes of Young Patients With Colon Cancer: A Population-based Study. Clin Colorectal Cancer. 2018;17:e651–e661. doi: 10.1016/j.clcc.2018.06.007. [DOI] [PubMed] [Google Scholar]
- 24.Lee J, Kim I, Kim JS, et al. Different clinical characteristics in sporadic young-age onset colorectal cancer. Medicine (Baltimore) 2016;95(37):e4840. doi: 10.1097/MD.0000000000004840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Chen FW, Sundaram V, Chew TA, Ladabaum U. Advanced-Stage Colorectal Cancer in Persons Younger Than 50 Years Not Associated With Longer Duration of Symptoms or Time to Diagnosis. Clin Gastroenterol Hepatol. 2017;15:728–737. doi: 10.1016/j.cgh.2016.10.038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Klos CL, Montenegro G, Jamal N, et al. Segmental versus extended resection for sporadic colorectal cancer in young patients. J Surg Oncol. 2014;110:328–32. doi: 10.1002/jso.23649. [DOI] [PubMed] [Google Scholar]