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. Author manuscript; available in PMC: 2011 Jun 8.
Published in final edited form as: J Natl Compr Canc Netw. 2009 Sep;7(8):883–894. doi: 10.6004/jnccn.2009.0058

The Challenges of Colorectal Cancer Survivorship

Crystal S Denlinger 1,, Andrea M Barsevick 2
PMCID: PMC3110673  NIHMSID: NIHMS292259  PMID: 19755048

Abstract

With advances in treatment, colorectal cancer is being transformed from a deadly disease to an illness that is increasingly curable. With this transformation has come increased interest in the unique problems, risks, needs, and concerns of survivors who have completed treatment and are cancer-free. Research has shown that physical and mental quality of life for colorectal cancer survivors was inferior when compared with age-matched individuals without cancer. Although issues and symptoms were most prominent during the first three years, long-term effects of treatment can persist and include fatigue, sleep difficulty, fear of recurrence, anxiety, depression, negative body image, sensory neuropathy, gastrointestinal problems, urinary incontinence, and sexual dysfunction. The unique challenges and issues of colorectal cancer survivors can and should be addressed by health care providers and the research community to ensure effective interventions and models of care to manage these problems. In this review, we discuss what is known about the long-term effects of colorectal cancer treatment on quality of life, the care of survivors, and existing models of survivorship care.

Keywords: Colorectal cancer, survivorship, quality of life, late effects, long-term effects


With advances in cancer prevention, early detection, and treatment, the population of cancer survivors in the United States is over 11 million and growing(1). However, colorectal cancer (CRC) remains the third most common cause of cancer and cancer death in both men and women, with an estimated 108,070 new cases of colon cancer and 40,740 new cases of rectal cancer, and an estimated 49,960 deaths attributed to colorectal cancer in 2008 (2). Over 90% of invasive colorectal cancers are diagnosed in patients over the age of 50, with 67% being diagnosed in patients over age 65, and CRC is the most common cancer diagnosis in patients over age 75 (3, 4).

Fortunately, the majority of patients will be diagnosed with local or regional disease, and may be candidates for curative therapy (3). Five-year survival rates for all stages of disease currently are 65% and 66% for colon and rectal cancer, respectively (2). This improvement in survival is likely due to earlier detection of tumors and improved therapy (5). The use of adjuvant 5-fluorouracil has resulted in an improvement in survival of approximately 30%, with an additional 20% improvement with the addition of oxaliplatin in stage III colon cancer (6, 7). The use of chemoradiotherapy in rectal cancer has resulted in improved survival and local control (8, 9).

With improved treatment comes the potential for late and long-term side effects that can affect quality of life. Long-term follow-up, health maintenance, and lifestyle modifications remain important components of the care of CRC survivors. Recommendations from the Institute of Medicine (Table 1) can shape a high quality approach to the care of cancer survivors (10). Because a significant proportion of individuals treated for CRC are likely to be cancer-free for longer intervals and potentially for the rest of their lives, this manuscript will focus on the survivor experience of those patients with stage I–III CRC who have completed primary treatment and have no evidence of disease. In this review, we will discuss quality of life after treatment, the late and long-term effects of treatment, lifestyle interventions, and models for the long-term care of CRC survivors.

Table 1.

Recommendations for the care of cancer survivors by the Institute of Medicine and National Research Council Committee on Cancer Survivorship (10)

1. Raise awareness of the needs of cancer survivors, establish cancer survivorship as a distinct phase of cancer care, and act to ensure the delivery of appropriate survivor care.
2. Provide a comprehensive care summary and follow-up plan, written by the providers who coordinated oncology treatment, that is clearly and effectly explained to the patient.
3. Develop and use evidence-based clinical practice guidelines, assessment tools, and screening instruments to identify and manage late effects of cancer and its treatment.
4. Develop quality of survivorship care measures and quality assurance programs to monitor and improve care received by survivors.
5.
6.
7.
8. Cancer survivors with short-term and long-term limitations in ability to work should be supported, while discrimination and adverse effects of cancer on employment should be actively eliminated.
9.
10.

Quality of Life and Psychosocial Issues

Quality of life (QOL), the subjective evaluation of one’s personal satisfaction with overall health and well-being, is an important outcome of cancer survivorship that includes physical, functional, psychological, and social functioning (11). Most reports of survivor QOL have focused on mixed groups of cancer diagnoses including CRC survivors. Mental and physical QOL was poorer for these mixed groups compared to age-matched individuals without cancer (12). The most prevalent concerns reported one year after diagnosis and treatment were fear of recurrence (68%), fatigue (67%), and sleep difficulties (48%) (13). When evaluated six and 12 months after diagnosis, more than 8% of survivors experienced distress that was severe enough to require follow-up (14). Long-term adult survivors had more physical limitations in sustained activities such as shopping, sports, and social events than individuals without cancer (53% versus 21%) (15). Gastrointestinal cancer survivors, including CRC, were found to be at higher risk for unemployment than healthy adults (48.8% versus 33.4%), while cancer survivors as a group had an almost 3-fold higher rate of disability causing unemployment compared to healthy controls (16).

Older adult cancer survivors were distinguished from older adults without cancer by more chronic conditions, poorer physical functioning, and poorer health ratings (17, 18). Older female long-term survivors reported more limitations of physical functioning such as inability to do housework, walk a half-mile, or walk up and down stairs compared to an age-matched group without cancer (19). Age, low income, symptom severity, and comorbidities were predictive of poorer physical functioning, perhaps due to cancer diagnosis, age, or some other combination of factors (12, 15, 18, 2024). Although elderly long-term survivors generally reported low levels of anxiety and depression overall, they had worse psychological outcomes and used more mental health services than individuals without cancer (2427). Thus, issues of CRC survivorship may be complicated by advancing age, as the age-adjusted rate of CRC for individuals over 65 years of age is more than three times higher than for persons aged 50–64 (3).

In contrast to other disease-based survivor populations, some studies have shown that CRC survivors report fewer physical problems and concerns (12, 2830) and that problems reported in the short-term generally improved within three years of diagnosis, with two thirds of survivors reporting no symptoms and less than 10% reporting more than two symptoms by four years after diagnosis (31, 32). The most commonly reported symptoms were fatigue (23%) and physical discomfort (19%), while stomachache was more frequent for survivors treated with chemotherapy (11% versus 3%), diarrhea more common after radiotherapy (24% versus 10%), and pain and cramping more prominent in those with ostomies (17% versus 5%) (32). Matched for age, long-term CRC survivors did not differ from their healthy counterparts with regard to physical functioning (15, 33). However, within the group of CRC survivors, increased age and number of comorbid conditions was associated with lower physical functioning (15).

A major limitation of research that includes both colon and rectal cancer survivor groups is that symptoms and problems averaged across groups with differences in diagnosis and treatment could lead to incorrect conclusions. For example, bowel symptoms tend to be more prominent for survivors of rectal rather than colon cancer due to more surgical techniques and therapies with long-term effects. The prevalence of rectal cancer is lower so averaging across both diagnoses could mask the severity of problems of rectal cancer survivors. Therefore, conclusions about symptom severity or quality of life are limited by differences in diagnosis and treatment between the two sites.

In a cross-sectional study of older CRC survivors, cohorts that were less than three years from diagnosis had lower overall QOL than cohorts that had been diagnosed more than three years previously; in all groups, QOL varied substantially across stages of disease (31). There was a trend for declining QOL in those with stage IV disease. Low income was associated with higher pain levels, difficulty ambulating, and lower social and emotional well-being. Pain remained a substantial problem that did not improve with time in this population. This population also had a high prevelance of comorbidities: 77% had one comorbid condition; 38% had two and 19% had three comorbid conditions. In another cross-sectional study of CRC survivors five or more years after diagnosis, a higher number of comorbid conditions was associated with poorer QOL (18). These results suggest that the physical and functional aspects of QOL improve three or more years after a CRC diagnosis for most survivors, but a small percentage continue to report distressing symptoms (Tables 2 and 3).

Table 2.

General Symptoms of Cancer Survivors (Not related to specific cancer or treatment)

Symptom Short-term (≤ 3 yrs post diagnosis) Long-term (> 3 yrs) Intervention

Fatigue 67% (13) 23% (32) NCCN Fatigue Guidelines (108)
ONS PEP Guidelines (109)

Sleep difficulty 48% (13) ONS PEP Guidelines (110)

Distress NCCN Distress Guidelines (35)
 • Anxiety 7% (14)
 • Depression 7% (14)
 • Negative feelings about body appearance 25% (32)
 • Fear of recurrence 67% (13)

Table 3.

Symptoms Most Common After Treatment of Rectal Cancer

Symptom Short-term (≤ 3 yrs post diagnosis) Long-term (> 3 yrs) Intervention

Stomach ache, cramping, pain 5% (32)

Bowel Dysfunction Antidiarrheal medication, bulk-forming agents (64)
 ▪ Clustering of BMs 42% (68)
 ▪ Night time BM 46% (68)
 ▪ Incontinence 39% (68) Diet modification: limit fats, meat, milk, raw vegetables, fiber (63, 70)
 ▪ Pad wearing 41% (68)
 ▪ Inability to defer BM 78% (68)
 ▪ Diarrhea (Schneider; Ramsey)
 ▪ Constipation (Schneider) 14%–49% (18, 32)
7% (32)

Urinary Incontinence (Surgery +/− Radiotherapy) 38% (74) Referral to Genito-urinary specialist
 • Difficulty bladder emptying 31% (74)
 • Need to void within 2 hrs 70% (41)
 • Pad wearing 57% (41)

Male Sexual Dysfunction * Sildenafil (80)
 • Loss of orgasm 50% (77)
 • General dysfunction 76% (75) Referral to Genito-urinary specialist
 • Erectile dysfunction 80% (75)
 • Ejaculatory problems 72% (75)
Female Sexual Dysfunction
 • General dysfunction 62% (75) * Vaginal Dilators (79, 81)
 • Dyspareunia 59% (75)
 • Vaginal dryness 57% (75) Referral to Genito-urinary specialist or Gynecologist
*

One or more positive small studies;

Efficacy not known

With regard to emotional status, depressive symptoms (measured by the CES-Depression Scale) of CRC survivors were not especially high at diagnosis and improved over the course of the first year after treatment (24). Survivors with more limitations of their daily social activities tended to be more depressed than those without limitations (24); those with better social networks consisting of more close friends and relatives as well as community involvement had better mental health outcomes (34). Despite low levels of depressive symptoms, 26–44% of long-term CRC survivors continued to worry about cancer recurrence, symptoms as cancer indicators, getting a second malignancy, or future diagnostic tests. Cancer-related health worries were associated with anxiety and depression, with 24% of the survivors reporting depression scores that were high enough to need evaluation for clinical depression (29). Thus, screening for psychological distress, depression, fatigue, and pain is warranted in all CRC survivors and may identify issues requiring intervention to improve their QOL after treatment (35).

The presence of a permanent stoma may affect QOL. Survivors with a permanent stoma who had been treated with radiotherapy followed by surgery for locally advanced rectal cancer reported improved bowel symptoms, fatigue, and pain compared to pretreatment levels (36). However, the presence of a stoma has also been associated with diminished body image and increased financial worries although global QOL was not affected (37, 38). Four years after treatment, survivors with a stoma were more likely to report negative feelings about body appearance at four years compared to non-stoma survivors (25% vs. 12% p=0.02) (32). Although social functioning one year after diagnosis was negatively impacted by the presence of a stoma (37, 39), follow-up over two years suggests that a permanent stoma did not have a durable impact on social functioning or activities of daily living (40, 41).

Late and Long-Term Effects of Treatment

Oxaliplatin-induced Peripheral Neuropathy

Recent studies of long-term CRC survivors have begun to address the late- and long-term effects of newer treatment regimens (Tables 3 and 4). Oxaliplatin-induced peripheral neuropathy has become a common and occasionally dose-limiting toxicity in the CRC survivor population, usually manifesting as sensory impairment of the peripheral nerves in a stocking-glove distribution. Symptoms of numbness, pain, paresthesias, dysesthesias, and changes in proprioception may affect fine motor skills such as writing, holding objects, buttoning shirts, picking up coins, and walking. Rarely, urinary retention and Lhermitte’s sign (electric-shock sensation shooting down spine with neck flexion) can occur (4244). Symptoms most commonly appear after cumulative doses of oxaliplatin exceeding 780 mg/m2, and are most likely due to oxaliplatin accumulation in the dorsal root ganglia with interference of calcium-dependent voltage-gated sodium channels by oxalate, a metabolite of oxaliplatin (42, 43, 4548).

Table 4.

Symptoms Due to Chemotherapy for Colorectal Cancer

Symptom Short-term (≤ 3 yrs post diagnosis) Long-term (> 3 yrs) Intervention
Sensory neuropathy (5FU & Oxaliplatin) 92% (49, 50) 12% (7) NSAIDs, opiods, referral to neurology (44)
*

One or more positive small studies;

Efficacy not known

In the adjuvant setting, up to 92% of survivors treated with oxaliplatin and infusional 5-fluororuacil (FOLFOX) or bolus 5-fluorouracil (FLOX) developed some degree of sensory neuropathy, with 8 to 12% developing severe neuropathy interfering with function (Grade 3) and 22% requiring premature discontinuation of oxaliplation for severe neuropathy (49, 50). While the majority of survivors have improvement or recovery of nerve function within 1 month of discontinuation of treatment, the median time to resolution of symptoms was approximately 9 months(51). Furthermore, 20% of survivors may experienced a worsening of their symptoms after treatment discontinuation and up to 12% had persistent symptoms four years after completion of adjuvant treatment (7, 51). Therefore, persistent numbess, tingling, and cold-induced pain may be a long-term problem in a small subset of survivors (52).

Measures to prevent or treat oxaliplatin-induced neuropathy are needed. In the metastatic setting, there is limited evidence that glutamine, reduced glutathione, alpha-lipoic acid, and oxycarbazepine may reduce the incidence and severity of sensory neuropathy while gabapentin and carbamazepine have not been shown to be effective (5358). A retrospective evaluation of calcium and magnesium infusions before and after oxaliplatin infusion suggested a reduction in chronic neuropathy without compromising chemotherapy efficacy, although randomized prospective studies have yet to confirm this (59, 60). In the adjuvant setting, the use of intravenous calcium gluconate and magnesium sulfate pre- and post- oxaliplatin infusion decreased the incidence of grade 2 neurotoxicity compared with placebo (28% vs. 58% p=0.01) (61), although the study was stopped prematurely due to initial concerns regarding lower tumor response with the same intervention in the metastatic setting (62). Non-steroidal anti-inflammatory medications, opioids, and referral to neurology or pain management for persistent symptoms may be useful, although their efficacy is unknown (44).

Bowel Dysfunction

Chronic diarrhea is reported by 13–50% of patients up to 10 years after treatment, with rectal cancer patients more likely than colon cancer patients to report diarrhea (24% vs. 10% p=0.04) (18, 32, 63). Diarrhea has been associated with limitations in activity and can negatively affect QOL (18, 32). Survivors who underwent an anterior resection reported a median of three bowel movements per day, frequency, urgency, evacuatory difficulties, and inability to differentiate stool and gas. These symptoms were most problematic during the first year after resection and were associated with fear, poor body image, and low self-confidence (38, 64).

Both preoperative and postoperative radiation for rectal cancer increases the risk of long-term bowel dysfunction. Preoperative short course radiation (5 Gray in 5 fractions) has been associated with a 2.5-fold higher rate of small bowel obstruction and 2-fold higher incidence of abdominal pain compared to those not treated in this manner (65) as well as increased bowel frequency and limitations in activities of daily living and social activities up to 5 years after treatment (41, 66). Postoperative radiation also results in frequent bowel movements similar to survivors who receive preoperative radiation and is associated up to five years after treatment with clustering of bowel movements (42%), increase in nighttime bowel movements (46%), incontinence (39%), pad wearing (41%), and inability to defer defecation (78%) (67, 68). Long-term anorectal dysfunction after radiation, including reduced reservoir capacity, can persist at 10 years (69).

Treatment for bowel problems after treatment for CRC typically includes anti-diarrheal medications, bulk-forming agents, use of undergarment pads, and diet manipulation (64). Elimination of specific foods (fats and oils, meat, milk products, raw vegetables, or fibrous foods) and the use of probiotic supplements has had limited benefit (63, 70). Attention to this issue is imperative as survivors may assume abnormal bowel symptoms are an inevitable consequence of treatment and may not address persistent symptoms at follow-up appointments (63, 71).

Pelvic Insufficiency Fractures after Radiation

Bone damage and risk of fractures may be increased after radiotherapy for rectal cancer. A large retrospective study of older women diagnosed with anal, cervical, or rectal cancer demonstrated a 65% increase in the cumulative incidence of pelvic fractures in rectal cancer survivors after radiation compared to nonirradiated patients (11.2% vs. 8.7% p<0.001), resulting in a possible increase in the absolute lifetime risk of fracture from 17% to 27%. The effect of radiation remained significant after controlling for other risk factors (72). The use of combined modality therapy may heighten the effect of radiation on bone density; medications and estrogen deficiency may further contribute to the risk of osteoporosis (73). Therefore, survivors who have received prior pelvic radiation should receive long-term monitoring of bone density, appropriate medical treatment of osteopenia and osteoporosis, and be carefully evaluated if symptoms suggesting fractures develop.

Urogenital Dysfunction

Urinary and sexual dysfunction are known complications of rectal cancer treatment, reported in at least 30% of patients undergoing definitive treatment (41, 7477). In studies of short course radiation followed by total mesorectal excision (TME) versus TME alone, symptoms at five years included urinary incontinence (38%), difficulties in bladder emptying (31%), need to void within two hours of voiding (70%), and need for protective pads (57%) (41, 74). Risk factors for postoperative incontinence included preoperative incontinence, being female, perioperative blood loss, preoperative bladder emptying difficulties, autonomic nerve damage, and presence of a permanent stoma (40, 41, 74). Severity of urinary incontinence increased with time, from 18% at 3 months to 31% at five years, and contributed to a lower overall perception of health status (41, 74).

While preservation of autonomic nerves during TME has been shown to minimize permanent sexual dysfunction, abdominoperineal resection has been associated with lower sexual function at 5 years compared to anterior resection (26% vs. 48% p=0.001) (38, 78). Males enrolled in a TME trial reported generalized sexual dysfunction (76.4%), erectile dysfunction (79.8%), and ejaculatory problems (72.2%) after surgery. Risk factors included preoperative radiation, presence of a stoma, perioperative blood loss, anastomotic leak, and autonomic nerve damage. Women reported an increase in generalized sexual dysfunction (62%), dyspareunia (59%), and vaginal dryness (56.6%) after treatment. Risk factors included preoperative radiation and the presence of a stoma (75). Vaginal stenosis can also occur after pelvic radiation and contribute to dyspareunia (79).

Few intervention trials have targeted urogenital dysfunction in rectal cancer survivors. A study of 32 men undergoing rectal resection for cancer or inflammatory bowel disease demonstrated that 79% of men receiving sildenafil reported reversal or satisfactory improvement in erectile dysfunction versus 13% receiving placebo (p=0.0009) (80). The use of vaginal dilators by women undergoing vaginal brachytherapy for cervical cancer has demonstrated benefit in maintaining vaginal patency, and dilators have been utilized empirically in rectal cancer survivors (79, 81).

Lifestyle and Behavior Interventions

While a careful assessment of QOL and treatment effects is an essential component of follow-up care for CRC, survivors are motivated to seek information on ways they can improve their outcomes, with informed choices especially important at the completion of treatment (82). Cancer survivors present unique opportunities to implement primary, secondary, and tertiary prevention strategies that may result in multiple beneficial outcomes (83). Many long-term survivors do not meet physical activity and dietary recommendations, and physicians can be powerful catalysts for promoting healthy behaviors (84, 85). In a prospective observational study of survivors with stage III colon cancer treated with adjuvant chemotherapy, Meyerhardt et al (86) demonstrated a 47% improvement in disease free survival (DFS) in those who engaged in at least 18 MET-hours per week of physical activity (6 or more hours per week of walking at an average pace) compared to inactive patients (less than 3 MET-hours per week) at a median follow-up of 2.7 years. Relapse-free (RFS) and overall survival (OS) were also improved. This effect was independent of other prognostic factors such as T stage, nodal status, treatment, performance status, age, or gender (86). In the Nurses’ Health Study, greater than 18 MET-hours per week of physical activity after a diagnosis of colorectal cancer was associated with reduced cancer-specific mortality and overall mortality. Those women who increased their level of physical activity after diagnosis had a significant improvement in colorectal cancer-specific and overall mortality in both stage I/II and stage III disease (87). Thus, physical activity may improve CRC-specific outcomes and prevent the development of other morbidities such as cardiovascular events and osteoporosis (82).

Body mass index (BMI) may predict outcome in CRC survivors (8890). Obese women had a significant increase in overall mortality but not in risk of colon cancer recurrence compared to normal weight women at a median follow-up of 9.4 years after adjuvant chemotherapy, a trend not seen in men (89). An evaluation of Dukes B and C colon cancer survivors who received adjuvant chemotherapy detected 27% increase in the risk of colon cancer recurrence or death, with a 38% excess risk of colon cancer events and a 51% excess risk of death before colon cancer or second primary cancer, among very obese (BMI ≥ 35 kg/m2) patients at a median follow-up of 11.2 years. Overall survival was also worse among very obese and underweight survivors (90). BMI and weight change after diagnosis in 1053 colon cancer survivors who received adjuvant chemotherapy was not associated with DFS, RFS or OS at a median follow-up of 5.3 years (91). Obese men with rectal cancer receiving adjuvant 5-FU and radiation were 61% more likely to have a local recurrence and 23% more likely to have an overall cancer recurrence compared to normal-weight men. Increasing BMI was also associated with a higher rate of abdominoperitoneal resection (92).

Visceral adiposity may be a better predictor of DFS, with those survivors exhibiting a visceral to subcutaneous fat ratio of greater than 50% having a significantly lower cumulative DFS rate compared to those with lower ratios in a small cohort of 161 patients (93). Thus, survivors should be counseled about the importance of weight control and exercise, which may reduce the risk of cancer recurrence and improve overall health status.

The role of diet, nutritional supplements, and tobacco use in preventing cancer recurrence is often a topic of interest to cancer survivors. In a prospective observational study of dietary patterns in 1009 colon cancer survivors who received adjuvant chemotherapy, higher intake of a Western diet pattern (high in meat, fat, refined grains, and dessert) was associated with a more than 3-fold decrease in DFS compared to those with the lowest intake of the same diet, with a similar decrease in relapse-free and overall survival. This association was independent of treatment group or other traditional prognostic factors. A prudent diet (high in fruits, vegetables, poultry, and fish) was not associated with cancer recurrence or mortality (94). Additional prospective cohort studies have shown lower overall and CRC-specific mortality with consistent aspirin use and high circulating levels of 25-hydroxyvitamin D (95, 96). Lifetime tobacco usage may also impact colon cancer recurrence, with trends toward lower DFS in survivors with a 20 pack-year or greater smoking history compared to never smokers (97). These studies provide hypotheses for further prospective investigation and possible interventions to improve outcomes in CRC survivors.

Promoting Quality Survivorship Care

Survivors must contend with risk of cancer recurrence, effects of cancer treatment, and non-cancer comorbidities. The majority of recurrences in stage II or III colon cancer occur within 3 years of diagnosis, with rates of recurrence declining with time (less than 1.5% at 5 years and 0.5% at 8 years) (98, 99). Non-cancer comorbidities may have more influence on overall QOL and long-term survival than the cancer diagnosis (100). Therefore, CRC survivor care should shift from surveillance for recurrence initially to management of comorbidities and receipt of appropriate preventive care long-term. With the majority of long-term survivors reporting at least one symptom attributed to previous cancer diagnosis or treatment and more than 70% of survivors having comorbid conditions, coordination of care is paramount for optimal care of cancer survivors to prevent functional decline and ensure receipt of necessary care for both cancer and non-cancer conditions (20).

Follow-up remains intensive after curative treatment for CRC, with increasing visits to primary care physicians (PCP) and decreasing visits to oncologists over time (101103). Although survivors followed only by a PCP did not perceive lower quality of care, PCPs reported significant uncertainty about surveillance protocols and side effects of treatments, and dissatisfaction with the transfer of care of survivors (102, 104). CRC survivors may receive less health behavior counseling and care for comorbid conditions compared to adults without cancer, and are more likely to experience an avoidable health outcome (100, 105). In addition, while receipt of preventive care is high in the early years after diagnosis, rates of preventive care received decreased after 5 years in CRC survivors (101). Survivors followed by both a PCP and an oncologist had the highest likelihood of receiving both preventive care (influenza vaccination, bone densitometry, and lipid monitoring), and cancer surveillance (colonoscopy, cervical cancer screening and mammography) (100, 101).

A shared model of care is ideal for survivorship care and may be facilitated by a survivorship care plan (106). In this plan, late effects (those that may occur in the future) and long-term effects (residual effects from treatment not expected to improve) can be delineated. The plan should be completed at the end of primary treatment by oncology providers, and include a summary of treatment received, a description of the plan for surveillance of cancer recurrence, ways to address the chronic physical and psychosocial effects of cancer, and necessary lifestyle and preventive care measures appropriate for the individual survivor (10, 107).

Conclusion

Survivorship is a distinct phase of colorectal cancer treatment. Goals of care include surveillance for recurrence, management of late and long-term toxicities associated with multimodality treatment, encouragement of healthy diet and lifestyle behaviors, and adherence to recommended preventive care guidelines. Coordination of care, including the use of a survivorship care plan, is paramount to ensuring longevity. Further research evaluating issues specific to CRC survivorship and potential interventions need to be a priority.

Acknowledgments

We would like to thank Drs. Yu-Ning Wong, Roger Cohen, and Paul Engstrom for guidance, review, and editorial comments in the preparation of this manuscript.

Footnotes

Conflicts of Interest: Dr. Denlinger receives research support from Merrimack Pharmaceuticals and Genentech, Inc.

Dr. Barsevick has no conflicts of interest or financial disclosures.

Contributor Information

Crystal S. Denlinger, Email: crystal.denlinger@fccc.edu, Department of Medical Oncology, Fox Chase Cancer Center, 333 Cottman Avenue, Philadelphia, PA 19111, Phone: (215) 728-2689, Fax: (215) 728-3639

Andrea M. Barsevick, Email: andrea.barsevick@fccc.edu, Department of Nursing, Fox Chase Cancer Center, 333 Cottman Avenue, Philadelphia, PA 19111, Phone: (215) 728-3578, Fax: (215) 728-2707.

References

  • 1.Rowland JH. What are cancer survivors telling us? Cancer J. 2008;14(6):361–8. doi: 10.1097/PPO.0b013e31818ec48e. [DOI] [PubMed] [Google Scholar]
  • 2.Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer Statistics, 2008. CA Cancer J Clin. 2008;58(2):71–96. doi: 10.3322/CA.2007.0010. [DOI] [PubMed] [Google Scholar]
  • 3.Rim SR, Seeff L, Ahmed F, King JB, Coughlin SS. Colorectal cancer incidence in the United States, 1999–2004. Cancer. 2009;115(9):1967–1976. doi: 10.1002/cncr.24216. [DOI] [PubMed] [Google Scholar]
  • 4.Edwards BK, Howe HL, Ries LAG, Thun MJ, Rosenberg HM, Yancik R, et al. Annual Report to the Nation on the status of cancer, 1973–1999, featuring implications of age and aging on U.S. cancer burden. Cancer. 2002;94(10):2766–2792. doi: 10.1002/cncr.10593. [DOI] [PubMed] [Google Scholar]
  • 5.Jemal A, Clegg LX, Ward E, Ries LAG, Wu X, Jamison PM, et al. Annual report to the nation on the status of cancer, 1975–2001, with a special feature regarding survival. Cancer. 2004;101(1):3–27. doi: 10.1002/cncr.20288. [DOI] [PubMed] [Google Scholar]
  • 6.Moertel C, Fleming T, Macdonald J, Haller D, Laurie J, Goodman P, et al. Levamisole and fluorouracil for adjuvant therapy of resected colon carcinoma. N Engl J Med. 1990;322(6):352–358. doi: 10.1056/NEJM199002083220602. [DOI] [PubMed] [Google Scholar]
  • 7.de Gramont A, Boni C, Navarro M, Tabernero J, Hickish J, Topham C, et al. Oxaliplatin/5FU/LV in adjuvant colon cancer: Updated efficacy results of the MOSAIC trial, including survival, with a median follow-up of six years. J Clin Oncol. 2007;25(18S):4007. [Google Scholar]
  • 8.Krook J, Moertel C, Gunderson L, Wieand H, Collins R, Beart R, et al. Effective surgical adjuvant therapy for high-risk rectal carcinoma. N Engl J Med. 1991;324(11):709–715. doi: 10.1056/NEJM199103143241101. [DOI] [PubMed] [Google Scholar]
  • 9.Sauer R, Becker H, Hohenberger W, Rodel C, Wittekind C, Fietkau R, et al. Preoperative versus Postoperative Chemoradiotherapy for Rectal Cancer. N Engl J Med. 2004;351(17):1731–1740. doi: 10.1056/NEJMoa040694. [DOI] [PubMed] [Google Scholar]
  • 10.Hewitt M, Greenfield S, Stovall E. From Cancer Patient to Cancer Survivor: Lost in Transition. Washington, D.C: The National Academies Press; 2006. [Google Scholar]
  • 11.Wilson IB, Cleary PD. Linking clinical variable with health-related quality of life. A conceptual model of patients outcomes. JAMA. 1995;273(1):59–65. [PubMed] [Google Scholar]
  • 12.Baker F, Haffer SC, Denniston M, Baker F, Haffer SC, Denniston M. Health-related quality of life of cancer and noncancer patients in Medicare managed care. Cancer. 2003;97(3):674–81. doi: 10.1002/cncr.11085. [DOI] [PubMed] [Google Scholar]
  • 13.Baker F, Denniston M, Smith T, West MM. Adult cancer survivors: how are they faring? Cancer. 2005;104(S11):2565–2576. doi: 10.1002/cncr.21488. [DOI] [PubMed] [Google Scholar]
  • 14.Lynch BM, Steginga SK, Hawkes AL, Pakenham KI, Dunn J, Lynch BM, et al. Describing and predicting psychological distress after colorectal cancer. Cancer. 2008;112(6):1363–70. doi: 10.1002/cncr.23300. [DOI] [PubMed] [Google Scholar]
  • 15.Stein KD, Syrjala KL, Andrykowski MA, Stein KD, Syrjala KL, Andrykowski MA. Physical and psychological long-term and late effects of cancer. Cancer. 2008;112(11 Suppl):2577–92. doi: 10.1002/cncr.23448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.de Boer AGEM, Taskila T, Ojajarvi A, van Dijk FJK, Verbeek JHAM. Cancer survivors and unemployment: a meta-analysis and meta-regression. JAMA. 2009;301(7):753–762. doi: 10.1001/jama.2009.187. [DOI] [PubMed] [Google Scholar]
  • 17.Hewitt M, Rowland JH, Yancik R, Hewitt M, Rowland JH, Yancik R. Cancer survivors in the United States: age, health, and disability. Journals of Gerontology Series A-Biological Sciences & Medical Sciences. 2003;58(1):82–91. doi: 10.1093/gerona/58.1.m82. [DOI] [PubMed] [Google Scholar]
  • 18.Ramsey SD, Berry K, Moinpour C, Giedzinska A, Andersen MR. Quality of life in long term survivors of colorectal cancer. Am J Gastroenterol. 2002;97(5):1228–1234. doi: 10.1111/j.1572-0241.2002.05694.x. [DOI] [PubMed] [Google Scholar]
  • 19.Sweeney C, Schmitz KH, Lazovich D, Virnig BA, Wallace RB, Folsom AR, et al. Functional limitations in elderly female cancer survivors. [see comment] Journal of the National Cancer Institute. 2006;98(8):521–9. doi: 10.1093/jnci/djj130. [DOI] [PubMed] [Google Scholar]
  • 20.Deimling GT, Sterns S, Bowman KF, Kahana B. Functioning and Activity Participation Restrictions among Older Adult, Long-Term Cancer Survivors. Cancer Investigation. 2007;25(2):106–116. doi: 10.1080/07357900701224813. [DOI] [PubMed] [Google Scholar]
  • 21.Given CW, Given B, Azzouz F, Stommel M, Kozachik S. Comparison of changes in physical functioning of elderly patients with new diagnoses of cancer. Medical Care. 2000;38(5):482–93. doi: 10.1097/00005650-200005000-00005. [DOI] [PubMed] [Google Scholar]
  • 22.Given BA, Given C, Azzouz F, Stommel M. Physical functioning of elderly cancer patients prior to diagnosis and following initial treatment. Nurs Res. 2001;50(4):222–32. doi: 10.1097/00006199-200107000-00006. [DOI] [PubMed] [Google Scholar]
  • 23.Deimling GT, Bowman KF, Wagner LJ, Deimling GT, Bowman KF, Wagner LJ. The effects of cancer-related pain and fatigue on functioning of older adult, long-term cancer survivors. Cancer Nursing. 2007;30(6):421–33. doi: 10.1097/01.NCC.0000300168.88089.2b. [DOI] [PubMed] [Google Scholar]
  • 24.Kurtz ME, Kurtz JC, Stommel M, Given CW, Given B. Predictors of depressive symptomatology of geriatric patients with colorectal cancer: a longitudinal view. Supportive Care in Cancer. 2002;10(6):494–501. doi: 10.1007/s00520-001-0338-8. [DOI] [PubMed] [Google Scholar]
  • 25.Robb C, Haley WE, Balducci L, Extermann M, Perkins EA, Small BJ, et al. Impact of breast cancer survivorship on quality of life in older women. Critical Reviews in Oncology-Hematology. 2007;62(1):84–91. doi: 10.1016/j.critrevonc.2006.11.003. [DOI] [PubMed] [Google Scholar]
  • 26.Hewitt M, Rowland JH, Hewitt M, Rowland JH. Mental health service use among adult cancer survivors: analyses of the National Health Interview Survey. J Clin Oncol. 2002;20(23):4581–90. doi: 10.1200/JCO.2002.03.077. [DOI] [PubMed] [Google Scholar]
  • 27.Mullens AB, McCaul KD, Erickson SC, Sandgren AK, Mullens AB, McCaul KD, et al. Coping after cancer: risk perceptions, worry, and health behaviors among colorectal cancer survivors. Psycho-Oncology. 2004;13(6):367–76. doi: 10.1002/pon.751. [DOI] [PubMed] [Google Scholar]
  • 28.Deimling GT, Sterns S, Bowman KF, Kahana B. The health of older-adult, long-term cancer survivors. Cancer Nursing. 2005;28(6):415–424. doi: 10.1097/00002820-200511000-00002. [DOI] [PubMed] [Google Scholar]
  • 29.Deimling GT, Wagner LJ, Bowman KF, Sterns S, Kercher K, Kahana B, et al. Coping among older-adult, long-term cancer survivors. Psycho-Oncology. 2006;15(2):143–59. doi: 10.1002/pon.931. [DOI] [PubMed] [Google Scholar]
  • 30.Stommel M, Kurtz ME, Kurtz JC, Given CW, Given BA. A longitudinal analysis of the course of depressive symptomatology in geriatric patients with cancer of the breast, colon, lung, or prostate. Health Psychology. 2004;23:564–73. doi: 10.1037/0278-6133.23.6.564. [DOI] [PubMed] [Google Scholar]
  • 31.Ramsey SD, Andersen MR, Etzioni R, Moinpour C, Peacock S, Potosky A, et al. Quality of life in survivors of colorectal carcinoma. Cancer. 2000;88(6):1294–303. [PubMed] [Google Scholar]
  • 32.Schneider EC, Malin JLK, KL, Ko CY, Adams J, Epstein AM. Surviving colorectal cancer: patient-reported symptoms 4 years after diagnosis. Cancer. 2007;110(9):2075–2082. doi: 10.1002/cncr.23021. [DOI] [PubMed] [Google Scholar]
  • 33.Trentham-Dietz A, Remington PL, moinpour CM, Hampton JM, Sapp AL, Newcomb PA. Health-related quality of life in female long-term colorectal cancer survivors. The Oncologist. 2003;8:342–349. doi: 10.1634/theoncologist.8-4-342. [DOI] [PubMed] [Google Scholar]
  • 34.Sapp AL, Trentham-Dietz A, Newcomb PA, Hampton JM, Moinpour CM, Remington PL. Social networks and quality of life among female long-term colorectal cancer survivors. Cancer. 2003;98:1749–1758. doi: 10.1002/cncr.11717. [DOI] [PubMed] [Google Scholar]
  • 35.NCCN. Practice Guidelines in Oncology. Distress Managment. 2008;1 [Google Scholar]
  • 36.Allal AS, Gervaz P, Gertsch P, Bernier J, Roth AD, Morel P, et al. Assessment of quality of life in patients with rectal cancer treated by preoperative radiotherapy: A longitudinal prospective study. International Journal of Radiation Oncology*Biology*Physics. 2005;61(4):1129–1135. doi: 10.1016/j.ijrobp.2004.07.726. [DOI] [PubMed] [Google Scholar]
  • 37.Sideris L, Zenasni F, Vernerey D, Dauchy S, Lasser P, Pignon J-P, et al. Quality of Life of Patients Operated on for Low Rectal Cancer: Impact of the Type of Surgery and Patients’ Characteristics. Diseases of the Colon & Rectum. 2005;48(12):2180–2191. doi: 10.1007/s10350-005-0155-0. [DOI] [PubMed] [Google Scholar]
  • 38.Guren MG, Eriksen MT, Wiig JN, Carlsen E, Nesbakken A, Sigurdsson HK, et al. Quality of life and functional outcome following anterior or abdominoperineal resection for rectal cancer. European Journal of Surgical Oncology. 2005;31(7):735–742. doi: 10.1016/j.ejso.2005.05.004. [DOI] [PubMed] [Google Scholar]
  • 39.Arndt V, Merx H, Stegmaier C, Ziegler H, Brenner H. Quality of Life in Patients With Colorectal Cancer 1 Year After Diagnosis Compared With the General Population: A Population-Based Study. J Clin Oncol. 2004;22(23):4829–4836. doi: 10.1200/JCO.2004.02.018. [DOI] [PubMed] [Google Scholar]
  • 40.Rauch P, Miny J, Conroy T, Neyton L, Guillemin F. Quality of Life Among Disease-Free Survivors of Rectal Cancer. J Clin Oncol. 2004;22(2):354–360. doi: 10.1200/JCO.2004.03.137. [DOI] [PubMed] [Google Scholar]
  • 41.Peeters KCMJ, van de Velde CJH, Leer JWH, Martijn H, Junggeburt JMC, Kranenbarg EK, et al. Late Side Effects of Short-Course Preoperative Radiotherapy Combined With Total Mesorectal Excision for Rectal Cancer: Increased Bowel Dysfunction in Irradiated Patients--A Dutch Colorectal Cancer Group Study. J Clin Oncol. 2005;23(25):6199–6206. doi: 10.1200/JCO.2005.14.779. [DOI] [PubMed] [Google Scholar]
  • 42.Cersosimo RJ. Oxaliplatin-associated neuropathy: a review. The Annals of Pharmacology. 2005;39:128–135. doi: 10.1345/aph.1E319. [DOI] [PubMed] [Google Scholar]
  • 43.Grothey A. Oxaliplatin-safety profile: neurotoxicity. Seminars in Oncology. 2003;30(4):5–13. doi: 10.1016/s0093-7754(03)00399-3. [DOI] [PubMed] [Google Scholar]
  • 44.Kaley TJ, DeAngelis LM. Therapy of chemotherapy-induced peripheral neuropathy. British Journal of Haematology. 2009 doi: 10.1111/j.1365-2141.2008.07558.x. [DOI] [PubMed] [Google Scholar]
  • 45.Cavaletti G, Petruccioli MG, Marmiroli P, Rigolio R, Galbiati S, Zoia C, et al. Circulating nerve growth factor levels changes during oxaliplatin treatment-induced neurotoxicity in the rat. Anticancer Research. 2002;22(6C):4199–4204. [PubMed] [Google Scholar]
  • 46.Gamelin L, Capitain O, Morel A, Dumont A, Traore S, Anne LB, et al. Predictive Factors of Oxaliplatin Neurotoxicity: The Involvement of the Oxalate Outcome Pathway. Clin Cancer Res. 2007;13(21):6359–6368. doi: 10.1158/1078-0432.CCR-07-0660. [DOI] [PubMed] [Google Scholar]
  • 47.Grolleau F, Gamelin L, Boisdron-Celle M, Lapied B, Pelhate M, Gamelin E. A Possible Explanation for a Neurotoxic Effect of the Anticancer Agent Oxaliplatin on Neuronal Voltage-Gated Sodium Channels. J Neurophysiol. 2001;85(5):2293–2297. doi: 10.1152/jn.2001.85.5.2293. [DOI] [PubMed] [Google Scholar]
  • 48.Park SB, Goldstein D, Lin CS-Y, Krishnan AV, Friedlander ML, Kiernan MC. Acute Abnormalities of Sensory Nerve Function Associated With Oxaliplatin-Induced Neurotoxicity. J Clin Oncol. 2009;27(8):1243–1249. doi: 10.1200/JCO.2008.19.3425. [DOI] [PubMed] [Google Scholar]
  • 49.Andre T, Boni C, Mounedji-Boudiaf L, Navarro M, Tabernero J, Hickish T, et al. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N Engl J Med. 2004;350(23):2343–2351. doi: 10.1056/NEJMoa032709. [DOI] [PubMed] [Google Scholar]
  • 50.Kuebler JP, Wieand S, O’Connell MJ, Smith RE, Colangelo LH, Yothers G, et al. Oxaliplatin combined with weekly bolus fluorouracil and leucovorin as surgical adjuvant chemotherapy for stage II and III colon cancer: results from NSABP C-07. J Clin Oncol. 2007;25(16):2198–2204. doi: 10.1200/JCO.2006.08.2974. [DOI] [PubMed] [Google Scholar]
  • 51.Land SR, Kopec JA, Cecchini RS, Ganz PA, Weiand S, Colangelo LH, et al. Neurotoxicity from oxaliplatin combined with weekly bolus fluorouracil and leucovorin as surgical adjuvant chemotherapy for stage II and III colon cancer: NSABP C-07. J Clin Oncol. 2007;25(16):2205–2211. doi: 10.1200/JCO.2006.08.6652. [DOI] [PubMed] [Google Scholar]
  • 52.Yothers G, Land SR, Ganz PA, Fehrenbacher L, Giguere JK, Wickerham DL, et al. Neurotoxicity (NT) in colon cancer (CC) survivors from NSABP Protocol C-07 comparing 5-FU + leucovorin (FULV) with the same regimen + oxaliplatin (FLOX): Preliminary results from NSABP Protocol LTS-01. J Clin Oncol (Meeting Abstracts) 2008;26(15_suppl):9575. [Google Scholar]
  • 53.Wang W-S, Lin J-K, Lin T-C, Chen W-S, Jiang J-K, Wang H-S, et al. Oral Glutamine Is Effective for Preventing Oxaliplatin-Induced Neuropathy in Colorectal Cancer Patients. Oncologist. 2007;12(3):312–319. doi: 10.1634/theoncologist.12-3-312. [DOI] [PubMed] [Google Scholar]
  • 54.Cascinu S, Catalano V, Cordella L, Labianca R, Giordani P, Baldelli AM, et al. Neuroprotective Effect of Reduced Glutathione on Oxaliplatin-Based Chemotherapy in Advanced Colorectal Cancer: A Randomized, Double-Blind, Placebo-Controlled Trial. J Clin Oncol. 2002;20(16):3478–3483. doi: 10.1200/JCO.2002.07.061. [DOI] [PubMed] [Google Scholar]
  • 55.Gedlicka C, Scheithauer W, Schull B, Kornek GV. Effective Treatment of Oxaliplatin-Induced Cumulative Polyneuropathy With Alpha-Lipoic Acid. J Clin Oncol. 2002;20(15):3359–3361. doi: 10.1200/JCO.2002.99.502. [DOI] [PubMed] [Google Scholar]
  • 56.Argyriou AA, Chroni E, Polychronopoulos P, Iconomou G, Koutras A, Makatsoris T, et al. Efficacy of oxcarbazepine for porphylaxis against cumulative oxaliplatin-induced neuropathy. Neurology. 2006;67:2253–2255. doi: 10.1212/01.wnl.0000249344.99671.d4. [DOI] [PubMed] [Google Scholar]
  • 57.Mitchell P, Goldstein D, Michael M, Beale P, Friedlander M, Zalcberg J, et al. Addition of Gabapentin to a Modified FOLFOX Regimen Does Not Reduce Oxaliplatin-Induced Neurotoxicity. Clinical Colorectal Cancer. 2006;6(2):146–151. doi: 10.3816/CCC.2006.n.032. [DOI] [PubMed] [Google Scholar]
  • 58.von Delius S, Eckel F, Wagenpfeil S, Mayr M, Stock K, Kullmann F, et al. Carbamazepine for prevention of oxaliplatin-related neurotoxicity in patients with advanced colorectal cancer: Final results of a randomised, controlled, multicenter phase II study. Investigational New Drugs. 2007;25(2):173–180. doi: 10.1007/s10637-006-9010-y. [DOI] [PubMed] [Google Scholar]
  • 59.Gamelin L, Boisdron-Celle M, Delva R, Guerin-Meyer V, Ifrah N, Morel A, et al. Prevention of Oxaliplatin-Related Neurotoxicity by Calcium and Magnesium Infusions: A Retrospective Study of 161 Patients Receiving Oxaliplatin Combined with 5-Fluorouracil and Leucovorin for Advanced Colorectal Cancer. Clin Cancer Res. 2004;10(12):4055–4061. doi: 10.1158/1078-0432.CCR-03-0666. [DOI] [PubMed] [Google Scholar]
  • 60.Hochster HS, Grothey A, Shpilsky A, Childs BH. Effect of intravenous (IV) calcium and magnesium (Ca/Mg) versus placebo on response to FOLFOX+bevacizumab (BEV) in the CONcePT trial. ASCO Gastrointestinal Cancers Symposium; Orlando, FL. 2008. [Google Scholar]
  • 61.Nikcevich DA, Grothey A, Sloan JA, Kugler JW, Silberstein PT, Dentchev T, et al. Effect of intravenous calcium and magnesium (IV CaMg) on oxaliplatin-induced sensory neurotoxicity (sNT) in adjuvant colon cancer: Results of the phase III placebo-controlled, double-blind NCCTG trial N04C7. J Clin Oncol (Meeting Abstracts) 2008;26(15_suppl):4009. [Google Scholar]
  • 62.Hochster HS, Grothey A, Childs BH. Use of Calcium and Magnesium Salts to Reduce Oxaliplatin-Related Neurotoxicity. J Clin Oncol. 2007;25(25):4028–4029. doi: 10.1200/JCO.2007.13.5251. [DOI] [PubMed] [Google Scholar]
  • 63.Gami B, Harrington K, Blake P, Dearnaley D, Tait D, Davies J, et al. How patients manage gastrointestinal symptoms after pelvic radiotherapy. Alimentary Pharmacology and Therapeutics. 2003;18(10):987–994. doi: 10.1046/j.1365-2036.2003.01760.x. [DOI] [PubMed] [Google Scholar]
  • 64.DeSnoo L, Faithfull S. A qualitative study of anterior resection syndrome: the experiences of cancer survivors who have undergone resection surgery. European Journal of Cancer Care. 2006;15(3):244–251. doi: 10.1111/j.1365-2354.2005.00647.x. [DOI] [PubMed] [Google Scholar]
  • 65.Birgisson H, Påhlman L, Gunnarsson U, Glimelius B. Late gastrointestinal disorders after rectal cancer surgery with and without preoperative radiation therapy. British Journal of Surgery. 2008;95(2):206–213. doi: 10.1002/bjs.5918. [DOI] [PubMed] [Google Scholar]
  • 66.Dahlberg M, Glimelius B, Graf W, Påhlman L. Preoperative irradiation affects functional results after surgery for rectal cancer. Diseases of the Colon & Rectum. 1998;41(5):543–549. doi: 10.1007/BF02235256. [DOI] [PubMed] [Google Scholar]
  • 67.Hassan I, Larson D, Cima R, Gaw J, Chua H, Hahnloser D, et al. Long-Term Functional and Quality of Life Outcomes After Coloanal Anastomosis for Distal Rectal Cancer. Diseases of the Colon & Rectum. 2006;49(9):1266–1274. doi: 10.1007/s10350-006-0640-0. [DOI] [PubMed] [Google Scholar]
  • 68.Kollmorgen CF, Meagher AP, Wolff BG, Pemberton JH, Martenson JA, Ilstrup DM. The long-term effect of adjuvant postoperative chemoradiotherapy for rectal carcinoma on bowel function. Annals of Surgery. 1994;220(5):676–682. doi: 10.1097/00000658-199411000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Lundby L, Krogh K, Jensen VJ, Gandrup P, Qvist N, Overgaard J, et al. Long-Term Anorectal Dysfunction After Postoperative Radiotherapy for Rectal Cancer. Diseases of the Colon & Rectum. 2005;48(7):1343–1352. doi: 10.1007/s10350-005-0049-1. [DOI] [PubMed] [Google Scholar]
  • 70.McGough C, Baldwin C, Frost G, Andreyev HJN. Role of nutritional intervention in patients treated with radiotherapy for pelvic malignancy. Br J Cancer. 2004;90(12):2278–2287. doi: 10.1038/sj.bjc.6601868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Andreyev J. Gastrointestinal complications of pelvic radiotherapy: are they of any importance? Gut. 2005;54(8):1051–1054. doi: 10.1136/gut.2004.062596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Baxter NN, Habermann EB, Tepper JE, Durham SB, Virnig BA. Risk of Pelvic Fractures in Older Women Following Pelvic Irradiation. JAMA. 2005;294(20):2587–2593. doi: 10.1001/jama.294.20.2587. [DOI] [PubMed] [Google Scholar]
  • 73.Small W, Jr, Kachnic L. Postradiotherapy Pelvic Fractures: Cause for Concern or Opportunity for Future Research? JAMA. 2005;294(20):2635–2637. doi: 10.1001/jama.294.20.2635. [DOI] [PubMed] [Google Scholar]
  • 74.Lange MM, Maas CP, Marijnen CAM, Wiggers T, Rutten HJ, Klein Kranenbarg E, et al. Urinary dysfunction after rectal cancer treatment is mainly caused by surgery. British Journal of Surgery. 2008;95(8):1020–1028. doi: 10.1002/bjs.6126. [DOI] [PubMed] [Google Scholar]
  • 75.Lange MM, Marijnen CAM, Maas CP, Putter H, Rutten HJ, Stiggelbout AM, et al. Risk factors for sexual dysfunction after rectal cancer treatment. European Journal of Cancer. doi: 10.1016/j.ejca.2008.12.014. In Press, Corrected Proof. [DOI] [PubMed] [Google Scholar]
  • 76.Pollack J, Holm T, Cedermark B, Altman D, Holmström B, Glimelius B, et al. Late adverse effects of short-course preoperative radiotherapy in rectal cancer. British Journal of Surgery. 2006;93(12):1519–1525. doi: 10.1002/bjs.5525. [DOI] [PubMed] [Google Scholar]
  • 77.Mannaerts GHH, Schijven MP, Hendrikx A, Martijn H, Rutten HJT, Wiggers T. Urologic and sexual morbidity following multimodality treatment for locally advanced primary and locally recurrent rectal cancer. European Journal of Surgical Oncology. 2001;27(3):265–272. doi: 10.1053/ejso.2000.1099. [DOI] [PubMed] [Google Scholar]
  • 78.Havenga K, Enker WE, McDermott K, Cohen AM, Minsky BD, Guillem J. Male and female sexual and urinary function after total mesorectal excision with autonomic nerve preservation for carcinoma of the rectum. Journal of the American College of Surgeons. 1996;182(6):495–502. [PubMed] [Google Scholar]
  • 79.Wolf JK. Prevention and treatment of vaginal stenosis resulting from pelvic radiation therapy. Community Oncology. 2006;3(10):665–671. [Google Scholar]
  • 80.Lindsey I, George B, Kettlewell M, Mortensen N. Randomized, double-blind, placebo-controlled trial of sildenafil (Viagra) for erectile dysfunction after rectal excision for cancer and inflammatory bowel disease. Diseases of the Colon & Rectum. 2002;45(6):727–732. doi: 10.1007/s10350-004-6287-9. [DOI] [PubMed] [Google Scholar]
  • 81.Decruze SB, Guthrie D, Magnani R. Prevention of vaginal stenosis in patients following vaginal brachytherapy. Clinical Oncology. 1999;11(1):46–48. doi: 10.1053/clon.1999.9008. [DOI] [PubMed] [Google Scholar]
  • 82.Brown JK, Byers T, Doyle C, Courneya KS, Demark-Wahnefried W, Kushi LH, et al. Nutrition and Physical Activity During and After Cancer Treatment: An American Cancer Society Guide for Informed Choices. CA Cancer J Clin. 2003;53(5):268–291. doi: 10.3322/canjclin.53.5.268. [DOI] [PubMed] [Google Scholar]
  • 83.Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM. Riding the Crest of the Teachable Moment: Promoting Long-Term Health After the Diagnosis of Cancer. J Clin Oncol. 2005;23(24):5814–5830. doi: 10.1200/JCO.2005.01.230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Blanchard CM, Courneya KS, Stein K. Cancer Survivors’ Adherence to Lifestyle Behavior Recommendations and Associations With Health-Related Quality of Life: Results From the American Cancer Society’s SCS-II. J Clin Oncol. 2008;26(13):2198–2204. doi: 10.1200/JCO.2007.14.6217. [DOI] [PubMed] [Google Scholar]
  • 85.Jones LW, Courneya KS, Fairey AS. Effects of an oncologist’s recommendation to exercise on self-reported exercise behavior in newly diagnosed breast cancer survivors: a single-blind, randomized controlled trial. Ann Behav Med. 2004;28:105–113. doi: 10.1207/s15324796abm2802_5. [DOI] [PubMed] [Google Scholar]
  • 86.Meyerhardt JA, Heseltine D, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, et al. Impact of Physical Activity on Cancer Recurrence and Survival in Patients With Stage III Colon Cancer: Findings From CALGB 89803. J Clin Oncol. 2006;24(22):3535–3541. doi: 10.1200/JCO.2006.06.0863. [DOI] [PubMed] [Google Scholar]
  • 87.Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, Colditz GA, et al. Physical Activity and Survival After Colorectal Cancer Diagnosis. J Clin Oncol. 2006;24(22):3527–3534. doi: 10.1200/JCO.2006.06.0855. [DOI] [PubMed] [Google Scholar]
  • 88.Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, Obesity, and Mortality from Cancer in a Prospectively Studied Cohort of U.S. Adults. N Engl J Med. 2003;348(17):1625–1638. doi: 10.1056/NEJMoa021423. [DOI] [PubMed] [Google Scholar]
  • 89.Meyerhardt JA, Catalano PJ, Haller DG, Mayer RJ, Benson AB, Macdonald JS, et al. Influence of body mass index on outcomes and treatment-related toxicity in patients with colon carcinoma. Cancer. 2003;98(3):484–495. doi: 10.1002/cncr.11544. [DOI] [PubMed] [Google Scholar]
  • 90.Dignam JJ, Polite BN, Yothers G, Raich P, Colangelo L, O’Connell MJ, et al. Body Mass Index and Outcomes in Patients Who Receive Adjuvant Chemotherapy for Colon Cancer. J Natl Cancer Inst. 2006;98(22):1647–1654. doi: 10.1093/jnci/djj442. [DOI] [PubMed] [Google Scholar]
  • 91.Meyerhardt JA, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, Nelson H, et al. Impact of Body Mass Index and Weight Change After Treatment on Cancer Recurrence and Survival in Patients With Stage III Colon Cancer: Findings From Cancer and Leukemia Group B 89803. J Clin Oncol. 2008;26(25):4109–4115. doi: 10.1200/JCO.2007.15.6687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Meyerhardt JA, Tepper JE, Niedzwiecki D, Hollis DR, McCollum AD, Brady D, et al. Impact of Body Mass Index on Outcomes and Treatment-Related Toxicity in Patients With Stage II and III Rectal Cancer: Findings From Intergroup Trial 0114. J Clin Oncol. 2004;22(4):648–657. doi: 10.1200/JCO.2004.07.121. [DOI] [PubMed] [Google Scholar]
  • 93.Moon H, Ju Y, Jeong C, Jung E, Lee Y, Hong S, et al. Visceral obesity may affect oncologic outcome in patients with colorectal cancer. Annals of Surgical Oncology. 2008;15(7):1918–1922. doi: 10.1245/s10434-008-9891-4. [DOI] [PubMed] [Google Scholar]
  • 94.Meyerhardt JA, Niedzwiecki D, Hollis D, Saltz LB, Hu FB, Mayer RJ, et al. Association of Dietary Patterns With Cancer Recurrence and Survival in Patients With Stage III Colon Cancer. JAMA. 2007;298(7):754–764. doi: 10.1001/jama.298.7.754. [DOI] [PubMed] [Google Scholar]
  • 95.Fuchs C, Meyerhardt JA, Heseltine DL, Niedzwiecki D, Hollis D, Chan AT, et al. Influence of regular aspirin use on survival for patients with stage III colon cancer: Findings from Intergroup trial CALGB 89803. J Clin Oncol (Meeting Abstracts) 2005;23(16_suppl):3530. [Google Scholar]
  • 96.Ng K, Meyerhardt JA, Wu K, Feskanich D, Hollis BW, Giovannucci EL, et al. Circulating 25-Hydroxyvitamin D Levels and Survival in Patients With Colorectal Cancer. J Clin Oncol. 2008;26(18):2984–2991. doi: 10.1200/JCO.2007.15.1027. [DOI] [PubMed] [Google Scholar]
  • 97.Jackson NA, Fuchs CS, Niedzwiecki D, Hollis DR, Saltz LB, Mayer RJ, et al. The impact of smoking on cancer recurrence and survival in patients with stage III colon cancer: Findings from intergroup trial CALGB 89803. J Clin Oncol (Meeting Abstracts) 2008;26(15_suppl):4039. [Google Scholar]
  • 98.Sargent DJ, Patiyil S, Yothers G, Haller DG, Gray R, Benedetti J, et al. End Points for Colon Cancer Adjuvant Trials: Observations and Recommendations Based on Individual Patient Data From 20,898 Patients Enrolled Onto 18 Randomized Trials From the ACCENT Group. J Clin Oncol. 2007;25(29):4569–4574. doi: 10.1200/JCO.2006.10.4323. [DOI] [PubMed] [Google Scholar]
  • 99.Sargent D, Sobrero A, Grothey A, O’Connell MJ, Buyse M, Andre T, et al. Evidence for Cure by Adjuvant Therapy in Colon Cancer: Observations Based on Individual Patient Data From 20,898 Patients on 18 Randomized Trials. J Clin Oncol. 2009;27(6):872–877. doi: 10.1200/JCO.2008.19.5362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 100.Earle CC, Neville BA. Under use of necessary care among cancer survivors. Cancer. 2004;101:1712–1719. doi: 10.1002/cncr.20560. [DOI] [PubMed] [Google Scholar]
  • 101.Snyder CF, Earle CC, Herbert RJ, Neville BA, Blackford AL, Frick KD. Preventive Care for Colorectal Cancer Survivors: A 5-Year Longitudinal Study. J Clin Oncol. 2008;26(7):1073–1079. doi: 10.1200/JCO.2007.11.9859. [DOI] [PubMed] [Google Scholar]
  • 102.Haggstrom D, Arora N, Oakley-Girvan I. Primary and subspecialty care models of follow-up care delivery among colorectal cancer survivors. J Clin Oncol (Meeting Abstracts) 2008;26(15_suppl):6540. [Google Scholar]
  • 103.Snyder C, Earle C, Herbert R, Neville B, Blackford A, Frick K. Trends in Follow-up and Preventive Care for Colorectal Cancer Survivors. Journal of General Internal Medicine. 2008;23(3):254–259. doi: 10.1007/s11606-007-0497-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Nissen MJ, Beran MS, Lee MW, Mehta SR, Pine DA, Swenson KK. Views of primary care physicians on follow-up care of cancer patients. Family Medicine. 2007;39(7):477–482. [PubMed] [Google Scholar]
  • 105.Sabatino SA, Coates RJ, Uhler RJ, Pollack LA, Alley LG, Zauderer LJ. Provider Counseling About Health Behaviors Among Cancer Survivors in the United States. J Clin Oncol. 2007;25(15):2100–2106. doi: 10.1200/JCO.2006.06.6340. [DOI] [PubMed] [Google Scholar]
  • 106.Oeffinger KC, McCabe MS. Models for Delivering Survivorship Care. J Clin Oncol. 2006;24(32):5117–5124. doi: 10.1200/JCO.2006.07.0474. [DOI] [PubMed] [Google Scholar]
  • 107.Earle CC. Failing to Plan Is Planning to Fail: Improving the Quality of Care With Survivorship Care Plans. J Clin Oncol. 2006;24(32):5112–5116. doi: 10.1200/JCO.2006.06.5284. [DOI] [PubMed] [Google Scholar]
  • 108.NCCN. Cancer-Related Fatigue. Vol. 1. 2009. Practice Guidelines in Oncology. [Google Scholar]
  • 109.Mitchell SA, Beck SL, Hood LE, Moore K, Tanner ER. Putting evidence into practice: evidence-based interventions for fatigue during and following cancer and its treatment. Clinical Journal of Oncology Nursing. 2007;11(1):99–113. doi: 10.1188/07.CJON.99-113. [DOI] [PubMed] [Google Scholar]
  • 110.Page MS, Berger AM, Johnson LB. Putting evidence into practice: evidence-based interventions for sleep-wake disturbances. Clinical Journal of Oncology Nursing. 2006;10(6):753–767. doi: 10.1188/06.CJON.753-767. [DOI] [PubMed] [Google Scholar]

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