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    Gut and Liver is an international journal of gastroenterology, focusing on the gastrointestinal tract, liver, biliary tree, pancreas, motility, and neurogastroenterology. Gut atnd Liver delivers up-to-date, authoritative papers on both clinical and research-based topics in gastroenterology. The Journal publishes original articles, case reports, brief communications, letters to the editor and invited review articles in the field of gastroenterology. The Journal is operated by internationally renowned editorial boards and designed to provide a global opportunity to promote academic developments in the field of gastroenterology and hepatology. +MORE

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    Yong Chan Lee Professor of Medicine
    Director, Gastrointestinal Research Laboratory
    Veterans Affairs Medical Center, Univ. California San Francisco
    San Francisco, USA

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    Jong Pil Im Seoul National University College of Medicine, Seoul, Korea
    Robert S. Bresalier University of Texas M. D. Anderson Cancer Center, Houston, USA
    Steven H. Itzkowitz Mount Sinai Medical Center, NY, USA
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Colorectal Cancer Screening and Surveillance in the Elderly: Updates and Controversies

Lukejohn W. Day*, and Fernando Velayos

*Division of Gastroenterology, Department of Medicine, San Francisco General Hospital and Trauma Center, University of California, San Francisco, CA, USA

Division of Gastroenterology, Department of Medicine, University of California, San Francisco, CA, USA

Correspondence to: Lukejohn W. Day, Division of Gastroenterology, Department of Medicine, San Francisco General Hospital and Trauma Center, 1001 Potrero Ave, 3D-5, San Francisco, CA 94110, USA, Tel: +1-415-206-3832, Fax: +1-415-206-5199, E-mail: lukejohn.day@ucsf.edu

Received: August 5, 2014; Accepted: September 4, 2014

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Gut Liver 2015;9(2):143-151. https://doi.org/10.5009/gnl14302

Published online March 15, 2015, Published date March 31, 2015

Copyright © Gut and Liver.

Colorectal cancer is common worldwide, and the elderly are disproportionately affected. Increasing age is a risk factor for the development of precancerous adenomas and colorectal cancer, thus raising the issue of screening and surveillance in older patients. Elderly patients are a diverse and heterogeneous group, and special considerations such as comorbid medical conditions, functional status and cognitive ability play a role in deciding on the utility of screening and surveillance. Colorectal cancer screening can be beneficial to patients, but at certain ages and under some circumstances the harm of screening outweighs the benefits. Increasing adverse events, poorer bowel preparation and more incomplete examinations are observed in older patients undergoing colonoscopy for diagnostic, screening and surveillance purposes. Decisions regarding screening, surveillance and treatment for colorectal cancer require a multidisciplinary approach that accounts not only for the patient’s age but also for their overall health, preferences and functional status. This review provides an update and examines the challenges surrounding colorectal cancer diagnosis, screening, and treatment in the elderly.

Keywords: Colorectal neoplasms, Colonoscopy, Screening, Surveillance, Elderly

Colorectal cancer is the second leading cause of cancer-related mortality worldwide and the fourth most commonly diagnosed malignant disease.1 In 2012 there were nearly 1.4 million new cases of colorectal cancer diagnosed in the world with over 2.4 million new cases of colorectal cancer expected to be diagnosed worldwide by 2035. Age is an important risk factor for developing colorectal cancer2 and the elderly are disproportionately affected by this disease, thereby necessitating the need for screening and surveillance in this group. Yet, screening and surveillance decisions in the elderly can be quite challenging. For example, the definition of elderly, based on age alone may not properly capture the appropriateness of screening in an individual person. The World Health Organization defines elderly as persons over the age of 65, yet it is well known that persons over 65 are a heterogeneous group ranging from incredibly healthy with a long life expectancy to those with multiple comorbid medical conditions, declining cognitive function and impaired functional status.

The following review will address a number of the challenges and controversies surrounding colorectal cancer and the elderly. First, we will review the epidemiology and clinical presentation of colorectal cancer in the elderly. Second, we will review the efficacy of screening modalities and examine the data regarding when not to screen a patient based on age. Moreover, we will discuss one of the most common colorectal cancer screening modalities, colonoscopy, and how various aspects of this procedure are impacted by age. Finally, we will discuss colorectal cancer treatment and how age influences the efficacy, safety and decision to treat elderly patients with colorectal cancer.

Colorectal cancer is common in the elderly. Approximately 90% of new colorectal cancers are diagnosed in patients over 50 years3 with the median age of diagnosis being 69 years. Furthermore, the incidence of colorectal cancer dramatically rises as one ages, regardless of sex and racial background (Fig. 1)3 and nearly doubles between the ages of 40 and 80 years.2

Colonic polyps are precursors to the development of colorectal cancer.4 Among precancerous polyps, both adenomatous and advanced adenomatous polyps (defined as polyp size >10 mm, villous/tubulovillous histological features, or having high grade dysplasia) have an increased prevalence and incidence in the elderly.57 In fact, adenoma and advanced adenoma prevalence in persons 70 to 75 years of age is more than double that of persons 40 to 49 years.5,8,9 In contrast, the prevalence of serrated lesions only slightly increases with age.1014 Moreover, age plays a role with respect to a number of other factors related to colonic polyps. Elderly patients are observed to have larger sized and more proximally located adenomatous polyps which may lead to higher rates of colorectal cancer in this population.15

On the other hand, the recurrence of adenomas, advanced adenomas, and serrated lesions is less impacted by age. Age does not appear to influence the recurrence of adenomas after diagnosis from an index colonoscopy.1618 Other factors such as index polyp size,17 number of polyps at index colonoscopy,19 and initial incomplete polyp resection20 are more associated with recurrence. Similar predictors of recurrence are present for advanced adenomas, but age may play a slightly greater role.21,22 In addition to polyp characteristics insufficient bowel preparation and incomplete examination have been additional factors noted to predict the recurrence of advanced adenomas detected on surveillance colonoscopies.19 Limited studies suggest that age does not impact recurrence of serrated polyps23 and consensus guidelines on surveillance intervals for serrated lesions focus more on the size, number and location of the index serrated lesion(s).24 While colorectal cancer incidence increases with age, the recurrence of it is not. Rather family history, findings on index colonoscopy25,26 and presenting symptoms,27 have a much stronger association (Table 1).

Given that age does not strongly influence the recurrence of either colonic polyps or colorectal cancer, surveillance guidelines have not been tailored by age.

Colorectal cancer presentation is similar in younger and older patients although more proximal cancer is detected in older patients.7 Likewise older patients may be less likely to present asymptomatically.28,29 Elderly patients with colorectal cancer may have a range of symptoms that include occult blood loss, rectal bleeding, change in stool caliber, unintentional weight loss or have signs of bowel obstruction or perforation. While no one presenting symptom predominates in elderly patients, it should be recognized that elderly patients may have a more subtle presentation of colorectal cancer such as vague abdominal pain or a new microcytic anemia. Such symptoms cannot be attributed to other etiologies and deserve a thorough cancer evaluation.

Colorectal cancer screening, which detects both precancerous polyps and colorectal cancer, can reduce both colorectal cancer incidence and mortality.3040 Through screening the incidence of colorectal cancer can be reduced by 17% to 33% with a mortality reduction of 11% to 53% depending on the modality employed.3034,36,37 While no one screening method is advocated a number of consensus documents offer several screening recommendations including those from the U.S. Preventative Services Task Force,41 American Cancer Society, U.S. Multi-Society Taskforce with the American College of Radiology,42 American College of Gastroenterology,43 and the National Comprehensive Cancer Network.44 Screening tests available and recommended include examining stool for occult blood or newer tests examining DNA mutations/alterations,45 radiologic or endoscopic methods (Table 2). To date, no one screening test has proven superior for colorectal cancer screening in the elderly.

1. Colonoscopy in elderly patients

Lower endoscopy, specifically colonoscopy, has been shown to significantly reduce both distal and proximal colorectal cancer in older individuals.46 As more elderly patients undergo colorectal cancer screening using colonoscopy one has to consider how specific factors, such as age, related to this procedure may interact with one another.

Several reviews4750 have addressed a number of issues related to the elderly and endoscopy. Few changes are recommended for elderly patients with respect to the preprocedure process and sedation, but some differences have been clarified. During the preprocedure assessment it is recommended that providers assess for elderly patient’s cognitive ability and capacity to understand the procedure and that functional status and depression screening be documented in an elderly patient’s medical record when they are undergoing endoscopy.50,51 Second, providers should use fewer sedative medications, at lower doses and be infused at slower rates when an elderly patient is being sedated.50 Furthermore, early recognition by the endoscopist of multiple factors such as an elderly patient’s comorbid medical conditions, cognitive function, mobility and polypharmacy need to occur prior to performing endoscopy.

2. Adverse events

The occurrence of adverse events during colonoscopy and how age may modify this risk are important considerations for the elderly patient. Age does not play a role in minor adverse events such as abdominal pain.52 Yet, major adverse events such as perforation, bleeding and cardiopulmonary complications are all affected by age, though the individual risk varies and can be influenced by additional factors. Of all adverse events associated with colonoscopy, the greatest risk associated with age is perforation. For example, elderly patients have a 30% higher risk of experiencing a perforation than younger patients undergoing colonoscopy and a 14-fold higher risk of having a perforation than patients of the same age who do not undergo the procedure.53 Lastly, older patients with more comorbid medical conditions have a greater risk of experiencing an adverse event if the colonoscopy is performed under general anesthesia.54

3. Bowel preparation

Bowel preparation is a significant issue to consider in patients undergoing colonoscopy. Two agents are available (polyethylene glycol electrolyte lavage solution [PEG] and oral sodium phosphate [OSP]). A number of adverse events are observed in elderly patients taking PEG and OSPs (Table 3). PEG has a much better safety profile compared to OSPs with a major concern that elderly patients taking OSPs are at greater risk of having electrolyte disturbances55,56 and experiencing acute kidney injury.15,57 It is for this reason that OSPs are no longer recommended in the elderly and that PEG is the preferred bowel preparation agent for this patient population.

However, there are concerns with PEG in regards to tolerability and compliance in the elderly with noncompliance rates of 3% to 32%.58 Also concerns do remain with the elderly being able to tolerate such a large volume of fluid required with PEG. While spilt PEG dosing regimens have been shown to be more effective59 versus standard one time dosing, this approach has not been well studied in the elderly. Finally, of critical importance is that elderly patients remain adequately hydrated when taking PEG.60

Poor bowel preparations in the elderly undergoing colonoscopy range from 4% to 57%29,6169 with bowel preparation being more difficult to achieve in very elderly patients (e.g., patients >80 years).63,67 Poorer bowel preparations observed in the elderly can occur for a variety of reasons including altered gastrointestinal motility, increased rates of medication-related constipation, previous surgeries, decreased understanding of bowel preparation instructions, greater burden of comorbid medical conditions, and/or functional limitations.

4. Completion of colonoscopy

Key to a high quality colonoscopy is the successful completion of it (e.g., intubation of the cecum). Endoscopists subjectively judge a colonoscopy to be more difficult in an elderly patient,70 but completion rates vary from 78% to 86% in the elderly and 52% to 95%61,62,71 in the very elderly.29,6365,6769 Age may be an independent risk factor for lower completions rates, but it is apparent that other factors such as poor bowel preparation and a patient’s underlying disease process play a stronger role.61,72

1. Comorbid medical conditions in the elderly and screening

Elderly patients have a greater number and severity of comorbid medical conditions with over one-quarter of patients >65 years of age having more than five comorbid medical conditions.73 This increase in comorbid medical conditions can impact not only the development of colorectal cancer, but can also reduce the benefit from screening and treatment in older patients. It is evident that the benefit of screening is reduced with increasing disease burden. For example, the greatest number needed to screen to prevent a colorectal cancer death is in older, more ill patients. Compounding this issue further is that screening related adverse events are greater than the benefit in this same group of patients.74,75 Furthermore, patients with greater comorbid medical conditions have lower survival rates after an initial diagnosis of colorectal cancer,7678 poorer survival after chemotherapy78,79 and prolonged hospitalizations as a consequence of their colorectal cancer.80

2. Debate on when to discontinue colorectal cancer screening in the elderly

Detecting colorectal cancer earlier is clearly beneficial but several controversial questions remain.

One important question is: Does screening extend life in older patients who may have a shorter life expectancy? On this topic a number of modeling studies have examined the impact of various colorectal screening methods on life expectancy at different age groups.8183 Younger patients have a greater decrease in life expectancy than do elderly patients after a diagnosis of colorectal cancer. At the same time, there is a 75% reduction in the benefit of screening for elderly patients when compared with younger patients regardless of which screening modality is used. Identical results have been noted in clinical studies addressing this same question. These studies have illustrated that the benefit of screening, after an initial negative screening test, is reduced in elderly patients as this group has a greater chance of passing away from other illnesses besides colorectal cancer.76 As a further example, in a recent study of elderly patients who had a positive fecal occult blood test, nearly half of the patients who did not undergo colonoscopy died from other causes. Of those who underwent colonoscopy 10% experienced an adverse event and the overwhelming majority of patients with a worse life expectancy obtained little benefit from screening.84

A second question that arises is: At what point does colorectal cancer screening cease to provide an important extension in life expectancy and therefore not be offered? Multiple studies have tackled this question and examined various ages at which colorectal cancer screening should be discontinued. A number of ages at which to stop screening have been proposed. Some have demonstrated that decreasing the screening age from 85 to 75 years yields small reductions in life years gained as well as utilizes fewer resources, and have concluded that stopping screening at 75 provides almost the same benefit as stopping at 85 years.85 Others have demonstrated diminishing returns for days of life lost after the age of 70 for any form of screening86 and that after the age of 60 the percentage of life years saved declines precipitously after a single colonoscopy.82 While this debate continues at lower ages, there does appear to be clear evidence and consensus on an age in which some patients achieve no benefit from screening. Men >85 years and women >90 years do not achieve any benefit from colorectal cancer screening regardless of modality,74 and patients over 80 years have a shortened life expectancy (median survival of <5 years) after a diagnosis of colorectal cancer regardless of comorbid medical conditions or functional status.76 Unfortunately, there is very little guidance on when to stop screening from national medical societies (Table 4).

In summary, health, life expectancy and functional status as well as age should all play a role when considering the option to discontinue colorectal cancer screening. However, this practice is quite variable. Some providers take an individualized approach with their elderly patients and colorectal cancer screening with more physicians choosing to engage healthier elderly patients.87 Whereas, a larger body of evidence suggests that others perform inappropriate colorectal cancer screening in patients with severe comorbid medical conditions and low life expectancies.88,89 Such disparities in practice highlight the need for greater education among providers on colorectal cancer screening in the elderly.

Treatment for colorectal cancer (both surgical and medical) in the elderly differs in comparison with younger patients. First, age plays a role in outcomes and the type of colorectal cancer surgery selected. Laparoscopic colorectal cancer surgery in the elderly appears to be a more effective procedure compared with an open approach with equal cure rates between the two procedures, but less adverse events,90 less blood loss9092 and shorter postoperative hospitalizations9092 noted with laparoscopic colectomy performed in elderly patients with colorectal cancer. Also, older patients are observed to have higher mortality rates after colorectal cancer surgery.93 Second, age impacts medical treatment for colorectal cancer, but to a lesser degree. Many oncologists reduce the dose of chemotherapy for perceived risks of impaired liver or renal function in older patients.94 However, most chemotherapeutic agents are safe in the elderly and can achieve the same therapeutic benefits of reduced recurrence and mortality as observed in younger patients, especially in the adjuvant setting.9597 Given this data most advocate that age alone not factor into one’s decision to treat colorectal cancer.95,98,99 One limitation of the current literature on chemotherapy data for colorectal cancer and the elderly is that advanced age is an exclusion factor in many clinical trials.98,100102 In fact, comorbid medical conditions play a much larger role in the decision to proceed with chemotherapy as this has a more pronounced impact on life expectancy after colorectal cancer diagnosis and treatment.78

Likewise, age appears to factor into colorectal cancer treatment on a number of other fronts. Elderly patients with colorectal cancer are less frequently discussed at multidisciplinary cancer team meetings,103,104 undergo less surgery,103,104 have less adjuvant chemotherapy prescribed,103,105,106 and undergo less palliative therapy.105 Furthermore, colorectal cancer is more complicated in older patients at diagnosis105 with more emergency surgery performed in the elderly.104 Also, while elderly patients represent half of metastatic colorectal cancer diagnoses, their survival is significantly less compared to younger patients with metastatic colorectal cancer.107 These data do not suggest these differences are appropriate or inappropriate, but rather that age impacts colorectal cancer treatment.

As a final point, with respect to colorectal cancer treatments in the elderly, oncologists do advocate the use of a variety of tools and approaches to help guide treatment decisions. The Comprehensive Geriatric Assessment was developed to evaluate elderly patients being considered for colorectal cancer treatment and its use has proven effective in reducing adverse outcomes among the elderly.108,109 Also, oncologists promote a multidisciplinary approach in treating elderly patients with colorectal cancer. A patient’s functional status, comorbid medical conditions, and preferences as well as cancer stage all have to be factored into the decision of determining what regimen (if any) to use when treating the elderly patient with colorectal cancer.98,100

Overall, a disproportionate number of colorectal cancer diagnoses and deaths occur in elderly patients. Advancing age is an independent risk factor associated with both colorectal cancer and adenomas whereas the detection of recurrent colorectal cancer and adenomas after a screening colonoscopy is not affected by age. A number of colorectal cancer screening modalities are available for elderly patients, but it is important to remember that at specific ages the risks and increased resources may outweigh the benefit of screening in some elderly patients. Controversy exists over when to discontinue colorectal cancer screening and surveillance in the elderly. Yet, most agree that the decision to proceed with screening and surveillance requires an individualized assessment of the elderly patient that takes into account the risks and benefits and balances this with the patients’ health, functional status, and preferences. Some aspects of screening, such as with colonoscopy, need to be factored into this decision making process. Older patients have a higher risk of adverse events during a colonoscopy, poorer bowel preparations and possibly lower successful completion rates. Finally, a variety of colorectal cancer treatments are available for elderly patients and, just as with decisions about when to discontinue screening, a patient’s functional status, comorbid medical conditions, and preferences have to be factored into the decision making process when determining which treatment regimen to offer.

Factors that Increase the Recurrence Risk of Adenomas, Advanced Adenomas, and Colorectal Cancer

Adenomas
 Index polyp size (polyp >1 cm)
 Number of index polyps
 Incomplete polypectomy
Advanced adenomas
 Number of index adenomas
 Index polyp size (polyp >1 cm)
 Villous histology on pathology
 Insufficient bowel preparation
 Incomplete examination (unable to reach farther than the distal colon)
Colorectal cancer
 Family history of colorectal cancer
 Presence of extracolonic malignancy
 Detection of synchronous lesions
 Coexisting adenomas
 Perforation at time of diagnosis
 Symptoms

Colorectal Cancer Screening Tests

Occult blood
 High sensitivity guaiac-based fecal occult blood test (gFOBT)
 Fecal immunochemical test (FIT)
 Multitarget stool DNA test*
Endoscopy
 Colonoscopy
 Flexible sigmoidoscopy
Radiology
 Double contrast barium enema
 Computerized tomography colonography

*Quantitative molecular assays for KRAS mutations, aberrant NDRG4 and BMP3 methylation and β-actin, in addition to a hemoglobin assay performed on stool samples.


Adverse Events Associated with Bowel Preparation in Elderly Patients

PEG (%)
 Dizziness (48)
 Fecal incontinence (27–39)
 Abdominal pain (7–23)
 Nausea (2–17.5)
 Insomnia (13)
 Fatigue (12.7)
 Headache (7.9)
 Hypokalemia (2.9–20.5)
 Dysnatremia (hyponatremia/hypernatremia) (4.1)
 Emesis (3.2)
 Aspiration pneumonia (<1)
 Pancreatitis (<1)
 Ischemic colitis (<1)
OSP (%)
 Hyperphosphatemia (58.1–100)
 Fecal incontinence (23–55)
 Elevated creatinine/renal injury (55.2)
 Hypocalcemia (5.1–58)
 Hypokalemia (5.4–56)
 Abdominal pain (11–32)
 Nausea (9–36)
 Insomnia (15)
 Dizziness (3–55)
 Emesis (4–7)
 Hypotension (4)

Colorectal Cancer Screening Guidelines and the Elderly

SocietyRecommendation
U.S. Multi-Society Task Force and the American Cancer Society (USMSTF/ACS)In those with a prior polyp: discontinuation of surveillance colonoscopy should be considered in persons with serious comorbidities and with less than 10 years of life expectancy.
American Gastroenterological Association (AGA)No comment on when to stop screening. Comment on need for shared decision making and individualized approach.
American Geriatrics Society (AGS)Not recommended in those unlikely to live more than 5 years or who have significant comorbidity that would preclude treatment.
British Society of GastroenterologyFecal occult blood test every 2 years offered to all persons 50–69 years of age (depending on location) with current plans to extend to age 75 in most areas.
Kaiser Permanent Care Management Institute (KPCMI)Discontinuation of screening is generally recommended at age 75, provided that there is a history of routine screening.
Discontinuation is recommended at age 80 for those with no history of routine screening. The decision to discontinue screening should be based on physician judgment, patient preference, the increased risk of complications in older adults, and existing comorbidities.

  1. Ferlay J, Pisani P, Parkin DM, International Agency for Research on Cancer. GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide. Lyon: IARC Press.
  2. Rabeneck, L, El-Serag, HB, Davila, JA, Sandler, RS. Outcomes of colorectal cancer in the United States: no change in survival (1986?1997). Am J Gastroenterol, 2003;98;471-477.
    Pubmed
  3. Howlader N, Krapcho M, Garshell J. SEER cancer statistics review, 1975?2010 [Internet]. Bethesda: National Cancer Institute, [cited 2013 Jul 20].
    Available from: http://seer.cancer.gov/csr/1975_2010/
  4. Vogelstein, B, Fearon, ER, Hamilton, SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med, 1988;319;525-532.
    Pubmed CrossRef
  5. Lieberman, DA, Weiss, DG, Bond, JH, Ahnen, DJ, Garewal, H, Chejfec, G. Use of colonoscopy to screen asymptomatic adults for colorectal cancer: Veterans Affairs Cooperative Study Group 380. N Engl J Med, 2000;343;162-168.
    Pubmed CrossRef
  6. Khullar, SK, DiSario, JA. Colon cancer screening: sigmoidoscopy or colonoscopy. Gastrointest Endosc Clin N Am, 1997;7;365-386.
    Pubmed
  7. Neugut, AI, Jacobson, JS, De Vivo, I. Epidemiology of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev, 1993;2;159-176.
    Pubmed
  8. Strul, H, Kariv, R, Leshno, M, et al. The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40?80 years. Am J Gastroenterol, 2006;101;255-262.
    Pubmed CrossRef
  9. Imperiale, TF, Wagner, DR, Lin, CY, Larkin, GN, Rogge, JD, Ransohoff, DF. Results of screening colonoscopy among persons 40 to 49 years of age. N Engl J Med, 2002;346;1781-1785.
    Pubmed CrossRef
  10. Omata, F, Brown, WR, Tokuda, Y, et al. Modifiable risk factors for colorectal neoplasms and hyperplastic polyps. Intern Med, 2009;48;123-128.
    Pubmed CrossRef
  11. Lieberman, DA, Prindiville, S, Weiss, DG, Willett, W, VA Cooperative Study Group 380. Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA, 2003;290;2959-2967.
    Pubmed CrossRef
  12. Johannsen, LG, Momsen, O, Jacobsen, NO. Polyps of the large intestine in Aarhus, Denmark: an autopsy study. Scand J Gastroenterol, 1989;24;799-806.
    Pubmed CrossRef
  13. Williams, AR, Balasooriya, BA, Day, DW. Polyps and cancer of the large bowel: a necropsy study in Liverpool. Gut, 1982;23;835-842.
    Pubmed KoreaMed CrossRef
  14. Vatn, MH, Stalsberg, H. The prevalence of polyps of the large intestine in Oslo: an autopsy study. Cancer, 1982;49;819-825.
    Pubmed CrossRef
  15. Singal, AK, Rosman, AS, Post, JB, Bauman, WA, Spungen, AM, Korsten, MA. The renal safety of bowel preparations for colonoscopy: a comparative study of oral sodium phosphate solution and polyethylene glycol. Aliment Pharmacol Ther, 2008;27;41-47.
    Pubmed CrossRef
  16. Noshirwani, KC, van Stolk, RU, Rybicki, LA, Beck, GJ. Adenoma size and number are predictive of adenoma recurrence: implications for surveillance colonoscopy. Gastrointest Endosc, 2000;51;433-437.
    Pubmed CrossRef
  17. Harewood, GC, Lawlor, GO. Incident rates of colonic neoplasia according to age and gender: implications for surveillance colonoscopy intervals. J Clin Gastroenterol, 2005;39;894-899.
    Pubmed CrossRef
  18. Harewood, GC, Lawlor, GO, Larson, MV. Incident rates of colonic neoplasia in older patients: when should we stop screening?. J Gastroenterol Hepatol, 2006;21;1021-1025.
    Pubmed CrossRef
  19. van Heijningen, EM, Lansdorp-Vogelaar, I, Kuipers, EJ, et al. Features of adenoma and colonoscopy associated with recurrent colorectal neoplasia based on a large community-based study. Gastroenterology, 2013;144;1410-1418.
    Pubmed CrossRef
  20. Pohl, H, Srivastava, A, Bensen, SP, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology, 2013;144;74-80.e1.
    Pubmed CrossRef
  21. Mart?nez, ME, Baron, JA, Lieberman, DA, et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology, 2009;136;832-841.
    Pubmed KoreaMed CrossRef
  22. Saini, SD, Kim, HM, Schoenfeld, P. Incidence of advanced adenomas at surveillance colonoscopy in patients with a personal history of colon adenomas: a meta-analysis and systematic review. Gastrointest Endosc, 2006;64;614-626.
    Pubmed CrossRef
  23. Teriaky, A, Driman, DK, Chande, N. Outcomes of a 5-year follow-up of patients with sessile serrated adenomas. Scand J Gastroenterol, 2012;47;178-183.
    Pubmed CrossRef
  24. Rex, DK, Ahnen, DJ, Baron, JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol, 2012;107;1315-1329.
    Pubmed KoreaMed CrossRef
  25. Togashi, K, Konishi, F, Ozawa, A, et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum, 2000;43;S47-S53.
    Pubmed CrossRef
  26. Harris, GJ, Church, JM, Senagore, AJ, et al. Factors affecting local recurrence of colonic adenocarcinoma. Dis Colon Rectum, 2002;45;1029-1034.
    Pubmed CrossRef
  27. M?kel?, JT, Laitinen, SO, Kairaluoma, MI. Five-year follow-up after radical surgery for colorectal cancer: results of a prospective randomized trial. Arch Surg, 1995;130;1062-1067.
    Pubmed CrossRef
  28. Trombold, J, Farmer, RW, McCafferty, M. The impact of colorectal cancer screening in a veteran hospital population. Am Surg, 2013;79;296-300.
    Pubmed
  29. Bat, L, Pines, A, Shemesh, E, et al. Colonoscopy in patients aged 80 years or older and its contribution to the evaluation of rectal bleeding. Postgrad Med J, 1992;68;355-358.
    Pubmed KoreaMed CrossRef
  30. Faivre, J, Dancourt, V, Lejeune, C, et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study. Gastroenterology, 2004;126;1674-1680.
    Pubmed CrossRef
  31. Hardcastle, JD, Chamberlain, JO, Robinson, MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet, 1996;348;1472-1477.
    Pubmed CrossRef
  32. Kronborg, O, Fenger, C, Olsen, J, Jørgensen, OD, Søndergaard, O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet, 1996;348;1467-1471.
    Pubmed CrossRef
  33. Lindholm, E, Brevinge, H, Haglind, E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg, 2008;95;1029-1036.
    Pubmed CrossRef
  34. Mandel, JS, Bond, JH, Church, TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood: Minnesota Colon Cancer Control Study. N Engl J Med, 1993;328;1365-1371.
    Pubmed CrossRef
  35. Quintero, E, Castells, A, Bujanda, L, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med, 2012;366;697-706.
    Pubmed CrossRef
  36. Atkin, WS, Edwards, R, Kralj-Hans, I, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet, 2010;375;1624-1633.
    Pubmed CrossRef
  37. Segnan, N, Senore, C, Andreoni, B, et al. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. J Natl Cancer Inst, 2005;97;347-357.
    Pubmed CrossRef
  38. Schoen, RE, Pinsky, PF, Weissfeld, JL, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med, 2012;366;2345-2357.
    Pubmed KoreaMed CrossRef
  39. Zauber, AG, Winawer, SJ, O’Brien, MJ, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med, 2012;366;687-696.
    Pubmed KoreaMed CrossRef
  40. Robertson, DJ, Greenberg, ER, Beach, M, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology, 2005;129;34-41.
    Pubmed CrossRef
  41. U. S. Preventive Services Task Force. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med, 2008;149;627-637.
    Pubmed CrossRef
  42. Levin, B, Lieberman, DA, McFarland, B, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology, 2008;134;1570-1595.
    Pubmed CrossRef
  43. Rex, DK, Johnson, DA, Anderson, JC, et al. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol, 2009;104;739-750.
    Pubmed CrossRef
  44. Benson, AB, Arnoletti, JP, Bekaii-Saab, T, et al. Colon cancer. J Natl Compr Canc Netw, 2011;9;1238-1290.
    Pubmed
  45. Imperiale, TF, Ransohoff, DF, Itzkowitz, SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med, 2014;370;1287-1297.
    Pubmed CrossRef
  46. Kahi, CJ, Myers, LJ, Slaven, JE, et al. Lower endoscopy reduces colorectal cancer incidence in older individuals. Gastroenterology, 2014;146;718-725.e3.
    Pubmed CrossRef
  47. Day, LW, Walter, LC, Velayos, F. Colorectal cancer screening and surveillance in the elderly patient. Am J Gastroenterol, 2011;106;1197-1206.
    Pubmed CrossRef
  48. Travis, AC, Pievsky, D, Saltzman, JR. Endoscopy in the elderly. Am J Gastroenterol, 2012;107;1495-1501.
    Pubmed CrossRef
  49. Jafri, SM, Monkemuller, K, Lukens, FJ. Endoscopy in the elderly: a review of the efficacy and safety of colonoscopy, esophagogastroduodenoscopy, and endoscopic retrograde cholangiopancreatography. J Clin Gastroenterol, 2010;44;161-166.
    Pubmed CrossRef
  50. Chandrasekhara, V, Early, DS, et al, ASGE Standards of Practice Committee. Modifications in endoscopic practice for the elderly. Gastrointest Endosc, 2013;78;1-7.
    Pubmed CrossRef
  51. Chow, WB, Rosenthal, RA, Merkow, RP, et al. Optimal preoperative assessment of the geriatric surgical patient: a best practices guideline from the American College of Surgeons National Surgical Quality Improvement Program and the American Geriatrics Society. J Am Coll Surg, 2012;215;453-466.
    Pubmed CrossRef
  52. Ko, CW, Riffle, S, Shapiro, JA, et al. Incidence of minor complications and time lost from normal activities after screening or surveillance colonoscopy. Gastrointest Endosc, 2007;65;648-656.
    Pubmed CrossRef
  53. Day, LW, Kwon, A, Inadomi, JM, Walter, LC, Somsouk, M. Adverse events in older patients undergoing colonoscopy: a systematic review and meta-analysis. Gastrointest Endosc, 2011;74;885-896.
    Pubmed KoreaMed CrossRef
  54. Cooper, GS, Kou, TD, Rex, DK. Complications following colonoscopy with anesthesia assistance: a population-based analysis. JAMA Intern Med, 2013;173;551-556.
    Pubmed KoreaMed CrossRef
  55. Beloosesky, Y, Grinblat, J, Weiss, A, Grosman, B, Gafter, U, Chagnac, A. Electrolyte disorders following oral sodium phosphate administration for bowel cleansing in elderly patients. Arch Intern Med, 2003;163;803-808.
    Pubmed CrossRef
  56. Caswell, M, Thompson, WO, Kanapka, JA, Galt, DJ. The time course and effect on serum electrolytes of oral sodium phosphates solution in healthy male and female volunteers. Can J Clin Pharmacol, 2007;14;e260-e274.
    Pubmed
  57. Russmann, S, Lamerato, L, Marfatia, A, et al. Risk of impaired renal function after colonoscopy: a cohort study in patients receiving either oral sodium phosphate or polyethylene glycol. Am J Gastroenterol, 2007;102;2655-2663.
    Pubmed CrossRef
  58. Hsu, CW, Imperiale, TF. Meta-analysis and cost comparison of polyethylene glycol lavage versus sodium phosphate for colonoscopy preparation. Gastrointest Endosc, 1998;48;276-282.
    Pubmed CrossRef
  59. Cohen, LB. Split dosing of bowel preparations for colonoscopy: an analysis of its efficacy, safety, and tolerability. Gastrointest Endosc, 2010;72;406-412.
    Pubmed CrossRef
  60. Lichtenstein, GR, Cohen, LB, Uribarri, J. Review article: bowel preparation for colonoscopy. The importance of adequate hydration. Aliment Pharmacol Ther, 2007;26;633-641.
    Pubmed CrossRef
  61. Karajeh, MA, Sanders, DS, Hurlstone, DP. Colonoscopy in elderly people is a safe procedure with a high diagnostic yield: a prospective comparative study of 2000 patients. Endoscopy, 2006;38;226-230.
    Pubmed CrossRef
  62. Ma, WT, Mahadeva, S, Kunanayagam, S, Poi, PJ, Goh, KL. Colonoscopy in elderly Asians: a prospective evaluation in routine clinical practice. J Dig Dis, 2007;8;77-81.
    Pubmed CrossRef
  63. Lukens, FJ, Loeb, DS, Machicao, VI, Achem, SR, Picco, MF. Colonoscopy in octogenarians: a prospective outpatient study. Am J Gastroenterol, 2002;97;1722-1725.
    Pubmed CrossRef
  64. Burtin, P, Bour, B, Charlois, T, et al. Colonic investigations in the elderly: colonoscopy or barium enema?. Aging (Milano), 1995;7;190-194.
    Pubmed
  65. Chatrenet, P, Friocourt, P, Ramain, JP, Cherrier, M, Maillard, JB. Colonoscopy in the elderly: a study of 200 cases. Eur J Med, 1993;2;411-413.
    Pubmed
  66. George, ML, Tutton, MG, Jadhav, VV, Abulafi, AM, Swift, RI. Colonoscopy in older patients: a safe and sound practice. Age Ageing, 2002;31;80-81.
    Pubmed CrossRef
  67. Schmilovitz-Weiss, H, Weiss, A, Boaz, M, Levin, I, Chervinski, A, Shemesh, E. Predictors of failed colonoscopy in nonagenarians: a single-center experience. J Clin Gastroenterol, 2007;41;388-393.
    Pubmed CrossRef
  68. Duncan, JE, Sweeney, WB, Trudel, JL, Madoff, RD, Mellgren, AF. Colonoscopy in the elderly: low risk, low yield in asymptomatic patients. Dis Colon Rectum, 2006;49;646-651.
    Pubmed CrossRef
  69. Syn, WK, Tandon, U, Ahmed, MM. Colonoscopy in the very elderly is safe and worthwhile. Age Ageing, 2005;34;510-513.
    Pubmed CrossRef
  70. Ristikankare, M, Hartikainen, J, Heikkinen, M, Janatuinen, E, Julkunen, R. The effects of gender and age on the colonoscopic examination. J Clin Gastroenterol, 2001;32;69-75.
    Pubmed CrossRef
  71. Ure, T, Dehghan, K, Vernava, AM, Longo, WE, Andrus, CA, Daniel, GL. Colonoscopy in the elderly: low risk, high yield. Surg Endosc, 1995;9;505-508.
    Pubmed CrossRef
  72. Nelson, DB, McQuaid, KR, Bond, JH, Lieberman, DA, Weiss, DG, Johnston, TK. Procedural success and complications of large-scale screening colonoscopy. Gastrointest Endosc, 2002;55;307-314.
    Pubmed CrossRef
  73. Yancik, R. Cancer burden in the aged: an epidemiologic and demographic overview. Cancer, 1997;80;1273-1283.
    Pubmed CrossRef
  74. Ko, CW, Sonnenberg, A. Comparing risks and benefits of colorectal cancer screening in elderly patients. Gastroenterology, 2005;129;1163-1170.
    Pubmed CrossRef
  75. Warren, JL, Klabunde, CN, Mariotto, AB, et al. Adverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med, 2009;150;849-857.
    Pubmed CrossRef
  76. Kahi, CJ, Azzouz, F, Juliar, BE, Imperiale, TF. Survival of elderly persons undergoing colonoscopy: implications for colorectal cancer screening and surveillance. Gastrointest Endosc, 2007;66;544-550.
    Pubmed CrossRef
  77. van de Poll-Franse, LV, Haak, HR, Coebergh, JW, Janssen-Heijnen, ML, Lemmens, VE. Disease-specific mortality among stage I?III colorectal cancer patients with diabetes: a large population-based analysis. Diabetologia, 2012;55;2163-2172.
    Pubmed KoreaMed CrossRef
  78. Gross, CP, McAvay, GJ, Guo, Z, Tinetti, ME. The impact of chronic illnesses on the use and effectiveness of adjuvant chemotherapy for colon cancer. Cancer, 2007;109;2410-2419.
    Pubmed CrossRef
  79. Stavrou, EP, Lu, CY, Buckley, N, Pearson, S. The role of comorbidities on the uptake of systemic treatment and 3-year survival in older cancer patients. Ann Oncol, 2012;23;2422-2428.
    Pubmed CrossRef
  80. Sarfati, D, Tan, L, Blakely, T, Pearce, N. Comorbidity among patients with colon cancer in New Zealand. N Z Med J, 2011;124;76-88.
    Pubmed
  81. Inadomi, JM, Sonnenberg, A. The impact of colorectal cancer screening on life expectancy. Gastrointest Endosc, 2000;51;517-523.
    Pubmed CrossRef
  82. Sonnenberg, A, Delc?, F. Cost-effectiveness of a single colonoscopy in screening for colorectal cancer. Arch Intern Med, 2002;162;163-168.
    Pubmed CrossRef
  83. Lin, OS, Kozarek, RA, Schembre, DB, et al. Screening colonoscopy in very elderly patients: prevalence of neoplasia and estimated impact on life expectancy. JAMA, 2006;295;2357-2365.
    Pubmed CrossRef
  84. Kistler, CE, Kirby, KA, Lee, D, Casadei, MA, Walter, LC. Long-term outcomes following positive fecal occult blood test results in older adults: benefits and burdens. Arch Intern Med, 2011;171;1344-1351.
    Pubmed KoreaMed CrossRef
  85. Zauber, AG, Lansdorp-Vogelaar, I, Knudsen, AB, Wilschut, J, van Ballegooijen, M, Kuntz, KM. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med, 2008;149;659-669.
    Pubmed KoreaMed CrossRef
  86. Maheshwari, S, Patel, T, Patel, P. Screening for colorectal cancer in elderly persons: who should we screen and when can we stop?. J Aging Health, 2008;20;126-139.
    Pubmed CrossRef
  87. Lewis, CL, Esserman, D, DeLeon, C, Pignone, MP, Pathman, DE, Golin, C. Physician decision making for colorectal cancer screening in the elderly. J Gen Intern Med, 2013;28;1202-1207.
    Pubmed KoreaMed CrossRef
  88. Walter, LC, Lindquist, K, Nugent, S, et al. Impact of age and comorbidity on colorectal cancer screening among older veterans. Ann Intern Med, 2009;150;465-473.
    Pubmed KoreaMed CrossRef
  89. Mittal, S, Lin, YL, Tan, A, Kuo, YF, El-Serag, HB, Goodwin, JS. Limited life expectancy among a subgroup of medicare beneficiaries receiving screening colonoscopies. Clin Gastroenterol Hepatol, 2014;12;443-450.e1.
    Pubmed KoreaMed CrossRef
  90. Fujii, S, Ishibe, A, Ota, M, et al. Short-term results of a randomized study between laparoscopic and open surgery in elderly colorectal cancer patients. Surg Endosc, 2014;28;466-476.
    Pubmed CrossRef
  91. Hatakeyama, T, Nakanishi, M, Murayama, Y, et al. Laparoscopic resection for colorectal cancer improves short-term outcomes in very elderly colorectal cancer patients. Surg Laparosc Endosc Percutan Tech, 2013;23;532-535.
    Pubmed CrossRef
  92. Nakamura, T, Sato, T, Miura, H, et al. Feasibility and outcomes of surgical therapy in very elderly patients with colorectal cancer. Surg Laparosc Endosc Percutan Tech, 2014;24;85-88.
    Pubmed CrossRef
  93. Ahmed, S, Howel, D, Debrah, S, NORCCAG (Northern Region Colorectal Cancer Audit Group). The influence of age on the outcome of treatment of elderly patients with colorectal cancer. J Geriatr Oncol, 2014;5;133-140.
    Pubmed CrossRef
  94. Shayne, M, Culakova, E, Wolff, D, et al. Dose intensity and hematologic toxicity in older breast cancer patients receiving systemic chemotherapy. Cancer, 2009;115;5319-5328.
    Pubmed CrossRef
  95. Dotan, E, Browner, I, Hurria, A, Denlinger, C. Challenges in the management of older patients with colon cancer. J Natl Compr Canc Netw, 2012;10;213-224.
    Pubmed KoreaMed
  96. Sundararajan, V, Mitra, N, Jacobson, JS, Grann, VR, Heitjan, DF, Neugut, AI. Survival associated with 5-fluorouracil-based adjuvant chemotherapy among elderly patients with node-positive colon cancer. Ann Intern Med, 2002;136;349-357.
    Pubmed CrossRef
  97. Jehn, CF, B?ning, L, Kr?ning, H, Pezzutto, A, L?ftner, D. Influence of comorbidity, age and performance status on treatment efficacy and safety of cetuximab plus irinotecan in irinotecan-refractory elderly patients with metastatic colorectal cancer. Eur J Cancer, 2014;50;1269-1275.
    Pubmed CrossRef
  98. Leo, S, Accettura, C, Gnoni, A, et al. Systemic treatment of gastrointestinal cancer in elderly patients. J Gastrointest Cancer, 2013;44;22-32.
    Pubmed CrossRef
  99. Balducci, L. Geriatric oncology. Crit Rev Oncol Hematol, 2003;46;211-220.
    Pubmed CrossRef
  100. Feliu, J, Sereno, M, Castro, JD, Belda, C, Casado, E, Gonz?lez-Bar?n, M. Chemotherapy for colorectal cancer in the elderly: whom to treat and what to use. Cancer Treat Rev, 2009;35;246-254.
    Pubmed CrossRef
  101. Yee, KW, Pater, JL, Pho, L, Zee, B, Siu, LL. Enrollment of older patients in cancer treatment trials in Canada: why is age a barrier?. J Clin Oncol, 2003;21;1618-1623.
    Pubmed CrossRef
  102. Lewis, JH, Kilgore, ML, Goldman, DP, et al. Participation of patients 65 years of age or older in cancer clinical trials. J Clin Oncol, 2003;21;1383-1389.
    Pubmed CrossRef
  103. Guillerme, F, Clavier, JB, Nehme-Schuster, H, et al. Age impacts the pattern of care for elderly patients with rectal cancer. Int J Colorectal Dis, 2014;29;157-163.
    Pubmed CrossRef
  104. Egenvall, M, Schubert Samuelsson, K, Klarin, I, et al. Management of colon cancer in the elderly: a population-based study. Colorectal Dis, 2014;16;433-441.
    Pubmed CrossRef
  105. Doat, S, Thi?baut, A, Samson, S, Ricordeau, P, Guillemot, D, Mitry, E. Elderly patients with colorectal cancer: treatment modalities and survival in France. National data from the ThInDiT cohort study. Eur J Cancer, 2014;50;1276-1283.
    Pubmed CrossRef
  106. Kim, GM, Ahn, JB, Rha, SY, et al. Changing treatment patterns in elderly patients with resectable colon cancer. Asia Pac J Clin Oncol, 2013;9;265-272.
    Pubmed CrossRef
  107. Golan, T, Urban, D, Berger, R, Lawrence, YR. Changing prognosis of metastatic colorectal adenocarcinoma: differential improvement by age and tumor location. Cancer, 2013;119;3084-3091.
    Pubmed CrossRef
  108. Wildes, TM, Ruwe, AP, Fournier, C, et al. Geriatric assessment is associated with completion of chemotherapy, toxicity, and survival in older adults with cancer. J Geriatr Oncol, 2013;4;227-234.
    Pubmed KoreaMed CrossRef
  109. Berretta, M, Di Benedetto, F, Di Francia, R, et al. Colorectal cancer in elderly patients: from best supportive care to cure. Anticancer Agents Med Chem, 2013;13;1332-1343.
    Pubmed CrossRef

Article

Review

Gut Liver 2015; 9(2): 143-151

Published online March 31, 2015 https://doi.org/10.5009/gnl14302

Copyright © Gut and Liver.

Colorectal Cancer Screening and Surveillance in the Elderly: Updates and Controversies

Lukejohn W. Day*, and Fernando Velayos

*Division of Gastroenterology, Department of Medicine, San Francisco General Hospital and Trauma Center, University of California, San Francisco, CA, USA

Division of Gastroenterology, Department of Medicine, University of California, San Francisco, CA, USA

Correspondence to: Lukejohn W. Day, Division of Gastroenterology, Department of Medicine, San Francisco General Hospital and Trauma Center, 1001 Potrero Ave, 3D-5, San Francisco, CA 94110, USA, Tel: +1-415-206-3832, Fax: +1-415-206-5199, E-mail: lukejohn.day@ucsf.edu

Received: August 5, 2014; Accepted: September 4, 2014

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Colorectal cancer is common worldwide, and the elderly are disproportionately affected. Increasing age is a risk factor for the development of precancerous adenomas and colorectal cancer, thus raising the issue of screening and surveillance in older patients. Elderly patients are a diverse and heterogeneous group, and special considerations such as comorbid medical conditions, functional status and cognitive ability play a role in deciding on the utility of screening and surveillance. Colorectal cancer screening can be beneficial to patients, but at certain ages and under some circumstances the harm of screening outweighs the benefits. Increasing adverse events, poorer bowel preparation and more incomplete examinations are observed in older patients undergoing colonoscopy for diagnostic, screening and surveillance purposes. Decisions regarding screening, surveillance and treatment for colorectal cancer require a multidisciplinary approach that accounts not only for the patient’s age but also for their overall health, preferences and functional status. This review provides an update and examines the challenges surrounding colorectal cancer diagnosis, screening, and treatment in the elderly.

Keywords: Colorectal neoplasms, Colonoscopy, Screening, Surveillance, Elderly

INTRODUCTION

Colorectal cancer is the second leading cause of cancer-related mortality worldwide and the fourth most commonly diagnosed malignant disease.1 In 2012 there were nearly 1.4 million new cases of colorectal cancer diagnosed in the world with over 2.4 million new cases of colorectal cancer expected to be diagnosed worldwide by 2035. Age is an important risk factor for developing colorectal cancer2 and the elderly are disproportionately affected by this disease, thereby necessitating the need for screening and surveillance in this group. Yet, screening and surveillance decisions in the elderly can be quite challenging. For example, the definition of elderly, based on age alone may not properly capture the appropriateness of screening in an individual person. The World Health Organization defines elderly as persons over the age of 65, yet it is well known that persons over 65 are a heterogeneous group ranging from incredibly healthy with a long life expectancy to those with multiple comorbid medical conditions, declining cognitive function and impaired functional status.

The following review will address a number of the challenges and controversies surrounding colorectal cancer and the elderly. First, we will review the epidemiology and clinical presentation of colorectal cancer in the elderly. Second, we will review the efficacy of screening modalities and examine the data regarding when not to screen a patient based on age. Moreover, we will discuss one of the most common colorectal cancer screening modalities, colonoscopy, and how various aspects of this procedure are impacted by age. Finally, we will discuss colorectal cancer treatment and how age influences the efficacy, safety and decision to treat elderly patients with colorectal cancer.

EPIDEMIOLOGY

Colorectal cancer is common in the elderly. Approximately 90% of new colorectal cancers are diagnosed in patients over 50 years3 with the median age of diagnosis being 69 years. Furthermore, the incidence of colorectal cancer dramatically rises as one ages, regardless of sex and racial background (Fig. 1)3 and nearly doubles between the ages of 40 and 80 years.2

Colonic polyps are precursors to the development of colorectal cancer.4 Among precancerous polyps, both adenomatous and advanced adenomatous polyps (defined as polyp size >10 mm, villous/tubulovillous histological features, or having high grade dysplasia) have an increased prevalence and incidence in the elderly.57 In fact, adenoma and advanced adenoma prevalence in persons 70 to 75 years of age is more than double that of persons 40 to 49 years.5,8,9 In contrast, the prevalence of serrated lesions only slightly increases with age.1014 Moreover, age plays a role with respect to a number of other factors related to colonic polyps. Elderly patients are observed to have larger sized and more proximally located adenomatous polyps which may lead to higher rates of colorectal cancer in this population.15

On the other hand, the recurrence of adenomas, advanced adenomas, and serrated lesions is less impacted by age. Age does not appear to influence the recurrence of adenomas after diagnosis from an index colonoscopy.1618 Other factors such as index polyp size,17 number of polyps at index colonoscopy,19 and initial incomplete polyp resection20 are more associated with recurrence. Similar predictors of recurrence are present for advanced adenomas, but age may play a slightly greater role.21,22 In addition to polyp characteristics insufficient bowel preparation and incomplete examination have been additional factors noted to predict the recurrence of advanced adenomas detected on surveillance colonoscopies.19 Limited studies suggest that age does not impact recurrence of serrated polyps23 and consensus guidelines on surveillance intervals for serrated lesions focus more on the size, number and location of the index serrated lesion(s).24 While colorectal cancer incidence increases with age, the recurrence of it is not. Rather family history, findings on index colonoscopy25,26 and presenting symptoms,27 have a much stronger association (Table 1).

Given that age does not strongly influence the recurrence of either colonic polyps or colorectal cancer, surveillance guidelines have not been tailored by age.

PRESENTATION

Colorectal cancer presentation is similar in younger and older patients although more proximal cancer is detected in older patients.7 Likewise older patients may be less likely to present asymptomatically.28,29 Elderly patients with colorectal cancer may have a range of symptoms that include occult blood loss, rectal bleeding, change in stool caliber, unintentional weight loss or have signs of bowel obstruction or perforation. While no one presenting symptom predominates in elderly patients, it should be recognized that elderly patients may have a more subtle presentation of colorectal cancer such as vague abdominal pain or a new microcytic anemia. Such symptoms cannot be attributed to other etiologies and deserve a thorough cancer evaluation.

SCREENING MODALITIES FOR COLORECTAL CANCER

Colorectal cancer screening, which detects both precancerous polyps and colorectal cancer, can reduce both colorectal cancer incidence and mortality.3040 Through screening the incidence of colorectal cancer can be reduced by 17% to 33% with a mortality reduction of 11% to 53% depending on the modality employed.3034,36,37 While no one screening method is advocated a number of consensus documents offer several screening recommendations including those from the U.S. Preventative Services Task Force,41 American Cancer Society, U.S. Multi-Society Taskforce with the American College of Radiology,42 American College of Gastroenterology,43 and the National Comprehensive Cancer Network.44 Screening tests available and recommended include examining stool for occult blood or newer tests examining DNA mutations/alterations,45 radiologic or endoscopic methods (Table 2). To date, no one screening test has proven superior for colorectal cancer screening in the elderly.

1. Colonoscopy in elderly patients

Lower endoscopy, specifically colonoscopy, has been shown to significantly reduce both distal and proximal colorectal cancer in older individuals.46 As more elderly patients undergo colorectal cancer screening using colonoscopy one has to consider how specific factors, such as age, related to this procedure may interact with one another.

Several reviews4750 have addressed a number of issues related to the elderly and endoscopy. Few changes are recommended for elderly patients with respect to the preprocedure process and sedation, but some differences have been clarified. During the preprocedure assessment it is recommended that providers assess for elderly patient’s cognitive ability and capacity to understand the procedure and that functional status and depression screening be documented in an elderly patient’s medical record when they are undergoing endoscopy.50,51 Second, providers should use fewer sedative medications, at lower doses and be infused at slower rates when an elderly patient is being sedated.50 Furthermore, early recognition by the endoscopist of multiple factors such as an elderly patient’s comorbid medical conditions, cognitive function, mobility and polypharmacy need to occur prior to performing endoscopy.

2. Adverse events

The occurrence of adverse events during colonoscopy and how age may modify this risk are important considerations for the elderly patient. Age does not play a role in minor adverse events such as abdominal pain.52 Yet, major adverse events such as perforation, bleeding and cardiopulmonary complications are all affected by age, though the individual risk varies and can be influenced by additional factors. Of all adverse events associated with colonoscopy, the greatest risk associated with age is perforation. For example, elderly patients have a 30% higher risk of experiencing a perforation than younger patients undergoing colonoscopy and a 14-fold higher risk of having a perforation than patients of the same age who do not undergo the procedure.53 Lastly, older patients with more comorbid medical conditions have a greater risk of experiencing an adverse event if the colonoscopy is performed under general anesthesia.54

3. Bowel preparation

Bowel preparation is a significant issue to consider in patients undergoing colonoscopy. Two agents are available (polyethylene glycol electrolyte lavage solution [PEG] and oral sodium phosphate [OSP]). A number of adverse events are observed in elderly patients taking PEG and OSPs (Table 3). PEG has a much better safety profile compared to OSPs with a major concern that elderly patients taking OSPs are at greater risk of having electrolyte disturbances55,56 and experiencing acute kidney injury.15,57 It is for this reason that OSPs are no longer recommended in the elderly and that PEG is the preferred bowel preparation agent for this patient population.

However, there are concerns with PEG in regards to tolerability and compliance in the elderly with noncompliance rates of 3% to 32%.58 Also concerns do remain with the elderly being able to tolerate such a large volume of fluid required with PEG. While spilt PEG dosing regimens have been shown to be more effective59 versus standard one time dosing, this approach has not been well studied in the elderly. Finally, of critical importance is that elderly patients remain adequately hydrated when taking PEG.60

Poor bowel preparations in the elderly undergoing colonoscopy range from 4% to 57%29,6169 with bowel preparation being more difficult to achieve in very elderly patients (e.g., patients >80 years).63,67 Poorer bowel preparations observed in the elderly can occur for a variety of reasons including altered gastrointestinal motility, increased rates of medication-related constipation, previous surgeries, decreased understanding of bowel preparation instructions, greater burden of comorbid medical conditions, and/or functional limitations.

4. Completion of colonoscopy

Key to a high quality colonoscopy is the successful completion of it (e.g., intubation of the cecum). Endoscopists subjectively judge a colonoscopy to be more difficult in an elderly patient,70 but completion rates vary from 78% to 86% in the elderly and 52% to 95%61,62,71 in the very elderly.29,6365,6769 Age may be an independent risk factor for lower completions rates, but it is apparent that other factors such as poor bowel preparation and a patient’s underlying disease process play a stronger role.61,72

DECISIONS REGARDING NOT TO SCREEN FOR COLORECTAL CANCER IN THE ELDERLY

1. Comorbid medical conditions in the elderly and screening

Elderly patients have a greater number and severity of comorbid medical conditions with over one-quarter of patients >65 years of age having more than five comorbid medical conditions.73 This increase in comorbid medical conditions can impact not only the development of colorectal cancer, but can also reduce the benefit from screening and treatment in older patients. It is evident that the benefit of screening is reduced with increasing disease burden. For example, the greatest number needed to screen to prevent a colorectal cancer death is in older, more ill patients. Compounding this issue further is that screening related adverse events are greater than the benefit in this same group of patients.74,75 Furthermore, patients with greater comorbid medical conditions have lower survival rates after an initial diagnosis of colorectal cancer,7678 poorer survival after chemotherapy78,79 and prolonged hospitalizations as a consequence of their colorectal cancer.80

2. Debate on when to discontinue colorectal cancer screening in the elderly

Detecting colorectal cancer earlier is clearly beneficial but several controversial questions remain.

One important question is: Does screening extend life in older patients who may have a shorter life expectancy? On this topic a number of modeling studies have examined the impact of various colorectal screening methods on life expectancy at different age groups.8183 Younger patients have a greater decrease in life expectancy than do elderly patients after a diagnosis of colorectal cancer. At the same time, there is a 75% reduction in the benefit of screening for elderly patients when compared with younger patients regardless of which screening modality is used. Identical results have been noted in clinical studies addressing this same question. These studies have illustrated that the benefit of screening, after an initial negative screening test, is reduced in elderly patients as this group has a greater chance of passing away from other illnesses besides colorectal cancer.76 As a further example, in a recent study of elderly patients who had a positive fecal occult blood test, nearly half of the patients who did not undergo colonoscopy died from other causes. Of those who underwent colonoscopy 10% experienced an adverse event and the overwhelming majority of patients with a worse life expectancy obtained little benefit from screening.84

A second question that arises is: At what point does colorectal cancer screening cease to provide an important extension in life expectancy and therefore not be offered? Multiple studies have tackled this question and examined various ages at which colorectal cancer screening should be discontinued. A number of ages at which to stop screening have been proposed. Some have demonstrated that decreasing the screening age from 85 to 75 years yields small reductions in life years gained as well as utilizes fewer resources, and have concluded that stopping screening at 75 provides almost the same benefit as stopping at 85 years.85 Others have demonstrated diminishing returns for days of life lost after the age of 70 for any form of screening86 and that after the age of 60 the percentage of life years saved declines precipitously after a single colonoscopy.82 While this debate continues at lower ages, there does appear to be clear evidence and consensus on an age in which some patients achieve no benefit from screening. Men >85 years and women >90 years do not achieve any benefit from colorectal cancer screening regardless of modality,74 and patients over 80 years have a shortened life expectancy (median survival of <5 years) after a diagnosis of colorectal cancer regardless of comorbid medical conditions or functional status.76 Unfortunately, there is very little guidance on when to stop screening from national medical societies (Table 4).

In summary, health, life expectancy and functional status as well as age should all play a role when considering the option to discontinue colorectal cancer screening. However, this practice is quite variable. Some providers take an individualized approach with their elderly patients and colorectal cancer screening with more physicians choosing to engage healthier elderly patients.87 Whereas, a larger body of evidence suggests that others perform inappropriate colorectal cancer screening in patients with severe comorbid medical conditions and low life expectancies.88,89 Such disparities in practice highlight the need for greater education among providers on colorectal cancer screening in the elderly.

TREATMENT

Treatment for colorectal cancer (both surgical and medical) in the elderly differs in comparison with younger patients. First, age plays a role in outcomes and the type of colorectal cancer surgery selected. Laparoscopic colorectal cancer surgery in the elderly appears to be a more effective procedure compared with an open approach with equal cure rates between the two procedures, but less adverse events,90 less blood loss9092 and shorter postoperative hospitalizations9092 noted with laparoscopic colectomy performed in elderly patients with colorectal cancer. Also, older patients are observed to have higher mortality rates after colorectal cancer surgery.93 Second, age impacts medical treatment for colorectal cancer, but to a lesser degree. Many oncologists reduce the dose of chemotherapy for perceived risks of impaired liver or renal function in older patients.94 However, most chemotherapeutic agents are safe in the elderly and can achieve the same therapeutic benefits of reduced recurrence and mortality as observed in younger patients, especially in the adjuvant setting.9597 Given this data most advocate that age alone not factor into one’s decision to treat colorectal cancer.95,98,99 One limitation of the current literature on chemotherapy data for colorectal cancer and the elderly is that advanced age is an exclusion factor in many clinical trials.98,100102 In fact, comorbid medical conditions play a much larger role in the decision to proceed with chemotherapy as this has a more pronounced impact on life expectancy after colorectal cancer diagnosis and treatment.78

Likewise, age appears to factor into colorectal cancer treatment on a number of other fronts. Elderly patients with colorectal cancer are less frequently discussed at multidisciplinary cancer team meetings,103,104 undergo less surgery,103,104 have less adjuvant chemotherapy prescribed,103,105,106 and undergo less palliative therapy.105 Furthermore, colorectal cancer is more complicated in older patients at diagnosis105 with more emergency surgery performed in the elderly.104 Also, while elderly patients represent half of metastatic colorectal cancer diagnoses, their survival is significantly less compared to younger patients with metastatic colorectal cancer.107 These data do not suggest these differences are appropriate or inappropriate, but rather that age impacts colorectal cancer treatment.

As a final point, with respect to colorectal cancer treatments in the elderly, oncologists do advocate the use of a variety of tools and approaches to help guide treatment decisions. The Comprehensive Geriatric Assessment was developed to evaluate elderly patients being considered for colorectal cancer treatment and its use has proven effective in reducing adverse outcomes among the elderly.108,109 Also, oncologists promote a multidisciplinary approach in treating elderly patients with colorectal cancer. A patient’s functional status, comorbid medical conditions, and preferences as well as cancer stage all have to be factored into the decision of determining what regimen (if any) to use when treating the elderly patient with colorectal cancer.98,100

SUMMARY

Overall, a disproportionate number of colorectal cancer diagnoses and deaths occur in elderly patients. Advancing age is an independent risk factor associated with both colorectal cancer and adenomas whereas the detection of recurrent colorectal cancer and adenomas after a screening colonoscopy is not affected by age. A number of colorectal cancer screening modalities are available for elderly patients, but it is important to remember that at specific ages the risks and increased resources may outweigh the benefit of screening in some elderly patients. Controversy exists over when to discontinue colorectal cancer screening and surveillance in the elderly. Yet, most agree that the decision to proceed with screening and surveillance requires an individualized assessment of the elderly patient that takes into account the risks and benefits and balances this with the patients’ health, functional status, and preferences. Some aspects of screening, such as with colonoscopy, need to be factored into this decision making process. Older patients have a higher risk of adverse events during a colonoscopy, poorer bowel preparations and possibly lower successful completion rates. Finally, a variety of colorectal cancer treatments are available for elderly patients and, just as with decisions about when to discontinue screening, a patient’s functional status, comorbid medical conditions, and preferences have to be factored into the decision making process when determining which treatment regimen to offer.

Fig 1.

Figure 1.Incidence rates for colon and rectal cancer for all races and both sexes from 2006 to 2010 in the U.S. population.
Gut and Liver 2015; 9: 143-151https://doi.org/10.5009/gnl14302

Table 1 Factors that Increase the Recurrence Risk of Adenomas, Advanced Adenomas, and Colorectal Cancer

Adenomas
 Index polyp size (polyp >1 cm)
 Number of index polyps
 Incomplete polypectomy
Advanced adenomas
 Number of index adenomas
 Index polyp size (polyp >1 cm)
 Villous histology on pathology
 Insufficient bowel preparation
 Incomplete examination (unable to reach farther than the distal colon)
Colorectal cancer
 Family history of colorectal cancer
 Presence of extracolonic malignancy
 Detection of synchronous lesions
 Coexisting adenomas
 Perforation at time of diagnosis
 Symptoms

Table 2 Colorectal Cancer Screening Tests

Occult blood
 High sensitivity guaiac-based fecal occult blood test (gFOBT)
 Fecal immunochemical test (FIT)
 Multitarget stool DNA test*
Endoscopy
 Colonoscopy
 Flexible sigmoidoscopy
Radiology
 Double contrast barium enema
 Computerized tomography colonography

*Quantitative molecular assays for KRAS mutations, aberrant NDRG4 and BMP3 methylation and β-actin, in addition to a hemoglobin assay performed on stool samples.


Table 3 Adverse Events Associated with Bowel Preparation in Elderly Patients

PEG (%)
 Dizziness (48)
 Fecal incontinence (27–39)
 Abdominal pain (7–23)
 Nausea (2–17.5)
 Insomnia (13)
 Fatigue (12.7)
 Headache (7.9)
 Hypokalemia (2.9–20.5)
 Dysnatremia (hyponatremia/hypernatremia) (4.1)
 Emesis (3.2)
 Aspiration pneumonia (<1)
 Pancreatitis (<1)
 Ischemic colitis (<1)
OSP (%)
 Hyperphosphatemia (58.1–100)
 Fecal incontinence (23–55)
 Elevated creatinine/renal injury (55.2)
 Hypocalcemia (5.1–58)
 Hypokalemia (5.4–56)
 Abdominal pain (11–32)
 Nausea (9–36)
 Insomnia (15)
 Dizziness (3–55)
 Emesis (4–7)
 Hypotension (4)

PEG, polyethylene glycol; OSP, oral sodium phosphate.


Table 4 Colorectal Cancer Screening Guidelines and the Elderly

SocietyRecommendation
U.S. Multi-Society Task Force and the American Cancer Society (USMSTF/ACS)In those with a prior polyp: discontinuation of surveillance colonoscopy should be considered in persons with serious comorbidities and with less than 10 years of life expectancy.
American Gastroenterological Association (AGA)No comment on when to stop screening. Comment on need for shared decision making and individualized approach.
American Geriatrics Society (AGS)Not recommended in those unlikely to live more than 5 years or who have significant comorbidity that would preclude treatment.
British Society of GastroenterologyFecal occult blood test every 2 years offered to all persons 50–69 years of age (depending on location) with current plans to extend to age 75 in most areas.
Kaiser Permanent Care Management Institute (KPCMI)Discontinuation of screening is generally recommended at age 75, provided that there is a history of routine screening.
Discontinuation is recommended at age 80 for those with no history of routine screening. The decision to discontinue screening should be based on physician judgment, patient preference, the increased risk of complications in older adults, and existing comorbidities.

References

  1. Ferlay J, Pisani P, Parkin DM, International Agency for Research on Cancer. GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide. Lyon: IARC Press.
  2. Rabeneck, L, El-Serag, HB, Davila, JA, Sandler, RS. Outcomes of colorectal cancer in the United States: no change in survival (1986?1997). Am J Gastroenterol, 2003;98;471-477.
    Pubmed
  3. Howlader N, Krapcho M, Garshell J. SEER cancer statistics review, 1975?2010 [Internet]. Bethesda: National Cancer Institute, [cited 2013 Jul 20]. Available from: http://seer.cancer.gov/csr/1975_2010/
  4. Vogelstein, B, Fearon, ER, Hamilton, SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med, 1988;319;525-532.
    Pubmed CrossRef
  5. Lieberman, DA, Weiss, DG, Bond, JH, Ahnen, DJ, Garewal, H, Chejfec, G. Use of colonoscopy to screen asymptomatic adults for colorectal cancer: Veterans Affairs Cooperative Study Group 380. N Engl J Med, 2000;343;162-168.
    Pubmed CrossRef
  6. Khullar, SK, DiSario, JA. Colon cancer screening: sigmoidoscopy or colonoscopy. Gastrointest Endosc Clin N Am, 1997;7;365-386.
    Pubmed
  7. Neugut, AI, Jacobson, JS, De Vivo, I. Epidemiology of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev, 1993;2;159-176.
    Pubmed
  8. Strul, H, Kariv, R, Leshno, M, et al. The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40?80 years. Am J Gastroenterol, 2006;101;255-262.
    Pubmed CrossRef
  9. Imperiale, TF, Wagner, DR, Lin, CY, Larkin, GN, Rogge, JD, Ransohoff, DF. Results of screening colonoscopy among persons 40 to 49 years of age. N Engl J Med, 2002;346;1781-1785.
    Pubmed CrossRef
  10. Omata, F, Brown, WR, Tokuda, Y, et al. Modifiable risk factors for colorectal neoplasms and hyperplastic polyps. Intern Med, 2009;48;123-128.
    Pubmed CrossRef
  11. Lieberman, DA, Prindiville, S, Weiss, DG, Willett, W, VA Cooperative Study Group 380. Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA, 2003;290;2959-2967.
    Pubmed CrossRef
  12. Johannsen, LG, Momsen, O, Jacobsen, NO. Polyps of the large intestine in Aarhus, Denmark: an autopsy study. Scand J Gastroenterol, 1989;24;799-806.
    Pubmed CrossRef
  13. Williams, AR, Balasooriya, BA, Day, DW. Polyps and cancer of the large bowel: a necropsy study in Liverpool. Gut, 1982;23;835-842.
    Pubmed KoreaMed CrossRef
  14. Vatn, MH, Stalsberg, H. The prevalence of polyps of the large intestine in Oslo: an autopsy study. Cancer, 1982;49;819-825.
    Pubmed CrossRef
  15. Singal, AK, Rosman, AS, Post, JB, Bauman, WA, Spungen, AM, Korsten, MA. The renal safety of bowel preparations for colonoscopy: a comparative study of oral sodium phosphate solution and polyethylene glycol. Aliment Pharmacol Ther, 2008;27;41-47.
    Pubmed CrossRef
  16. Noshirwani, KC, van Stolk, RU, Rybicki, LA, Beck, GJ. Adenoma size and number are predictive of adenoma recurrence: implications for surveillance colonoscopy. Gastrointest Endosc, 2000;51;433-437.
    Pubmed CrossRef
  17. Harewood, GC, Lawlor, GO. Incident rates of colonic neoplasia according to age and gender: implications for surveillance colonoscopy intervals. J Clin Gastroenterol, 2005;39;894-899.
    Pubmed CrossRef
  18. Harewood, GC, Lawlor, GO, Larson, MV. Incident rates of colonic neoplasia in older patients: when should we stop screening?. J Gastroenterol Hepatol, 2006;21;1021-1025.
    Pubmed CrossRef
  19. van Heijningen, EM, Lansdorp-Vogelaar, I, Kuipers, EJ, et al. Features of adenoma and colonoscopy associated with recurrent colorectal neoplasia based on a large community-based study. Gastroenterology, 2013;144;1410-1418.
    Pubmed CrossRef
  20. Pohl, H, Srivastava, A, Bensen, SP, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology, 2013;144;74-80.e1.
    Pubmed CrossRef
  21. Mart?nez, ME, Baron, JA, Lieberman, DA, et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology, 2009;136;832-841.
    Pubmed KoreaMed CrossRef
  22. Saini, SD, Kim, HM, Schoenfeld, P. Incidence of advanced adenomas at surveillance colonoscopy in patients with a personal history of colon adenomas: a meta-analysis and systematic review. Gastrointest Endosc, 2006;64;614-626.
    Pubmed CrossRef
  23. Teriaky, A, Driman, DK, Chande, N. Outcomes of a 5-year follow-up of patients with sessile serrated adenomas. Scand J Gastroenterol, 2012;47;178-183.
    Pubmed CrossRef
  24. Rex, DK, Ahnen, DJ, Baron, JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol, 2012;107;1315-1329.
    Pubmed KoreaMed CrossRef
  25. Togashi, K, Konishi, F, Ozawa, A, et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum, 2000;43;S47-S53.
    Pubmed CrossRef
  26. Harris, GJ, Church, JM, Senagore, AJ, et al. Factors affecting local recurrence of colonic adenocarcinoma. Dis Colon Rectum, 2002;45;1029-1034.
    Pubmed CrossRef
  27. M?kel?, JT, Laitinen, SO, Kairaluoma, MI. Five-year follow-up after radical surgery for colorectal cancer: results of a prospective randomized trial. Arch Surg, 1995;130;1062-1067.
    Pubmed CrossRef
  28. Trombold, J, Farmer, RW, McCafferty, M. The impact of colorectal cancer screening in a veteran hospital population. Am Surg, 2013;79;296-300.
    Pubmed
  29. Bat, L, Pines, A, Shemesh, E, et al. Colonoscopy in patients aged 80 years or older and its contribution to the evaluation of rectal bleeding. Postgrad Med J, 1992;68;355-358.
    Pubmed KoreaMed CrossRef
  30. Faivre, J, Dancourt, V, Lejeune, C, et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study. Gastroenterology, 2004;126;1674-1680.
    Pubmed CrossRef
  31. Hardcastle, JD, Chamberlain, JO, Robinson, MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet, 1996;348;1472-1477.
    Pubmed CrossRef
  32. Kronborg, O, Fenger, C, Olsen, J, Jørgensen, OD, Søndergaard, O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet, 1996;348;1467-1471.
    Pubmed CrossRef
  33. Lindholm, E, Brevinge, H, Haglind, E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg, 2008;95;1029-1036.
    Pubmed CrossRef
  34. Mandel, JS, Bond, JH, Church, TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood: Minnesota Colon Cancer Control Study. N Engl J Med, 1993;328;1365-1371.
    Pubmed CrossRef
  35. Quintero, E, Castells, A, Bujanda, L, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med, 2012;366;697-706.
    Pubmed CrossRef
  36. Atkin, WS, Edwards, R, Kralj-Hans, I, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet, 2010;375;1624-1633.
    Pubmed CrossRef
  37. Segnan, N, Senore, C, Andreoni, B, et al. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. J Natl Cancer Inst, 2005;97;347-357.
    Pubmed CrossRef
  38. Schoen, RE, Pinsky, PF, Weissfeld, JL, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med, 2012;366;2345-2357.
    Pubmed KoreaMed CrossRef
  39. Zauber, AG, Winawer, SJ, O’Brien, MJ, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med, 2012;366;687-696.
    Pubmed KoreaMed CrossRef
  40. Robertson, DJ, Greenberg, ER, Beach, M, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology, 2005;129;34-41.
    Pubmed CrossRef
  41. U. S. Preventive Services Task Force. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med, 2008;149;627-637.
    Pubmed CrossRef
  42. Levin, B, Lieberman, DA, McFarland, B, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology, 2008;134;1570-1595.
    Pubmed CrossRef
  43. Rex, DK, Johnson, DA, Anderson, JC, et al. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol, 2009;104;739-750.
    Pubmed CrossRef
  44. Benson, AB, Arnoletti, JP, Bekaii-Saab, T, et al. Colon cancer. J Natl Compr Canc Netw, 2011;9;1238-1290.
    Pubmed
  45. Imperiale, TF, Ransohoff, DF, Itzkowitz, SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med, 2014;370;1287-1297.
    Pubmed CrossRef
  46. Kahi, CJ, Myers, LJ, Slaven, JE, et al. Lower endoscopy reduces colorectal cancer incidence in older individuals. Gastroenterology, 2014;146;718-725.e3.
    Pubmed CrossRef
  47. Day, LW, Walter, LC, Velayos, F. Colorectal cancer screening and surveillance in the elderly patient. Am J Gastroenterol, 2011;106;1197-1206.
    Pubmed CrossRef
  48. Travis, AC, Pievsky, D, Saltzman, JR. Endoscopy in the elderly. Am J Gastroenterol, 2012;107;1495-1501.
    Pubmed CrossRef
  49. Jafri, SM, Monkemuller, K, Lukens, FJ. Endoscopy in the elderly: a review of the efficacy and safety of colonoscopy, esophagogastroduodenoscopy, and endoscopic retrograde cholangiopancreatography. J Clin Gastroenterol, 2010;44;161-166.
    Pubmed CrossRef
  50. Chandrasekhara, V, Early, DS, et al, ASGE Standards of Practice Committee. Modifications in endoscopic practice for the elderly. Gastrointest Endosc, 2013;78;1-7.
    Pubmed CrossRef
  51. Chow, WB, Rosenthal, RA, Merkow, RP, et al. Optimal preoperative assessment of the geriatric surgical patient: a best practices guideline from the American College of Surgeons National Surgical Quality Improvement Program and the American Geriatrics Society. J Am Coll Surg, 2012;215;453-466.
    Pubmed CrossRef
  52. Ko, CW, Riffle, S, Shapiro, JA, et al. Incidence of minor complications and time lost from normal activities after screening or surveillance colonoscopy. Gastrointest Endosc, 2007;65;648-656.
    Pubmed CrossRef
  53. Day, LW, Kwon, A, Inadomi, JM, Walter, LC, Somsouk, M. Adverse events in older patients undergoing colonoscopy: a systematic review and meta-analysis. Gastrointest Endosc, 2011;74;885-896.
    Pubmed KoreaMed CrossRef
  54. Cooper, GS, Kou, TD, Rex, DK. Complications following colonoscopy with anesthesia assistance: a population-based analysis. JAMA Intern Med, 2013;173;551-556.
    Pubmed KoreaMed CrossRef
  55. Beloosesky, Y, Grinblat, J, Weiss, A, Grosman, B, Gafter, U, Chagnac, A. Electrolyte disorders following oral sodium phosphate administration for bowel cleansing in elderly patients. Arch Intern Med, 2003;163;803-808.
    Pubmed CrossRef
  56. Caswell, M, Thompson, WO, Kanapka, JA, Galt, DJ. The time course and effect on serum electrolytes of oral sodium phosphates solution in healthy male and female volunteers. Can J Clin Pharmacol, 2007;14;e260-e274.
    Pubmed
  57. Russmann, S, Lamerato, L, Marfatia, A, et al. Risk of impaired renal function after colonoscopy: a cohort study in patients receiving either oral sodium phosphate or polyethylene glycol. Am J Gastroenterol, 2007;102;2655-2663.
    Pubmed CrossRef
  58. Hsu, CW, Imperiale, TF. Meta-analysis and cost comparison of polyethylene glycol lavage versus sodium phosphate for colonoscopy preparation. Gastrointest Endosc, 1998;48;276-282.
    Pubmed CrossRef
  59. Cohen, LB. Split dosing of bowel preparations for colonoscopy: an analysis of its efficacy, safety, and tolerability. Gastrointest Endosc, 2010;72;406-412.
    Pubmed CrossRef
  60. Lichtenstein, GR, Cohen, LB, Uribarri, J. Review article: bowel preparation for colonoscopy. The importance of adequate hydration. Aliment Pharmacol Ther, 2007;26;633-641.
    Pubmed CrossRef
  61. Karajeh, MA, Sanders, DS, Hurlstone, DP. Colonoscopy in elderly people is a safe procedure with a high diagnostic yield: a prospective comparative study of 2000 patients. Endoscopy, 2006;38;226-230.
    Pubmed CrossRef
  62. Ma, WT, Mahadeva, S, Kunanayagam, S, Poi, PJ, Goh, KL. Colonoscopy in elderly Asians: a prospective evaluation in routine clinical practice. J Dig Dis, 2007;8;77-81.
    Pubmed CrossRef
  63. Lukens, FJ, Loeb, DS, Machicao, VI, Achem, SR, Picco, MF. Colonoscopy in octogenarians: a prospective outpatient study. Am J Gastroenterol, 2002;97;1722-1725.
    Pubmed CrossRef
  64. Burtin, P, Bour, B, Charlois, T, et al. Colonic investigations in the elderly: colonoscopy or barium enema?. Aging (Milano), 1995;7;190-194.
    Pubmed
  65. Chatrenet, P, Friocourt, P, Ramain, JP, Cherrier, M, Maillard, JB. Colonoscopy in the elderly: a study of 200 cases. Eur J Med, 1993;2;411-413.
    Pubmed
  66. George, ML, Tutton, MG, Jadhav, VV, Abulafi, AM, Swift, RI. Colonoscopy in older patients: a safe and sound practice. Age Ageing, 2002;31;80-81.
    Pubmed CrossRef
  67. Schmilovitz-Weiss, H, Weiss, A, Boaz, M, Levin, I, Chervinski, A, Shemesh, E. Predictors of failed colonoscopy in nonagenarians: a single-center experience. J Clin Gastroenterol, 2007;41;388-393.
    Pubmed CrossRef
  68. Duncan, JE, Sweeney, WB, Trudel, JL, Madoff, RD, Mellgren, AF. Colonoscopy in the elderly: low risk, low yield in asymptomatic patients. Dis Colon Rectum, 2006;49;646-651.
    Pubmed CrossRef
  69. Syn, WK, Tandon, U, Ahmed, MM. Colonoscopy in the very elderly is safe and worthwhile. Age Ageing, 2005;34;510-513.
    Pubmed CrossRef
  70. Ristikankare, M, Hartikainen, J, Heikkinen, M, Janatuinen, E, Julkunen, R. The effects of gender and age on the colonoscopic examination. J Clin Gastroenterol, 2001;32;69-75.
    Pubmed CrossRef
  71. Ure, T, Dehghan, K, Vernava, AM, Longo, WE, Andrus, CA, Daniel, GL. Colonoscopy in the elderly: low risk, high yield. Surg Endosc, 1995;9;505-508.
    Pubmed CrossRef
  72. Nelson, DB, McQuaid, KR, Bond, JH, Lieberman, DA, Weiss, DG, Johnston, TK. Procedural success and complications of large-scale screening colonoscopy. Gastrointest Endosc, 2002;55;307-314.
    Pubmed CrossRef
  73. Yancik, R. Cancer burden in the aged: an epidemiologic and demographic overview. Cancer, 1997;80;1273-1283.
    Pubmed CrossRef
  74. Ko, CW, Sonnenberg, A. Comparing risks and benefits of colorectal cancer screening in elderly patients. Gastroenterology, 2005;129;1163-1170.
    Pubmed CrossRef
  75. Warren, JL, Klabunde, CN, Mariotto, AB, et al. Adverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med, 2009;150;849-857.
    Pubmed CrossRef
  76. Kahi, CJ, Azzouz, F, Juliar, BE, Imperiale, TF. Survival of elderly persons undergoing colonoscopy: implications for colorectal cancer screening and surveillance. Gastrointest Endosc, 2007;66;544-550.
    Pubmed CrossRef
  77. van de Poll-Franse, LV, Haak, HR, Coebergh, JW, Janssen-Heijnen, ML, Lemmens, VE. Disease-specific mortality among stage I?III colorectal cancer patients with diabetes: a large population-based analysis. Diabetologia, 2012;55;2163-2172.
    Pubmed KoreaMed CrossRef
  78. Gross, CP, McAvay, GJ, Guo, Z, Tinetti, ME. The impact of chronic illnesses on the use and effectiveness of adjuvant chemotherapy for colon cancer. Cancer, 2007;109;2410-2419.
    Pubmed CrossRef
  79. Stavrou, EP, Lu, CY, Buckley, N, Pearson, S. The role of comorbidities on the uptake of systemic treatment and 3-year survival in older cancer patients. Ann Oncol, 2012;23;2422-2428.
    Pubmed CrossRef
  80. Sarfati, D, Tan, L, Blakely, T, Pearce, N. Comorbidity among patients with colon cancer in New Zealand. N Z Med J, 2011;124;76-88.
    Pubmed
  81. Inadomi, JM, Sonnenberg, A. The impact of colorectal cancer screening on life expectancy. Gastrointest Endosc, 2000;51;517-523.
    Pubmed CrossRef
  82. Sonnenberg, A, Delc?, F. Cost-effectiveness of a single colonoscopy in screening for colorectal cancer. Arch Intern Med, 2002;162;163-168.
    Pubmed CrossRef
  83. Lin, OS, Kozarek, RA, Schembre, DB, et al. Screening colonoscopy in very elderly patients: prevalence of neoplasia and estimated impact on life expectancy. JAMA, 2006;295;2357-2365.
    Pubmed CrossRef
  84. Kistler, CE, Kirby, KA, Lee, D, Casadei, MA, Walter, LC. Long-term outcomes following positive fecal occult blood test results in older adults: benefits and burdens. Arch Intern Med, 2011;171;1344-1351.
    Pubmed KoreaMed CrossRef
  85. Zauber, AG, Lansdorp-Vogelaar, I, Knudsen, AB, Wilschut, J, van Ballegooijen, M, Kuntz, KM. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med, 2008;149;659-669.
    Pubmed KoreaMed CrossRef
  86. Maheshwari, S, Patel, T, Patel, P. Screening for colorectal cancer in elderly persons: who should we screen and when can we stop?. J Aging Health, 2008;20;126-139.
    Pubmed CrossRef
  87. Lewis, CL, Esserman, D, DeLeon, C, Pignone, MP, Pathman, DE, Golin, C. Physician decision making for colorectal cancer screening in the elderly. J Gen Intern Med, 2013;28;1202-1207.
    Pubmed KoreaMed CrossRef
  88. Walter, LC, Lindquist, K, Nugent, S, et al. Impact of age and comorbidity on colorectal cancer screening among older veterans. Ann Intern Med, 2009;150;465-473.
    Pubmed KoreaMed CrossRef
  89. Mittal, S, Lin, YL, Tan, A, Kuo, YF, El-Serag, HB, Goodwin, JS. Limited life expectancy among a subgroup of medicare beneficiaries receiving screening colonoscopies. Clin Gastroenterol Hepatol, 2014;12;443-450.e1.
    Pubmed KoreaMed CrossRef
  90. Fujii, S, Ishibe, A, Ota, M, et al. Short-term results of a randomized study between laparoscopic and open surgery in elderly colorectal cancer patients. Surg Endosc, 2014;28;466-476.
    Pubmed CrossRef
  91. Hatakeyama, T, Nakanishi, M, Murayama, Y, et al. Laparoscopic resection for colorectal cancer improves short-term outcomes in very elderly colorectal cancer patients. Surg Laparosc Endosc Percutan Tech, 2013;23;532-535.
    Pubmed CrossRef
  92. Nakamura, T, Sato, T, Miura, H, et al. Feasibility and outcomes of surgical therapy in very elderly patients with colorectal cancer. Surg Laparosc Endosc Percutan Tech, 2014;24;85-88.
    Pubmed CrossRef
  93. Ahmed, S, Howel, D, Debrah, S, NORCCAG (Northern Region Colorectal Cancer Audit Group). The influence of age on the outcome of treatment of elderly patients with colorectal cancer. J Geriatr Oncol, 2014;5;133-140.
    Pubmed CrossRef
  94. Shayne, M, Culakova, E, Wolff, D, et al. Dose intensity and hematologic toxicity in older breast cancer patients receiving systemic chemotherapy. Cancer, 2009;115;5319-5328.
    Pubmed CrossRef
  95. Dotan, E, Browner, I, Hurria, A, Denlinger, C. Challenges in the management of older patients with colon cancer. J Natl Compr Canc Netw, 2012;10;213-224.
    Pubmed KoreaMed
  96. Sundararajan, V, Mitra, N, Jacobson, JS, Grann, VR, Heitjan, DF, Neugut, AI. Survival associated with 5-fluorouracil-based adjuvant chemotherapy among elderly patients with node-positive colon cancer. Ann Intern Med, 2002;136;349-357.
    Pubmed CrossRef
  97. Jehn, CF, B?ning, L, Kr?ning, H, Pezzutto, A, L?ftner, D. Influence of comorbidity, age and performance status on treatment efficacy and safety of cetuximab plus irinotecan in irinotecan-refractory elderly patients with metastatic colorectal cancer. Eur J Cancer, 2014;50;1269-1275.
    Pubmed CrossRef
  98. Leo, S, Accettura, C, Gnoni, A, et al. Systemic treatment of gastrointestinal cancer in elderly patients. J Gastrointest Cancer, 2013;44;22-32.
    Pubmed CrossRef
  99. Balducci, L. Geriatric oncology. Crit Rev Oncol Hematol, 2003;46;211-220.
    Pubmed CrossRef
  100. Feliu, J, Sereno, M, Castro, JD, Belda, C, Casado, E, Gonz?lez-Bar?n, M. Chemotherapy for colorectal cancer in the elderly: whom to treat and what to use. Cancer Treat Rev, 2009;35;246-254.
    Pubmed CrossRef
  101. Yee, KW, Pater, JL, Pho, L, Zee, B, Siu, LL. Enrollment of older patients in cancer treatment trials in Canada: why is age a barrier?. J Clin Oncol, 2003;21;1618-1623.
    Pubmed CrossRef
  102. Lewis, JH, Kilgore, ML, Goldman, DP, et al. Participation of patients 65 years of age or older in cancer clinical trials. J Clin Oncol, 2003;21;1383-1389.
    Pubmed CrossRef
  103. Guillerme, F, Clavier, JB, Nehme-Schuster, H, et al. Age impacts the pattern of care for elderly patients with rectal cancer. Int J Colorectal Dis, 2014;29;157-163.
    Pubmed CrossRef
  104. Egenvall, M, Schubert Samuelsson, K, Klarin, I, et al. Management of colon cancer in the elderly: a population-based study. Colorectal Dis, 2014;16;433-441.
    Pubmed CrossRef
  105. Doat, S, Thi?baut, A, Samson, S, Ricordeau, P, Guillemot, D, Mitry, E. Elderly patients with colorectal cancer: treatment modalities and survival in France. National data from the ThInDiT cohort study. Eur J Cancer, 2014;50;1276-1283.
    Pubmed CrossRef
  106. Kim, GM, Ahn, JB, Rha, SY, et al. Changing treatment patterns in elderly patients with resectable colon cancer. Asia Pac J Clin Oncol, 2013;9;265-272.
    Pubmed CrossRef
  107. Golan, T, Urban, D, Berger, R, Lawrence, YR. Changing prognosis of metastatic colorectal adenocarcinoma: differential improvement by age and tumor location. Cancer, 2013;119;3084-3091.
    Pubmed CrossRef
  108. Wildes, TM, Ruwe, AP, Fournier, C, et al. Geriatric assessment is associated with completion of chemotherapy, toxicity, and survival in older adults with cancer. J Geriatr Oncol, 2013;4;227-234.
    Pubmed KoreaMed CrossRef
  109. Berretta, M, Di Benedetto, F, Di Francia, R, et al. Colorectal cancer in elderly patients: from best supportive care to cure. Anticancer Agents Med Chem, 2013;13;1332-1343.
    Pubmed CrossRef
Gut and Liver

Vol.19 No.1
January, 2025

pISSN 1976-2283
eISSN 2005-1212

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