Hong Kong Med J 2017 Oct;23(5):503–16 | Epub 1 Sep 2017
Cancer screening for older people: to screen or not to screen
Claudia KY Lai, PhD, RN1; Ayumi Igarashi, PhD, RN2; Natalie MY Lau, MN, BA1; Clare TK Yu, BSc1
1 School of Nursing, The Hong Kong Polytechnic University, Hunghom, Hong Kong
2 School of Health Sciences and Nursing, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Corresponding author: Dr Claudia KY Lai (firstname.lastname@example.org)
In this scoping review, the evidence of the benefits of screening older people for the five most common types of cancer in Hong Kong, namely colorectal, lung, breast, liver, and prostate cancers, is discussed. Although cancer treatments can be extensive and a good prognosis is less likely if cancer is diagnosed at a late stage, screening programmes for older people in primary care remain a matter of contention. The general recommendation for the screening of older people is to adopt an individualised approach that takes account of not only age but also co-morbidity, life expectancy, harms and benefits, and patient’s preference.
Cancer, a word that evokes fear in most people, is the second leading cause of death worldwide; 8.8 million of deaths due to cancer are estimated to have occurred in 2015.1 Globally, the most common types of cancer are lung, breast, bowel, and prostate.2 In Hong Kong, the five leading types of cancer (combining both males and females) are, in order of incidence, colorectal, lung, breast, liver, and prostate cancers.3 Because the incidence of cancer increases with age, early detection can help reduce the burden of treatment and is more likely to lead to a better outcome if the cancer is adequately treated. Although there are guidelines on the recommended ages at which to begin screening for different types of cancer, there is less guidance on the screening needs of older adults.4
Controversies over cancer screening for older people
Cancer screening for early detection is promoted globally because of the link between an ageing population and an increase in the prevalence of cancer worldwide, on the supposition that this will improve the prognosis of cancer patients and may therefore be beneficial for older people.5 Of note, 33 countries have joined the International Cancer Screening Network and are participating in active population-based screening programmes for breast, colorectal, cervical, and lung cancers.6 There are practice guidelines recommending the ages at which to start screening for various types of cancer, but there is less information about when to cease screening, specifically in older people. Epidemiological studies of cancer in people aged 70 years or older are rarely reported in the literature; even if there are such studies, only subgroup analyses are found.7 The efficacy of screening older people for cancer remains controversial. Even though cancer rates have increased with age, this does not imply that routine cancer screening is recommended or even appropriate for older people.8
The aims of this review were to examine the evidence regarding screening for cancer in older people and to present an overview of the current state of knowledge about controversies and recommendations with regard to screening for the top five most common kinds of cancer in older people in Hong Kong.
A scoping review was conducted to explicate current discussions of recommendations for screening older adults for cancer. A scoping review was deemed to be appropriate because it is often used to address broad topics, the literature on which may include studies with numerous designs. The approach described by Arksey and O’Malley was adopted.9
The databases of MEDLINE, EMBASE, the Web of Science, the Cochrane Library, CINAHL, and SCOPUS were searched using the following strategies:
• Strategy 1—(Elder*) and (Cancer screening or cancer prevention) and (Mortality or morbidity)
• Strategy 2—(Elder*) and (Cancer screening or cancer prevention) and (Effect or efficacy or effective*)
• Strategy 1—(Elder*) and (Cancer screening or cancer prevention) and (Mortality or morbidity)
• Strategy 2—(Elder*) and (Cancer screening or cancer prevention) and (Effect or efficacy or effective*)
Searches were conducted for studies in which the population was restricted to those aged 65 years or above. The search fields included abstracts and titles, studies written in English, and studies published in the last 10 years only (January 2007 to April 2017). We included only studies that evaluated screening for five types of cancer (colorectal, lung, breast, liver, and prostate). Studies that employed retrospective data analysis, simulation modelling, and observational, experimental (randomised controlled trials [RCTs]) or uncontrolled clinical trials were included. Systematic reviews were also included, but discussion papers that did not describe the process by which the database searches were conducted were excluded. Articles that discussed knowledge or attitudes to cancer screening and surveillance monitoring were also excluded.
Three members of the team screened all of the titles of the papers that were retrieved; papers that were considered irrelevant were discarded. Next, irrelevant papers were also excluded after the abstract and/or the full paper had been reviewed. At least two members independently read the full text of all of the papers that were potentially relevant and selected those that met the criteria for inclusion. The final selection of papers was achieved through a series of virtual online discussions that continued until a consensus was reached.
Other reports relevant to the topic found or cited in text in the reviewed papers were also included. As a result, 13 papers were added to the 23 papers from the scoping search. A total of 36 papers were included for review, with 13, 3, 14, 1, and 10 papers that concerned the screening of colorectal, lung, breast, liver, and prostate cancers, respectively (Fig). Three of the papers examined the evidence of more than one type of cancer and have therefore been included in different sections for review purposes. Recommendations for screening guidelines from national institutes or professional associations have also been included in each section after discussion of the reviewed papers. In the papers being reviewed, ‘benefit’ in screening is defined as early detection, survival, or reduced risk in mortality or co-morbidity; ‘harm’ is defined as mortality (death due to the specific type of cancer under investigation), false-positive and false-negative test results, or overdiagnosis.
Colorectal cancer screening
The faecal occult blood test (FOBT), barium enema, sigmoidoscopy, and colonoscopy are used to screen for colorectal cancer.4 10 Quarini and Gosney11 reviewed all available articles on colorectal cancer screening in MEDLINE from 1990 to 2007. They found limited evidence relating to the screening of older people.11
In a recent population-based simulation study, Meester et al12 analysed the number of deaths from colorectal cancer that were attributable to non-screening in the US; most such deaths were attributable to non-screening. Similar findings have been reported in Germany where screening colonoscopy has been offered since 2002. Brenner et al13 14 used simulation modelling based on Germany’s national data and found that screening colonoscopies have great potential in the prevention and early detection of colorectal cancer, with a low risk of over-diagnosis. Moreover, the majority of prevented cases would have occurred at the age of 75 years or older.14 Rozen et al15 also reported that those aged 75 years or older, rather than younger individuals, could benefit from screening.
Using colorectal cancer–specific mortality data between 1991 and 2001 obtained from the National Center for Health Statistics database in the US, Maheshwari et al16 compared the impact of prematurely stopping screening with the maximal potential benefit expected from lifelong screening. A total of 80% of the maximal benefit from screening was achieved by screening up to the age of 82 years. Kahi et al17 examined the survival of older people after colonoscopy using a retrospective cohort analysis of those aged 75 years or above and followed up for a median of 5.95 years. The authors reported that colonoscopy was safe and yielded clinically significant findings in 15% of older patients.17
van Hees et al18 used a simulation model to determine up to what age colorectal cancer screening should be considered in unscreened older people with no, moderate, or severe co-morbidity. They concluded that if the physical condition of unscreened older people with different co-morbidity status permits them to undergo a colonoscopy, screening should be considered up to the ages of 86, 83, and 80 years for no, moderate, and severe co-morbidity, respectively. van Hees’ team also reported that fewer co-morbidities were associated with screening at older ages.19 Lansdorp-Vogelaar et al20 and Gross et al21 whose studies are included in this review, also arrived at a similar conclusion.
Not all studies found positive results for colorectal screening. A longitudinal study by Fillenbaum et al22 observed no significant association between cancer screening and population-level health-related outcomes (including mortality).
Over-diagnosis and complications from treatment are often concerns in the promotion of screening. Although colorectal polyps are detected more frequently in older people, especially those over the age of 80 years, the view is that to conduct a colonoscopy in older people is to introduce a higher risk for only a smaller gain in life expectancy (15%) than would be the case with younger people.23 Cancer screening in people older than 75 years remains controversial because they have not been included in RCTs on the efficacy of screening studies.10
The guidelines from the National Cancer Institute,24 the American Cancer Society,25 and the US Preventive Services Task Force (USPSTF)26 generally recommend that people who are at an average risk of developing colorectal cancer or who have a family history of colorectal cancer or colorectal polyps begin regular screening for colorectal cancer at the age of 50 years. Specifically, the USPSTF recommends against screening with colonoscopy beyond the age of 85 years.27 The Canadian Task Force on Preventive Health Care recommends against screening with colonoscopy at all ages, but it does support the use of FOBT or faecal immunochemical testing for screening every alternate year and with sigmoidoscopy every 10 years for those aged 50 to 74 years.27
In Hong Kong, the Department of Health launched a 3-year Colorectal Cancer Screening Pilot Programme in 2016 to provide subsidised screening for those born between 1946 and 1948. The Hong Kong Anti-Cancer Society recommends that individuals aged 50 to 75 years with an average risk of developing colorectal cancer should consider undergoing an annual FOBT and flexible sigmoidoscopy every 5 years or a colonoscopy every 10 years.28 Overall, the current literature suggests that colorectal cancer screening is beneficial, but that age as well as morbidity and life expectancy should be considered when determining the age at which screening should stop. Screening colonoscopy in very elderly patients (aged ≥80 years) should be performed only after carefully considering the potential benefits and risks, and the preferences of the patient. A summary of the literature review of screening for colorectal cancer is shown in Table 1.11 12 13 14 15 16 17 18 19 20 21 22 27
Table 1. Screening for colorectal cancer: summary of literature review11 12 13 14 15 16 17 18 19 20 21 22 27
Lung cancer screening
Chest X-rays, sputum cytology, and low-dose computed tomography (CT) have been used to screen for lung cancer.29 Although chest X-rays or sputum cytology have been used to check for signs of lung cancer, there is less evidence from RCTs to show that using them can lead to a reduction in the number of associated deaths.29 There is, however, some evidence from large-scale RCTs that low-dose CT screening can reduce lung cancer deaths.30
Oken et al31 compared annual chest radiographic screening with the usual care in the Prostrate, Lung, Colorectal, and Ovarian (PLCO) cancer screening trial. The participants were aged 55 to 74 years and were heavy smokers. Radiographic screening did not reduce lung cancer mortality when compared with the usual care. Aberle et al’s National Lung Screening Trial32 in the US examined the effects of lung cancer screening by low-dose CT for participants aged 55 to 74 years who were either current or former (within the past 15 years) heavy smokers (at least 30 packs of cigarettes/year). An annual low-dose CT for 3 years reduced 20% of deaths from lung cancer when compared with chest radiography.
Using simulation modelling, McMahon et al33 examined the potential benefits (life years saved or lung cancer deaths avoided) of 576 lung cancer screening programmes that included a variety of screening criteria in terms of age, smoking history, and the number and frequency of CT screenings. They concluded that it would be more efficient (measured in terms of the number of cancer deaths compared with no screening) if screening were extended to the age of 80 or 85 years. The potential harm of low-dose CT, however, should also be noted, such as false-positive and false-negative results, overdiagnosis, exposure to radiation, and an emotional toll on the individual concerned.
Based on the National Lung Screening Trial,32 a systematic evidence review30 and modelling studies, the USPSTF has updated their guidelines. They now recommend that people aged 55 to 80 years who currently smoke or who have quit smoking within the past 15 years should undergo annual screening with low-dose CT.34 The USPSTF also recommends that screening be discontinued for those who have quit smoking for 15 years or who have developed a health problem that substantially limits their life expectancy or their ability or willingness to undergo curative lung surgery.30 The Hong Kong Anti-Cancer Society does not recommend any routine screening for the general population. Considering both life expectancy and co-morbidity status would help physicians to decide the necessity of screening in different individuals.35 A summary of the literature review of screening for lung cancer is shown in Table 2.31 32 33
Breast cancer screening
Clinical breast examinations and breast self-examinations, mammograms, ultrasound, and magnetic resonance imaging, are all measures to screen for breast cancer, with the mammogram being the most widely used test.
A systematic review by Galit et al36 suggested that with a reasonable life expectancy and without severe co-morbidities, women aged 75 years or above are likely to benefit from mammography. Mo et al37 found that mammography screening alone for Chinese women over the age of 70 years with positive clinical breast examination results would save on the cost of ultrasonography without any loss in the effectiveness of screening. When co-morbidity and screening are considered, Lansdorp-Vogelaar et al20 showed that the benefits of a biennial mammography existed until the median ages of 76, 74, 72, and 66 years for older women with no, mild, moderate, or severe co-morbidity, respectively.
The EUROSCREEN Working Group reviewed observational studies and reported that the reduction of the breast cancer mortality rate was 38% to 48% for women who had actually been screened, with the rate of over-diagnosis of only 6.5%.38 39 They argued that the current controversy is related to the use of inappropriate methods that are incapable of revealing the true effect of screening, and that population-based mammography screening is of greater benefit than harm.
Using simulation modelling, Tejada et al40 evaluated seven screening policies to determine which combination of upper age limit and screening interval could maximise screening benefits for older women. Annual screening with an upper age limit of 80 years was found to be most effective in increasing the survival rate.40 Similarly, Sanderson et al41 found a significant reduction in the breast cancer mortality rate of older women who underwent an annual mammography compared with those who underwent a biennial or irregular mammography.
Some researchers have nonetheless taken a contrary view. Fillenbaum et al22 found no significant association between breast cancer screening and health-related outcomes such as self-rated health and mortality. Similarly, the benefits of screening were found to be limited due to a huge number of cases of over-diagnosis in the older population.5 Mandelblatt et al42 evaluated the effectiveness of 20 different mammography screening programmes using six established models of cancer incidence and mortality trends in the US. They reported that if the age of cessation was set at after 69 years, the reduction in mortality would be slight.
A Cochrane review examined the effect of mammography screening in terms of mortality and morbidity in a total sample of 600 000 women.43 Screening led to a 15% reduction in mortality but the over-diagnosis and over-treatment rate was 30%. The authors suggested that screening might not be doing more good than harm.43 Of note, only one trial in this Cochrane review included women up to the age of 69 years. In their retrospective cohort study, Parvinen et al44 found that a mammography screening programme for women up to the age of 74 years effectively reduced mortality rates in the older population, but that the reduction in rate was only 20%. Their conclusion was that the gain in benefits may not justify the harm from screening.
Mammography screening is unlikely to benefit those with a life expectancy of less than 5 years as reported in Tazkarji et al’s study.27 Braithwaite et al45 found that the benefits of screening decrease with increasing age and co-morbidity. Their sample of women aged 65 years or above without severe co-morbidity showed only a slight improvement in life expectancy. They, too, argued that the magnitude of the benefit may not justify screening given the potential harm. Citing the Canadian National Breast Screening Study with 25 years of follow-up, the National Cancer Institute in the US concluded that the benefits of mammography screening are uncertain.46
In summary, the overall effect of breast cancer screening in older women remains a controversial topic. Currently, the American Cancer Society suggests that women who are at an ‘average risk’ of developing breast cancer have an annual mammogram starting at the age of 40 years, with no specific age mentioned as the marker for discontinuation, while the USPSTF now suggests that regular screening should start from the age of 50 years and end at the age of 74 years. The Hong Kong Breast Cancer Foundation recommends that women over the age of 40 years consider undergoing a mammography every 2 years.47 A summary of the literature review of screening for breast cancer is shown in Table 3.5 20 22 27 36 37 38 39 40 41 42 43 44 45
Table 3. Screening for breast cancer: summary of literature review5 20 22 27 36 37 38 39 40 41 42 43 44 45
Liver cancer screening
There are no widely recommended tests to screen for liver cancer among the general public except for those who are at a high risk of developing the disease. Alpha-fetoprotein (AFP) and abdominal ultrasound are the two most common tests in use. Nonetheless the sensitivity and specificity levels of AFP are unsatisfactory.48 This protein has also been shown to be unreliable in detecting small liver cancer.
There is hardly any evidence of the benefits of screening older people for liver cancer. Huang et al49 conducted a two-stage community screening programme (first with blood tests and then by ultrasonogram for identified high-risk cases) on a sample of 1002 people with a mean age of 68.3 years for women and men in an area where the hepatitis C virus is endemic. They observed that older patients who had early-stage hepatocellular carcinoma and who were being treated had a good prognosis for survival.
Currently, the American Cancer Society offers no recommendations for liver cancer screening in the general population. Cancer Research UK recommends a liver screening test only for high-risk individuals.50 Similarly, the Hong Kong Department of Health does not recommend routine cancer screening for people at ‘average risk’—only for those at high risk, such as carriers of the hepatitis B and/or C viruses and those with cirrhosis.51 In summary, screening tests for liver cancer should not be performed in a routine manner but should be recommended only for people who are at a high risk of developing the disease. A summary of the literature review of screening for liver cancer is shown in Table 4.49
Table 4. Screening for liver cancer: summary of literature review49
Prostate cancer screening
Prostate-specific antigen (PSA) testing, digital rectal examination, and prostate biopsy are the three main approaches usually used in combination with screening prostate cancer.4 There is no single effective and reliable test to screen for early prostate cancer in healthy men.50 It is not uncommon for men to have some cancer cells in their prostate by the age of 80 years although only one in 25 will actually die from prostate cancer.50 To date, the debate over PSA screening remains heated even though screening was first introduced in the late 1980s.
Konety et al52 reported the work of a 30-member panel of US experts who recommended that the initiation of screening for prostate cancer in men older than 75 years should be undertaken only after careful consideration, and that age-normed PSA values should be used to determine ‘normal’ levels.
Using mathematical modelling, Etzioni et al53 found that by 2000, 45% to 70% of the observed decline in prostate cancer mortality could be plausibly attributed to screening. They concluded that PSA screening might account for much of the observed drop in prostate cancer mortality. Etzioni et al54 also studied the link between PSA screening and the decline in the incidence of late-stage prostate cancer. Their tested model showed that screening explained about 80% of the observed decline in the incidence of distant-stage (as opposed to locoregional stage) prostate cancer. Nonetheless the team suggested that other factors such as awareness and advances in treatment might also play certain roles.
Telesca et al55 used data derived from the Surveillance, Epidemiology, and End Results (SEER) registry of the National Cancer Institute in the US to examine the increase and subsequent decline in the incidence of prostate cancer after the adoption of PSA screening, and arrived at the opposite conclusion. They maintained that the disease would not have continued to increase in incidence in the absence of PSA screening. Also using the SEER data, Welch and Albertsen56 used age-specific population estimates from the US Census data to determine the excess or deficit in the number of men diagnosed and treated each year after 1986. Since 1986, an estimated additional 1.3 million men were diagnosed and more than 1 million of them were treated. They concluded that most of the excess incidence must be the result of over-diagnosis.
Two large-scale RCTs published in 2009—the European Randomized Study of Screening for Prostate Cancer57 and the US PLCO cancer screening trial58—produced conflicting results on screening for prostate cancer with PSA testing, providing fuel for further debate.
Jemal et al59 conducted an interesting study that examined changes in the incidence of stage-specific prostate cancer and PSA screening rates for the period 2005 to 2012 using the US National Cancer Institute database. Both the incidence of early-stage prostate cancer and rates of PSA screening had declined, coinciding with the 2012 USPSTF recommendation to omit PSA screening from routine primary care. Nonetheless, the authors also recommended a longer follow-up period to ascertain whether these decreases were indeed associated with mortality trends. Thus, whether reduced screening would lead to reductions in over-diagnoses or to missed opportunities for early detection remains an open question.
The American Cancer Society states that a screening test should not be offered to men who do not have any symptoms of prostate cancer and who have a life expectancy of about 10 more years or less, because of its slow-growing prognosis. The USPSTF and the American Academy of Family Physicians do not recommend the use of the PSA test to screen for prostate cancer, as there is little evidence to show that the benefits outweigh the harm. They argue against screening for men 75 years of age and older because of a lack of evidence to support screening.
In brief, views about the desirability of prostate cancer screening are polarised, and much confusion over the issue remains.60 Observational evidence to date has not always supported the efficacy of PSA screening in reducing mortality; rather, a growing body of observational evidence points to the overdiagnosis and over-treatment of prostate cancer triggered by PSA testing.61 Randomised trials have produced conflicting results. Thus, the efficacy of prostate cancer screening for old men remains a point of contention. A summary of the literature review of screening for prostate cancer is shown in Table 5.20 27 52 53 54 55 56 57 58 59
To screen or not to screen older people
To screen or not to screen older people for common types of cancer remains controversial, especially for people over the age of 75 years. Screening may reduce the risk that individuals will develop a condition or its complications, but it may not guarantee protection. Most of the papers and guidelines suggested that screening has to be individualised for this particular age-group. Even though the risk of cancer increases with age, it should not be the only factor taken into account when making decisions about screening. Routine cancer screening does not benefit those with a limited life expectancy.62 Estimating life expectancy will help guide decision-making for preventive screening and treatment plans.27 Because life expectancy varies in relation to co-morbidity status, taking co-morbidity–adjusted life expectancy into consideration may be helpful to physicians.35
In any screening programme, there is an irreducible minimum of false-positive and false-negative results.23 The feelings and overall health status of the patient also need to be considered. It may be appropriate to screen patients with a life expectancy sufficiently long to experience the potential benefits of screening. Personalised consideration might benefit older people if the positive impacts can outweigh the negative, even for the oldest-old.
Cancer is common in the older population and, for them, the benefits of screening for common types of cancer remain controversial. The evidence is strongest for the efficacy of colorectal cancer screening, even for older people aged 75 years and beyond. Low-dose CT for screening for lung cancer has benefits for heavy smokers. Liver cancer screening is recommended only for those at high risk of developing the disease. The evidence for screening older people for breast cancer is conflicting; as is the evidence for the effectiveness of PSA tests for screening for prostate cancer. Although some screening tests can bring certain benefits, other factors related to advancing age may be present, such as co-morbidities that may cause harm and would eventually outweigh the benefits of cancer screening. More research is indeed needed to understand the relationship between cancer and ageing, and also the risks and benefits of cancer screening for older people, to ultimately promote good health and functional longevity.
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