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Screening Mammography and Breast Cancer Reduction: Examining the Evidence
Screening Mammography and Breast Cancer Reduction: Examining the Evidence Ruth Tupper, MS, RN, and Karyn Holm, PhD, RN ABSTRACT
Better treatment and awareness may explain much of the decline in breast cancer deaths in recent years, not mammography. For women without a family history of breast cancer, the risks of screening mammography may outweigh the benefits, particularly for women younger than age 50. Mammography carries the risk of overdiagnosis of tumors that would not have caused death. Nurse practitioners are advised to educate their patients on mammography risks and benefits while increasing their emphasis on the clinical symptoms of breast cancer and ways to reduce risk, including weight control, decreased alcohol use, and decreased use of menopausal estrogen. Keywords: breast cancer, cancer prevention, evidence-based practice, mammography, overdiagnosis, screening Ó 2014 Elsevier, Inc. All rights reserved.
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eferral for a mammogram has long been an important item on a checklist for any woman older than age 40 seeing her primary care provider. After all, using a mammogram to screen for breast cancer makes intuitive sense; catching a tumor even before it is clinically evident allows for earlier treatment and results in fewer women dying.1 As evidence, the death rate from breast cancer has been declining.2 In 1975, the death rate for breast cancer in the United States was 31.45 per 100,000, staying stable in the 30 to 32 range until 1998 when it started to drop steadily; in 2010, it reached its lowest point of 21.92 per 100,000.2 An estimated 39,500 women died from breast cancer in 2012, including an estimated 4,100 in the 40- to 49-year age group.3 Some researchers have challenged these longheld assumptions about the benefits of mammograms and breast self-examinations (BSEs) for women not at high risk for the disease.4-6 Otis Brawley of the American Cancer Society went so far as to say that at least half of the decrease in breast cancer mortality “if not most” was because of better treatment and greater awareness of breast cancer among women and their providers, with www.npjournal.org
only 15% to 40% of the decline attributed to screening.3 A decline in the use of menopausal estrogen may also have contributed to this decrease; a nationwide drop by women in the use of hormone replacement therapy in 2002 was followed by a 8.6% decrease in the US in new cases of breast cancer in 2003.7 The introduction of tamoxifen may explain the 37% decline in breast cancer mortality in Sweden for women younger than 50 between 1989 and 2005 before screening had been introduced.8 Autier et al6 also found that breast cancer deaths in Sweden had been dropping even before screening was introduced. Mammography critics have further stated that the benefits of screening for women not at high risk in terms of lives saved do not outweigh the risks in terms of false positives or, even more alarming, overdiagnosis.8,9 Overdiagnosis refers to a case in which a cancer that is diagnosed by screening would never have been otherwise diagnosed in the woman’s lifetime and would not have caused symptoms or death.9 With overdiagnosis, some cancers caught on screening may never progress and may even go away or the cancer may be so slow growing that the patient dies from another cause first9 (Figure 1). The Journal for Nurse Practitioners - JNP
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The screening debate culminated in 2009 when the US Preventive Services Task Force (USPSTF) advised that mammograms not start until age 50 and be done every 2 years,10 going against the recommendations of virtually every professional society, all of which had called for annual mammograms starting at age 40.11 The debate over the value of screening has not abated in the 5 years since the task force issued its guidelines. Indeed, some researchers have advised women not to get mammograms at all.12 To be sure, patients with a genetic mutation, such as BRCA1 or BRCA2, or a history of chest radiation or an increased risk of breast cancer need to get mammograms before the age of 50.13 But, for everyone else, it may turn out that the best payoff in terms of optimal outcome will be in preventing breast cancer. This article addresses arguments on both sides of the controversy and provides nurse practitioners (NPs) with helpful information to guide their patients in making important decisions regarding the benefits and risks of screening. Other ways to lower their risk of dying from breast cancer besides screening mammography are also discussed. INCIDENCE AND PREVALENCE
On January 1, 2010, the prevalence, or total number of women with breast cancer in the US, was 2.83 million, including those with active disease and those
cured of the disease. A woman’s lifetime risk of being diagnosed with breast cancer is 1 in 8, but the breast cancer mortality is, in fact, lower because many women will die of another disease first before they die of breast cancer.2 A more useful statistic is the probability that a woman between the ages of 50 and 70 will develop breast cancer (5.59%).2 In 2013, the incidence, or number of new cases of breast cancer in the US, was estimated at 232,340 with 39,260 deaths.2 Between the years 2006 and 2010, the incidence of breast cancer in the US averaged out to 123.8 per 100,000 women per year.2 Figure 2 shows the incidence and deaths from breast cancer per 100,000 women by racial and ethnic group. The incidence was highest for white women, followed by black women, Asian/Pacific Islander women, Hispanic women, and American Indian/Alaska Native. Death rates, however, were the highest for black women, followed by white, American Indian/Alaskan Native, Hispanic, and Asian/Pacific Islander women. Between 2006 and 2010, the median age of death for breast cancer was 68 years old. Figure 3 shows the incidence and deaths from breast cancer by age as a percentage of total women. The incidence and death rate were highest between the ages of 55 and 64, with 25.2% of all women diagnosed with breast cancer in that age group and 21.6% of the deaths in
Figure 1. Different types of cancer progression.
The Fast arrow represents a cancer that quickly results in clinical symptoms and death. The Slow arrow represents a cancer that is slow growing and takes many years to manifest clinically. The Very Slow arrow represents a cancer that is so slow growing that the patient will die of another disease before breast cancer. The Non-progressive arrow represents either a cancer that actually regresses or a cancer that will never cause clinical symptoms although it meets the pathological criteria for a cancer diagnosis on screening. Reprinted by permission of Oxford University Press from Welch HG, Black WC. Overdiagnosis in cancer. J Natl Cancer Inst. 2010;102(9):605-613. 722
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Figure 2. Breast cancer new cases and deaths per 100,000 women per year by racial/ethnic group (2006-2010).
Data from National Cancer Institute.2
that age group. Only 5.3% of breast cancer deaths were from women between 35 and 44 years old, whereas 14.6% of deaths were from women 45 to 54 years old. Although the incidence of new cases dropped off after age 65, the death rate as a percentage of all women remained high, with 20.2% of the women dying from breast cancer in the 65- to 74-year age group and 21.5% of the total women dying in the 75- to 84-year age group.
HISTORY OF THE CONTROVERSY OVER SCREENING
The earliest use of x-rays to identify breast cancer goes back to 1913, but it was not until the 1960s that the use of mammograms to screen for breast cancer became accepted.14 The use of mammography for screening purposes became controversial in the 1970s because epidemiologic studies examined the numbers of lives saved for entire populations, as opposed to looking at individual cases.14 John Bailar, a physician who had
Figure 3. Percentage of total women with new cases and deaths from breast cancer by age group.
Data from National Cancer Institute.2 www.npjournal.org
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been trained in biostatistics and epidemiology, pointed out that routine mammograms could detect slowgrowing cancers, such as ductal and lobular carcinoma in situ, that would likely never turn into clinically significant breast cancer.15 This detection of slowgrowing cancers would make screening seem more beneficial than it actually was by reporting women whose lives were “saved” because of screening when, in fact, their cancers would never have killed them in the first place. Bailar15 also pointed out the danger of radiation from the mammogram itself. In response to these concerns, the American Cancer Society and the National Cancer Institute revised the consent form to inform women of potential risks of mammography and also hastened the process to standardize the radiation dosages.14 They also decided to recommend giving mammograms to women younger than age 50 only if they were at “high risk.” The problem was that high risk was defined so broadly (ie, a woman with merely a fear of breast cancer was considered “high risk”) that it included 80% of the women in the 35- to 50-year age bracket.14 In 1983, the American Cancer Society recommended a screening mammogram every 1 to 2 years for women 40 to 49 years old.14 The American Cancer Society made its recommendation after concluding that screening saved lives for women younger than 50.16 The American College of Radiology joined the American Cancer Society in 1988 in recommending routine mammograms for women 40 to 50 years old. The tide began to turn in 1993. A series of randomized controlled trials including women in their 40s concluded that mammography had no benefit for younger women.13 In 2001, a study published in Lancet17 found that 6 of 8 mammography studies during the previous 3 decades were found to be deeply flawed. This analysis called into question the requirement that women get annual mammograms starting at any age. The task force analysis16 temporarily put to rest the controversy. The US PSTF is an independent panel of internists, pediatricians, and family physicians who are experts in prevention and evidence-based medicine and who work outside the federal government but serve under the auspices of the Federal Agency for Healthcare Research and Quality. The 2002 task force analysis examined 8 randomized controlled trials of mammography and 154 724
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publications of the results of these trials. It concluded that for the studies rated “fair or better,” mammography did reduce breast cancer mortality among women ages 40 to 74 with absolute risk reduction greater in the older women. Still, the authors pointed out that mammography’s benefit in reducing death from breast cancer may be so small that any bias in studies could erase its benefits and that future studies should be directed at improving the sensitivity and specificity of mammography.16 The analysis showed that the studies had concluded that 1,224 women had to be screened to prevent 1 death after 14 years of observation, with 1,792 women needing to be screened to prevent 1 death if they were younger than 50 years old. The task force study16 also found no evidence that BSEs saved lives in 2 randomized controlled trials with a 5- to 10-year follow-up. Breast cancer mortality was no different in the group who did BSE versus controls. In both studies, the women were “meticulously trained” in the proper technique of BSE. The only difference between the 2 groups was that those trained in BSE had more physician visits and more biopsies for benign breast lesions. Lives Saved per 1,000 Screened Women
One part of the debate has focused on how many women’s lives per 1,000 screened would be saved. An analysis of trials conducted in Sweden found that for every 1,000 women screened every 2 years, after 12 years, 1 breast cancer death was avoided.17 Studies by Duffy et al18 of women in England and Sweden found more lives saved per 1,000 screened women. Comparing a randomized trial in Sweden and a breast screening program in England, Duffy et al found that both had significant reductions in mortality, estimated at 8.8 deaths prevented per 1,000 women screened for 20 years starting at age 50 in the Swedish trial and 5.7 deaths per 1,000 women screened prevented in the English program. So, which is it—1 life saved per 1,000 screened or 8.8 lives saved per 1,000? Different years of follow-up is 1 reason for the different conclusions. Another reason for the different conclusions is that the denominators were not consistent; in the screening, the denominator was made up of women who had received a breast cancer diagnosis from screening, Volume 10, Issue 9, October 2014
which could include those “overdiagnosed,” whereas in the control group, the denominator was made up of women who had received a diagnosis from symptoms, presumably a smaller group. In other words, the screening group death rate looked smaller because its denominator included women whose cancers may never have been found without screening and turned into a lethal disease. Based on a new systematic review,19 in 2009, the task force updated its 2002 recommendations, now advising biennial screening mammography for women between the ages 50 and 74 and no routine screening for women younger than age 50. For both groups of women, those in the 40- to 49-age range and those in the 50- to 59-age range, the task force stated that research had found the relative risk reduction for screening is similar, 15% and 14%, respectively, but the absolute risk reduction is greater in the older women simply because the risk increases with age. Therefore, the task force study concluded that “net benefits were small” for the age range of 40 to 49 years. The task force also stated that there were not enough data to determine the benefits and harms of mammograms for women older than age 75. The task force study authors also pointed out potential harms of screening, in particular the risk of overdiagnosis with ductal carcinoma in situ (DCIS).10 Half or fewer cases of DCIS progress to invasive cancer, but standard treatment had called for surgery plus radiation and hormone therapy.10 Screening has dramatically increased the diagnosis of DCIS: 4,900 cases were diagnosed in 1983 compared with 67,770 in 2008.10 Another study of women with DCIS by Ernster and Barclay as cited by Humphrey et al16 found that 44% of the women had mastectomies and 23% to 30% had lumpectomies. In other words, there may be have been approximately 15,000 unnecessary mastectomies in 2008, if these figures hold true. RISKS OF SCREENING
Researchers have studied the risks of screening with different conclusions about the specific numbers. They include anxiety generated by false-positive results, risks from being exposed to radiography itself, and risk of overdiagnosis.5 Potential harms from screening also include the risk of ill effects on a woman’s sexual well-being and sexual relationships.5 www.npjournal.org
False Positives
A false positive rate is calculated by determining the number of mammograms read as abnormal or needing more follow-up in women who subsequently were found not to have cancer divided by the total number of women who screened positive. One study estimated the false-positive rate to be 63% after 10 screening mammograms.20 Other studies have determined the rate to be 21% to 49% after 10 years of screening mammograms for women of all ages and 56% after 10 years of mammograms for women ages 40 to 49.19 In a review of research done between 1995 and 2007, studies showed that for up to 2 years after screening, women with false-positive results had increased levels of breast cancer worries, changes in mood, higher anxiety, and more cases of intrusive thinking compared with before they had the mammogram.21 Another study found that 3 years after women with falsepositive diagnoses were told they were actually cancer free, they still had higher negative psychosocial scores than women who had been given true-negative findings.22 However, women may have a high tolerance for false-positives results if they save someone’s life.16 A 2000 study by Schwartz et al (as cited by Humphrey et al16) found that 63% of women would tolerate 500 false-positive results to save 1 life. Radiography Risks
Radiation from the mammogram also presents a risk, albeit small. Of 100,000 women being screened for 10 years starting at age 40, no more than 8 additional breast cancer deaths would occur because of radiation.16 Overdiagnosis
The most compelling argument against screening is that of overdiagnosis. Although screening may result in a reduction of breast cancer deaths, they may increase deaths from other causes.23 In other words, although breast cancer mortality has dropped after screening, overall mortality has not. Given the high stakes, it is no wonder that those on opposing sides of the controversy offer differing figures as to what the true rate of overdiagnosis is.24-27 It also represents an entirely new way of thinking that a cancer can be so slow growing or even regress so that no treatment is necessary or advisable.9 The Journal for Nurse Practitioners - JNP
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It is impossible to directly determine if any particular breast cancer case was overdiagnosed. Thus, researchers must use estimates based on population studies that compared observed deaths from breast cancer with those expected. In particular, overdiagnosis rate estimations come from the changes in breast cancer incidence rates after screening has been introduced in a population. Because of no agreed-upon method, the estimates can vary from 5% to 50% of cases of cancer being overdiagnosed.24 For example, 1 study of women in Sweden and England estimated a rate of 4% to 7% of cases of cancer being overdiagnosed.18 Another analysis found an overdiagnosis rate estimated to be between 16% and 24% depending on the denominator used.9 The USPSTF study estimated that overdiagnosis ranges from 1% to 10%.19
Just how is overdiagnosis calculated? A 2006 study by Zackrisson et al27 illustrates how. After a 10-year trial, 150 more women had been diagnosed with breast cancer in a mammography group than in a control group. This made sense because mammography works by diagnosing breast cancer that is missed without screening before the tumor becomes clinically evident. The women were then followed for another 15 years. During the follow-up, both groups received mammography so the cancers in the originally nonscreened control group could presumably “catch up” with the study group and be properly diagnosed clinically. This “catching up” in number of diagnosed cases would be expected with 2 samples drawn from the same population. But, after 14 years, still 115 more women were diagnosed in the original study group than in the control group. Why didn’t
Table. Comparison Chart of Breast Cancer Screening Guidelines Issued by US Professional Societies and Organizations Professional Society or Group (Year of Recommendation)
Age to Definitely Screen Asymptomatic Women not at Increased Risk for Breast Cancer
Frequency of Screening
American Cancer Society (2013)
Age 40 and continuing for as long as women is in good health
Yearly
American College of Obstetricians and Gynecologists (2011)
Age 40
Yearly
American College of Physicians (2007)
Age 50 (women ages 40-49 need to assess risks for breast cancer to help guide decision; physicians should inform women of benefits and harms of mammography; reasonable to start at age 40 if women does not wish to discuss decision)
Every 1 to 2 years
American College of Radiology (2013)
Age 40 but no definite age when screening should end as long as patient is in good health
Yearly
American College of Surgeons (2009)
Age 40
Yearly
American Medical Association (2012)
Age 40, but patients should talk to doctor as to whether screening is right for them
NA
American Association of Family Physicians (2014)
Age 50-74 (mammograms for women younger than age 50 should take into account their risks of getting breast cancer as well as their values on benefits and harms; women age 75 and older should talk to their physicians about benefits and harms of screening)
Every 2 years
National Research Center for Women & Families’ Cancer Prevention and Treatment Fund (2007)
One mammogram at age 40 or 45 and then wait until age 50 if it is normal
NA
US Preventive Services Task Force (2009)
Age 50 until age 74
Every 2 years
NA ¼ not applicable; US ¼ United States.
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the number of cancers in the control group catch up? The authors concluded that the excess was because of overdiagnosis, meaning a suspicious lesion was identified that would never become clinically significant. Zackrisson et al27 calculated that about 1 in 6 cancers are overdiagnosed. IMPLICATIONS FOR NURSING PRACTICE
NPs will need to provide their patients with the facts regarding both sides of the screening controversy given the lack of agreement. Factors increasing the risk of breast cancer, such as family history or genetic mutations, may well tilt the balance in favor of starting at age 40 with the benefits outweighing the risks.28 Much education is needed because awareness of the task force guidelines among women is low; only 12% were aware of the 2009 USPSTF guidelines (Table) recommending starting screening at age 50.28 In addition, some NPs may find that with either outcome, screening is self-reinforcing; negative results bring what could be false relief and positive results provide the consolation of being saved from what is believed to be a harmful tumor, without necessarily knowing whether it is or not.29 Explaining the risks and benefits will empower patients to decide for themselves whether they want to start mammography screening at age 40, wait until age 50, or forgo screening altogether if they believe the benefit does not outweigh the risk. One way to allow a woman to decide for herself is to show her the numbers; for every 10,000 women who receive a regular mammogram for 10 years, starting at age 40, 6 women will have reduced their risk of death from breast cancer.30 During this 10-year period of regular mammograms, as many as 5,000 of the 10,000 women will get a false-positive result requiring them to return for more testing.30 For the 626 women out of the 10,000 who receive a diagnosis of breast cancer,27 anywhere from 20 (3.2% overdiagnosis31) to 156 (15%-25% overdiagnosis32) of these women may be receiving unnecessary treatment. Paying for the mammogram may be another consideration if insurance policies change to not cover mammograms for certain women. Currently, however, mammograms are covered by the majority of insurance plans, and free screening is offered for many low-income women. www.npjournal.org
No matter what decision the patients make in consultation with their primary care provider, it is prudent to makes sure they understand that more than 1 “right” answer exists currently regarding screening. Look to the author of a scholarly article to determine if a bias may exist; for example, radiologists are more likely to advocate routine screening.33 In light of this, to protect against lawsuits, the rationale for or against screening should be documented along with the final decision of the patient.34 It may also be helpful to know that most claims for missed or delayed diagnosis of breast cancer were caused by failure to properly evaluate clinical manifestations of the disease, such as palpable lumps or abnormalities on mammograms, and not caused by inadequate screening in otherwise healthy patients.34 At the same time, a stepped-up emphasis on the awareness of breast cancer and prevention will do much to lower mortality risks. NPs can teach women to be aware of their own breasts and what represents a change, urging them to seek immediate medical attention if they notice any nipple discharge, inverted nipples, “orange”-like peau appearance of the skin, or, of course, a lump. Excess weight, alcohol, early menarche, and use of estrogen have all been linked to an increased risk of breast cancer.35,36 Therefore, NPs may want to go back to the basics—recommending that their patients keep their weight down (leading to a 25%-50% reduction in the risk of breast cancer35) and limit alcohol (even moderate consumption of alcohol increases the risk of breast cancer 36), advising parents to keep their preadolescent daughters thinner to prevent a too-early 1st menarche (our ancestors had 160 ovulations over their lifetime and breast cancer was rare vs now when we have 450 ovulations per lifetime35), and discouraging their menopausal patients from using estrogen. Breastfeeding for 12 months also lowers the relative risk by 4.3%, whereas each birth lowers it by 7%.36 Black women should be informed of statistics showing their higher mortality from breast cancer2 so they may take prompt action if a lump is found to get treatment. Finally, for those women who do want to get mammograms, NPs can provide evidence-based research on the risks and benefits. Based on this research, some patients perhaps even take a cue from men with prostate cancer diagnoses and choose the option of “watchful waiting” if the results come out The Journal for Nurse Practitioners - JNP
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positive, particularly in the case of DCIS. The watchful waiting allows for the possibility that the tumor may be slow growing or even regress.37 CONCLUSION
Thinking about mammography continues to evolve. Experts disagree on the extent of the risk, not the risks themselves. Making women aware of the controversy and encouraging them to think about their own particular situation may be the wisest course because there is no absolute correct answer. Women will have to consider their own particular risks; for example, statistics show that black women are more likely to die of breast cancer so that may influence their decisions about screening and prevention. Future studies should also look at the way costs influence individual decisions in an era when health care spending is becoming increasingly scrutinized. References 1. Magnus MC, Ping M, Shen MM, Bourgeois J, Magnus JH. Effectiveness of mammography screening in reducing breast cancer mortality in women aged 39-49 years: a meta-analysis. J Womens Health. 2011;20(6): 845-852. 2. Howlader N, Noone AM, Krapcho M, et al., eds. SEER Cancer Statistics Review, 1975-2010. Bethesda, MD: National Cancer Institute. http://seer .cancer.gov/statfacts/html/breast.html. Accessed July 13, 2013. 3. Brawley OW. Risk-based mammography screening: an effort to maximize the benefits and minimize the harms. Ann Intern Med. 2012;156:662-663. 4. Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367(21):1998-2005. 5. Gotzsche PC, Hartling OJ, Nielsen M, Brodersen J, Jorgensen KJ. Breast screening: the facts—or maybe not. BMJ. 2009;338:446-448. 6. Autier P, Koechlin A, Smans M, Vatten L, Bonio M. Mammography screening and breast cancer mortality in Sweden. J Natl Cancer Inst. 2012;104(14): 1080-1093. http://dx.doi.org/10.1093/jnci/djs272. 7. Ravdin PM, Cronin KA, Howlader N, et al. The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med. 2007;356: 1670-1674. 8. Gotzsche PC. Time to stop mammography screening? CMAJ. 2011;182:1957-1958. 9. Welch HG, Black WC. Overdiagnosis in Cancer. J Natl Cancer Inst. 2010;102:605-613. 10. US Preventive Services Task Force. Screening for breast cancer: US Preventive Services Task Force Recommendation Statement. Ann Intern Med. 2009;151:716-726. 11. Drukteinis JS, Mooney BP, Flowers CI, Gatenby RA. Beyond mammography: new frontiers in breast cancer screening. Am J Med. 2013;126(6):472-479. 12. Gotzsche PC, Jorgensen KJ, Zahl P-H, Maehlen J. Why mammography screening has not lived up to expectations from the randomized trials. Cancer Causes Control. 2012;23:15-21. 13. Van Ravesteyn NT, Miglioretti DL, Stout NK, et al. What level of risk tips the balance of benefits and harms to favor screening mammography starting at age 40? Ann Intern Med. 2012;156(9):609-617. 14. Lerner BH. To see today with the eyes of tomorrow: a history of screening mammography. Background paper for the Institute of Medicine Report, Mammography and beyond: developing technologies for the early detection of breast cancer. http://www.oup-usa.isbn/0195142616.html. Accessed July 13, 2013. 15. Bailar JC. Mammography: a contrary view. Ann Intern Med. 1976;84(1):77-84. 16. Humphrey LL, Helfand M, Chan BKS, Woolf SH. Breast cancer screening: a summary of the evidence for the US Preventive Services Task Force. Ann Intern Med. 2002;137(5):E347-E367.
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17. Gotzsche PC, Olsen O. Is screening for breast cancer with mammography justifiable? Lancet. 2000;355:129-134. 18. Duffy SW, Tabar L, Olsen AH, et al. Absolute numbers of lives saved and overdiagnosis in breast cancer screening, from a randomized trial and from the Breast Screening Programme in England. J Med Screen. 2010;17:25-30. 19. Nelson HD, Tyne K, Naik A, Bougatsos C, Chan BK, Humphrey L. Screening for breast cancer: an update for the US Preventive Services Task Force. Ann Intern Med. 2009;151:727-737. 20. Hubbard RA, Miglioretti DL, Smith RA. Modeling the cumulative risk of a false-positive screening test. Stat Methods Med Res. 2010;19(5):426-449. 21. Hafslund B, Nortvedt MW. Mammography’s screening from the perspective of quality of life: a review of the literature. Scand J Caring Sci. 2009;23: 539-548. 22. Brodersen J, Siersma VD. Long-term psychosocial consequences of falsepositive screening mammography. Ann Fam Med. 2013;11(2):106-115. 23. Newman DH. Screening for breast and prostate cancers: moving toward transparency. J Natl Cancer Inst. 2010;102:1008-1011. 24. Duffy SW, Parmar D. Overdiagnosis in breast cancer screening: the importance of observation period and lead time. Breast Cancer Res. 2013;15:R41. 25. Kalager M, Adami H-O, Bretthauer M, Tamimi RM. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med. 2012;156(7):491-499. 26. Welch HG. Overdiagnosis and mammography screening. BMJ. 2009; 339(7714):1425. 27. Zackrisson S, Andersson I, Janzon L, Manjer J, Garne JP. Rate of overdiagnosis of breast cancer 15 years after end of Malmo mammographic screening trial: follow up study. BMJ. 2006;332:689-692. http://dx.doi.org/ 10.1136/bmj.38764.572569.7C. 28. Kiviniemi MT, Hay JL. Awareness of the 2009 US Preventive Services Task Force recommended changes in mammography screening guidelines, accuracy of awareness, sources of knowledge about recommendations, and attitudes about updated screening guidelines in women ages 40-49 and 50þ. Public Health. 2012;12:899. http://dx.doi.org/10.1186/1471-2458 -12-899. 29. Hale PJ, de Valpine MG. Screening mammography: revisiting assumptions about early detection. J Nurse Pract. 2014;10(3):183-188. 30. Elmore JG, Choe JH. Breast cancer screening for women in their 40s: moving from controversy about data to helping women. Ann Intern Med. 2007;146:529-531. 31. Paci E, Miccinesi G, Pulti D, et al. Estimate of overdiagnosis of breast cancer due to mammography after adjustment for lead time. A service screening study in Italy. Breast Cancer Res. 2006;8(6):R68. http://dx.doi.org/10.1186/bor1625. 32. Kalager M, Zelen M, Langmark F, Adami H-O. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010;363(13):1203-1210. 33. Norris SL, Burda BU, Holmer HK, et al. Author’s specialty and conflicts of interest contribute to conflicting guidelines for screening mammography. J Clin Epidemiol. 2012;65(7):725-733. 34. Marmot MG. Sorting through the arguments on breast screening. JAMA. 2013;309(24):2553-2556. 35. Howell A, Astley S, Warwick J. Prevention of breast cancer in the context of a national breast screening programme. J Intern Med. 2012;271:321-330. 36. Tirona MT, Sehgal R, Ballester O. Prevention of breast cancer (part 1): erpidemiology, risk factors and risk assessment tools. Cancer Investig. 2010;28:743-750. 37. Zahl PH, Maehlen J, Welch HG. The natural history of invasive breast cancers detected by screening mammography. Arch Intern Med. 2008;168(21):2311-2316.
Ruth Tupper, MS, RN, is a guest instructor at DePaul University School of Nursing in Chicago, IL, and can be reached at [email protected]. Karyn Holm, PhD, RN, FAAN, FAHA, is professor and associate dean for research at the Marcella Niehoff School of Nursing, Loyola University Chicago in Maywood, IL. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/14/$ see front matter © 2014 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2014.07.018
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Better treatment and awareness may explain much of the decline in breast cancer deaths in recent years, not mammography. For women without a family history of breast cancer, the risks of screening mammography may outweigh the benefits, particularly for women younger than age 50. Mammography carries the risk of overdiagnosis of tumors that would not have caused death. Nurse practitioners are advised to educate their patients on mammography risks and benefits while increasing their emphasis on the clinical symptoms of breast cancer and ways to reduce risk, including weight control, decreased alcohol use, and decreased use of menopausal estrogen. Keywords: breast cancer, cancer prevention, evidence-based practice, mammography, overdiagnosis, screening Ó 2014 Elsevier, Inc. All rights reserved.
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eferral for a mammogram has long been an important item on a checklist for any woman older than age 40 seeing her primary care provider. After all, using a mammogram to screen for breast cancer makes intuitive sense; catching a tumor even before it is clinically evident allows for earlier treatment and results in fewer women dying.1 As evidence, the death rate from breast cancer has been declining.2 In 1975, the death rate for breast cancer in the United States was 31.45 per 100,000, staying stable in the 30 to 32 range until 1998 when it started to drop steadily; in 2010, it reached its lowest point of 21.92 per 100,000.2 An estimated 39,500 women died from breast cancer in 2012, including an estimated 4,100 in the 40- to 49-year age group.3 Some researchers have challenged these longheld assumptions about the benefits of mammograms and breast self-examinations (BSEs) for women not at high risk for the disease.4-6 Otis Brawley of the American Cancer Society went so far as to say that at least half of the decrease in breast cancer mortality “if not most” was because of better treatment and greater awareness of breast cancer among women and their providers, with www.npjournal.org
only 15% to 40% of the decline attributed to screening.3 A decline in the use of menopausal estrogen may also have contributed to this decrease; a nationwide drop by women in the use of hormone replacement therapy in 2002 was followed by a 8.6% decrease in the US in new cases of breast cancer in 2003.7 The introduction of tamoxifen may explain the 37% decline in breast cancer mortality in Sweden for women younger than 50 between 1989 and 2005 before screening had been introduced.8 Autier et al6 also found that breast cancer deaths in Sweden had been dropping even before screening was introduced. Mammography critics have further stated that the benefits of screening for women not at high risk in terms of lives saved do not outweigh the risks in terms of false positives or, even more alarming, overdiagnosis.8,9 Overdiagnosis refers to a case in which a cancer that is diagnosed by screening would never have been otherwise diagnosed in the woman’s lifetime and would not have caused symptoms or death.9 With overdiagnosis, some cancers caught on screening may never progress and may even go away or the cancer may be so slow growing that the patient dies from another cause first9 (Figure 1). The Journal for Nurse Practitioners - JNP
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The screening debate culminated in 2009 when the US Preventive Services Task Force (USPSTF) advised that mammograms not start until age 50 and be done every 2 years,10 going against the recommendations of virtually every professional society, all of which had called for annual mammograms starting at age 40.11 The debate over the value of screening has not abated in the 5 years since the task force issued its guidelines. Indeed, some researchers have advised women not to get mammograms at all.12 To be sure, patients with a genetic mutation, such as BRCA1 or BRCA2, or a history of chest radiation or an increased risk of breast cancer need to get mammograms before the age of 50.13 But, for everyone else, it may turn out that the best payoff in terms of optimal outcome will be in preventing breast cancer. This article addresses arguments on both sides of the controversy and provides nurse practitioners (NPs) with helpful information to guide their patients in making important decisions regarding the benefits and risks of screening. Other ways to lower their risk of dying from breast cancer besides screening mammography are also discussed. INCIDENCE AND PREVALENCE
On January 1, 2010, the prevalence, or total number of women with breast cancer in the US, was 2.83 million, including those with active disease and those
cured of the disease. A woman’s lifetime risk of being diagnosed with breast cancer is 1 in 8, but the breast cancer mortality is, in fact, lower because many women will die of another disease first before they die of breast cancer.2 A more useful statistic is the probability that a woman between the ages of 50 and 70 will develop breast cancer (5.59%).2 In 2013, the incidence, or number of new cases of breast cancer in the US, was estimated at 232,340 with 39,260 deaths.2 Between the years 2006 and 2010, the incidence of breast cancer in the US averaged out to 123.8 per 100,000 women per year.2 Figure 2 shows the incidence and deaths from breast cancer per 100,000 women by racial and ethnic group. The incidence was highest for white women, followed by black women, Asian/Pacific Islander women, Hispanic women, and American Indian/Alaska Native. Death rates, however, were the highest for black women, followed by white, American Indian/Alaskan Native, Hispanic, and Asian/Pacific Islander women. Between 2006 and 2010, the median age of death for breast cancer was 68 years old. Figure 3 shows the incidence and deaths from breast cancer by age as a percentage of total women. The incidence and death rate were highest between the ages of 55 and 64, with 25.2% of all women diagnosed with breast cancer in that age group and 21.6% of the deaths in
Figure 1. Different types of cancer progression.
The Fast arrow represents a cancer that quickly results in clinical symptoms and death. The Slow arrow represents a cancer that is slow growing and takes many years to manifest clinically. The Very Slow arrow represents a cancer that is so slow growing that the patient will die of another disease before breast cancer. The Non-progressive arrow represents either a cancer that actually regresses or a cancer that will never cause clinical symptoms although it meets the pathological criteria for a cancer diagnosis on screening. Reprinted by permission of Oxford University Press from Welch HG, Black WC. Overdiagnosis in cancer. J Natl Cancer Inst. 2010;102(9):605-613. 722
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Figure 2. Breast cancer new cases and deaths per 100,000 women per year by racial/ethnic group (2006-2010).
Data from National Cancer Institute.2
that age group. Only 5.3% of breast cancer deaths were from women between 35 and 44 years old, whereas 14.6% of deaths were from women 45 to 54 years old. Although the incidence of new cases dropped off after age 65, the death rate as a percentage of all women remained high, with 20.2% of the women dying from breast cancer in the 65- to 74-year age group and 21.5% of the total women dying in the 75- to 84-year age group.
HISTORY OF THE CONTROVERSY OVER SCREENING
The earliest use of x-rays to identify breast cancer goes back to 1913, but it was not until the 1960s that the use of mammograms to screen for breast cancer became accepted.14 The use of mammography for screening purposes became controversial in the 1970s because epidemiologic studies examined the numbers of lives saved for entire populations, as opposed to looking at individual cases.14 John Bailar, a physician who had
Figure 3. Percentage of total women with new cases and deaths from breast cancer by age group.
Data from National Cancer Institute.2 www.npjournal.org
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been trained in biostatistics and epidemiology, pointed out that routine mammograms could detect slowgrowing cancers, such as ductal and lobular carcinoma in situ, that would likely never turn into clinically significant breast cancer.15 This detection of slowgrowing cancers would make screening seem more beneficial than it actually was by reporting women whose lives were “saved” because of screening when, in fact, their cancers would never have killed them in the first place. Bailar15 also pointed out the danger of radiation from the mammogram itself. In response to these concerns, the American Cancer Society and the National Cancer Institute revised the consent form to inform women of potential risks of mammography and also hastened the process to standardize the radiation dosages.14 They also decided to recommend giving mammograms to women younger than age 50 only if they were at “high risk.” The problem was that high risk was defined so broadly (ie, a woman with merely a fear of breast cancer was considered “high risk”) that it included 80% of the women in the 35- to 50-year age bracket.14 In 1983, the American Cancer Society recommended a screening mammogram every 1 to 2 years for women 40 to 49 years old.14 The American Cancer Society made its recommendation after concluding that screening saved lives for women younger than 50.16 The American College of Radiology joined the American Cancer Society in 1988 in recommending routine mammograms for women 40 to 50 years old. The tide began to turn in 1993. A series of randomized controlled trials including women in their 40s concluded that mammography had no benefit for younger women.13 In 2001, a study published in Lancet17 found that 6 of 8 mammography studies during the previous 3 decades were found to be deeply flawed. This analysis called into question the requirement that women get annual mammograms starting at any age. The task force analysis16 temporarily put to rest the controversy. The US PSTF is an independent panel of internists, pediatricians, and family physicians who are experts in prevention and evidence-based medicine and who work outside the federal government but serve under the auspices of the Federal Agency for Healthcare Research and Quality. The 2002 task force analysis examined 8 randomized controlled trials of mammography and 154 724
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publications of the results of these trials. It concluded that for the studies rated “fair or better,” mammography did reduce breast cancer mortality among women ages 40 to 74 with absolute risk reduction greater in the older women. Still, the authors pointed out that mammography’s benefit in reducing death from breast cancer may be so small that any bias in studies could erase its benefits and that future studies should be directed at improving the sensitivity and specificity of mammography.16 The analysis showed that the studies had concluded that 1,224 women had to be screened to prevent 1 death after 14 years of observation, with 1,792 women needing to be screened to prevent 1 death if they were younger than 50 years old. The task force study16 also found no evidence that BSEs saved lives in 2 randomized controlled trials with a 5- to 10-year follow-up. Breast cancer mortality was no different in the group who did BSE versus controls. In both studies, the women were “meticulously trained” in the proper technique of BSE. The only difference between the 2 groups was that those trained in BSE had more physician visits and more biopsies for benign breast lesions. Lives Saved per 1,000 Screened Women
One part of the debate has focused on how many women’s lives per 1,000 screened would be saved. An analysis of trials conducted in Sweden found that for every 1,000 women screened every 2 years, after 12 years, 1 breast cancer death was avoided.17 Studies by Duffy et al18 of women in England and Sweden found more lives saved per 1,000 screened women. Comparing a randomized trial in Sweden and a breast screening program in England, Duffy et al found that both had significant reductions in mortality, estimated at 8.8 deaths prevented per 1,000 women screened for 20 years starting at age 50 in the Swedish trial and 5.7 deaths per 1,000 women screened prevented in the English program. So, which is it—1 life saved per 1,000 screened or 8.8 lives saved per 1,000? Different years of follow-up is 1 reason for the different conclusions. Another reason for the different conclusions is that the denominators were not consistent; in the screening, the denominator was made up of women who had received a breast cancer diagnosis from screening, Volume 10, Issue 9, October 2014
which could include those “overdiagnosed,” whereas in the control group, the denominator was made up of women who had received a diagnosis from symptoms, presumably a smaller group. In other words, the screening group death rate looked smaller because its denominator included women whose cancers may never have been found without screening and turned into a lethal disease. Based on a new systematic review,19 in 2009, the task force updated its 2002 recommendations, now advising biennial screening mammography for women between the ages 50 and 74 and no routine screening for women younger than age 50. For both groups of women, those in the 40- to 49-age range and those in the 50- to 59-age range, the task force stated that research had found the relative risk reduction for screening is similar, 15% and 14%, respectively, but the absolute risk reduction is greater in the older women simply because the risk increases with age. Therefore, the task force study concluded that “net benefits were small” for the age range of 40 to 49 years. The task force also stated that there were not enough data to determine the benefits and harms of mammograms for women older than age 75. The task force study authors also pointed out potential harms of screening, in particular the risk of overdiagnosis with ductal carcinoma in situ (DCIS).10 Half or fewer cases of DCIS progress to invasive cancer, but standard treatment had called for surgery plus radiation and hormone therapy.10 Screening has dramatically increased the diagnosis of DCIS: 4,900 cases were diagnosed in 1983 compared with 67,770 in 2008.10 Another study of women with DCIS by Ernster and Barclay as cited by Humphrey et al16 found that 44% of the women had mastectomies and 23% to 30% had lumpectomies. In other words, there may be have been approximately 15,000 unnecessary mastectomies in 2008, if these figures hold true. RISKS OF SCREENING
Researchers have studied the risks of screening with different conclusions about the specific numbers. They include anxiety generated by false-positive results, risks from being exposed to radiography itself, and risk of overdiagnosis.5 Potential harms from screening also include the risk of ill effects on a woman’s sexual well-being and sexual relationships.5 www.npjournal.org
False Positives
A false positive rate is calculated by determining the number of mammograms read as abnormal or needing more follow-up in women who subsequently were found not to have cancer divided by the total number of women who screened positive. One study estimated the false-positive rate to be 63% after 10 screening mammograms.20 Other studies have determined the rate to be 21% to 49% after 10 years of screening mammograms for women of all ages and 56% after 10 years of mammograms for women ages 40 to 49.19 In a review of research done between 1995 and 2007, studies showed that for up to 2 years after screening, women with false-positive results had increased levels of breast cancer worries, changes in mood, higher anxiety, and more cases of intrusive thinking compared with before they had the mammogram.21 Another study found that 3 years after women with falsepositive diagnoses were told they were actually cancer free, they still had higher negative psychosocial scores than women who had been given true-negative findings.22 However, women may have a high tolerance for false-positives results if they save someone’s life.16 A 2000 study by Schwartz et al (as cited by Humphrey et al16) found that 63% of women would tolerate 500 false-positive results to save 1 life. Radiography Risks
Radiation from the mammogram also presents a risk, albeit small. Of 100,000 women being screened for 10 years starting at age 40, no more than 8 additional breast cancer deaths would occur because of radiation.16 Overdiagnosis
The most compelling argument against screening is that of overdiagnosis. Although screening may result in a reduction of breast cancer deaths, they may increase deaths from other causes.23 In other words, although breast cancer mortality has dropped after screening, overall mortality has not. Given the high stakes, it is no wonder that those on opposing sides of the controversy offer differing figures as to what the true rate of overdiagnosis is.24-27 It also represents an entirely new way of thinking that a cancer can be so slow growing or even regress so that no treatment is necessary or advisable.9 The Journal for Nurse Practitioners - JNP
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It is impossible to directly determine if any particular breast cancer case was overdiagnosed. Thus, researchers must use estimates based on population studies that compared observed deaths from breast cancer with those expected. In particular, overdiagnosis rate estimations come from the changes in breast cancer incidence rates after screening has been introduced in a population. Because of no agreed-upon method, the estimates can vary from 5% to 50% of cases of cancer being overdiagnosed.24 For example, 1 study of women in Sweden and England estimated a rate of 4% to 7% of cases of cancer being overdiagnosed.18 Another analysis found an overdiagnosis rate estimated to be between 16% and 24% depending on the denominator used.9 The USPSTF study estimated that overdiagnosis ranges from 1% to 10%.19
Just how is overdiagnosis calculated? A 2006 study by Zackrisson et al27 illustrates how. After a 10-year trial, 150 more women had been diagnosed with breast cancer in a mammography group than in a control group. This made sense because mammography works by diagnosing breast cancer that is missed without screening before the tumor becomes clinically evident. The women were then followed for another 15 years. During the follow-up, both groups received mammography so the cancers in the originally nonscreened control group could presumably “catch up” with the study group and be properly diagnosed clinically. This “catching up” in number of diagnosed cases would be expected with 2 samples drawn from the same population. But, after 14 years, still 115 more women were diagnosed in the original study group than in the control group. Why didn’t
Table. Comparison Chart of Breast Cancer Screening Guidelines Issued by US Professional Societies and Organizations Professional Society or Group (Year of Recommendation)
Age to Definitely Screen Asymptomatic Women not at Increased Risk for Breast Cancer
Frequency of Screening
American Cancer Society (2013)
Age 40 and continuing for as long as women is in good health
Yearly
American College of Obstetricians and Gynecologists (2011)
Age 40
Yearly
American College of Physicians (2007)
Age 50 (women ages 40-49 need to assess risks for breast cancer to help guide decision; physicians should inform women of benefits and harms of mammography; reasonable to start at age 40 if women does not wish to discuss decision)
Every 1 to 2 years
American College of Radiology (2013)
Age 40 but no definite age when screening should end as long as patient is in good health
Yearly
American College of Surgeons (2009)
Age 40
Yearly
American Medical Association (2012)
Age 40, but patients should talk to doctor as to whether screening is right for them
NA
American Association of Family Physicians (2014)
Age 50-74 (mammograms for women younger than age 50 should take into account their risks of getting breast cancer as well as their values on benefits and harms; women age 75 and older should talk to their physicians about benefits and harms of screening)
Every 2 years
National Research Center for Women & Families’ Cancer Prevention and Treatment Fund (2007)
One mammogram at age 40 or 45 and then wait until age 50 if it is normal
NA
US Preventive Services Task Force (2009)
Age 50 until age 74
Every 2 years
NA ¼ not applicable; US ¼ United States.
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the number of cancers in the control group catch up? The authors concluded that the excess was because of overdiagnosis, meaning a suspicious lesion was identified that would never become clinically significant. Zackrisson et al27 calculated that about 1 in 6 cancers are overdiagnosed. IMPLICATIONS FOR NURSING PRACTICE
NPs will need to provide their patients with the facts regarding both sides of the screening controversy given the lack of agreement. Factors increasing the risk of breast cancer, such as family history or genetic mutations, may well tilt the balance in favor of starting at age 40 with the benefits outweighing the risks.28 Much education is needed because awareness of the task force guidelines among women is low; only 12% were aware of the 2009 USPSTF guidelines (Table) recommending starting screening at age 50.28 In addition, some NPs may find that with either outcome, screening is self-reinforcing; negative results bring what could be false relief and positive results provide the consolation of being saved from what is believed to be a harmful tumor, without necessarily knowing whether it is or not.29 Explaining the risks and benefits will empower patients to decide for themselves whether they want to start mammography screening at age 40, wait until age 50, or forgo screening altogether if they believe the benefit does not outweigh the risk. One way to allow a woman to decide for herself is to show her the numbers; for every 10,000 women who receive a regular mammogram for 10 years, starting at age 40, 6 women will have reduced their risk of death from breast cancer.30 During this 10-year period of regular mammograms, as many as 5,000 of the 10,000 women will get a false-positive result requiring them to return for more testing.30 For the 626 women out of the 10,000 who receive a diagnosis of breast cancer,27 anywhere from 20 (3.2% overdiagnosis31) to 156 (15%-25% overdiagnosis32) of these women may be receiving unnecessary treatment. Paying for the mammogram may be another consideration if insurance policies change to not cover mammograms for certain women. Currently, however, mammograms are covered by the majority of insurance plans, and free screening is offered for many low-income women. www.npjournal.org
No matter what decision the patients make in consultation with their primary care provider, it is prudent to makes sure they understand that more than 1 “right” answer exists currently regarding screening. Look to the author of a scholarly article to determine if a bias may exist; for example, radiologists are more likely to advocate routine screening.33 In light of this, to protect against lawsuits, the rationale for or against screening should be documented along with the final decision of the patient.34 It may also be helpful to know that most claims for missed or delayed diagnosis of breast cancer were caused by failure to properly evaluate clinical manifestations of the disease, such as palpable lumps or abnormalities on mammograms, and not caused by inadequate screening in otherwise healthy patients.34 At the same time, a stepped-up emphasis on the awareness of breast cancer and prevention will do much to lower mortality risks. NPs can teach women to be aware of their own breasts and what represents a change, urging them to seek immediate medical attention if they notice any nipple discharge, inverted nipples, “orange”-like peau appearance of the skin, or, of course, a lump. Excess weight, alcohol, early menarche, and use of estrogen have all been linked to an increased risk of breast cancer.35,36 Therefore, NPs may want to go back to the basics—recommending that their patients keep their weight down (leading to a 25%-50% reduction in the risk of breast cancer35) and limit alcohol (even moderate consumption of alcohol increases the risk of breast cancer 36), advising parents to keep their preadolescent daughters thinner to prevent a too-early 1st menarche (our ancestors had 160 ovulations over their lifetime and breast cancer was rare vs now when we have 450 ovulations per lifetime35), and discouraging their menopausal patients from using estrogen. Breastfeeding for 12 months also lowers the relative risk by 4.3%, whereas each birth lowers it by 7%.36 Black women should be informed of statistics showing their higher mortality from breast cancer2 so they may take prompt action if a lump is found to get treatment. Finally, for those women who do want to get mammograms, NPs can provide evidence-based research on the risks and benefits. Based on this research, some patients perhaps even take a cue from men with prostate cancer diagnoses and choose the option of “watchful waiting” if the results come out The Journal for Nurse Practitioners - JNP
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positive, particularly in the case of DCIS. The watchful waiting allows for the possibility that the tumor may be slow growing or even regress.37 CONCLUSION
Thinking about mammography continues to evolve. Experts disagree on the extent of the risk, not the risks themselves. Making women aware of the controversy and encouraging them to think about their own particular situation may be the wisest course because there is no absolute correct answer. Women will have to consider their own particular risks; for example, statistics show that black women are more likely to die of breast cancer so that may influence their decisions about screening and prevention. Future studies should also look at the way costs influence individual decisions in an era when health care spending is becoming increasingly scrutinized. References 1. Magnus MC, Ping M, Shen MM, Bourgeois J, Magnus JH. Effectiveness of mammography screening in reducing breast cancer mortality in women aged 39-49 years: a meta-analysis. J Womens Health. 2011;20(6): 845-852. 2. Howlader N, Noone AM, Krapcho M, et al., eds. SEER Cancer Statistics Review, 1975-2010. Bethesda, MD: National Cancer Institute. http://seer .cancer.gov/statfacts/html/breast.html. Accessed July 13, 2013. 3. Brawley OW. Risk-based mammography screening: an effort to maximize the benefits and minimize the harms. Ann Intern Med. 2012;156:662-663. 4. Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367(21):1998-2005. 5. Gotzsche PC, Hartling OJ, Nielsen M, Brodersen J, Jorgensen KJ. Breast screening: the facts—or maybe not. BMJ. 2009;338:446-448. 6. Autier P, Koechlin A, Smans M, Vatten L, Bonio M. Mammography screening and breast cancer mortality in Sweden. J Natl Cancer Inst. 2012;104(14): 1080-1093. http://dx.doi.org/10.1093/jnci/djs272. 7. Ravdin PM, Cronin KA, Howlader N, et al. The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med. 2007;356: 1670-1674. 8. Gotzsche PC. Time to stop mammography screening? CMAJ. 2011;182:1957-1958. 9. Welch HG, Black WC. Overdiagnosis in Cancer. J Natl Cancer Inst. 2010;102:605-613. 10. US Preventive Services Task Force. Screening for breast cancer: US Preventive Services Task Force Recommendation Statement. Ann Intern Med. 2009;151:716-726. 11. Drukteinis JS, Mooney BP, Flowers CI, Gatenby RA. Beyond mammography: new frontiers in breast cancer screening. Am J Med. 2013;126(6):472-479. 12. Gotzsche PC, Jorgensen KJ, Zahl P-H, Maehlen J. Why mammography screening has not lived up to expectations from the randomized trials. Cancer Causes Control. 2012;23:15-21. 13. Van Ravesteyn NT, Miglioretti DL, Stout NK, et al. What level of risk tips the balance of benefits and harms to favor screening mammography starting at age 40? Ann Intern Med. 2012;156(9):609-617. 14. Lerner BH. To see today with the eyes of tomorrow: a history of screening mammography. Background paper for the Institute of Medicine Report, Mammography and beyond: developing technologies for the early detection of breast cancer. http://www.oup-usa.isbn/0195142616.html. Accessed July 13, 2013. 15. Bailar JC. Mammography: a contrary view. Ann Intern Med. 1976;84(1):77-84. 16. Humphrey LL, Helfand M, Chan BKS, Woolf SH. Breast cancer screening: a summary of the evidence for the US Preventive Services Task Force. Ann Intern Med. 2002;137(5):E347-E367.
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17. Gotzsche PC, Olsen O. Is screening for breast cancer with mammography justifiable? Lancet. 2000;355:129-134. 18. Duffy SW, Tabar L, Olsen AH, et al. Absolute numbers of lives saved and overdiagnosis in breast cancer screening, from a randomized trial and from the Breast Screening Programme in England. J Med Screen. 2010;17:25-30. 19. Nelson HD, Tyne K, Naik A, Bougatsos C, Chan BK, Humphrey L. Screening for breast cancer: an update for the US Preventive Services Task Force. Ann Intern Med. 2009;151:727-737. 20. Hubbard RA, Miglioretti DL, Smith RA. Modeling the cumulative risk of a false-positive screening test. Stat Methods Med Res. 2010;19(5):426-449. 21. Hafslund B, Nortvedt MW. Mammography’s screening from the perspective of quality of life: a review of the literature. Scand J Caring Sci. 2009;23: 539-548. 22. Brodersen J, Siersma VD. Long-term psychosocial consequences of falsepositive screening mammography. Ann Fam Med. 2013;11(2):106-115. 23. Newman DH. Screening for breast and prostate cancers: moving toward transparency. J Natl Cancer Inst. 2010;102:1008-1011. 24. Duffy SW, Parmar D. Overdiagnosis in breast cancer screening: the importance of observation period and lead time. Breast Cancer Res. 2013;15:R41. 25. Kalager M, Adami H-O, Bretthauer M, Tamimi RM. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med. 2012;156(7):491-499. 26. Welch HG. Overdiagnosis and mammography screening. BMJ. 2009; 339(7714):1425. 27. Zackrisson S, Andersson I, Janzon L, Manjer J, Garne JP. Rate of overdiagnosis of breast cancer 15 years after end of Malmo mammographic screening trial: follow up study. BMJ. 2006;332:689-692. http://dx.doi.org/ 10.1136/bmj.38764.572569.7C. 28. Kiviniemi MT, Hay JL. Awareness of the 2009 US Preventive Services Task Force recommended changes in mammography screening guidelines, accuracy of awareness, sources of knowledge about recommendations, and attitudes about updated screening guidelines in women ages 40-49 and 50þ. Public Health. 2012;12:899. http://dx.doi.org/10.1186/1471-2458 -12-899. 29. Hale PJ, de Valpine MG. Screening mammography: revisiting assumptions about early detection. J Nurse Pract. 2014;10(3):183-188. 30. Elmore JG, Choe JH. Breast cancer screening for women in their 40s: moving from controversy about data to helping women. Ann Intern Med. 2007;146:529-531. 31. Paci E, Miccinesi G, Pulti D, et al. Estimate of overdiagnosis of breast cancer due to mammography after adjustment for lead time. A service screening study in Italy. Breast Cancer Res. 2006;8(6):R68. http://dx.doi.org/10.1186/bor1625. 32. Kalager M, Zelen M, Langmark F, Adami H-O. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010;363(13):1203-1210. 33. Norris SL, Burda BU, Holmer HK, et al. Author’s specialty and conflicts of interest contribute to conflicting guidelines for screening mammography. J Clin Epidemiol. 2012;65(7):725-733. 34. Marmot MG. Sorting through the arguments on breast screening. JAMA. 2013;309(24):2553-2556. 35. Howell A, Astley S, Warwick J. Prevention of breast cancer in the context of a national breast screening programme. J Intern Med. 2012;271:321-330. 36. Tirona MT, Sehgal R, Ballester O. Prevention of breast cancer (part 1): erpidemiology, risk factors and risk assessment tools. Cancer Investig. 2010;28:743-750. 37. Zahl PH, Maehlen J, Welch HG. The natural history of invasive breast cancers detected by screening mammography. Arch Intern Med. 2008;168(21):2311-2316.
Ruth Tupper, MS, RN, is a guest instructor at DePaul University School of Nursing in Chicago, IL, and can be reached at [email protected]. Karyn Holm, PhD, RN, FAAN, FAHA, is professor and associate dean for research at the Marcella Niehoff School of Nursing, Loyola University Chicago in Maywood, IL. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest. 1555-4155/14/$ see front matter © 2014 Elsevier, Inc. All rights reserved. http://dx.doi.org/10.1016/j.nurpra.2014.07.018
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