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Breast Cancer Screening in Women Previously Treated for Hodgkin’s Disease: A Prospective Cohort Study

From the Departments of Medicine, Pediatrics, and Radiation Oncology, Harvard Medical School; Departments of Pediatrics, Adult Oncology, Radiology, and Biostatistics, Dana-Farber Cancer Institute; Massachusetts General Hospital; Brigham and Women’s Hospital; and Children’s Hospital, Boston, MA.

Address reprint requests to Lisa Diller, MD, Dana-Farber Cancer Institute, 44 Binney St, Dana 367, Boston, MA 02115; email: Lisa_Diller{at}dfci.harvard.edu

	ABSTRACT

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PURPOSE: Young women who are exposed to chest irradiation for Hodgkin’s disease (HD) are at increased risk of breast cancer; this study investigated patient awareness of breast cancer risk and patient screening behavior and assessed the utility of mammographic screening in HD survivors.

PATIENTS AND METHODS: This is a prospective cohort study of 90 female long-term survivors of HD who had been treated 8 years previously with mantle irradiation (current age, 24 to 51 years). Participants completed surveys of their perceptions of breast cancer risk and screening behaviors and received written recommendations for breast examinations and mammography. Annual follow-up was conducted through medical records, telephone, and/or mailed questionnaires.

RESULTS: At baseline, women were often unaware of their increased risk of breast cancer; 40% (35 of 87) reported themselves to be at equal or lower risk than women of the same age. Only 47% (41 of 87) reported having had a mammogram in the previous 24 months. Women who had received information from an oncologist were more likely to assess correctly their risk than women who received information from other sources (P < .001). Ten women developed 12 breast cancers (ductal carcinoma-in-situ [n = 2], invasive ductal carcinoma [n = 10]) during the study; two were diagnosed at study entry, and 10 during follow-up (median, 3.1 years). All cancers were evident on mammogram, and eight of 10 invasive cancers were node negative.

CONCLUSION: Practitioners who care for women after HD therapy need to educate patients regarding their risks and begin early screening. Screening by mammography can detect small, node-negative breast cancers in these patients.

	INTRODUCTION

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DURING THE PAST 25 years, a diagnosis of Hodgkin’s disease (HD) has carried an excellent prognosis, with the majority of patients having been cured of their primary tumor. However, late complications of therapy in survivors are increasingly recognized, with follow-up studies of HD survivors showing a significant risk of new cancers.^1-3 Of particular concern in this group is the increased risk of breast cancer among female HD survivors. Increases in relative risk are most pronounced for women who are treated with radiation for HD at a young age, with relative risks of breast cancer increased more than 30-fold in women who are treated with radiation therapy at age less than 30 years in several studies.^3-7 The absolute excess risk of breast cancer in HD survivors is also elevated, with women who are treated at age less than 30 showing an excess risk of 23 to 47 cases per 10,000 person-years of follow-up.³ This increased risk of breast malignancy is detectable by approximately 10 years after HD treatment, with additional increases at 15 or more years of follow-up. Bhatia et al² reported a high actuarial cumulative probability of breast cancer of 35% at age 40 in a cohort of North American and West European HD survivors. In a population-based cohort study of survivors of childhood HD using the Nordic countries’ registries, Sankila et al⁶ found a cumulative risk of breast cancer of 12% (95% confidence interval, 5.2% to 18%) for female survivors at 30 years after HD.

Reports of breast cancer after HD have suggested that tumors are usually evident on mammograms.^8,9 The age at breast cancer diagnosis in these patients is much younger than the general population, with many cancers occurring before age 40. Many HD survivors may not be aware of their increased risk, and little is known about how best to inform patients about their risk, how to follow them clinically, and whether the early initiation of mammographic screening will result in decreases in morbidity and mortality from breast cancer.

In 1995, we began a prospective cohort study of female HD survivors who had received mantle irradiation as part of their lymphoma treatment. We sought to evaluate, at baseline, the patient’s knowledge of breast cancer risk, sources of information regarding risk, and the baseline characteristics of mammograms, including breast density. Other end points were the incidence of radiographically and clinically detected breast cancers and the incidence of other cancers in follow-up.

	PATIENTS AND METHODS

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Eligibility, Enrollment, and Participation
Eligible patients were women who were aged 20 to 50 at the time of first contact for the study. Patients must have received a diagnosis of HD before age 30 and must have undergone mantle irradiation as a part of the treatment for HD. Treatment with radiation must have occurred at least 8 years before enrollment, and there could be no history of breast cancer, although a history of other malignancies was not an exclusion criterion. The study was approved by the institutional review board at the Dana-Farber Cancer Institute. Potential eligibility was determined by examination of clinical databases from the Dana-Farber Cancer Institute and the Harvard Joint Center for Radiation Therapy and its affiliated hospitals.

Potential patients received a letter from the study investigators; this letter included a consent form, a baseline questionnaire, a medical record release form, and a recommended mammography schedule. These patients were able to participate by filling out the questionnaire and either submitting an outside mammogram for central review or coming to the Dana-Farber Cancer Institute for a mammogram. In addition, eligible patients who presented for follow-up at the Dana-Farber Cancer Institute could receive the enrollment packet. The information given to participants recommended a mammogram every other year beginning at 8 years after radiation until age 30, and then annually. Annual breast examination by a medical professional and monthly breast self-examination were also recommended. Although patients were encouraged to participate in all aspects of the study (baseline questionnaires, mammogram review, and follow-up), partial participation was permitted.

Risk Questionnaire
The risk questionnaire was adapted from a questionnaire used in the Cancer Risk and Prevention Clinic at the Dana-Farber Cancer Institute. The participants were asked whether they thought that their risk of breast cancer was the same or different from the average woman of the same age. They were asked about their sources of breast cancer risk information, where they received their follow-up care for HD, and their source of primary care (if different). They were also asked about their breast health practices, including the frequency of breast self-examination and their mammography schedule at the time of the receipt of the questionnaire.

Medical Record Review
Medical records and/or clinical databases were reviewed to obtain information regarding each participant’s history of HD. In particular, patient records were abstracted for date of diagnosis, age at diagnosis, stage, treatment, and history of relapse. For patients who developed breast cancer during the study, medical records regarding the diagnosis of breast cancer, staging, and treatment were obtained.

Mammogram Review
Attempts were made to review all mammograms performed on cohort members during the study, including those performed at outside institutions. A mammogram was considered a baseline study when it was performed within 1 year before study enrollment. Magnification views and ultrasound were used for evaluation of suspicious foci. All patients with abnormal mammograms received a recommendation for either follow-up mammography in 6 months (for probably benign findings) or biopsy (for suspicious lesions). Mammogram density was evaluated semiquantitatively in the first 43 participants who submitted mammograms in the study, using a five-point density scale (1 = very dense, 2 = moderately dense, 3 = mildly dense, 4 = mildly fatty, 5 = fatty). The mammograms were reviewed by three independent experienced mammographers, and discrepant results were recorded and adjusted by consensus. Funding was available during the first year of the study to conduct density scoring. An additional 16 baseline and all follow-up mammograms were reviewed clinically.

Statistical Analysis
Descriptive statistics are provided for the demographic and clinical features of the cohort, questionnaire results, mammograms, and breast cancer detection. To determine whether relationships between risk factors and perception of high-risk status exist, we used Fisher’s exact test.¹⁰

To ascertain which clinical features predicted whether patients had a mammogram in the 2 years before enrollment, we used multivariate logistic regression modeling. The models included both main effects and interactions. A backward selection technique was also used to isolate the most influential variables.¹⁰ To determine whether there was an association between breast density and age, we used a Wilcoxon rank sum test.¹¹ To test for differences between breast cancer patients and the other HD patients in the cohort, we used Fisher’s exact test and the Wilcoxon rank sum test.^10,11 The number of breast cancers per person-year of mammographic follow-up and overall follow-up was calculated for this cohort. The number of breast cancers per person-year of follow-up was compared with population-based data¹² by calculating the relative risk.¹³ In addition, a 95% confidence interval for the relative risk was calculated assuming that the number of breast cancers detected per person-years of follow-up had a Poisson distribution.¹⁴

	RESULTS

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Characteristics of the Cohort
By database review, we were able to identify 167 eligible women. Of these, 120 were contacted successfully either by mail or on presentation to clinic; 47 did not respond to mailings on two occasions. Of the 120 patients who were contacted, 90 participated, resulting in an enrollment rate of contacted patients of 75%. The overall enrollment rate (including the patients who were lost to follow-up) was 54%. The demographic characteristics of the study participants are listed in Table 1. Of note, there is no difference in age, age at diagnosis of HD, or time since HD between the participants and the nonparticipants (data not shown).

Questionnaire Results
All enrollees were asked to respond to a baseline questionnaire. We received completed baseline questionnaires from 87 women (52% of the 167 offered enrollment, 73% of the women located, and 97% of the women actually enrolled). The questionnaire results indicate that these women, at the time of enrollment in the study, were not universally aware of their increased risk of breast cancer or consistently participating in any defined screening programs for high-risk women. Subjects were asked, "Compared to other women your age, how likely is it that you will develop breast cancer?" Of the 87 respondents, 52 (60%) answered "more" or "much more" likely, 32 (37%) answered "same," and three (3%) answered "less" or "much less" likely. Most of the women (79 of 87 [91%]) did not perform regular breast self-examination. Mammograms had been performed on 63 of 87 (72%) women at some time, but only 47% (41 of 87) had had a mammogram in the previous 2 years before enrollment.

To assess predictors of active breast cancer screening and of correct perception of increased risk, we analyzed demographic, treatment-related, and questionnaire data. These results are listed in Table 2. Participants who reported having received their breast cancer risk information from an oncologist were more likely to report themselves to be at high risk (P < .001). Younger patients (age < 35 years) were more likely to get their information from an oncologist, with 25 of 33 citing their oncologist as their source of risk information compared with 20 of 48 of the patients who were 35 or older (P = .01). However, women who perceived themselves to be at high risk were not more likely to have had a mammogram in the previous 2 years (P = .83). Older patients were significantly more likely (P = .0008) to have had a mammogram in the previous 2 years, with only nine of 35 younger patients (< 35 years) reporting having had a mammogram in the previous 2 years, compared with 32 of 50 older patients. Multivariate analysis revealed that older patients who understood that they were at high risk and received risk information from an oncologist were seven times more likely than patients without this profile to have had a mammogram in the previous 2 years. However, this effect did not reach statistical significance, possibly because only 14 women met these criteria. Only age greater than 35 was a positive predictor of having had a mammography in the previous 2 years.

Five of the 10 women who developed breast cancer during the study were included in the density-scored subcohort. Their breast densities on baseline mammogram, using the same semiquantitative scale described above, were dense (n = 2), moderate density (n = 1), mildly fatty (n = 1), and fatty (n = 1).

Baseline mammograms from 59 women were submitted for central review; an additional 20 patients reported having a normal mammogram at enrollment. Of these 79 study-entry mammograms, 69 were read as normal or with benign-appearing findings. Of the 10 abnormal studies, 5 required immediate biopsy, two of which were nonpalpable invasive breast cancers (one was lobular carcinoma-in-situ, and two were benign fibroadenomas). Of note, one of the invasive tumors was detected on central review of an outside mammogram that had been previously read as normal. For the remaining five women, the recommended course of action was a 6-month interval mammogram; none of these five was associated with a known eventual breast cancer diagnosis during the course of the study. However, one of these patients withdrew from the study on receiving the recommendation of a 6-month repeat mammogram. She stated that she was too upset to continue the study, having been told by her local radiologist that her breasts were too small and dense to continue mammography on a regular basis. No additional information is available on this patient.

Of note, six women in the cohort refused mammography. Reasons given for not having mammograms included "too young" (n = 3), "breasts are too dense according to primary physician" (n = 1), and no reason given (n = 2). Four patients withdrew from the study. Reasons for withdrawal included "no time" (n = 1), "too upsetting to deal with" (see above paragraph) (n = 1), and no reason (n = 2).

The median time of follow-up in the cohort is 3.1 years (range, 0 to 4.2 years). As noted above, two breast cancers were detected during baseline evaluations. In the follow-up period of the study, an additional 10 breast cancers were detected. One was a metachronous contralateral cancer in one of the women who had breast cancer detected at baseline. One subject developed synchronous bilateral breast cancer. Therefore, in our original group of 90 women, a total of 10 women developed 12 breast cancers, eight women with unilateral and two with bilateral cancer.

Clinical Characteristics of Breast Cancer Cases
The median age at breast cancer diagnosis was 43 years (range, 29 to 50 years). The median time from HD to breast cancer diagnosis was 19.5 years (range, 12 to 28 years). The clinical and treatment characteristics are listed in Table 3. All 12 cancers were ductal; two were ductal carcinoma-in-situ (DCIS), and 10 were invasive ductal carcinoma. All 12 lesions were detectable on mammograms, and seven of these were initially detected by mammography. All invasive tumors were T1 (size < 2 cm), except for two multifocal tumors. Eight of the 10 invasive tumors were node negative. Six of the invasive tumors were estrogen receptor–positive. There were no deaths from breast cancer, although one breast cancer patient died during the study period from previously diagnosed primary lung cancer.

Cancer Incidence and Mortality
Excluding incident breast cancer cases detected at enrollment, there were eight new breast cancer cases detected in the 219.8 person-years of follow-up (or approximately four breast cancers per 100 person-years of follow-up). Of note, in the United States between 1973 and 1997, the risk of breast cancer (invasive and DCIS) for women younger than 50 was 0.039 per 100 person-years of follow-up.¹² The relative risk of developing breast cancer, therefore, comparing our entire cohort with population-based data, is 93 (95% confidence interval, 40 to 184). The cumulative incidence of breast cancer in our cohort is shown in Fig 1. Seven women died during the course of the study. The cause of death was malignancy in six and a cardiac event in one participant. No woman died of breast cancer or HD during the study period.

View larger version (13K): [in this window] [in a new window]   Fig 1. Cumulative probability of breast cancer (DCIS and invasive) in 90 female patients with history of mantle irradiation for HD. Incident cases diagnosed at entry to study are excluded. Median time from HD diagnosis to enrollment was 16 years (range, 8 to 30 years).

	DISCUSSION

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This is the first prospectively studied group of female survivors of HD to have participated in a protocol to assess breast cancer risk perception and screening. Wolden et al¹⁵ recently reported a series of breast cancer cases in HD survivors in the Stanford cohort, retrospectively evaluating the presentation, treatment, and outcome of breast cancers. They showed that the proportion of patients with early-stage disease was higher in breast cancer cases that were diagnosed after 1990. They suggested that this is due to the more frequent use of mammography in HD survivors, as physicians are more aware of the increased risk of breast cancer. Dershaw et al⁸ retrospectively studied 29 cases of breast cancer in HD survivors and reported that 26 (89.6%) cancers were mammographically evident. Although only a randomized clinical trial could determine the true impact of early mammography in HD survivors’ breast cancer mortality, our prospective data and previous retrospective data suggest that mammograms detect small tumors in HD survivors.

We could find no published studies of patients’ understanding of breast cancer risk after therapeutic radiation for HD. Although members of our cohort were enrolled well after 1990, when increased awareness of breast cancer risk in HD survivors was appreciated,¹⁵ a substantial proportion (40%) did not seem to understand that they were at higher breast cancer risk than the average woman of the same age. Patients who had been followed by an oncologist were more likely to understand that they were at higher risk. However, women who perceived themselves to be at higher risk were not more likely to have had a mammogram in the previous 2 years, suggesting that few care providers had adopted a policy of early screening. Providers may not recognize the magnitude of breast cancer risk after HD or the potential utility of mammography for detecting early disease in this group. Another possible explanation is that the patients themselves are not compliant with early mammography recommendations; we were unable to assess this directly, as we do not know what precise recommendations had been given to the participants before the study.

A potential concern in interpreting the results of this study is incomplete participation. However, the participants and nonparticipants were not different from each other in terms of current age, age at diagnosis of HD, or time since HD. Given the long median follow-up time (and that the cohort was young and female), it is not surprising that 28% of the potentially eligible women were not successfully contacted for the study. Of the successfully contacted women, 75% participated. Of note, a recent clinical database review of the 77 nonparticipants revealed two women with a diagnosis of breast cancer during the study period, compared with 10 with breast cancer in the 90 women in the cohort. We do not know whether nonparticipants are more or less likely to be aware of their breast cancer risk, and we were unable to assess screening behavior in the nonparticipants.

The optimum follow-up cancer surveillance regimens for cancer survivors are not well established. Increasingly, cancer centers and oncologists are providing long-term follow-up care for cancer survivors so that newly appreciated risks of late complications are communicated to patients in a timely manner. Oncologists must also communicate recommendations to primary care providers so that screening studies, such as mammography, can be initiated in the appropriate risk interval. In the current study, mammography screening began at 8 years after radiation and was recommended every other year until age 30 and then annually. Others have recommended beginning annual mammograms at 8 years from treatment^9,16; mammograms 5 years after radiation or at age 40, whichever occurs first,¹⁵ baseline mammogram at 5 years after radiation and then annually at 10 years¹⁷; and, for pediatric HD survivors, a baseline study at age 25 and then every 2 to 3 years until age 40 and then annually.¹⁸ Clinical breast examination every 6 months and breast self-examination monthly have been recommended.^15,17 Whichever schedule for mammography and examination is chosen, clinicians and radiologists need to interpret results in light of the patient’s previous exposure to radiation and her subsequent high risk of breast cancer.

A total of 21 cancers were diagnosed in this small cohort in a relatively short time, 12 breast cancers and nine other cancers. It should be acknowledged that the characteristics of this cohort—female, young median age at radiation, long median interval since radiation—make it a very select cohort at high risk for secondary cancers, especially breast cancer. However, this extraordinarily high risk of malignancy in a relatively young group of patients should alert clinicians to the need for active follow-up of HD patients during the young adult years and thereafter. Clinical trials that might result in early detection, prevention, or risk reduction in these patients should be actively pursued. We have recently begun a pilot trial of tamoxifen chemoprevention in HD survivors, and a study of breast magnetic resonance imaging for these patients is under way. Reduction in the use of radiation in the current treatment of HD may result in future decreases in the incidence of secondary breast cancer, but we remain responsible for investigating ways to decrease morbidity and mortality in these long-term survivors.

	ACKNOWLEDGMENTS

 
Supported by the David B. Perini Jr Quality-of-Life Program (L.D.) and the Dyson Foundation (L.D. and J.G.).

	REFERENCES

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2. Bhatia S, Robison LL, Oberlin O, et al: Breast cancer and other second neoplasms after childhood Hodgkin’s disease. N Engl J Med 334: 745-751, 1996[Abstract/Free Full Text]

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4. Mauch PM, Kalish LA, Marcus KC, et al: Second malignancies after treatment for laparotomy staged IA-IIIB Hodgkin’s disease: Long-term analysis of risk factors and outcome. Blood 87: 3625-3632, 1996[Abstract/Free Full Text]

5. van Leeuwen FE, Klokman WJ, Veer MB, et al: Long-term risk of second malignancy in survivors of Hodgkin’s disease treated during adolescence or young adulthood. J Clin Oncol 18: 487-497, 2000[Abstract/Free Full Text]

6. Sankila R, Garwicz S, Olsen JH, et al: Risk of subsequent malignant neoplasms among 1,641 Hodgkin’s disease patients diagnosed in childhood and adolescence: A population-based cohort study in the five Nordic countries. Association of the Nordic Cancer Registries and the Nordic Society of Pediatric Hematology and Oncology. J Clin Oncol 14: 1442-1446, 1996[Abstract/Free Full Text]

7. Travis LB, Curtis RE, Boice JD Jr: Late effects of treatment for childhood Hodgkin’s disease. N Engl J Med 335: 352-353, 1996[Free Full Text]

8. Dershaw DD, Yahalom J, Petrek JA: Breast carcinoma in women previously treated for Hodgkin’s disease: Mammographic evaluation. Radiology 184: 421-423, 1992[Abstract/Free Full Text]

9. Yahalom J, Petrek JA, Biddinger PW, et al: Breast cancer in patients irradiated for Hodgkin’s disease: A clinical and pathologic analysis of 45 events in 37 patients. J Clin Oncol 10: 1674-1681, 1992[Abstract/Free Full Text]

10. Cox DR: Analysis of Binary Data. London, Methuen & Co Ltd, 1970

11. Wilcoxon F: Individual comparisons by ranking methods. Biometrics 1: 80-83, 1945[CrossRef]

12. Ries LAG, Eisner MP, et al (eds): SEER Cancer Statistics Review, 1973-1997. Bethesda, MD, National Cancer Institute, 2000

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14. Pearson ES, Hartley HO: Confidence Limits for the Expectation, m, of a Poisson Variable. Biometrika Tables for Statisticians (ed 3, vol 1). London, Charles Griffin and Co., Ltd., for the Biometrika Trustees, 1976, pp 81-83, 227

15. Wolden SL, Hancock SL, Carlson RW, et al: Management of breast cancer after Hodgkin’s disease. J Clin Oncol 18: 765-772, 2000[Abstract/Free Full Text]

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17. Peters MH, Sonpal IM, Batra MK: Breast cancer in women following mantle irradiation for Hodgkin’s disease. Am Surg 61: 763-766, 1995[Medline]

18. Hudson MM, Poquette CA, Lee J, et al: Increased mortality after successful treatment for Hodgkin’s disease. J Clin Oncol 16: 3592-3600, 1998[Abstract]

Submitted June 26, 2001; accepted January 28, 2002.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Diller, L. Articles by Garber, J. Search for Related Content PubMed PubMed Citation Articles by Diller, L. Articles by Garber, J.