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Health Outcomes After External-Beam Radiation Therapy for Clinically Localized Prostate Cancer: Results From the Prostate Cancer Outcomes Study

From the Keck School of Medicine of the University of Southern California, Department of Preventive Medicine, Los Angeles, CA; Fred Hutchinson Cancer Research Center, Seattle, WA; Division of Urology, University of Connecticut Health Center, Farmington, CT; Division of Urology, University of Utah School of Medicine, Salt Lake City, UT; Medicine Service, Department of Veterans Affairs Medical Center and New Mexico Tumor Registry, Albuquerque, NM; Georgia Center for Cancer Statistics, Rollins School of Public Health, Emory University, Atlanta, GA; and Applied Research Program, National Cancer Institute, Bethesda, MD.

Address reprint requests to Ann S. Hamilton, PhD, Keck School of Medicine of the University of Southern California, Department of Preventive Medicine, 1441 Eastlake Ave, Room 3427, MC 9175, Los Angeles, CA 90089-9175; email: ahamilt{at}hsc.usc.edu

	ABSTRACT

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PURPOSE: Studies reporting effects of radiotherapy for prostate cancer on sexual, bowel, and urinary function have been conducted primarily in referral centers or academic institutions. Effects of external-beam radiotherapy for prostate cancer among a population-based cohort were assessed.

PATIENTS AND METHODS: The study population included 497 white, Hispanic, and African-American men with localized prostate cancer from six US cancer registries who were diagnosed between October 1, 1994, and October 31, 1995, and treated initially with external-beam radiotherapy. They were interviewed at regular intervals, and medical records were reviewed. Distributions of responses for bowel-, urinary-, and sexual-related functions at 6, 12, and 24 months after diagnosis and adjusted mean composite change scores for each domain were analyzed.

RESULTS: Declines of 28.9% in the sexual function score and 5.4% in the bowel function score occurred by 24 months, whereas at this time, the urinary function score was relatively unchanged. A total of 43% of those who were potent before diagnosis became impotent after 24 months. More than two thirds of the men were satisfied with their treatment and would make the same decision again.

CONCLUSION: Sexual function was the most adversely affected quality-of-life domain, with problems continuing to increase between 12 and 24 months. Bowel function problems increased at 6 months, with partial resolution observed by 24 months. Despite the side effects, satisfaction with therapy was high. These results are representative of men in community practice settings and may be of assistance to men and to clinicians when making treatment decisions.

	INTRODUCTION

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PROSTATE CANCER is the foremost nonskin cancer facing men today, with an estimated 180,400 cases expected to be diagnosed in the US in 2000.¹ Treatment options for prostate cancer can depend on a man’s age and life expectancy, stage and grade of disease at diagnosis, and health status. Men with clinically localized disease and 10 or more years of life expectancy² can be offered therapy intended to eliminate the cancer, including radical prostatectomy or radiation therapy. Radiation therapy is often recommended for older patients and those who are poorer surgical candidates, but who are young enough that cure is important for achieving full life expectancy.³ Although elimination of the prostate cancer is usually the paramount consideration, potential long-term complications of treatment may also be important factors in selecting therapy.⁴

Earlier studies have reported adverse effects of radiation therapy on sexual, bowel, and urinary function.^3,5-13 However, most of these studies were small, cross-sectional, and conducted in referral centers or academic institutions. In comparison, this study examines long-term complications of external-beam radiation therapy for prostate cancer among a population-based cohort where treatment outcomes are more representative of the experience of most men with this disease.

The data are from the Prostate Cancer Outcomes Study (PCOS), a population-based study that included a random sample of men with clinically localized prostate cancer from six population-based cancer registries in the United States.¹⁴ With nearly 500 men treated with external-beam radiotherapy included, it is one of the largest such studies conducted to date. The study was designed to obtain information prospectively on changes in general and disease-specific health outcomes after diagnosis and initial treatment. We examined changes in urinary, bowel, and sexual function as well as general domains of health-related quality of life in the 2-year period after diagnosis. This report follows a previous description of health-related quality of life after radical prostatectomy among men from the same cohort.¹⁵

	PATIENTS AND METHODS

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The methods used have been previously described.¹⁴ Briefly, the study subjects were randomly selected from men diagnosed with primary prostate cancer between October 1, 1994, and October 31, 1995, who resided in areas covered by six population-based SEER (Surveillance, Epidemiology, and End Results) cancer registries. The areas of residence included the states of Connecticut, New Mexico, and Utah, the Atlanta, GA, metropolitan area, Los Angeles County, CA, and King County, WA (which includes the city of Seattle). African-American, white, and Hispanic men who were younger than 90 years at the time of diagnosis were eligible in five of the registries, and those between 60 and 89 years of age were eligible in King County. The study was approved by the institutional review board of each participating institution. Participants in the study completed a self-administered, mailed questionnaire at approximately 6, 12, and 24 months after diagnosis and had their medical records reviewed.

We identified a total of 11,137 men in these registry areas who met the diagnostic, residency, race and ethnicity, and age eligibility criteria. From this group, 5,672 men were randomly selected according to specified probability levels in age group, race and ethnicity, and study center strata. Letters requesting participation were sent to 4,736 (83.5%) of these selected men. Reasons for lack of contact included physician refusal (n = 380), inability to locate the patient (n = 413), and illness or mental incompetence of the patient (n = 143). A total of 3,533 (62.3%) men completed a 6-month survey, a 12-month survey, or both. Reasons for nonresponse included patient refusal (n = 1,087) and other reasons (n = 116), including foreign language other than Spanish. The questionnaires were translated into Spanish and interviews were conducted in Spanish when necessary. Medical record abstracts were completed for 3,486 (98.7%) of the sampled participating patients.

For this analysis, we selected all PCOS patients (n = 497) with clinically localized disease who underwent external-beam radiotherapy as primary treatment within 6 months of diagnosis and who did not receive hormonal therapy (either before or after radiation therapy) or radical prostatectomy. Men who received additional therapy were excluded because our goal was to describe the effects of external-beam radiotherapy alone on later quality of life.

Data Collection
Selected patients whose doctors gave us approval to contact were mailed the self-administered questionnaire approximately 6 months after diagnosis and were asked to return it, along with signed release forms to obtain medical records. If no response was received, telephone follow-up efforts were conducted, and on occasion, a personal interview was conducted. In total, 90% of the surveys were completed by mail and 10% by telephone or personal interview. The 12-month survey was sent to men who were originally sampled and who had completed the 6-month survey; it was also sent to men who did not respond to the 6-month questionnaire who did not actively refuse. The 24-month survey was sent to men who had completed one or both of the 6- and 12-month surveys. Of the 497 men receiving external-beam radiotherapy as their primary treatment within 6 months of diagnosis, 457 (92.0%) completed a survey at 6 months after diagnosis, 447 (89.9%) completed a survey at 12 months, and 421 (84.7%) completed a survey at 24 months. A total of 377 (75.9%) completed all three surveys. Among the men who did not respond to surveys after the 6-month survey, 13% did not complete the remaining surveys because they died.

The survey instruments at each time point included identical questions on urinary, sexual, and bowel function domains that were adapted from previously developed instruments with demonstrated reliability and validity.^16-18 For each domain, we asked four to five questions relating to level of function and a single question relating to how much the level of dysfunction was perceived as a problem to the respondent. To obtain general health information relevant to quality of life, selected scales from the Medical Outcomes Study 36-item short form health survey (known as SF-36) were used.¹⁹ At each survey time, the men were asked to respond to these questions for the month before the survey was administered. At 6 months, the men were also asked to recall baseline levels, which referred to the time just before their cancer was diagnosed. Other survey questions pertained to comorbidities (ie, other health conditions occurring at the same time as the prostate cancer), symptoms of prostate cancer, and satisfaction with care.

Dates of radiotherapy were obtained from the patients’ doctors’ offices and from outpatient clinic and hospital records. Information on stage of disease and Gleason scores were also taken from these records. The interval between the end of radiotherapy treatment and completion of the survey may impact the results relating to quality of life. The mean intervals between completion of radiotherapy and the date of the questionnaire responses were 2.8 months; 8.6 months, and 20.8 months for the 6-month, 12-month, and 24-month surveys, respectively.

Statistical Analysis
The effects of external-beam radiotherapy on bowel, urinary, and sexual functioning and other outcomes were assessed by two methods. First, univariate weighted distributions of responses to individual questions in each domain were cross-sectionally tabulated at each time point. For ease of presentation, the responses in these tables were usually grouped into three categories per question, combining categories to reflect clinically meaningful distinctions. To statistically compare changes between time points, the levels of responses were assigned a score based on an ordinal scale (ie, from 1 to 3) and the significance of the mean changes in the scores was assessed by paired t test.

Second, a composite score ranging from 0 to 100 was calculated at each time period for each respondent based on the average transformed score across the four or five individual items in each domain. Each item was transformed to a standard 0 to-100 scale because of the varying number of response categories across items.¹¹ For this summary score, all categories of response to each question were used. A man who was not limited in any of the functions included for each domain would receive a score of 100. For a composite score based on five questions (with four levels each), a decline of one level for any question would result in a 5% decline (1/20). An overall adjusted baseline mean score was calculated by a multivariate least-squares linear regression model that included age at diagnosis, race and ethnicity, clinical stage, education, income, marital status, and comorbidity index. An adjusted least-square mean change score between the baseline level and each survey time point was calculated and was adjusted for the above-mentioned variables as well as the baseline score and the time interval between the last day of therapy and completion of the survey. The paired t test was used to determine the statistical significance of the change scores. A comparison of baseline and change scores at 6 months was made between those who responded to all three surveys versus those who did not to assess possible drop-out bias that may be due to functional status.

Because the sample for the study was selected according to different probabilities by stratum defined by race and ethnicity, age group, and cancer registry, the data were weighted by the Horvitz-Thompson weight (the inverse of the sampling fraction for each sampling stratum) to provide results that could be generalized to the total eligible population in the six regions. The Survey Data Analysis (SUDAAN)²⁰ statistical software program was used for all weighted analyses because it was designed to produce unbiased variance estimates for data from complex surveys. All tables include the weighted values.

	RESULTS

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More than 60% of the patients treated with external-beam therapy were diagnosed when they were between 65 and 74 years of age; 82% were non-Hispanic white ( Table 1). Approximately 22% had not graduated from high school, and a comparable percentage had a household income of less than $20,000. Most were retired (70%). Although all these men were selected because they had localized disease, approximately 29% had T1 disease, and the remainder were T2 or T1/2. Most of the patients had Gleason scores between 5 and 7. The most common self-reported health conditions were hypertension, arthritis, and diabetes. A comorbidity index was created on the basis of the number of conditions reported (out of 12), and an average of 1.3 other conditions was reported per person. The only significant demographic or clinical difference between those who completed all three surveys and those who did not is that the partial nonresponders were more likely to be Hispanic or African-American.

Urinary Function
Urinary function was minimally disrupted by external-beam radiotherapy ( Table 3). Before therapy, 68% of men had total urinary control, as compared with 65% at 24 months after diagnosis. We saw a similar small decline in the proportion of men experiencing no urinary incontinence, and we saw no change in the proportion of men who used pads. We also saw significant improvement shown in the symptom of urinary frequency (ie, having to urinate less than 2 hours after finishing urination) before diagnosis and at 24 months after diagnosis. Overall, we saw no change in the responses to the question concerning how big a problem incontinence was before and after external-beam therapy. The adjusted urinary function summary score was virtually unchanged between baseline and 24 months after diagnosis. Among those who responded initially but then dropped out, the baseline summary score was slightly lower (81.0), and by 6 months, they had experienced an average decline of 5.2 points, suggesting that their experience may have been slightly worse than those who responded throughout the study period (whose score increased by 0.5 points at 6 months).

The amount and percentage of decline by 24 months was higher among those who were potent before treatment (-24.6 points, -31.9%) than among those who were impotent initially (-4.8 points, -17.5%). Among men who were potent before therapy (57% of the total), 43% were not able to achieve erections firm enough for sexual intercourse at 24 months after diagnosis, and the proportion of them feeling that sexual function was a moderate to big problem increased from 15% to 40% (data not shown; P < .0001). In contrast, little change was seen in men who were impotent before therapy. Approximately 43% of them felt that sexual function was a moderate to big problem before therapy versus 42% at 24 months.

Among men younger than 65 years and those between 65 and 74 years of age, the percentage who felt that sexual function was a moderate to big problem doubled, even though the proportion of men able to achieve an erection firm enough for intercourse declined only slightly among men in the younger age group ( Table 5). The men aged 75 years and older had significant sexual function problems before diagnosis (45% did not engage in sexual activity), and the impact of therapy on the perception of problems related to sexual function was much less pronounced.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

Both larger and smaller declines in loss of potency have been reported compared with our results, which indicated that 43% of previously potent men were unable to have firm erections after 24 months of follow-up. Nearly 60% of those who were potent before therapy were unable to have intercourse at 24 months after therapy, according to two studies,^21,22 compared with a reported 35% loss of potency in another.²³ Better results have been reported among those receiving conformal beam therapy (which we were unable to distinguish), with potency lost in just 29%²⁴ and 13%,²⁵ although the results from the latter study were based on a median time of 13 months after diagnosis. We and others²¹ have found that sexual function continued to decline after 12 months.

As found in other studies,^26,27 urinary function was the least affected by external-beam therapy after 24 months of follow-up, and some improvement was shown in function (especially in reduction in the frequency of the need to urinate) after therapy. Another study reporting improvement in urinary function attributed the change to a reduction in bladder neck obstruction.²⁸ These questions did not measure hematuria and other immediate acute effects that may occur during the administration of the radiotherapy.

The largest effects on bowel function were seen immediately after external-beam therapy, and despite some recovery, long-term declines in bowel-related outcomes were seen. Other estimates of the prevalence of bowel morbidity after external-beam radiotherapy have included 19% reporting moderate and 2% with major morbidity,²⁷ 14% requiring intervention for bowel problems,²² and 11% with self-reported major alterations in bowel function.²³ In a study that compared conventional to conformal radiotherapy,²⁹ those receiving conventional therapy had more moderate or major changes in bowel function than those receiving conformal therapy (34% v 10%; P < .04). In our study, the proportion reporting at least some bowel problems increased from 31% at baseline to 41% at 24 months.

We found steady and significant improvements over time in the impact of prostate cancer and its treatment on quality of daily life, as measured by reduction in physical discomfort, in worry about health, and in limitation of activities. At 24 months, approximately two thirds of the men were delighted or pleased with their treatment. Other studies have found that men had generally positive feelings about their treatment.⁶

The major advantage of the PCOS is that it has prospectively observed patients randomly selected from population-based registries in six areas of the country and thus is highly representative of results in community practice settings. Measurements of outcomes have been made at specified times after diagnosis by validated questionnaire instruments supplemented by information abstracted from the medical record. The sample size is large and includes a diverse group of men from three major race and ethnicity groups (non-Hispanic white, white-Hispanic, and African-American) and from all socioeconomic status levels.

Limitations of this study include the possible bias due to potential differences in respondents versus nonrespondents at the different phases of the study. Among men not responding to any of the surveys versus those who participated in at least one, we had lower response rates among older men, Hispanics, and African-Americans. Those who responded to the 6-month survey but did not respond at 24 months were also more likely to be older, Hispanic, and African-American, and more likely to be of unknown or lower income than those responding to all of the surveys (n = 377). Some indication existed that the later nonrespondents may have had poorer function at baseline and slightly larger declines in function at 6 months after diagnosis than those who continued with the study. Because reasons for dropping out of the study included death, it is likely that some of those who did not continue had poorer functional status and prognosis from the outset. Thus, these results should be viewed as underestimating to some extent the functional losses due to therapy.

Other potential limitations include the possibility of some misclassification of baseline information because it was recalled at 6 months after diagnosis. Some other studies have shown that men may overestimate their sexual function before therapy.³⁰ The effect of this type of overestimation would be to artificially increase the amount of decline between baseline and the time points after diagnosis. A validity study was conducted that compared the baseline information obtained at 6 months with that obtained right after diagnosis for a subset of men.³¹ Although some overestimation of sexual function at baseline was shown for sexual frequency and interest, it was not sufficient to account for the extent of decline demonstrated in the study and would not affect the decline seen between 12 and 24 months. In general, the information on baseline urinary and bowel that was recalled at 6 months was found to be comparable to the information recalled at the time of diagnosis. Finally, because we were not able to obtain information on the specific type of external-beam therapy received, the use of conformal therapy could not be analyzed separately.

Along with previously published PCOS results on health outcomes after other therapies,^15,32 our findings should assist men and their physicians in making treatment decisions regarding prostate cancer. Because follow-up of this cohort is ongoing, information on the longer-term effects of radiotherapy will be available. Other studies have found that the adverse effects of radiotherapy have continued to impact patient quality of life up to 5 years after treatment.³³

	ACKNOWLEDGMENTS

 
Supported by the National Cancer Institute, National Institutes of Health, Bethesda, MD (contract nos. NO1-PC-67007, NO1-PC-67009, NO1-PC-67010, NO1-PC-67006, NO1-PC-67005, and NO1-PC-67000).

We thank the men who, by their participation in the PCOS, have contributed to a better understanding of the effects of prostate cancer on men’s lives. We also thank the physicians who assisted in the collection of data from their patients and from medical records. We thank Jennifer Stevens, Information Management Services Inc, Silver Spring, MD, who serves as the data coordinator for the PCOS for her work in data management. We also thank the people in each region who locally managed data collection: Terri Watson and Mary Baker, Seattle; Noell Stone, Dan Welsh, Anna Marie Davidson, New Mexico; Eric Acosta, Yvonne Paredes, Linda Schmidt, and Richard Soto, Los Angeles; Judith Fine, Susan Walters, Nancy Dittes, Denise Denning, Connecticut; Judy Andrews, Betsy Bridgman, Atlanta; Rosemary Dibble, Belinda Taylor, Utah.

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Submitted September 26, 2000; accepted February 7, 2001.

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