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Quality of Life and Sexual Functioning in Cervical Cancer Survivors

From the Departments of Gynecologic Oncology, Behavioral Science, Biostatistics and Applied Mathematics, Radiation Oncology, and Clinical Cancer Prevention, The University of Texas M.D. Anderson Cancer Center, Houston, TX.

Address reprint requests to Michael Frumovitz, MD, MPII, Department of Gynecologic Oncology, 1155 Herman Pressler, CPB6.3244, Unit 1362, Houston, TX 77030; e-mail: mfrumovitz{at}mdanderson.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: To compare quality of life and sexual functioning in cervical cancer survivors treated with either radical hysterectomy and lymph node dissection or radiotherapy.

METHODS: Women were interviewed at least 5 years after initial treatment for cervical cancer. Eligible women had squamous cell tumors smaller than 6 cm at diagnosis, were currently disease-free, and had either undergone surgery or radiotherapy, but not both. The two treatment groups were then compared using univariate analysis and multivariate linear regression with a control group of age- and race-matched women with no history of cancer.

RESULTS: One hundred fourteen patients (37 surgery, 37 radiotherapy, 40 controls) were included for analysis. When compared with surgery patients and controls using univariate analysis, radiation patients had significantly poorer scores on standardized questionnaires measuring health-related quality of life (physical and mental health), psychosocial distress and sexual functioning. The disparity in sexual function remained significant in a multivariate analysis. Univariate and multivariate analyses did not show significant differences between radical hysterectomy patients and controls on any of the outcome measures.

CONCLUSION: Cervical cancer survivors treated with radiotherapy had worse sexual functioning than did those treated with radical hysterectomy and lymph node dissection. In contrast, these data suggest that cervical cancer survivors treated with surgery alone can expect overall quality of life and sexual function not unlike that of peers without a history of cancer.

	INTRODUCTION

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Papanicolaou smear screening has led to a decrease in the incidence of cervical cancer with 10,370 new cases diagnosed and 3,710 attributable deaths in 2005 in the United States.¹ Additionally, over half of women are diagnosed with stage I disease when the tumor is clinically limited to the cervix.² Primary treatment with surgery or irradiation alone cures 85% to 90% of patients with stage I cervical cancer.^3-6 Despite similar effectiveness, however, each treatment modality involves distinct clinical acute and late complications.

The surgical approach to early-stage cervical cancer consists of radical hysterectomy and bilateral lymph node dissection, with or without accompanying oophorectomy or ovarian transposition. Blood loss remains the most significant intraoperative complication with transfusion rates reaching as high as 80%.^7,8 Postoperatively, patients may experience febrile morbidity, deep vein thrombosis, pulmonary embolism, wound dehiscence, postoperative bladder dysfunction, and fistula formation. In addition, a small but real risk of operative mortality exists with the surgery. Long-term complications can include bladder hypotonia requiring chronic self-catheterization, ureteral strictures, and chronic leg lymphedema.^9,10

Radiotherapy, typically consisting of external beam radiation followed by intracavitary radiation, has its own spectrum of complications. Potential complications from intracavitary radiation include uterine perforation and febrile morbidity. Although deep vein thrombosis, pulmonary embolism, and even death are potential risks with intracavitary radiotherapy, they are exceedingly rare.¹¹ Patients who receive radiation may also experience early small bowel complications (obstruction); early or late large bowel complications (bleeding, stricture, fistulae, perforation); late urinary complications (hematuria, ureteral stenosis, vesicovaginal fistula); and vaginal atrophy, shortening, or agglutination.¹² The latter can make sexual intercourse difficult or even impossible. Although radical hysterectomy and radiotherapy are associated with comparable rates of complications, the quality, chronicity, and severity of these complications are difficult to compare.^13,14

Whether the patient undergoes primary surgery or radiotherapy depends on a variety of factors, including tumor characteristics, comorbid medical conditions, and patient and provider preference. Patients who are likely to require adjuvant radiotherapy following radical hysterectomy often undergo primary radiotherapy in an effort to minimize the morbidity and mortality associated with combined treatment modalities. Factors that might dispose physicians to recommend primary radiotherapy include large tumor volume, lymphatic involvement, aggressive tumor histology, and depth of invasion.¹⁴ In reality, however, many women with stage IB1 tumors are equally good candidates for either surgical management or radiotherapy. In these situations, the clinical decision is often based on patient or provider preference.

The objective of this study was to perform a comparison of the quality of life (QOL) of women with early-stage cervical cancer that could be treated equally effectively with either surgery or radiotherapy. Standardized questionnaires were used to measure outcomes, and a group of healthy age- and race-matched women with no personal history of cancer was included in the comparison to determine if any differences in QOL exist between women with cervical cancer and women without a history of cancer. The ultimate aim of the study was to provide patients and providers with additional empirical information to help guide their treatment choice.

	METHODS

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Study Population
The protocol was approved by the institutional review board at The University of Texas M.D. Anderson Cancer Center. Women with cervical cancer treated at M.D. Anderson from 1991 to 1998 were identified through an institutional patient database. Patients whose primary language was English or Spanish were eligible if they were younger than 55 years at the time of treatment; had undergone treatment at least 5 years previously; had squamous cell, adenocarcinoma, or adenosquamous histologies; and had lesions smaller than 6 cm in diameter confined to the cervix (stage I). Although International Federation of Gynecology and Obstetrics (FIGO) subdivides stage I disease into stages Ia1, Ia2, Ib1, and Ib2, tumors 6 cm confined to the cervix was chosen for inclusion, as these lesions are thought to, clinically, behave similarly. Patients were excluded if they received a combination of surgical and radiation therapies, had concurrent chemoradiotherapy therapy, developed recurrent disease, or were treated for other malignancies (except for adequately treated basal cell or squamous cell skin cancer). Radiation patients received a mean dose of 85.7 Gy to point A.

Age- and race-matched controls were recruited from the M.D. Anderson Cancer Center Cancer Prevention Clinic. Exclusion criteria were previous cancer diagnosis other than adequately treated basal cell or squamous cell skin cancers and previous hysterectomy.

Instruments
Health-related QOL was measured using the Short Form-12 (SF-12).¹⁵ This 12-item version of the widely used SF-36 questionnaire provides mental health (MCS) and physical health (PCS) component summary scores that measure self-perceived health-related QOL.

Emotional distress was assessed using the Brief Symptom Index-18 (BSI-18).¹⁶ The BSI-18 yields three primary dimension scores—somatization, depression, and anxiety—as well as a Global Severity Index (GSI), which summarizes the overall level of psychological distress.

Severity of menopausal symptoms was calculated with the Menopausal Survey.¹⁷ The survey has seven questions that target common physical and psychological symptoms of menopause.

Two instruments were used to examine how treatment affected social relationships. The Abbreviated Dyadic Adjustment Scale (A-DAS), a seven-question survey, was administered to women who were married or who had been in a serious relationship for at least 6 months.¹⁸ Participants who were single and not in a serious relationship were asked the five-item dating subscale of the Cancer Rehabilitation Evaluation System (CARES), which measures comfort in dating.¹⁹ This subscale of the larger CARES instrument has not been validated as a stand-alone survey.

Finally, the Female Sexual Function Index (FSFI), a 19-item multiple-choice questionnaire, was administered. This survey measures five domains, including sexual desire, arousal (both subjective and physiologic), lubrication, orgasm, satisfaction, and pain.²⁰

For the SF-12 and FSFI surveys, multiple-choice items have response formats that range, for example, from "never" to "always," or "very low" to "very high." The other four instruments employ Likert-type numbered scales. Higher scores correlate with better functioning on the SF-12, FSFI, A-DAS, and CARES instruments while lower scores reflect better functioning on the BSI-18 and menopausal survey.

Demographic data, including age, race, level of education, and medical comorbidities, were collected for all participants. Radiation patients were assumed to be menopausal by virtue of their treatment. Menopausal status of surgical patients was assessed by review of ovarian procedures performed at time of radical hysterectomy. Controls were asked their perceived menopausal status. Clinical stage, histology, tumor grade, depth of invasion, and other pertinent characteristics were abstracted from patient charts.

Administration
Letters of introduction were mailed to eligible patients and controls describing the nature of the study and asking for the woman's participation. The letter also stated that a project interviewer would telephone eligible women and specified that $15 would be given to all participants.

The same female bilingual (English and Spanish) interviewer administered all the surveys. The interviewer was blinded to each patient's treatment history. Once women verbally agreed to participate, they were read an informed consent statement that met criteria defined by the Health Insurance Portability and Accountability Act (HIPAA), as well as by our institution. The survey took an average of 32 minutes to administer (range, 15 to 60 minutes).

Statistical Analysis
The study was powered to detect a 15% relative difference on the SF-12 between the two treatment groups and the control group. The Bonferroni adjustment was used to control for multiple comparisons, and an level of .017 was considered significant. To achieve 80% power, we calculated that a sample size of 38 women per group was necessary.

For comparisons between the treatment groups, t tests for independent samples, Mann-Whitney U tests, and ² tests were utilized. For univariate comparison of outcome measures between the treatment groups with the control group, one-way ANOVA and ² analyses were conducted. Univariate analyses were adjusted for multiple comparisons using Tukey's HSD (honestly significant difference) Test. Multivariate linear regression models were then constructed. For the SF-12 PCS, SF-12 MCS, BSI-18 GSI, and FSFI overall scores, univariate analyses were performed for the following independent variables: age, marital status, religion, education, body mass index, current smoking status, number of cigarette packs smoked per year, medical comorbidities, menopausal symptom scores, and study group (radiation, surgery, and control). Backward elimination (P < .10 on univariate analysis to be considered in model) was used to identify which independent variables were associated with SF-12 PCS, SF-12 MCS, BSI-18 GSI, and FSFI overall scores when comparing the three arms. A similar analysis with the addition of stage, histology and tumor grade was also modeled to compare the radical hysterectomy and irradiated patients. All data were analyzed using SPSS 11.5 for Windows (SPSS Inc, Chicago, IL).

	RESULTS

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One hundred forty-five patients (90 treated with radical hysterectomy and 55 treated with radiotherapy) who met the inclusion criteria were identified. Sixty-seven were eliminated because they could not be contacted (n = 61) or declined participation (n = 6). The remaining 78 were interviewed for an overall response rate of 54%. Four were excluded after data collection for the following reasons: two patients underwent both radiation and hysterectomy, one patient exceeded the age limit, and one patient was found to have two separate primary cancers at time of surgery. The remaining 74 patients were evenly distributed among the two treatment modalities (n = 37 per group). Ninety-two age- and race-matched women from our Cancer Prevention Clinic were identified for participation. Of these, 23 could not be reached due to incorrect or unattainable contact information, 19 declined participation, and 10 were excluded because of prior hysterectomy. The final control group consisted of 40 women who were interviewed for a response rate of 43%.

Demographic and Medical Characteristics
Demographic and clinical characteristics of patients and controls are presented in Table 1. No significant differences existed among the three groups with regard to current age, body mass index, race, history of tobacco use, hypertension/coronary artery disease, diabetes, hypothyroidism, asthma/chronic obstructive pulmonary disease, or other comorbidities (hepatitis [n = 1], migraines [n = 2], and fibromyalgia [n = 1]). Although no differences existed among the three groups in terms of ever having smoked, a significant difference did exist in the amount of tobacco used, as defined by the packs per year with radiation patients reporting significantly greater tobacco use (P = .03) irradiated patients also reported less education than surgically treated patients and controls (P < .001). Women in the control group had more clinical diagnoses of depression than women in the treatment groups (P = .02).

Menopausal Symptoms
Radiation patients reported a significantly higher frequency of symptoms such as hot flashes, vaginal dryness, and urinary complaints than did surgery patients and controls. Overall menopausal symptoms were significantly more bothersome for women who had received radiotherapy. No difference in menopausal symptoms existed in the subscales or overall scores between surgery patients and controls.

Eleven (30%) of 37 surgical patients also underwent concurrent bilateral salpingoophorectomy. When this group of patients made surgically menopausal was compared with irradiated women, radiotherapy patients described significantly more menopausal symptoms.

Sexual Function and Relationship Satisfaction
Scores on the FSFI did not reveal any difference in sexual desire as reported by the three groups. However, irradiated women had more difficulty becoming sexually aroused, attaining vaginal lubrication, reaching orgasm, and achieving sexual satisfaction. Also, irradiated women reported significantly more pain with intercourse than did radical hysterectomy or control group women. The total scores of irradiated patients revealed significantly worse overall sexual functioning than did the scores of surgery patients or controls. No statistical difference existed between the surgery patients or controls in any of the sexual functioning subscales or the overall score. No statistically significant difference existed in satisfaction with dating or committed relationships among the three groups on the A-DAS or CARES surveys.

Multivariate Analyses of Outcome Variables
Multivariate analyses were performed to assess the independent association of variables with four of the outcome measures, the SF-12 PCS, the SF-12 MCS, the BSI-18 GSI, and overall sexual functioning on the FSFI (Table 5). Irradiated patients showed significantly worse sexual functioning as measured by the FSFI. Their self-perceived physical well-being was also worse than that of the others (P = .07). Interestingly, menopausal symptoms had a significant negative association with all four outcome measures. Women who smoked reported poorer mental health and more emotional distress. Conversely, being married was related to better physical health and sexual functioning.

	DISCUSSION

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Traditionally, oncologists have focused their efforts on maximizing the overall survival of their patients. Although many oncologists acknowledge that QOL after cancer therapy is an important aspect of patient care, it is often not the main consideration when recommending cancer treatment. However, when competing treatment options result in equivalent clinical outcomes, QOL considerations become particularly important.

To our knowledge, this is the first study to measure not just sexual functioning, but also emotional adjustment, relationship satisfaction, and menopause symptoms after surgery or radiation treatment alone in patients with cervical cancer, as well as in a group of women without a cancer diagnoses. The consistently increased morbidity across all measures in irradiated women is striking, and persists for sexual functioning even after controlling for potentially confounding factors such as educational level and tumor stage.

Although the desire for sexual intimacy was equal among all groups, irradiated patients had significantly more sexual dysfunction than women in the other two groups. These findings agree with the previous prospective studies comparing women treated with surgery alone or radiation therapy alone.^21-23 Jensen et al²² found women treated with radiation therapy had more severe sexual dysfunction at 2-year follow-up, with 85% of women reporting no interest in sex, 55% having dyspareunia, and 50% having vaginal shortening. These problems were significant compared with the women's own premorbid sexual function and when compared with age-matched controls.

The timing of follow-up is very important in these patients since sexual and other morbidities improve during the first year after radical hysterectomy,²³ whereas the chronic fibrotic changes in pelvic tissue after radiotherapy create persistent, or even worsening vaginal atrophy at least up to 2 years post-treatment.^21,23 It is not surprising then to find continued adverse sexual functioning in these women who were irradiated 5 or more years ago. For these reasons, we strongly recommend either the use of a vaginal dilator or the engagement in sexual intercourse frequently after completion of radiotherapy for cervical cancer in an effort to maintain the length, width, and elasticity of the vaginal canal. Future research might follow these patients longitudinally with pretreatment baseline sexual functioning data.

Patients who had undergone radical hysterectomy did not differ in sexual functioning from age- and race-matched peers. This finding is in accord with a previous study that of early-stage cervical cancer patients treated with radical surgery.²⁴ In their second study, Jensen et al²³ also found no significant difference in overall sexual function between women posthysterectomy and healthy controls. In contrast to our results, women in the radical hysterectomy group were almost three times more likely than controls to have difficulty with vaginal lubrication. However, nearly one third of these patients had undergone concurrent bilateral salpingo-oophorectomy, and no attempt was made to control for menopausal status between treatment and control arms.

Bergmark et al²⁵ have published the largest series on sexual functioning in cervical cancer survivors. In their study, they surveyed 256 Swedish cervical cancer survivors (4 to 6 years after treatment) and compared them to controls matched for age and geographic region. Their cancer arm was women with local (stage IB) or locoregional (stage IIA) disease who had been treated with a variety of modalities including radical hysterectomy alone, radiation alone, and combination radiotherapy and surgery. When comparing the entire cancer cohort to controls, they found no difference in sexual desire or orgasm between the groups but found an increase age-adjusted risk ratio for the cancer patients in regards to vaginal lubrication, genital swelling/arousal, perceived vaginal length and elasticity, dyspareunia, and coital bleeding. When they performed a subanalysis grouped by treatment, they found no difference in lubrication, genital swelling/arousal, vaginal elasticity or length, or libido when comparing surgery patients with irradiated patients to patients who had received multiple modality therapy. They did, however, find that the surgery only patients reported statistically significant differences in vaginal lubrication, vaginal length, and vaginal elasticity when compared with controls.

These findings contrast with the current study, which showed significant differences on all subscales of the FSFI (except arousal) for irradiated patients and no differences between surgery only patients and controls. There are multiple possibilities for these discrepancies. First, Bergmark et al utilized a survey created by them and not one that had been subjected to tests of reliability and validity. Next, they did not report or account for any ovarian procedures performed during radical hysterectomy. Many of those women were made menopausal with either surgery or radiation with little or no accounting. In addition, their patient population, which included women as old as 80 years and patients who had multiple modality treatment differs greatly from ours. Finally, although they reported hormonal status for both patients and controls, they made no attempt to control for it, or any other factor, in a regression analysis, which likely introduced multiple confounders into the study.

The regression model we used performed the backwards elimination in two steps. First, all of the demographic, medical comorbidity, tumor, and treatment variables were added; the menopausal symptom score was then inserted into the model. Irradiated patients had statistically significant worse sexual functioning, physical health, and emotional distress after the first step, before the addition of the menopause symptom score. After accounting for the menopause score, only sexual functioning remained significantly worse for those women who been irradiated. We believe that the irradiated patients probably had worse physical health and possibly more psychologic distress, but the menopausal symptom overall scores masked the treatment effect in the statistical analysis because of the high one-to-one correlation between adverse menopausal symptoms and the radiotherapy patients. Therefore, the menopausal symptom score likely overshadowed the other relationships observed before its addition into the multivariate model. When we compared patients rendered menopausal by surgical oophorectomy with those made climacteric by radiotherapy, menopausal symptom scores were significantly worse for the irradiated women. This was probably due to the fact that many of the symptoms surveyed by the instrument can be attributed to either menopause or radiotherapy. This may explain why the two groups with loss of ovarian function had similar rates of hot flashes (symptoms unique to menopause) but differed significantly in their assessment of vaginal dryness and urinary symptoms (likely a result of radiotherapy). In addition to causing ovarian failure, radiotherapy directly affects the vaginal mucosa by decreasing blood flow to the vaginal walls and causing pelvic fibrosis. For these reasons, even topical estrogen cream is less well absorbed and less effective in reversing menopausal changes in the vagina after radiotherapy.²⁶

Severity of menopausal symptom scores correlated with poor QOL on all four modeled measures. Not surprisingly, patients who reported increased menopausal symptoms also had poor sexual functioning. Abrupt and premature menopause resulting from cancer treatment has also been observed to account for most of the sexual dysfunction women experience after breast cancer.²⁷ In published studies, effects of menopause on physical and emotional QOL have not been clearly established.^28-30 The association seen in our study may be due to the sudden and severe nature of menopause onset resulting from pelvic irradiation.

We did not specifically ask participants whether or not they were taking hormone replacement at the time of the survey. Our study was conducted in the wake of the publication of the Women's Health Initiative data and the ensuing publicity created in both the medical and lay media. Many of the women who reported menopausal symptoms may have recently discontinued their hormone replacement therapy and therefore may have been experiencing more climacteric dysfunction. Since more irradiated patients were rendered menopausal than surgery patients, the timing of the survey may have falsely elevated their menopausal symptom scores skewing some of the results.

Other interesting variables affected QOL in our study population. For example, smoking was shown to have a negative correlation with mental and emotional well-being. Other investigators have also found higher rates of depression³¹ and suicide³² among smokers. It is possible, however, that women who are aware of the role of smoking in cervical cancer, but who continue to smoke after their treatment, may have a particularly negative perception of their health status.

Although these data support anecdotal experience associated with the two treatment modalities, we are not suggesting that all patients with cervical cancer who are surgical candidates should be treated with radical hysterectomy. Careful patient selection must be made in an effort to avoid the need for adjuvant radiotherapy after radical surgery. Even some patients with clinical stage IB1 cancers will need postoperative radiotherapy,³³ and this risk increases with tumor size and clinical stage.³⁴ Complication rates for patients requiring both treatment modalities are higher than for those having had either treatment alone.^33,35

While the few baseline differences that existed between the treatment groups and the controls were accounted for in the multivariate models, other factors biasing the results cannot be excluded. For example, although all tumors were limited to the cervix and smaller than 6 cm in diameter, surgical patients all had earlier stage tumors than did those treated with radiation. However, we believe that these lesions behave in a similar manner clinically and therefore this difference in substage (all patients had stage I [localized] disease) should not affect these outcome measures. Furthermore, a statistically significant difference in tumor histologies existed between the two treatment arms. The radical hysterectomy group had larger numbers of adenocarcinoma and adenosquamous carcinoma. Grade for grade, these histologies tend to be more aggressive than squamous lesions. Patients who were not cured of these more malignant lesions by primary treatment would likely have been excluded from this study because of persistent or recurrent disease or additional surgical or radiotherapies after initial treatment.

The radiation group was treated without concurrent chemotherapy, which is now the standard of care. Patients in this study were diagnosed at least 5 years ago when chemoradiotherapy was administered only on experimental protocols. However, it is unlikely that concurrent chemotherapy would improve the ultimate QOL in patients undergoing radiotherapy for cervical cancer, given reports of increased acute complications and lack of reduction in delayed complications.³⁶

As with all studies based on surveys, response bias may affect results. Selection bias occurs if patients and control group participants who take part in the study have a better quality of life than those who are unreachable or refuse to participate. Also, not all patients interviewed have been followed at M.D. Anderson since the completion of their treatment. The low socioeconomic status of this population as well as the long interval from treatment to contact for this study made locating and recruiting these patients difficult. A standard recruitment goal in retrospective survey studies is a response rate of at least 60%.³⁷ For both treatment groups surveyed, the response rate was 54%, so the results may not be generalizable to the general population of cervical cancer survivors. Finally, since data were collected retrospectively, we do not know if a quality of life difference may have existed in the treatment groups before therapy.

Our data suggest that cervical cancer survivors treated primarily with radical hysterectomy and lymph node dissection have less sexual dysfunction than patients treated with radiotherapy. In addition, patients treated surgically seemingly have no difference in QOL, psychosocial stress, or sexual functioning than age- and race-matched control group participants who neither had cancer nor a hysterectomy. At present we do not know how current protocols that combine surgery with adjuvant radiotherapy affect QOL, so these results should be used judiciously in recommending surgery over radiation for bulky or advanced-stage disease. By incorporating empirical data regarding long-term quality-of-life outcomes into the clinical decision-making process for treating early-stage cervix cancer, our data may assist both the patient and her physician in selecting the most appropriate treatment.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank Robert Coleman for his contribution to the editing of this manuscript.

	NOTES

 
Supported by the Deferred Tuition Fund grant from The University of Texas at Houston School of Public Health.

Presented at the 35th Annual Meeting of the Society of Gynecologic Oncologists, San Diego, CA, February 7-11, 2004.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

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Submitted November 6, 2004; accepted June 29, 2005.

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