Behavioral and psychosocial factors are critical to every aspect of cervical cancer control, from the prevention of human papillomavirus (HPV) transmission and early detection of preinvasive disease, through the posttreatment rehabilitation and recovery process, to management of symptoms and maintenance of quality of life. With the importance of these factors in mind, a group of behavioral scientists joined physicians, nurses, and laboratory and clinical researchers at the Second International Conference on Cervical Cancer (Houston, TX, April 11–14, 2002). During the conference, they reviewed selected behavioral factors related to cervical cancer, including women's receptivity to emerging cervical cancer screening and diagnostic technologies, variables that influence adherence to follow-up colposcopy recommendations, and the quality of life of cervical cancer survivors. To offer a view of the topics under investigation in this field, in the current article, we present synopses of the presentations. They include descriptions of 1) methods used to increase participation in cervical cancer screening, specifically among low-income women; 2) acceptance of new screening technologies and women's adherence to protocols that employ the new approaches; 3) women's responses to health information in stressful situations; and 4) women's perceptions of posttreatment quality of life, particularly sexual aspects. Research priorities that become apparent in review of these investigations include finding methods to modify sexual behavior and prevent risk-enhancing behaviors, diffusing effective interventions to promote regular screening, and promoting understanding of barriers to screening in disenfranchised and vulnerable communities and identifying ways to overcome them.
Behavioral and psychosocial factors affect all aspects of cervical cancer control, from prevention to posttreatment rehabilitation. Behavioral scientists gathered at the Second International Conference on Cervical Cancer (Houston, TX, April 11–14, 2002) reviewed selected studies of behavioral factors related to cervical cancer, including women's receptivity to emerging cervical cancer screening and diagnostic technologies, factors that influence adherence to follow-up colposcopy recommendations, and cervical cancer survivors' quality of life. Researchers reported that reduced distress during examinations with new technology may improve adherence to cervical cancer screening recommendations. Until new technology becomes mainstream, research shows that distress is reduced and adherence improves when health care providers match interventions to patients' informational processing styles. Investigations of survivors' quality of life report conflicting findings, but studies indicate that survivors experience anger over reproductive loss, loss of interest in sex, and perhaps a greater vulnerability to sexual dysfunction compared with survivors of other cancers. Survivors also report a need for posttherapy support programs. Primary prevention of cervical cancer should remain a priority as research in behavioral interventions and barriers to screening, especially among vulnerable populations, moves forward. Cancer 2003;98(9 Suppl):2009–2014. © 2003 American Cancer Society.
EARLY DETECTION OF CERVICAL CANCER: ADHERENCE TO SCREENING AND FOLLOW-UP RECOMMENDATIONS
Although cervical cancer remains a serious problem in developing countries, incidence and mortality rates have decreased significantly in developed countries over the past 50 years; nonetheless, risk of cervical cancer remains high among medically underserved populations. One reason for this elevated risk is underutilization of cervical cancer screening in these populations.
Most interventions to increase breast or cervical cancer screening rates have been either community based or practice based. Community interventions use such strategies as targeted mailings or mass media broadcasts of educational or motivational information and group or individual educational sessions conducted by lay or professional health educators. Medical practice-based interventions include mailed reminders to patients, prompts for health care providers, clinic educational sessions, and telephone reminders and/or counseling for patients. Electra D. Paskett and colleagues have combined the community-based and practice-based approaches to increase cervical cancer screening among low-income women older than 40 years who live in low-income housing communities in North Carolina.1 The researchers combined public health clinic interventions, which were aimed at both health care providers and patients, with such community outreach strategies as educational sessions, literature distribution, community events, media outreach, and church programs. This multipronged approach to increasing screening rates was successful. Cervical cancer screening rates improved from 73% to 87% (P = 0.003); whereas, in a comparison city, the rates showed a nonsignificant decline from 67% to 60%. Survey respondents in the intervention city also reported fewer barriers to Papanicolaou (Pap) smear screening at follow-up compared with the women in the comparison city. In a more recent study, Cyrus-David et al. examined adherence to risk-appropriate Pap smear utilization among low-income minority women in a rural county in North Carolina.2 Risk-appropriate screening suggests that women at higher risk for cervical cancer (i.e., those who engage in risky sexual behaviors, smoke, or have HPV) should be screened at least annually, whereas woman at normal risk may be screened at least every 3 years. In that study, over 80% of the 897 women surveyed were at high risk. Overall, only 52% of all women were screened appropriately.
Early detection of cervical cancer requires that women go to health care providers to obtain screening and that health care providers provide the test to women who need it. Furthermore, adherence to follow-up recommendations is necessary once an abnormality has been identified on the screening test. For women with Pap smears that show atypical squamous cells of undetermined significance (ASCUS), this may mean repeating the Pap smear at more frequent intervals; however, some patients with ASCUS results and other patients with dysplasia of a higher grade will be referred for colposcopy.
Adherence to follow-up colposcopy is a major problem. Estimated rates of nonadherence range from 7% to 50%, depending on the population. Factors associated with delayed or incomplete follow-up are similar to those associated with nonadherence to cervical cancer screening: younger or older age, financial barriers, lower education, lower income, lower social support, and nonwhite race.3
Certain aspects of current practice may have a negative effect on adherence to both initial Pap smear testing and subsequent follow-up of abnormal results. One is the inevitable delay in the process of determining whether a woman has cervical neoplasia and requires treatment. After having an initial Pap smear, women typically wait several weeks for the results of the test. If colposcopy is recommended, then scheduling often forces women to wait for colposcopy. After the colposcopy, women and health care providers face another delay—again, usually for several weeks—before obtaining the results of any biopsies taken and learning whether treatment will be needed. Women must attend multiple visits over a period of several months before they know whether they have a problem that requires treatment, and each appointment is a potential missed appointment.
A second factor that has been shown to affect adherence to follow-up recommendations is women's fears about colposcopy and follow-up. Receiving a positive Pap smear result and undergoing colposcopy, biopsy, and treatment can be quite stressful. A positive result raises fears of cancer in most women in addition to concerns about the loss of reproductive and sexual functioning, medical procedures, and anxiety about their bodies ‘betraying’ them.4–7 Compared with women who have negative screening results, women who have positive test results are more anxious, experience more general distress and mood disturbance, and worry more specifically about cervical cancer.8–11 In addition, impairments in sleep and sexual interest have been noted.9 The length of the delay between having the Pap smear and receiving results is correlated with distress for patients with positive or mildly abnormal results but not for women with negative results.8 Also, women who do not comply with colposcopy recommendations suffer the greatest emotional impairments.9
New technologies are being developed to improve screening and diagnosis, to reduce false positive and false negative rates, and to provide immediate feedback and treatment options. For example, optical spectroscopy has the potential to provide more accurate information about cervical dysplasia than the Pap smear and to provide real-time information that can be used to provide immediate feedback to the patient and enable the immediate treatment of lesions.
There is a need to evaluate new technologies for patient receptivity. If new technologies are unacceptable to patients and, thus, decrease adherence to early detection examinations, then it may negate the advantage of improved accuracy. Karen Basen-Engquist, Ph.D., M.P.H., and colleagues at The University of Texas M. D. Anderson Cancer Center are studying the effect of emerging cervical screening and diagnostic technologies on patient receptivity and adherence. Their current study, focusing on optical spectroscopy, has shown that participants reported significantly less pain and anxiety during optical spectroscopy than during Pap smear and colposcopically directed biopsy. For the most part, participants were more satisfied with optical spectroscopy than the usual care procedures, but they were more likely to feel that optical spectroscopy took too long. In terms of accuracy, participants rated optical spectroscopy as more sensitive and specific than Pap smear but less sensitive and specific than biopsy. The reduced distress during the examination and higher level of satisfaction may enhance adherence to cervical cancer screening.
Until newer, improved technologies are available widely, effective interventions to improve patient adherence to colposcopy and treatment are needed. The research of Suzanne M. Miller, Ph.D., at Fox Chase Cancer Center has focused on different approaches to processing of threat-related information in stressful situations. Much of this work has focused on increasing adherence to colposcopy and reducing distress associated with the procedure. This work delineates two characteristic attentional styles, or behavioral ‘signatures’: high monitoring, which involves scanning for threatening cues, and low monitoring, which involves distraction from threatening cues.12, 13
In response to cervical cancer risk feedback and other health stressors, patients considered high monitors tend to respond with heightened and more sustained perceived vulnerability, greater negative expectations about their health, less satisfaction with health-related information, more disease-specific distress and physiologic arousal, and diminished self-efficacy regarding their ability to cope with the health threat. This pattern of response to diagnostic feedback can lead to intrusive ideation that triggers avoidant thoughts and behaviors, which ultimately may be detrimental to health behaviors and adherence over the long term,14, 15 particularly when less information and support are available. Patients considered low monitors (blunters) are more likely to ignore and psychologically distance themselves from cancer threats and tend to be less distressed in the face of diagnostic feedback, particularly when not presented with voluminous information, but they also are less adherent from the onset.13, 16
Informational processing styles have implications for the design of interventions tailored to manage distress during stressful medical procedures, specifically colposcopy, and for interventions meant to increase adherence to future follow-up and screening.17, 18 In a study on distress during colposcopy, patients were assigned randomly to two interventions to manage distress: one intervention presented extensive information about the procedures, and the other intervention used methods to distract individuals from the procedure. Patients who received an intervention that matched their informational processing style experienced less distress compared with patients who received an intervention that was inconsistent with their style.18 Specifically, individuals who used a blunting informational processing style experienced less distress when they received an intervention that distracted them from the procedures, whereas high monitors were less distressed and better adjusted when they were provided with detailed preparatory information.
Later studies showed that monitors and blunters also fared better with different types of messages about adherence.17 Colposcopy patients were presented with positively framed, negatively framed, or neutral messages about adherence. When negatively framed messages were presented to high monitors, they resulted in increased intrusive ideation and decreased adherence to health-protective behavior recommendations because of the greater baseline focus on threat among these individuals. For blunters (who are less attentive to threat), negatively framed messages increased knowledge retention and increased adherence to health-protective behavior without affecting intrusive ideation. A study that tested different kinds of preparatory information (stress inoculation, general health information, and usual care) before a colposcopy appointment found that, for blunters, intrusive ideation was increased (from low to moderate levels) when they received either of the two preparatory interventions; for monitors, the intervention decreased intrusive ideation (from high to moderate levels). Furthermore, intrusive ideation was associated with adherence to follow-up screening 1 year later, indicating that a moderate degree of intrusive ideation was optimal for adherence in both groups. The researchers concluded that the interventions decreased the intrusive ideation of monitors to a manageable level, whereas the preparatory communications for blunters raised both intrusive and avoidant ideation; nonetheless, including action plans for effective adherence may offset the distressing focus on risk feedback.
QUALITY OF LIFE OF CERVICAL CANCER SURVIVORS
Cervical cancer and its treatment potentially may cause multiple survivorship challenges and quality-of-life disruptions. Social, sexual, and psychologic sequelae frequently are reported among both newly diagnosed patients and long-term cervical cancer survivors. However, there has been limited research on long-term cervical cancer survivors, and findings have conflicted with one another. It has been found that women who have cervical cancer have more psychologic and psychosomatic symptoms compared with women who have endometrial cancer,19–21 but they have scores on quality-of-life measures during and after treatment similar to those of women who have other gynecologic cancers.22 Younger women with cervical cancer may experience problems specifically related to their diagnosis and treatment.23 Lari B. Wenzel, Ph.D., and colleagues at the University of California–Irvine, conducted a study of quality-of-life concerns and long-term sequelae of women of childbearing age who were long-term (5–10 years) survivors of cervical cancer, gestational trophoblastic disease, or lymphoma. Cervical cancer cases were identified and accrued through tumor registries in Colorado and California. Results on a global quality-of-life measure indicated that, overall, survivors enjoy good quality of life. However, important survivor-specific issues emerged. For example, a greater proportion of cervical cancer survivors scored in the lowest quartile on general health, vitality, and mental health subscales than would be expected based on normative scores (P < 0.058). Significant differences also were observed on coping efforts between groups, with a trend for the cervical cancer survivors to report more coping responses than survivors of lymphoma or gestational trophoblastic disease. Similarly, cervical cancer survivors also reported that they had greater difficulty with social and emotional well-being, sexual discomfort, and gynecologic symptoms compared with the other women. Survivors also responded to qualitative questions, which demonstrated the importance of obtaining education and support well into survivorship. The majority of cervical cancer survivors indicated that they would have been very likely to participate in a support program after diagnosis if it were available, and approximately 60% would be likely to participate now, long into survivorship.
Leslie Schover has summarized the literature on effects of cervical cancer treatment on sexuality. Reproductive concerns also were a major issue for the survivors of cervical cancer. They reported significantly more anger related to reproductive loss compared with survivors of lymphoma or gestational trophoblastic disease. Approximately one-third of cervical cancer survivors reported that they were somewhat sad to very much sad about their inability to have children and were not able to talk openly about their infertility. Twenty-five percent expressed frustration about their inability to have children.
Treatment for cervical cancer can result in anatomic and physiological changes (e.g., changes in vaginal lubrication, vaginal stenosis) that potentially may affect sexual functioning. Although research on sexual dysfunction after treatment for cervical cancer has been conducted for over 30 years, little more is known today than in the 1970s about the causes of sexual problems after cervical cancer, the relation between type of treatment for cervical cancer and prevalence of different types of sexual problems, or the kinds of behavioral or medical interventions that may remediate them effectively. Such sexual problems as loss of interest in sex or pain with sexual activity are common in women who survive cervical cancer.24, 25 Bergmark et al. found that a similar percentage of cervical cancer survivors (5 years from diagnosis) and controls reported low sexual desire, but that this reduced desire was more distressing to survivors.24 Survivors reported less vaginal lubrication and genital swelling when sexually aroused compared with controls and were more distressed by these problems. They also reported more dyspareunia, vaginal bleeding during intercourse, and vaginal changes (reduction in length or elasticity of the vagina) compared with healthy controls but were similar in frequency of intercourse and the prevalence of problems with orgasm.
The epidemiology of cervical cancer may create unusual vulnerability to sexual dysfunction. Women with low educational levels are at increased risk of cervical cancer. National surveys also have shown that women with less education have higher rates of sexual dysfunction.26 Women with cervical cancer also may have experienced high rates of sexual trauma and domestic violence,27 which may result in sexual dysfunction, even before cancer diagnosis and treatment. Few studies have compared rates of sexual dysfunction at the time of cancer diagnosis with the rates after treatment.28
Despite theories that radical hysterectomy may impair women's ability to feel erotic pleasure and reach orgasm, prospective and retrospective case series suggest that hysterectomy, along with oophorectomy, does not have a negative impact on women's sexual function.25, 29 Evidence is stronger that radiation therapy for cervical cancer impairs sexual function, especially by leading to dyspareunia related to vaginal atrophy and fibrosis.25 It is possible that regular sexual activity and/or use of dilators can help prevent this problem; however, the great majority of women do not use dilators as advised, and interventions thus far have had limited success. A group intervention for endometrial and cervical cancer survivors in Canada increased the rate of dilator use from 6% to 44% among the younger participants but had no impact on older women30; however, the intervention did not appear to improve sexual functioning. Little is known about the effectiveness of other interventions (e.g., estradiol, sildenafil) to improve sexual functioning in this population.
Prevention and Early Detection
One area that was not addressed in the presentations but was identified as a high priority was the primary prevention of cervical cancer through modifying sexual behavior that transmits HPV infection. A significant amount of progress has been made in the area of preventing human immunodeficiency virus and other sexually transmitted disease that also may be applied to cervical cancer prevention, but more research is needed to determine which sexual behaviors increase and decrease the risk of HPV transmission. With regard to adherence to screening and colposcopy, additional research should focus on the diffusion of effective interventions into clinical and community settings. More research is needed on the specific barriers to cervical cancer screening that are faced by immigrant populations and by women in developing countries. In addition, further research is needed on patient receptivity to other emerging technologies (e.g., HPV testing) and the impact of new technologies on adherence in settings outside of clinical trials. Finally, another area of research in cervical cancer prevention that was not included in these presentations is the interrelationships among psychologic variables, such as stress, avoidant coping, and depression; smoking and other drug use; immune parameters; and HPV infection.
Future attention should be directed at examining efforts to assist vulnerable populations of cancer survivors, which may include young women who have had cervical cancer. In so doing, comprehensive rehabilitation programs could be initiated at an earlier phase in the survivorship trajectory, thus mitigating some of the negative long-term sequelae. With regard to sexuality, the most important research needs are to characterize the prevalence and types of sexual dysfunctions associated with differing modalities of cancer therapy for cervical cancer and to develop and evaluate both medical and behavioral interventions to remediate these problems. Such interventions need to be culturally sensitive to women most at risk for cervical cancer, who often belong to subcultures with conservative values about sexuality and gender roles.
Behavioral, psychologic, and social factors are critical to all phases of cervical cancer control. Early detection methods require women to adhere to screening and follow-up, and new methods of diagnosing cervical neoplasia will have to be acceptable to patients to achieve their promised effects. Treatment for cervical cancer is most effective when patients adhere completely to treatment recommendations. In addition, because treatment for cervical cancer may have a profound impact on the cancer survivors' quality of life, attention also should turn to rehabilitative behavioral interventions.