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Do Follow-up Recommendations for Abnormal Papanicolaou Smears Influence Patient Adherence?
Joy Melnikow, MD, MPH;
Benjamin K. S. Chan, MS;
Gary K. Stewart, MD, MPH
Arch Fam Med. 1999;8:510-514.
ABSTRACT
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Objective To compare adherence to follow-up recommendations for colposcopy or repeated Papanicolaou (Pap) smears for women with previously abnormal Pap smear results.
Design Retrospective cohort study.
Setting Three northern California family planning clinics.
Patients All women with abnormal Pap smear results referred for initial colposcopy and a random sample of those referred for repeated Pap smear. Medical records were located and reviewed for 90 of 107 women referred for colposcopy and 153 of 225 women referred for repeated Pap smears.
Intervention Routine clinic protocols for follow-up—telephone call, letter, or certified letter—were applied without regard to the type of abnormality seen on a Pap smear or recommended examination.
Main Outcome Measures Documented adherence to follow-up within 8 months of an abnormal result. Attempts to contact the patients for follow-up, adherence to follow-up recommendations, and patient characteristics were abstracted from medical records. The probability of adherence to follow-up vs the number of follow-up attempts was modeled with survival analysis. Cox proportional hazards models were used to examine multivariate relationships related to adherence.
Results The rate of overall adherence to follow-up recommendations was 56.0% (136/243). Adherence to a second colposcopy was not significantly different from that to a repeated Pap smear (odds ratio, 1.40; 95% confidence interval, 0.80-2.46). The use of as many as 3 patient reminders substantially improved adherence to follow-up. Women without insurance and women attending 1 of the 3 clinics were less likely to adhere to any follow-up recommendation (hazard ratio for no insurance, 0.43 [95% confidence interval, 0.20-0.93], and for clinic, 0.35 [95% confidence interval, 0.15-0.73]).
Conclusions Adherence to follow-up was low in this family planning clinic population, no matter what type of follow-up was advised. Adherence was improved by the use of up to 3 reminders. Allocating resources to effective methods for improving adherence to follow-up of abnormal results may be more important than which follow-up procedure is recommended.
INTRODUCTION
PATIENTS NOT returning for follow-up is a serious concern for any preventive screening examination. Screening programs for cancer prevention and early detection are based on the concept that the treatment of disease identified in the asymptomatic state will reduce morbidity or mortality to a greater extent than treatment at the symptomatic phase of disease. Patients who do not return for follow-up after having abnormalities detected on a screening test will not benefit from the opportunity for early treatment, despite having incurred the risks and costs of the initial screening.
The use of the Papanicolaou (Pap) smear to screen for cancer and precancerous conditions of the cervix is widely accepted1 as effective. For cancerous changes and high-grade squamous intraepithelial lesions (HGSIL), wide consensus2-3 favors early evaluation and treatment. Considerable controversy exists, however, about which clinical strategy is preferred for the evaluation and management of mild abnormalities.3-6 A substantial proportion of these lesions are either false-positives or will regress without treatment.2-3 Some experts7-8 recommend an early colposcopic examination and therapy for atypical squamous cells of undetermined significance (ASCUS) and low-grade squamous intraepithelial lesions (LGSIL), whereas others3, 9 recommend observation with Pap smear test repeated in 6-month intervals for up to 24 months, and for the evaluation and treatment only of those lesions that progress or persist.
This controversy is fueled by a concern about women who do not return for follow-up. Patients whose low-grade or borderline abnormal results represent clinically important lesions will not benefit from early evaluation and treatment if they do not return for follow-up. If women are more likely to return for a colposcopic examination than a repeated Pap smear because they think that this examination signifies a serious health problem that warrants attention, observation by repeated Pap smears would carry greater risks. Conversely, if referral for colposcopy substantially increases anxiety, women may return for follow-up less frequently. Published research10-15 shows a wide variation in follow-up rates for women who have abnormal Pap smear results, and only 1 report16 has compared follow-up rates for colposcopy with those for repeated Pap smears.
We reviewed medical records and appointment logs to determine whether management recommendations for colposcopy or repeated Pap smears influenced follow-up rates for women in 3 family planning clinics with abnormal Pap smear results and examined other factors that might influence follow-up rates.
PATIENTS AND METHODS
STUDY POPULATION
Data for the study were collected at 3 northern California family planning clinics where both Pap smear tests and colposcopy were performed. The 3 clinics served as colposcopy referral centers for their own patients and for 4 other family planning clinics in outlying areas located 16 to 48 km (10-30 miles) away. The population served by these clinics consisted predominantly of young women (90% younger than 35 years) seeking reproductive health services. Most were uninsured or receiving Medi-Cal (California's Medicaid) assistance. Some coverage for reproductive health services is provided by the California Office of Family Planning. The ethnic distribution was approximately 9% African American, 15% Hispanic, 72% white, and 4% other.
The study protocol was considered exempt from review by the University of California–Davis Human Subjects Committee and was approved by the National Medical Committee of Planned Parenthood Federation of America.
CLINICAL PROTOCOLS
All patients requiring follow-up for abnormal Pap smear results were listed in logs at each clinic. Follow-up recommendations were based on predetermined protocols. Patients having Pap smears showing ASCUS were advised to return for a second Pap smear in 4 months. Patients whose Pap smears showed ASCUS on 2 consecutive smears, and all patients whose smears showed LGSIL or worse were advised to have colposcopy. Atypical glandular cells of undetermined significance were an extremely rare finding in this patient population. Patients with this finding were not included in the study because none had this result during the study period. All patients were advised of follow-up recommendations by telephone, if possible. Patients failing to keep their follow-up appointment were contacted a second time by telephone. Certified letters were sent to patients who had not responded to 2 attempts to contact them. This letter mentioned the possibility that cervical cancer could develop if the patient did not return for follow-up. In a few patients, generally those with higher-grade lesions, additional contact attempts were made by telephone or letter. No distinction was made between patients based on the severity of the abnormality reported on the Pap smear. Follow-up protocols were the same for all abnormalities in each group. Follow-up efforts were documented in the medical record.
DATA COLLECTION
The study sample consisted of all patients listed in the logs as having abnormal Pap smear results who were referred for colposcopy between February 1, 1994, and January 15, 1996, and a computer-generated random sample of all patients advised to have repeated Pap smears during the same period. A sample size of 200 patients having follow-up Pap smears and 200 having colposcopies was projected to have a power of 85% to 90% to detect a 15% difference in adherence with an  of .05 and an estimated baseline adherence of 60%. Trained research assistants using a pretested abstracting form reviewed medical records from March 1994 to August 1996 to determine the reason for referral to colposcopy or repeated Pap smear, the number and type of attempts to contact patients for follow-up, and adherence to follow-up advice and to subsequent follow-up or treatment recommendations after the initial repeated Pap smear or colposcopy. Initial abstractions were doubly reviewed by the principal investigator or research coordinator (J.M.) to ensure accuracy. Women who had received the recommended initial follow-up procedure within 3 months of the first contact attempt were considered adherent. Women for whom a plan to obtain follow-up from another provider was documented were also considered adherent. Billing records from September 1996 to May 1997 were searched to determine if the patients returned at a later time to any of the family planning clinics in the system. Based on the billing codes, the likelihood that a patient received follow-up care was determined. Demographic variables, primary language, postal zip code of residence, insurance status, and history of substance abuse were also abstracted from the medical record.
STATISTICAL ANALYSIS
We used the  2 test for categorical variables and t tests for continuous variables to compare characteristics of the group referred for colposcopy with those referred for a repeated Pap smear. Survival analysis was used to model the probability of appointment adherence vs the number of follow-up attempts. Adherence to a scheduled appointment within 8 months of the abnormal result was the analysis end point. Data for women not adherent and not receiving further follow-up attempts were censored at the point of the last attempt. Kaplan-Meier product-limit estimates were used to examine individual factors related to adherence. Cox proportional hazards models17 were used to examine multivariate relations.
RESULTS
A random sample of 225 women was selected from the logs of 311 women with abnormal Pap smear results requiring repeated Pap smears during the study period. All women recommended for colposcopy in the same period (n=107) were selected. Of these 352 women, medical records for 243 women were located and reviewed. Characteristics of these women are shown in Table 1. Ninety women were referred for colposcopy, and 153 women were advised to have a repeated Pap smear. They ranged in age from 15 to 66 years (mean age, 25.9 years). The mean number of appointment reminders was 1.5 (range, 1-4) among women referred for a repeated Pap smear and 1.6 (range, 1-6) among women referred for colposcopy. Twenty-six women (10.7%) were uninsured, and 29 women (11.9%) spoke Spanish as their primary language. Nearly 90% of women were covered by the California Office of Family Planning funds or Medi-Cal.
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Table 1. Characteristics of 243 Women Recommended for Follow-up of Abnormal Papanicolaou (Pap) Smear Results*
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Women referred for repeated Pap smears were similar in age and primary language to those referred for colposcopy. They were slightly more likely to have health insurance and slightly less likely to have a documented problem with substance abuse, but these differences were not significant (P=.15 for insurance; P=.24 for substance abuse). The mean number of follow-up attempts was similar for women referred for a repeated Pap smear or colposcopy. Women referred for colposcopy were more likely to have a referral Pap smear result showing LGSIL or HGSIL, consistent with the clinic protocols.
The number of follow-up attempts (telephone call, letter, or certified letter) ranged from 0 to 6 (mean, 1.5). Of the 243 women, 153 (63.0%) received 1 reminder, 57 (23.5%) received 2 reminders, 27 (11.1%) received 3 reminders, 4 (1.6%) received 4 reminders, and 2 (0.8%) received 6 reminders. Overall, 136 women (56.0%) adhered to recommendations to have either a repeated Pap smear or colposcopy, 81 women (52.9%) for repeated Pap smears and 55 (61.1%) for colposcopy. These proportions were not significantly different (P=.22); the odds ratio for adherence to colposcopy compared with a repeated Pap smear was 1.40 (95% confidence interval [CI], 0.80-2.46). In these groups, 3 women in the group having a repeated Pap smear and 2 in the colposcopy group obtained follow-up from an outside provider; this information was documented in the medical record as based on a telephone conversation with clinic staff. These women were considered adherent.
The initial contact resulted in overall adherence of 39.1% (95 of 243 women). For those women receiving continuing follow-up attempts, the second and third attempts improved adherence by approximately 20% with each attempt. Improvements in adherence diminished markedly after the third reminder, with extensive overlap of 95% CIs for adherence after the third reminder. Figure 1 shows the effect of reminders on adherence patterns for women referred for repeated Pap smears and those referred for colposcopy. The effect of reminders was not significantly different in 1 group compared with the other (P=.48), with extensive overlap of 95% CIs.
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Cumulative probability of adherence to first follow-up appointment, stratified by scheduled follow-up procedure and 95% confidence intervals (vertical bars). No subjects had only 5 appointment reminders. Pap indicates Papanicolaou.
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Women with ASCUS were less likely to be referred for colposcopy and more likely to adhere to the colposcopy appointment than to a repeated Pap smear (unadjusted odds ratio, 4.06; 95% CI, 1.36-14.58) (Table 2). The effect on appointment adherence of patient characteristics, referral Pap smear results, referral clinic, and whether the patient was referred for repeated Pap smear or colposcopy was evaluated with bivariate analysis and then using a Cox proportional hazards model. The adjusted hazard ratios for follow-up appointment adherence with 95% CIs are shown in Table 3. Women without insurance, those having LGSIL or HGSIL reported on their Pap smear and referred for colposcopy (compared with women with either finding who were referred for repeated Pap smear) and those referred to clinic C were significantly less likely to adhere to their follow-up appointment. Women with ASCUS referred for colposcopy (compared with women with ASCUS referred for repeated Pap smear) were more likely to adhere to their appointments (hazard ratio, 2.67; 95% CI, 1.22-5.86). Age, primary language, recorded substance abuse, and distance to the clinic did not appear to influence the likelihood of adherence.
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Table 2. Unadjusted Odds Ratios for Follow-up Appointment Adherence to Colposcopy vs Repeated Papanicolaou (Pap) Smear, by Initial Pap Smear Result*
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Table 3. Follow-up Appointment Adherence in Cox Proportional Hazards Model*
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A search of billing records for evidence of subsequent visits among the 103 women unavailable for follow-up yielded 17 women (11 originally scheduled for a repeated Pap smear, and 6 scheduled for colposcopy), resulting in a total long-term return rate of 63% (n=153). Further follow-up or treatment after the first follow-up visit for a repeated Pap smear or colposcopy was recommended for 92 women (60.1%). Among those for whom an additional visit was recommended after colposcopy, 25 (53%) were adherent. Twenty-one (47%) of 45 women adhered to an additional visit following a repeated Pap smear.
COMMENT
In a group of women attending family planning clinics, adherence to follow-up appointments for a repeated Pap smear or colposcopy was low, with 44.0% failing to return for follow-up. Appointment adherence was improved incrementally by as many as 3 reminders. The effect of reminders beyond 3 appeared to be minimal, although the number of women receiving more than 3 reminders was small. The failure to return for follow-up was not substantially different for women referred for a repeated Pap smear compared with those referred for colposcopy, and in multivariate analysis, women with more serious abnormalities reported on Pap smear were apparently less likely to return for a colposcopy than for a repeated Pap smear.
Our study was limited by its retrospective design. Women were not randomly assigned to referral for colposcopy or repeated Pap smear. A substantial number of medical records could not be located for review. We have no reason, however, to think that any systematic bias influenced which records were missing.
The patient population attending family planning clinics is at high risk for not returning for follow-up. Previous studies in family planning clinics and inner-city walk-in clinics have found similar adherence rates for follow-up of abnormal Pap smear results,10-13 although studies14-15 conducted in other countries and different practice settings have reported adherence rates as high as 96%. Only 1 other study that we know of has compared adherence rates between groups of women referred for colposcopy and those referred for a repeated Pap smear. Block and Branham16 found an 80% follow-up rate among women referred for a repeated Pap smear and a 90% follow-up rate among women referred for colposcopy. This difference was not significant.
Based on our actual sample size and an of .05, the power of our study to detect a 15% difference in adherence between groups was approximately 65%; the power to detect a 20% difference in adherence was more than 80%. Although a significant difference could have been missed because of the relatively small sample, results of the multivariable analysis suggest that women most likely to harbor higher grades of cervical dysplasia are less likely to adhere to colposcopy appointments. This may be because most women with ASCUS referred for colposcopy had already had a repeated Pap smear and, therefore, represented a selected, more adherent subgroup of all women with ASCUS. This concerning relationship between the severity of the abnormality and the failure to return for follow-up may also be related to anxiety generated by the referral or to other characteristics of this group of women.18-20 Similar findings have been reported in a retrospective study that Carey and Gjerdingen21 conducted in a Minnesota family practice residency clinic. They found that Southeast Asian women were most likely to have moderately severe abnormal results on Pap smear and least likely to adhere to follow-up recommendations. Our study was unable to examine ethnicity as a variable because it was not consistently recorded in the medical records. Prospective studies are needed to confirm these findings.
The lower adherence to follow-up at clinic C was striking and cannot be explained by our data. Clinic C is a busy clinic in a low-income neighborhood near a closed military base. No referrals from outlying clinics were made to this clinic. Turnover among staff and patients has been higher than at other clinics, but clinic staff were unable to identify any other reason for the difference in adherence. Clinic protocols were the same at all sites.
Our study confirms the findings of previous work13 on the value of patient reminders but clarifies that little is gained beyond 3 attempts to arrange follow-up. Regardless of the clinical approach taken, a high rate of failing to return for follow-up should be anticipated with traditional follow-up strategies for cervical cancer screening programs that are part of family planning services for low-income women.
Our findings highlight the importance of improving follow-up for women with abnormal Pap smear results. The clinical approach selected for follow-up does not appear to influence the follow-up rate. Benefits of cervical cancer screening are limited to women obtaining follow-up procedures for abnormal results. Specific interventions, including motivational or educational brochures,10, 22 telephone counseling,23-24 and assistance with transportation,25 have been shown in randomized trials to improve adherence to follow-up for abnormal Pap smear results. If screening for cervical cancer is incorporated into programs designed primarily to provide other services, such as family planning or the treatment of sexually transmitted diseases, additional resources may be better allocated to such alternative follow-up approaches in place of providing more frequent colposcopy. Targeting interventions to women with more serious abnormalities reported on Pap smear will have greater potential effects because they are most likely to benefit from intervention and they may be less likely to adhere to their appointments.
AUTHOR INFORMATION
Accepted for publication February 4, 1999.
This study was funded by grant 1RO1 CA 70104 from the National Cancer Institute, Bethesda, Md.
We thank Mary Paliescheskey for the coordination of data collection, the clinic staff of Planned Parenthood Mar Monte East for assistance with data collection, and Stephen Birch, DPhil, for critically reviewing the manuscript.
This study is dedicated to the memory of our friend and colleague, Gary Stewart, MD, MPH.
Corresponding author: Joy Melnikow, MD, MPH, Department of Family and Community Medicine, University of California–Davis School of Medicine, 4860 Y St, Suite 2300, Sacramento, CA 95817 (e-mail: jamelnikow{at}ucdavis.edu).
From the Departments of Family and Community Medicine (Dr Melnikow), Internal Medicine (Mr Chan), and Obstetrics and Gynecology (Dr Stewart), University of California–Davis School of Medicine, Sacramento. Mr Chan is now with the Division of Medical Informatics and Outcomes Research, Oregon Health Sciences University, Portland. Dr Stewart is deceased.
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