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Management Choice and Adherence to Follow-up After Colposcopy in Women With Cervical Intraepithelial Neoplasia 1

From the Reproductive Health Clinic, Division of Health and Human Services, Municipality of Anchorage, Anchorage, Alaska; and Psychology Department, University of Alaska, Anchorage, Alaska

Address reprint requests to: Lynn E. Hartz, MSN, 3104 Brook-side Drive, Anchorage, AK 99517-1882; E-mail: lhartz{at}alaska.com.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: To determine women’s preference when given a choice of management between cryotherapy and cytology surveillance and to compare subsequent adherence to serial cytologic follow-up after being diagnosed with cervical intraepithelial neoplasia grade 1 (CIN1).

METHODS: Two hundred nineteen low-income women with biopsyproven CIN1 seen in a reproductive health clinic from August 1995 through December 1999 were offered cryotherapy or cytology surveillance, followed by cytologic testing every 4 months until three consecutive results were normal. Endpoints of the study were: successful completion of follow-up; transferred or referred out of clinic; or lost to follow-up.

RESULTS: Ninety-four women (42.9%) chose cryotherapy, compared with 125 women (57.1%) who chose cytology surveillance (P < .05). Cryotherapy patients were more likely to return for at least one visit (their treatment visit) after colposcopy compared with cytology surveillance patients (P < .001). In contrast to their initial return for treatment of 98.9%, cryotherapy patients were less likely to return for their first follow-up cytology visit compared to surveillance-only patients (68.1% and 83.2%, respectively, P < .01). Thirty-seven percent of the total group successfully completed follow-up at the clinic, 30.1% transferred or were referred, and 32.9% were lost to follow-up.

CONCLUSION: Successful completion of a commonly recommended protocol for serial cytology follow-up was low. Management choice affected initial adherence but not adherence to long-term follow-up.

Mass screening with the Papanicolaou test has been credited with reducing the incidence of cervical cancer and associated mortality by more than 40 percent since 1973.¹After an abnormal Papanicolaou smear, colposcopy and directed biopsy provide a colposcopic impression and histologic diagnosis upon which treatment recommendations can be based. In the continuum of screening throughout treatment, compliance has been and remains a major issue both in follow-up of abnormal Papanicolaou test results and adherence to treatment recommendations after colposcopy.^2–7

Cervical intraepithelial neoplasia grade 1 (CIN1) is a common diagnosis after colposcopy, which represents a small but documented risk for development of CIN2 and CIN3 and invasive cancer of the cervix.^8,9 Management of CIN1 includes ablation, excision, or careful follow-up without treatment. Both surveillance without treatment and all of the treatment modalities require cytologic and/or colposcopic follow-up to detect progression, persistence, or recurrence of disease. A common follow-up or surveillance protocol is to have the woman return for a Papanicolaou test every 4–6 months until three consecutive Papanicolaou tests are normal.^10,11

Although serial cytology is a common recommendation, there are few studies that describe women’s adherence to completing the three consecutive normal Papanicolaou smears required, either as surveillance without treatment or after treatment.^12,13 Completion of the full series of cytologic follow-up visits is crucial. Returning for one treatment visit or Papanicolaou smear follow-up is not sufficient to ensure that the lesion is resolved. Untreated CIN1 entails a risk of persistence of 22–32% and a risk of progression of 13–17%.^8,9 Common treatments for CIN of all grades carries a risk of persistence of 3–5% and a risk of recurrence of 13–19%.¹⁴ A meta-analysis of the accuracy of the Papanicolaou test reported the sensitivity of the Papanicolaou test as 51%.¹ One or even two normal Papanicolaou results after treatment or during surveillance would still leave a substantial risk of undetected disease.¹⁵

In the absence of an optimal management strategy, allowing women their preference in management of CIN1 might increase adherence. Women are being asked for their preference in management of cytologic results of atypical squamous cells of undetermined significance (ASCUS) or low-grade squamous intraepithelial lesions (LSIL), with the underlying premise being that a consideration of women’s preferences should positively contribute to their compliance.^16,17

This study describes women’s preferences when given a choice of management between cryotherapy and cytology surveillance and their subsequent adherence to serial cytologic follow-up after being diagnosed on biopsy with CIN1.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Data were obtained from the Colposcopy Clinic treatment and management database at the Municipality of Anchorage Reproductive Health Clinic (Anchorage, AK). Women attending the Reproductive Health Clinic who have abnormal Papanicolaou smears are referred into the Colposcopy Clinic. Data on follow-up after colposcopy have been collected prospectively on each patient treated and observed at the clinic since inception of the management arm of the program in August 1995. The clinic offers cryotherapy and cytology surveillance only; patients needing loop electrosurgical excisional procedure (LEEP) or laser vaporization are referred. Patients who become pregnant are referred, as the clinic provides no prenatal or abortion services. Criteria for inclusion of cases for analysis were a diagnosis of biopsy-proved CIN1 at the initial colposcopy visit and the patient being given a choice of management between cryotherapy or cytology surveillance without treatment.

Treatment and follow-up recommendations were based on a standardized algorithm followed by the staff nurse practitioner colposcopists. The study, treatment, and management protocols were approved by the clinic medical advisory committee and the Medical Officer of the Municipality of Anchorage, Department of Health and Human Services.

In addition to a histologic diagnosis of CIN1, additional criteria for offering a choice in management were: 1) negative endocervical curettage; 2) satisfactory colposcopy exam; 3) concordance between cytology, colposcopic impression, and histology; 4) nonpregnant; and 5) signing a treatment recommendation form and consent to choosing management and follow-up at the clinic.

Women who chose cryotherapy at the clinic but did not return for treatment were included and analyzed as part of the cryotherapy group. In analyzing adherence to follow-up, women who initially chose cytology surveillance but later had cryotherapy were still considered part of the cytology surveillance group. This is because these women did not change management until at least two visits were accomplished, leaving their initial choice as having the most impact on their return for the first few visits.

The cryotherapy group and the cytology surveillance group had nearly identical follow-up protocols based on published guidelines.^10,11 Both groups were required to have a Papanicolaou smear every 4 months until three consecutive Papanicolaou smears were within normal limits before being released back to annual exams. Yearly colposcopy exams were performed on women in active follow-up. Triggers for immediate repeat colposcopy were evidence of a persistent or recurrent squamous intraepithelial lesion on cytology in those patients who had cryotherapy, or an increase in severity of one grade on Papanicolaou smear in those patients on cytology surveillance. Cytology results were categorized according to the Bethesda System for cervical/vaginal cytologic diagnosis. Because the introduction of the Bethesda System at the cytopathology laboratory contracted to the clinic coincided with the beginning of the management program, there was some uncertainty of the implication of cytologic results of benign cellular changes. Consequently, in the follow-up protocol, a Papanicolaou smear showing benign cellular changes was not considered within normal limits. The rate of benign cellular changes for the cytology laboratory over the period of the study was 1.2%. The same laboratory was used for cytology and histology.

Strategies used to encourage compliance included allowing this group of patients their preference between cryotherapy or cytology surveillance, written follow-up instructions as part of a clinician- and patient-signed management agreement, optional postcard reminders, reminder letters in case of missed appointments, a tracking system, and an assigned nurse practitioner responsible for monitoring compliance with follow-up and case management. The clinic has a sliding fee scale, and no patient is turned away for inability to pay.

Cases were closed to follow-up when one of three endpoints was reached: successful completion, meaning the patient completed three consecutive Papanicolaou smears within normal limits, regardless of how many follow-up visits were required to achieve those consecutive results; transfer, meaning the woman transferred out of the clinic by choice or was referred; or lost to follow-up, meaning the patient did not respond after three reminder letters, the last of which was sent by certified mail.

Data were entered prospectively in an Epi Info 6.04 database (Epi Info; Centers for Disease Control and Prevention, Atlanta, GA). Association between outcome and return for follow-up visits between the treatment and surveillance groups was assessed by ² statistical analysis. Differences in continuous variables between groups were tested with the analysis of variance or t test. Statistical significance was defined as P .05.

Previous studies reported rates of adherence to serial cytology follow-up after colposcopy from 30% to 75%.^12,13,18 Assuming 50% adherence in one group and a sample size of 94 (the smaller of the two n values), this analysis would be able to detect a 20% difference in the proportion adherent with .80 power.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Two hundred sixty-one cases of women diagnosed with CIN1 on biopsy and who met study criteria were entered into the database from August 1995 through December 31, 1999. To date, 219 of those cases have been closed to follow-up, as they had reached one of the three endpoints of the study. There was no difference in age, income, or management choice between closed and unclosed cases. This report describes findings in the 219 closed cases.

Age, income, and ethnicity of the study group are presented in Table 1. Most patients in the study group were white. They tended to be young, with a mean age of 24, and low income, with a mean monthly income of $934. Ninety-seven percent of patients reported having no private health insurance, and 98% were without Medicaid. Based on a sliding fee schedule used at the clinic, 69% of patients were not charged for services because of their income status.

One hundred ninety-seven women (90%) returned for at least one visit after colposcopy, either for cryotherapy or for their first Papanicolaou follow-up visit. Patients who chose cryotherapy were more likely to return for treatment than were Papanicolaou surveillance patients to return for their first postcolposcopy Papanicolaou smear. Ninety-three of 94 women (98.9%) who chose cryotherapy returned for treatment, and 104 of 125 cytology surveillance patients (83.2%) returned for their first cytology follow-up visit (² = 13.01, P < .001).

A comparison of return for serial cytology visits by type of management is shown in Table 2. One hundred four women (83.2%) who chose cytology surveillance returned for the first follow-up Papanicolaou smear compared with 64 (68.1%) of cryotherapy patients (P = .01). The return rate for the second and third Papanicolaou smear visits did not differ by group. Of the total group, 168 women (76.7%) returned for at least one follow-up Papanicolaou smear, but only 100 (45.7%) returned for three.

Of the 81 women successfully completing follow-up, 66 (81.5%) did so with three cytology visits. Fifteen women (18.5%) had to have additional Papanicolaou smears before successful completion. Mean length of time to completion of follow-up after colposcopy was 14.7 months (median 13, range 8–31 months). There was no difference in time to completion of follow-up between patients who had cryotherapy and those choosing cytology surveillance.

Of the 66 women who transferred out of the clinic, 45 (68.2%) had completed at least one follow-up Papanicolaou smear, 24 (36.4%) completed at least two Papanicolaou smears, 13 (19.7%) completed at least three Papanicolaou smears, and six (9.7%) returned for four or more Papanicolaou smears.

Of the 72 cases lost to follow-up, 42 women (58.3%) completed at least one Papanicolaou smear, 20 (27.8%) returned for at least two Papanicolaou smears, six (8.3%) returned for at least three Papanicolaou smears, and two (2.8%) returned for at least four or more Papanicolaou smears.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The majority of cases in this group of women with CIN1 were lost to follow-up (32.9%) or transferred (30.1%) before a third follow-up Papanicolaou smear was accomplished, which left a minority of patients to successfully complete serial cytology follow-up. Of the women who entered the management program and whose cases were closed, only 37% successfully completed serial cytology follow-up at the clinic.

The women in this study demonstrated a preference for cytology surveillance (57.1%) over cryotherapy (42.9%), although it was not marked. There was no association between choice of management and outcome. Neither age nor income appeared to affect preference in management of CIN1.

Initial adherence with management recommendations in this study was viewed from two different perspectives: first visit after colposcopy versus first cytology follow-up visit. Counting the treatment visit for the cryotherapy group as reflecting their initial adherence after colposcopy, and adding the cytology surveillance groups’ rate of return for their first Papanicolaou smear visit gives a combined initial adherence rate of 90% and can be compared with the reported rates of compliance of 54% and 55% reported by Massad and Meyer³ and Gold et al,⁵ respectively, as the definitions of compliance are comparable.

The cryotherapy group had a significantly better initial return than the surveillance group, with a possible explanation being the different time interval from colposcopy to the first follow-up appointment. Initially, the treatment group appeared more compliant, but their required return was about 1 month after colposcopy compared with the 4-month interval for the surveillance group. In contrast, when the two groups were compared based solely on their return rate for each cytology follow-up visit, the cytology surveillance group showed a significantly higher return for the first Papanicolaou smear visit. At that point, the surveillance group was 4 months from colposcopy, and the cryotherapy group was at least 5 months from colposcopy because of having had treatment. The differences in initial adherence of the two groups were no longer significant by the time of the second follow-up cytology visit and were negligible by the third.

There appeared then a steady loss to follow-up as the time from colposcopy and diagnosis increased, regardless of treatment status. This would explain the differing initial return rates seen in this study and would also be consistent with the findings of Gold and associates, who found that women recommended to follow-up within 1 month of their colposcopy were more likely to be compliant than those women recommended to return in 4 months, regardless of whether the 1-month follow-up was for treatment or a repeat colposcopy.⁵ The length of time between colposcopy and recommended management may have a greater impact on compliance than other factors. Because the nature of cytology surveillance precludes a short length of time between colposcopy and follow-up, unlike returning for cryotherapy, the effect of treatment versus time interval on adherence was not addressed.

Eger and Peipert¹³ as well as Massad and Meyer³ found that women with higher grades of histology and those in whom treatment was advised were more likely to be compliant. In both of those studies, women with all grades of cervical neoplasia were included. Histologic grade was not a factor in our study because only women with CIN1 were included; treatment recommendation was also not a factor, as women in this study were all considered equal candidates for either cryotherapy or cytology surveillance and were allowed to make their own choice.

The finding that income was significantly related to final outcome in adherence was puzzling because the clinic does not turn patients away for inability to pay, and the majority of the women were not charged for services because of their low income. In contrast, Eger and Peipert did not find socioeconomic status a significant factor in compliance.¹³ Perhaps income serves as a marker for other characteristics affecting adherence.

The follow-up regime of requiring three consecutive normal Papanicolaou smears post-treatment or in lieu of treatment proved difficult to carry out. Those patients who transferred out of the clinic—and even those lost to follow-up—may indeed have obtained additional Papanicolaou smears at other sites, but few clinics have the resources to confirm that follow-up is accomplished outside of the clinic. The amount of staff time absorbed in monitoring follow-up, sending out reminders, and case management issues was substantial, even when limited to patients who remained "in-house." Yet without that confirmation, the recommended follow-up of a minimum of three Papanicolaou smears is left to the level of understanding of the patient and the variable access to health care services elsewhere.

There are few studies with which to compare adherence with serial cytology follow-up. Fifty-seven percent of the total group returned for at least two Papanicolaou smear visits. This is comparable to the 59% reported by Eger and Peipert, who studied completion of follow-up after colposcopy in women with various grades of cervical disease.¹³ A study on management of patients with CIN1 that reported follow-up data on women after cryotherapy had return rates for three follow-up visits at 66%, 54%, and 29%, respectively,¹⁸ which are similar to our cryotherapy return rates of 68.1%, 54.3%, and 45.7%.

The majority of women transferred or referred or lost to follow-up dropped out early in the process. Of the 66 women transferred or referred out of the clinic, 42 (63.6%) had done so before the second cytology visit. More importantly, of the 72 women lost to follow-up, 52 (72.2%) never returned for a second cytology visit.

This study was limited to primarily low-income women attending a public clinic. It is possible that an older, less mobile, and more affluent population would have a greater ability to adhere to serial cytology visits after colposcopy. In addition, in clinics able to offer a full array of services, fewer women would need to be referred out, potentially increasing the number of women successfully completing follow-up.

The findings of this study have several clinical implications that might be useful in like populations. First, intervention to improve follow-up adherence should be aimed at the first follow-up visit for patients on cytology surveillance, as most in our study returned for that visit. This might involve just a few minutes of education and reinforcement on how many Papanicolaou smears are necessary and why multiple Papanicolaou smears are necessary. Second, for cryotherapy patients, intervention should be timed for the cryotherapy visit or post-cryotherapy check, as only 68.1% of them returned for the first follow-up Papanicolaou smear. Third, the importance of transferring records in case of changes in residence and other life circumstances should also be discussed early on, in anticipation of the high number of women likely to exit follow-up before completion. For the same reason, colposcopy chart forms should be designed with portability and the ability to fax in mind.

Cytology surveillance in lieu of treatment appears reasonable on a theoretical basis because of the high rate of spontaneous regression of CIN1, yet the safety of that protocol rests on an assumption of adherence to multiple follow-up visits, which is not supported in the literature and was not found in this study. In studies investigating compliance after colposcopy, there do not appear to be easily identifiable risk factors that would tell us which patients will be able to adhere to follow-up and which patients will not.^3,5,13,19 Most of the management guidelines that describe surveillance without treatment as an option stipulate that it be restricted to patients who are compliant.^10,11,15 In the absence of identifiable risk factors for noncompliance, and rates of noncompliance after colposcopy that range from 23% to 64%,^3,13,18 it would seem prudent to approach surveillance without treatment for women with CIN1 with caution.

Technical advances that would shorten follow-up time or that would identify cases with no risk of progression need to be sought and tested. Any method that would decrease the length of time in follow-up would increase the attractiveness of more conservative methods of management for women with CIN1.

	Footnotes

 
This study was supported by a grant from USPHS Region 10 Title X Family Planning.

PII S0029-7844(01)01526-5

Received February 27, 2001. Received in revised form June 5, 2001. Accepted June 15, 2001.

	REFERENCES

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
1. McCrory DC, Mather DB, Bastian L, Datta S, Hassesblad V, Hickey JD, et al. Evaluation of cervical cytology. Evidence Report/Technology Assessment No. 5. (Prepared by Duke University under contract no. 290-97-0014). AHCPR publication no. 99-E010. Rockville, Maryland: Agency for Health Care Policy and Research, 1999.

2. Marcus AC, Crane LA, Kaplan CP, Reading AE, Savage E, Gunning J, et al. Improving adherence to screening follow-up among women with abnormal Pap smears: Results from a large clinic-based trial of three intervention strategies. Medical Care 1992;30:216–30.[Medline]

3. Massad LS, Meyer PM. Predicting compliance with follow-up recommendations after colposcopy among indigent urban women. Obstet Gynecol 1999;94:371–6.[Abstract/Free Full Text]

4. Laedtke TW, Dignan M. Compliance with therapy for cervical dysplasia among women of low socioeconomic status. South Med J 1992;85:5–8.[Medline]

5. Gold MA, Dunton CJ, Macones GA, Hunter Dixon L, Carlson JA. Knowledge base as a predictor of follow-up compliance after colposcopy. J Lower Genital Tract Dis 1997;1:132–6.

6. Melnikow J, Chan BK, Stewart GK. Do follow-up recommendations for abnormal Papanicolaou smears influence patient adherence? Arch Fam Med 1999;8:510–4.[Abstract/Free Full Text]

7. Lerman C, Hanjani P, Caputo C, Miller S, Delmoor E, Nolte S, et al. Telephone counseling improves adherence to colposcopy among lower-income minority women. J Clin Oncol 1992;10:330–3.[Abstract]

8. Nasiell K, Roger V, Nasiell M. Behavior of mild cervical dysplasia during long-term follow-up. Obstet Gynecol 1986;67:665–9.[Abstract]

9. Ostor AG. Natural history of cervical intraepithelial neoplasia: A critical review. Int J Gynecol Pathol 1993;12:186–92.[Medline]

10. Kurman RJ, Henson DE, Herbst AL, Noller KL, Schiffman MH. Interim guidelines for management of abnormal cervical cytology. JAMA 1994;271:1866–9.[Medline]

11. American College of Obstetricians and Gynecologists. Cervical cytology: Evaluation and management of abnormalities. ACOG technical bulletin no. 183. Washington DC: American College of Obstetricians and Gynecologists, 1993.

12. Stewart DE, Buchegger PM, Lickrish GM, Sierra S. The effect of educational brochures on follow-up compliance in women with abnormal Papanicolaou smears. Obstet Gynecol 1994;83:583–5.[Abstract]

13. Eger RR, Peipert JF. Risk factors for noncompliance in a colposcopy clinic. J Reprod Med 1996;41:671–4.[Medline]

14. Mitchell MF, Tortolero-Luna G, Cook E, Whittaker L, Rhodes-Morris H, Silva E. A randomized clinical trial of cryotherapy, laser vaporization, and loop electrosurgical excision for treatment of squamous intraepithelial lesions of the cervix. Obstet Gynecol 1998;92:737–44.[Abstract]

15. Cox JT, Massad LS, Lonky N, Tosh R, Waxman A, Wilkinson EJ. ASCCP practice guidelines: Management guidelines for the follow-up of cytology read as low grade squamous intraepithelial lesion. J Lower Genital Tract Dis 2000;4:83–92.

16. Ferris DG, Kriegel D, Cote L, Litaker M, Woodward L. Women’s triage and management preferences for cervical cytologic reports demonstrating atypical squamous cells of undetermined significance and low-grade squamous intra-epithelial lesions. Arch Fam Med 1997;6:348–53.[Abstract]

17. Meana M, Stewart DE, Lickrish GM, Murphy J, Rosen B. Patient preference for the management of mildly abnormal Papanicolaou smears. J Women’s Health Gend Based Med 1999;8:941–7.[Medline]

18. Elit L, McLachlin M, Kirk ME, Carey M, Robins R. Management of colposcopy patients with biopsy-proven cervical intraepithelial neoplasia grade 1. J Lower Genital Tract Dis 1999;3:191–5.

19. Parham GP, Andrews NR, Lee ML. Comparison of immediate and deferred colpsocopy in cervical screening program. Obstet Gynecol 2000;95:340–4.[Abstract/Free Full Text]

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