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Obstetrics & Gynecology:
doi: 10.1097/AOG.0b013e318293ab22
Original Research

Overtreatment in a See-and-Treat Approach to Cervical Intraepithelial Lesions

Bosgraaf, Remko P. MD; Mast, Peter-Paul MD; Struik-van der Zanden, Petronella H. T. H.; Bulten, Johan MD, PhD; Massuger, Leon F. A. G. MD, PhD; Bekkers, Ruud L.M. MD, PhD

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Author Information

Departments of Obstetrics and Gynaecology and Pathology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands.

Corresponding author: Remko P. Bosgraaf, MD, Radboud University Nijmegen Medical Centre, Department of Obstetrics & Gynaecology (internal mail 791), PO Box 9101, 6500 HB Nijmegen, The Netherlands; e-mail: R.Bosgraaf@obgyn.umcn.nl.

Financial Disclosure The authors did not report any potential conflicts of interest.

Presented in part at the 28th International Papillomavirus Conference and Workshops, November 30–December 6, 2012, San Juan, Puerto Rico.

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Abstract

OBJECTIVE: To determine the overtreatment rate at colposcopy in women who underwent a see-and-treat protocol.

METHODS: We identified 3,192 patients (mean age 36 years, standard deviation 8.7) who underwent a see-and-treat protocol in Radboud University Nijmegen Medical Center between January 1981 and December 2010. Overtreatment, defined as cervical intraepithelial neoplasia 1 or less at final histopathology analysis, was investigated in relation to the age of the women, time of referral, cervical smear result, colposcopic impression, and histopathology result.

RESULTS: A total of 579 women (18.1%, 95% confidence interval [CI] 16.7–19.5) were overtreated. The lowest overtreatment rate (4.5%, 95% CI 3.5–5.5) was seen in women with both a high-grade cervical smear result and a high-grade colposcopic impression. Women aged younger than 40 years were less likely to be overtreated (13.1%, 95% CI 11.7–14.5) than women aged 40–49 years (24.2% 95% CI 21.2–27.4, number needed to harm nine) and aged 50 years and older (42.2%, 95% CI 36.5–47.7, number needed to harm three).

CONCLUSIONS: The overtreatment rate is low for patients with both a high-grade smear result and a high-grade colposcopic impression, justifying a see-and-treat approach for these patients. In women with either a high-grade smear result or a high-grade impression on colposcopy, a see-and-treat approach may still be preferable but has higher overtreatment rates. Given the side effects of cervical surgery on pregnancy outcome, young women, in particular those who have either a low-grade smear result or low-grade impression on colposcopy, are better served by a two-step approach. In older women, a see-and-treat policy may be preferable.

LEVEL OF EVIDENCE: III

Cervical cancer is a major cause of death and potentially preventable by screening for, and treatment of, precancerous lesions.1,2 In The Netherlands, cervical cancer screening started in the early 1970s. Since the subsequent restructuring of the Dutch screening program in 1988 and 1996, there has been a nationwide program targeting women aged 30–60 years. Those women are invited at 5-year intervals for conventional cervical smears, often taken by their general practitioner or practice assistants.3,4 The Dutch screening program had contributed to a reduction in morbidity and mortality of cervical cancer.5,6 In the Dutch national screening program, 0.8% of the women need direct referral for colposcopy of whom 75.4% are subsequently treated for a high-grade cervical lesion.7 Treatment is deemed necessary in the case of a high-grade intraepithelial lesion, ie, cervical intraepithelial neoplasia (CIN) grade 2 or worse. Under some circumstances, treatment is also applied for (persistent) low-grade intraepithelial lesions.

In general there are two management options for women referred for colposcopy. In the two-step procedure, biopsies of colposcopically suspicious areas are taken, and further treatment is based on the biopsy results during a second visit. In a see-and-treat approach, treatment is performed during the initial colposcopy, when the colposcopist is convinced that the cervical lesion is high grade. This conviction is based on the cervical smear result and the colposcopic impression. If in either method no treatment is performed during the initial colposcopy, or if biopsies do not show a high-grade lesion, women are monitored with cervical smears at 6-month intervals and colposcopy is repeated if necessary.

Advantages of the see-and-treat procedure include a single visit to the hospital because diagnosis and treatment are combined, fewer costs, and less emotional stress.8,9 A concern of the see-and-treat procedure is overtreatment. Complications like hemorrhage, infection, cervical stenosis, and the risk of preterm birth are rare but possibly preventable if overtreatment can be avoided.10–14

The objective of this study was to investigate the percentage of overtreatment during the past 30 years in relation to the cervical smear result, age of the patient, and colposcopic impression. With these results we hope to improve the standard of care for patients referred for colposcopy, because this will facilitate shared decision-making by the patient and physician regarding the preferred management strategy in the colposcopy clinic.

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MATERIALS AND METHODS

Since 1980, referral cervical smear results, colposcopic impression, histologic findings, and background information of patients referred for colposcopy have been entered into a database. We have assessed all 4,808 patients who underwent an initial colposcopy at the outpatient clinic of the Department of Obstetrics and Gynecology of Radboud University Nijmegen Medical Center between January 1981 and December 2010. Patients were referred to the department because of an abnormal cervical smear result, obtained during population screening, taken opportunistically, or because of cervical complaints. Over a 30-year period, 3,192 (66%) out of a total of 4,808 patients underwent a see-and-treat protocol. These 3,192 patients were analyzed in the current study.

Direct referral indications for colposcopy in The Netherlands are moderate dyskaryosis or worse (equaling high-grade squamous intraepithelial lesion [HSIL]). In borderline or mildly dyskaryotic cases, a cervical smear is repeated after 6 months and again (if negative) after 12 months. When cytology is persistently abnormal, women are referred to the gynecologist where colposcopic examination is performed. Triage using high-risk human papillomavirus (HPV) testing for women with a persistent borderline or mildly dyskaryotic cytology has been recommended in the Dutch guidelines since 2008. Referral for colposcopy is only required if persistence of high-risk HPV is demonstrated. Women can stay in the screening program without referral to the gynecologist if no high-risk HPV infection can be determined.

Cervical smear results were classified according to the Pap terminology with descriptive diagnoses. Since 1996, cervical smear results have been classified according to the CISOE-A classification (Composition, Inflammation, Squamous epithelium, Other and endometrium, Endocervical columnar epithelium, and Adequacy of the smear), which is now used as the standard classification system for cytology in The Netherlands. The CISOE-A classification can easily be translated into Pap classification or the Bethesda System.15,16

Cervical smear results diagnosed as equal to or more severe than moderate dysplasia or moderate atypia were marked as high grade. All other smear results were marked as low grade.

Our main focus was to investigate patients who underwent a see-and-treat protocol at the time and for whom a histology result was registered (n=3,192). In 14 (0.4%) cases, the cervical smear result was not known (Table 1). In 847 cases (26.5%), the colposcopic impression during treatment was not recorded in the database (Table 2). In four cases, neither cervical smear result nor colposcopic impression during treatment was recorded. That left a total of 2,335 women for whom both a cervical smear result and a colposcopic impression were registered.

Table 1
Table 1
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Table 2
Table 2
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The ethical committee of Radboud University Nijmegen Medical Centre stated that the current study did not fall within the purview of the Medical Research Involving Human Subjects Act. Therefore, it was possible to conduct the study without approval by an accredited research ethics committee.

Colposcopic examination is performed as an outpatient procedure at our department. Trained physicians, supervised by an experienced gynecologist, performed all examinations. After application of a 3% acetic acid solution, the transformation zone was examined.17 When the cervical smear result, the colposcopic impression of the lesion, or both was suggestive of a high-grade CIN (CIN 2 or worse), immediate treatment followed (see-and-treat approach). In the case of a low-grade cervical smear result and a low-grade colposcopic impression, no biopsy was taken and no further treatment was given. Follow-up with repeat cervical smears every 6 months was needed in all these patients. Specific circumstances made treatment preferable; eg, expected inadequate follow-up, a pregnancy wish for the near future, or complaints of a symptomatic ectropion.

When treatment was deemed necessary, local anesthesia was applied, and the whole transformation zone was removed using a low-voltage diathermy loop. This procedure is known as large loop excision of the transformation zone. After the procedure, hemostasis was obtained using diathermic coagulation. The CIN grade was determined by the pathologist using the international standard classification. In the case of an inadequate colposcopic examination, defined as an incomplete visualization of the transformation zone, no visualization of the entire lesion, if present, or no correlation between cytologic findings and the colposcopist's impression, diagnostic treatment was needed.

Some patients did not undergo a see-and-treat protocol for various reasons. Some patients preferred a biopsy first instead of treatment with the see-and-treat protocol. Other patients had lesions too large to remove in an outpatient setting or no lesion was seen during colposcopy in case of a high-grade smear result. Furthermore, some patients were too anxious to be treated in the outpatient clinic and therefore the colposcopist chose not to treat these patients in an outpatient setting.

In this study, overtreatment was defined as treatment for no CIN or low-grade CIN (CIN 1) found during final histopathology analysis. We investigated the rate of overtreatment for different subgroups. Subgroups were categorized by referral cervical smear result, colposcopic impression, histopathology results, age, and time of referral. These groups were analyzed separately and combined. For our combined analysis we excluded those patients with no referral cervical smear result, no registered colposcopic impression, or both (n=857).

For statistical analysis we used SPSS 18.0.1. Proportions were compared using χ2 tests. The effect of age on overtreatment was estimated using logistic regression adjusted for the combined effects of initial smear result and colposcopic impression. Two-sided P≤.05 was considered statistically significant.

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RESULTS

From January 1, 1981, to December 31, 2010, a total of 4,808 women were initially referred to our clinic for colposcopic assessment. The mean age was 37 years (standard deviation 9.3 years, range 17–81 years). The referral cervical smear result showed a low-grade squamous intraepithelial lesion in 1,675 (34.8%) cases and HSIL in 3,090 (64.3%) cases. In 82 (2.7%) of HSIL cases, the smear result suggested a carcinoma (Pap 5). Histologic examination revealed 741 (15.4%) cases of no CIN or low-grade CIN and 2,985 (62.1%) cases of high-grade CIN, of which 200 (4.2%) cases of carcinoma (Table 1).

A see-and-treat protocol was used in a total of 3,192 (66%) of 4,808 patients. The mean age of the see-and-treat group was 36 years (standard deviation 8.7 years, range 17–81 years) (Table 1). A total of 78.4% of the women belonged to the age group of the population screening for cervical cancer (aged 30–60 years), 20% were younger than 30 years, and 1.6% exceeded the age-related eligibility for screening. The referral cervical smear result of 646 (20.2%, 95% confidence interval [CI] 18.8–21.7) cases showed low-grade squamous intraepithelial lesion and 2,532 (79.3%, 95% CI 77.8–80.7) cases of HSIL (Table 1). Histologic examination of the 3,192 excised samples revealed 579 cases (18.1%, 95% CI 16.7–19.5) with no CIN or low-grade CIN lesions and 2,613 cases (81.9%, 95% CI 80.6–83.2) with high-grade CIN lesions. We identified 177 cases (5.5%, 95% CI 4.8–6.4) with carcinoma. Based on the definition described in the “Methods” section, 579 (18.1%, 95% CI 16.7–19.5) women were overtreated (Table 2). Histopathology examination of cervical tissue from patients with a high-grade cervical smear result with any colposcopic impression and patients with a high-grade colposcopic impression with any smear result revealed 223 (8.8%, 95% CI 7.8–10.0) and 147 (8.1%, 95% CI 6.9–9.5) cases of no CIN or low-grade CIN, respectively. Women with a high-grade cervical smear result and a high-grade colposcopic impression were overtreated in 70 cases (4.5%, 95% CI 3.5–5.5) (Table 2).

Women aged younger than 40 years had the lowest rates of overtreatment (13.1%, 95% CI 11.7–14.5). With increasing age, the chance of unnecessary treatment rises: 24.2% (95% CI 21.2–27.4, adjusted odds ratio [OR] 1.77) for women aged 40–49 years and 42.2% (95% CI 36.5–47.7, adjusted OR 3.39) for women aged 50 years and older when compared with women aged younger than 40 years. This trend is seen for high-grade and low-grade cervical smear results, high-grade and low-grade colposcopic impression, and these groups combined (Table 3). The number needed to harm for women aged 40–49 and 50 years and older is nine and three, respectively.

Table 3
Table 3
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In 1996, major changes were implemented in the Dutch cervical screening program. First, the CISOE-A classification for cytology was introduced and the use of this classification system increased the efficacy of screening.15 Second, the Dutch screening program changed from a 3-year program for women aged 35–55 years into a 5-year program for women aged 30–60 years. Third, more stringent criteria for cytologic diagnosis of atypical squamous cells of undetermined significance were introduced.18 Therefore, we compared overtreatment rates before and after 1996 as shown in Table 4. Except for a small but significant decrease in overtreatment rates, the group with a high-grade cervical smear result, and a high-grade colposcopic impression (P=.04), no significant differences were found between women referred before and after 1996.

Table 4
Table 4
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DISCUSSION

Since the implementation of the see-and-treat approach in our hospital in 1980, a database has been constructed, which now results in a large, single-institution, case series. This database allowed the current study to describe age influences on the rate of overtreatment.

The overall 18.1% overtreatment rate in the group who underwent a see-and-treat protocol is quite low compared with overtreatment rates reported in other studies.19–21 In previous studies considering a see-and-treat management, a number of strategies was used to assess and treat a patient referred for colposcopy. This is the main reason why overtreatment rates in the literature range from 8.0% to as much as 83.3%.12,17,19,20,22–25 In 1990, Bigrigg and colleagues19 were the first to describe the outcome of a see-and-treat protocol and reported an overtreatment rate of 27.9%.

When a see-and-treat protocol is applied only to those women with a high-grade cervical smear result, the rate of overtreatment decreases dramatically. In the present study, we found 8.8% overtreatment for patients referred with a high-grade smear result, whereas in previous studies, the range of overtreatment varied from 3.0% to 39.4% for high-grade smear results at referral.26,27 Apart from the varying quality of laboratories and screening, a possible explanation for the variation in the rate of overtreatment in the literature is the design of the national screening program for cervical cancer in different countries. In The Netherlands, organized screening is offered to all women aged 30–60 years every 5 years, whereas other countries offer screening to a much wider group with a shorter interval.28 The percentage of abnormal cytologic smear results within these screening programs varies from 1.5% to 8% between countries.28 This may reflect differences in the prevalence of neoplastic lesions or differences in guidelines and cutoff points for referral. It is certainly clear that different rates of abnormal smear results and referral do influence the rate of overtreatment. It is also known that narrowing the screening interval increases the risk of unnecessary treatment.29

In the present study, the rate of overtreatment was lowest (2.8%) when a see-and-treat protocol was applied to women aged younger than 40 years who were referred with a high-grade cervical smear result and showed a high-grade colposcopic impression. This very low overtreatment rate must be considered “best practice” and is comparable to the lowest overtreatment rate reported in the literature. It is even lower than overtreatment rates after a two-step procedure in colposcopy clinics.30–32 The low overtreatment rate in this age group might be the result of a more conservative approach of the colposcopists to the treatment of fertile women, because of the increased risk of preterm birth, low birth weight, and premature rupture of membranes after large loop excision of the transformation zone.11,13

With increasing age, the chance of unnecessary treatment increases (adjusted OR 1.77, number needed to harm nine for women aged 40–49 years and adjusted OR 3.39, number needed to harm three for women aged 50 years and older) when compared with women aged younger than 40 years. Women aged older than 40 years, whether the lesion is high grade or low grade, might be treated more easily and at slighter pretenses than women aged younger than 40 years because fertility is no longer an issue.

Major changes implemented in the Dutch cervical screening program in 1996, as described in the “Results” section, had a great effect on the Dutch screening practice. Except for a small decrease in overtreatment rates in the group with a high-grade cervical smear result and a high-grade colposcopic impression, no significant differences were found between women referred before and after 1996. Only since 2008, high-risk HPV testing for women with a persistent borderline or mildly dyskaryotic cytology has been recommended in the Dutch guidelines. Therefore, we do not expect an effect of this recent change on the data of the current study.

Considerable research has been conducted on patient convenience and clinical and economic aspects of follow-up after an abnormal cervical smear result. A see-and-treat protocol seems to be an efficient policy, because diagnosis and treatment are combined, which results in cost savings for both the clinic and patient.8,33,34 Using a see-and-treat protocol improves patient convenience with only one disruption of the daily schedule and this increases compliance.9

One of the main criticisms of a see-and-treat procedure is the risk of overtreatment. Our study showed that the rate of overtreatment is very low when applied to a specific group of women for whom see-and-treat might be the preferred procedure. Punch biopsies and selective recall may be better for patients more likely to be overtreated, although in some cases, a see-and-treat approach is still justifiable. The results of the current study permit us to counsel patients effectively with regard to overtreatment, allowing patients to be actively involved in the decision-making so they receive care that meets their needs and wishes.

A disadvantage of this study is the lack of colposcopic impressions in 847 cases (26.5%). The largest part of these missing data (668 cases [78.9%]) was not registered in the first 10 years of data collection. These data could not be retrieved. However, the long period of study in a single institution, with prospective registration of all data, makes the outcomes a very reliable reflection of day-to-day practice at the outpatient clinic of the department.

The see-and-treat approach was also used in cases of inadequate colposcopic examination in our clinic. In these cases, we used the see-and-treat approach as a diagnostic treatment, eg, in case of high-grade endocervical cells in the cervical smear result and a normal colposcopic impression. Exact numbers of diagnostic treatment in these cases could not be established but are expected to be low and supposedly have no influence on the overall overtreatment rate.

In conclusion, this study shows that the overtreatment rate is low for patients in all age groups who were referred with a high-grade smear result and subsequently were found to have a high-grade colposcopic impression. We strongly recommend a see-and-treat approach as the preferred management strategy to be adopted for these patients. For patients in all age groups referred with a low-grade smear result and with a low-grade colposcopic impression, conservative management and surveillance with repeated cytology and colposcopy to exclude progression to (micro)invasive cervical cancer should be adopted. In women with either a high-grade smear result or high-grade colposcopic impression, a see-and-treat approach may still be preferred but has higher overtreatment rates. Given the side effects of cervical surgery on pregnancy outcome, young women may benefit from a two-step approach. Older women may prefer a see-and-treat policy.

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