J Am Board Fam Pract: first published as 10.3122/jabfm.10.6.390 on 1 November 1997. Downloaded from Is Cervicography a Useful Diagnostic Test? A Systematic Overview of the Literature jim Nuovo, MD, joy Melnikow, MD, MPH, Brian Hutchison, MD, MS(,~ and Mary Paliescheskey
.Background: The appropriate approach to women with mild dyskaryotic changes on Papanicolaou smear is subject to controversy. Our aim was to assess the usefulness of cervicography as a diagnostic test in detecting cervical cancer or its precursors. Metbods: We undertook an extensive literature search looking for pertinent studies of cervicography pubUshed between 1966 and 1996. EUgible studies included those in which the reference standard (colposcopy) was done on all patients. The following information was calculated: sensitivity, specificity, positive predictive value, negative predictive value, disease prevalence, and Ukelihood ratios. Results: Cervicography has a high false-positive rate. This rate ranged from 8.2 to 61.0 percent (median 42.1 percent) for any dysplasia and 9.8 to 63.4 percent (median 50.6 percent) for high-grade cervical lesions. UkeUhood ratios for a positive test result ranged from 1.0 to 10.6. Likelihood ratios for a negative result ranged from 0.02 to 1.0. Conclusions: The usefuIDess of cervicography is heavily dependent on the approach used to evaluate abnormal findings on a Papanicolaou smear. If a provider typically offers colposcopy to all patients with low-grade cytologic findings on a Papanicolaou smear, cervicography will decrease colposcopy use and allow for detection of cases of high-grade dysplasia missed by the index Papanicolaou smear. If a provider typically uses watchful waiting with repeat Papanicolaou smears for all patients who have low-grade cytologic findings, cervicography will substantially increase the use of colposcopy. Many of these colposcopies will be done as a result of false-positive cervigrams. (J Am Board Fam Pract 1997; 10:390-7.)
The goal of cervical cytology screening is to de ter application of acetic acid. The resulting cervi tect cervical cancer and its precursors. During the gram is then examined by an expert who looks for last 40 years regular screening with a Papanico evidence of pathologic changes consistent with a laou smear has proved to be effective in reducing dysplastic process. If the changes are found, the http://www.jabfm.org/ the morbidity and mortality from this disease. 1 patient is referred for colposcopy and directed Yet despite the success of the Papanicolaou smear, biopsies.3,4 When compared with colposcopy, the there are concerns about its limitations, the most advantages of cervicography are that it is simple to notable of which is the false-negative rate. Al perform, less expensive, and noninvasive. though there is a wide range of reported values Development of a new diagnostic test has par for the false-negative rate of Papanicolaou ticular relevance for detection of cervical cancer smears, even with optimal conditions the false and its precursors. Recently the debate has inten on 24 September 2021 by guest. Protected copyright. negative rate can be as high as 29 percent.2 sified over the appropriate management for New techniques and devices are being investi women with atypical or low-grade cytologic ab gated to address this problem, and cervicography normalities. Management can range from imme is one such method.3,4 The technique of cervicog diate colposcopy to watchful waiting with repeat raphy involves a photograph of the cervix taken af- Papanicolaou smears.5-7 A new diagnostic test such as cervicography can have an impact on both of these strategies. Submitted, revised, 6 March 1997. Before adoption and diffusion of cervicography From the Department of Family Practice, University of Cali become widespread, it is important to review the fornia, Davis ONJM,MP), and the Centre for Health Economics existing evidence on the performance characteris and Policy Analysis, McMaster University, Hamilton, Ontario, tics of this test. Our study reviewed the published Canada (8H). Address reprint requests to Jim Nuovo, MD, De partment of Family Practice, School of Medicine, University of research on cervicography and addressed the fol California, Davis, 2221 Stockton Blvd, Sacramento, CA 95817. lowing question: Is cervicography useful as a pri-
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Table 1. Summary of Baseline Data and Methods of Eligible Studies. Number of Author Year Subjects Study Site Methods Cecchini et a127 1992 606 Colposcopy 606 conset'Utive women referred to clinic, Italy District of Florence Col poscopy Clinic. Atypical Papanicolaou smear (57.6%), CrN I (7.6%), CIN II-III (5.0%), self-referred (29.9%). All women had cervicography at time of colposcopy Jones et a128 1987 236 2 university 236 consecutive referred nonpregnant obstetric women with class II atypia evaluated by gynecology colposcopy and cervicography clinics, USA Kesic et aj29 1993 418 University One-year study of 418 asymptomatic obstetric women as part of a screening program. gynecology Most had never been screened before. clinic, Yugoslavia Class II atypia or greater (8.6%). All had . cytology testing, colposcopy, and cervicography Schauberger et apo (a) 1991 100 Colposcopy Retrospective chart review of 100 women clinic, USA with class II atypia who had undergone colposcopy and cervicography Schauberger et aP! (b) 1991 105 Colposcopy Retrospective chart review of 105 women clinic, USA with active condyloma, history of condyloma, or partner with condyloma, who had undergone colposcopy and cervicography Soutter et aP2 1991 211 ColposcoPI; 211 women undergoing colposcopy had clinic, Eng and simultaneous cervigram. Baseline cytologic abnormalities not recorded Spitzer et aPJ 1987 97 Obstetrics- 97 women with an atypical Papanicolaou ~ecology smear were evaluated by colposcopy and c inic, USA cervicography
CIN - cervical intraepithelial neoplasia. mary screening test, as an adjunct to a screening "colpophotography." Articles were selected that Papanicolaou smear, or as a secondary triage tool reported data from studies in which cervicogra http://www.jabfm.org/ in the detection of cervical cancer and its precur phy was used for cervical cancer screening. The sors? When done concomitantly with a screening reference list of each retrieved report was scanned Papanicolaou smear, cervicography could serve for potential additional studies. A manual search one of two clinical policy objectives: (1) address of the Index Medicus was performed as well. We the false-negative rate problem currentlyencoun contacted the first authors of selected studies and tered with cytology screening; or (2) help distin requested information on any studies that were on 24 September 2021 by guest. Protected copyright. guish those women who have abnormal findings not included in our list of relevant reports. on Papanicolaou smear who should be referred Baseline data were obtained from each report for immediate colposcopy from those for whom retrieved (Table 1). For Papanicolaou smear find follow-up with repeat Papanicolaou smears is ap ings, synonymous terminology for borderline ab propriate. As a secondary triage tool, the objec normalities included atypia and atypical squa tive of cervicography is to determine which mous cells of undetermined significance. For women have atypical or low-grade cytologic ab low-grade lesions, equivalent terminology in normalities that can be safely managed with re cluded mild dyskaryosis, mild dysplasia, class II peat Papanicolaou smears. atypia, low-grade dysplasia, cervical intraepithe lial neoplasia (eIN) grade I, changes consistent Methods with human papillomavirus (HPV) infection, and AMEDLINE search of studies published in Eng low-grade squamous intraepitheliallesion (SIL). lish from 1966 through 1996 was conducted us For high-grade lesions, equivalent terminology ing the following key words: "cervicography" and included moderate or severe dyskaryosis, class III
Cervicography 391 J Am Board Fam Pract: first published as 10.3122/jabfm.10.6.390 on 1 November 1997. Downloaded from
Table 2. Quality Scoring <:riteria and Results for dysplasia or of only high-grade dysplasia. The test ":ligible Studies (n =7). calculations included and then excluded unsatis Studies t"
analysis. vious Papanicolaou smear. In a study by Schau http://www.jabfm.org/ Each eligible report was reviewed using a qual berger et al,31 those who had all active condy ity assessment instrument. The quality assess loma, a history of condyloma, or a partner with ment criteria, adapted from previous works on as condyloma were eligible. The wide differences in sessment of diagnostic test research, are listed in entry criteria and study I->,lrticipant~ lllade mcta 'Table 2.')-11 Two of the authors (fN,]M) indepen analytic techniques inappropriatc.II
dently reviewed each article for quality assess Cervigrams described as unsatisfactory or tech on 24 September 2021 by guest. Protected copyright. ment criteria. Disagreements were discussed, and nically defective ranged from 2.0 to 15.5 percent the final scoring wa~ assigned by consensus. (median = '7.7 percent) among the eligible studies. For each eligible report the percentage of un satisfactory or technically defective cervi grams Quality Assessment and the results of colposcopy (normal, any dyspla Results of the quality assessment scoring are pre sia, low-grade dysplasia, high-grade dysplasia, and sented in Elble 2. No study received a score of cancer) were extracted. Sensitivity, specificity, pos greater than 3 (with a maximum possible score (0). itive predictive value, negative predictive value, disease prevalence, and likelihood ratios for a pos Test Parameters itive test result (true-positive ratelfalse-positive The results of the scnsitivity, specificity, positive rate) and for a negative result (false-negative predictive values, ncgative predictivc values, dis rate/true-negative rate) were calculated. True ease prevalence and likelihood ratios are pre po~itive cervigrarns were defined as those that had sented in 'Elble 3. The values incorporate techni histologic findings on colposcopy of either any cally defective or unsatisfactory cervigrallls ill all
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Table 3. Summary of Cervicography Test Characteristics from Seven Eligible Studies. Likelihood Likelihood Dysplasia False- Ratio, Ratio, Prevalence Positive Ne~ativc Found on Positive Positive N~ative of Predictive Pre( ictive Authors Colposcopy Sensitivity Specificity Rate" Test est' Dysplasiat Value* Value§
Atypia on index Papanicolaou smear Jones Any 90.4 60.4 39.6 2.3 0.44 25.8 44.3 94.7 et aJ2s High grade 100.0 49.4 50.6 2.0 0.02 4.5 8.5 100.0 Schauherger Any 19.4 82.3 17.7 1.1 0.97 36.7 38.9 63.8 et allo High grade 18.2 81.6 18.4 1.0 1.0 11.2 11.1 88.8 Spitzer Any 93.3 39.0 61.0 1.5 0.18 15.5 21.9 96.9 et alB High grade 100.0 36.6 63.4 1.6 0.03 7.2 10.9 100 Colposcopy clinic patients Cecchini An~(a)" 81.8 57.7 42.3 1.9 0.31 28.8 43.9 88.5 et aJ27 (h) , 82.1 43.3 56.4 1.5 0:42 29.2 37.6 85.4 High grade (a)" 95.5 48.1 51.9 1.8 0.08 3.9 6.9 99.6 (h)" 90.5 37.0 63.0 1.4 0.24 3.8 5.4 99.0 Soutter Any 73.0 64.0 36.0 2.0 0.42 29.9 45.5 84.8 et aIl2 Screening population Kesic et aJ29 Any 88.9 81.8 8.2 10.6 0.12 5.8 44.4 99.1 High grade 89.5 90.2 9.8 9.1 0.11 4.8 31.5 99.4 Patients with condyloma Schauherger Any 89.5 58.1 41.9 2.1 0.17 18.1 32.1 96.2 et aill High grade 100.0 53.1 48.9 2.1 0.02 6.7 13.2 100.0 ----.------..• ._--- "1- specificity. tPretest likelihood of dysplasia. *Posttest likelihood of dysplasia if test positive. §Posttest likelihood of no dysplasia if test negative. "In the study by Cecchini et alp a and b represent the results of two different cervicography readers. http://www.jabfm.org/ denominators. There was no substantive differ of any dysplasia and 9.8 to 63.4 percent (median ence in the analysis by inclusion or exclusion of 50.6 percent) for high-grade lesions. Likelihood these cervi grams. ratios for a positive result ranged from 1.0 to 2.3 There is a considerable difference in positive for six of the seven studies. The study by Kesic et predictive value within each of the studies when aF9 represents an outlier, as it had relatively on 24 September 2021 by guest. Protected copyright. comparing the detection of any dysplasia with higher values for most of the test parameters eval high-grade dysplasia. The positive predictive val uated. This study was the only one using cer ues for detection of any dysplasia (median 41.1 vicography as a primary screening test. The nega percent, range 21.9 to 45.5 percent) were greater tive predictive values for most of the studies were than the positive predictive values for detection of high, particularly for high-grade dysplasias (range high-grade dysplasia (median 10.9 percent, range 88.8 to 100 percent). The calculated likelihood 5.4 to 31.5 percent). ratios for a negative test result ranged from 0.12 The difference between the positive predictive to 0.97 for any dysplasia and from 0.02 to 1.0 for value (ie, the posttest likelihood of disease if the high-grade dysplasias. In four of the six studies test results are positive) and disease prevalence reporting both any dysplasia and high-grade dys (ie, the pretest likelihood of disease) was small for plasia,27,28,31,H the likelihood ratio for a negative high-grade lesions. The false-positive rate was result was substantially lower for high-grade le generally high. It ranged from 8.2 to 61.0 percent sions (0.02 to 0.24) than for any lesion (0.18 to (median 42.1 percent) for the histologic finding 0.44).
Cervicography 393 J Am Board Fam Pract: first published as 10.3122/jabfm.10.6.390 on 1 November 1997. Downloaded from
Only one study examined interobserver vari able. 3s The relatively high frequency of l1oJ1diag ability of cervi grams. Cecchini et aJ27 found good nostic histologic findings after colposcopy, ie, interobserver agreement beyond chance using 29.0 to 45.4 percent of colposcopy-directed biop two independent reviewers of cervi grams (kappa sies, is also consistent with this range of false-pos , = 0.(2). itive findings. r.-3H When cervicography is llsed as an adjunct to a Discussion Papanicolaou smear, the impact of a high false Quality ofResearch on Cervicography positive rate would be a high-recall rate for repeat The quality of research on cervicography is gen examinations or excessive referrals for colpo erally poor. Sixteen of the 23 retrieved reports did scopic examination. Although only women with not apply the reference standard of colposcopy to precancerous changes or cancer of the cervix are all test participants. The most common method at risk for a false-negative test result, all women ologic error was to perform colposcopy only on without disease who are screened are at risk for a those participants with positive findings on either false-positive result.H Papanicolaou smear or cervi gram. It has been Cervicography has a high sensitivity (low false well-documented that the properties of a diag negative rate) for high-grade dysplasia. In six of nostic test will be distorted if its results influence the seven studies cervicography had a high sensi whether patients undergo confirmation by a ref tivity (89.5 to 100 percent) for high-grade dyspla erence standard.34 This problem has been de sia. In three of these studies, the sensitivity was scribed as ascertainment, verification, or workup 100 percent. The likelihood ratio for a negative bias. This bias will falsely increase the sensitivity test result ranged from 0.02 to 0.24 for high of the test being evaluated, because the number of grade dysplasia in six of the seven eligible studies. false-negative results is unknown if patients with The percentage of defective or unsatisfactory a negative test result do not receive the reference cervigrams poses a problem for general applica standard test. 34 bility of cervicography. There was a wide range in The findings also indicate that the seven eligi defective or unsatisfactory cervi grams; from 2.0 ble studies did not adequately address nine ac to 15.5 percent. A defective cervigram results cepted methodologic standards for the evaluation from either improper technique or the inability of diagnostic tests. Inadequate appraisal of diag to visualize the transformation zone adequately, a nostic tests in the medical literature has been pre common problem in postmenopausal women.
viously reportedY The study by Spitzer et a133 was the only one to http://www.jabfm.org/ address the issue of cervicography in this group. Cervicography Test Characteristics They found that "cervicography for women over Cervicography has a high false-positive rate. Our age 45 is probably not useful as 8 of 13 cervi grams analysis documents a false-positive rate that were uninterpretable." If cervicography is recom ranged from 8.2 to 61.0 percent (median 42.1 mended as a screening test or triage tool for pa percent) for any dysplasia and 9.8 to 63.4 percent tients with minor cytologic abnormalities, the on 24 September 2021 by guest. Protected copyright. (median 50.6 percent) for high-grade lesions. procedure will be performed by many providers. Similar ranges of false-positive rates are reported It is likely that providers will have a rate of unsat in the studies excluded from the overview. This isfactory cervi grams approaching the upper level problem is not surprising and not without prece of what has been reported (15.5 percent). A sub dent. During colposcopic examination of the stantial number of repeat examinations will have cervix, many different processes in the transfor an impact on the cost effectiveness of this test. mation zone can mask the underlying blood ves sels by focally increasing the cell density. Overlap Cervicography as a Secondary Triage Tool between the acetowhite changes occurs not only The impact of cervicography as a secondary as a result of dysplasia but also as a result of in triage tool depends heavily on the comparison flammation and squamous metaplasia and condy strategy used for evaluating atypical or low-grade loma without dysplasia. It is predictable that dif cytologic findings. It is critical to evaluate diag ferentiation on cervicography of low-grade nostic test characteristics in the context of how dysplasias from these other processes is not reli- the test will influence current practice. The test
394 JABFP Nov.-Dec. 1997 Vol. 10 No.6 J Am Board Fam Pract: first published as 10.3122/jabfm.10.6.390 on 1 November 1997. Downloaded from characteristics delineated in this study show that the two techniques was similar (0.92 and 0.94). cervicography can be useful in ruling out disease. The study included many patients who had never The relatively high negative predictive value and been screened for cervical cancer by any method. low likelihood ratio for a negative result are desir It is likely that inclusion of these patients led to a able characteristics of a triage test. With the ex higher rate of detected high-grade lesions. It will ception of one study, Schauberger et al,30 the be important for future studies to address cer prevalence of high-grade lesions (pretest likeli vicography in previously screened populations. hood of disease) ranges from 3.8 to 7.2 percent, These results suggest that it would be appro whereas the posttest likelihood of a high-grade priate to undertake further studies comparing the lesion after a negative cervi gram ranges from 0.0 clinical and economic efficiency of cervicography to 1.0 percent. with that of cervical cytology as an initial screen Recently published practice guidelines allow ing test. Such a study is currently in progress. for different management strategies to be applied to women with atypical or low-grade cytologic Need for Rigorous Assessment ofNtnIJ TeeImology findings, that is, immediate colposcopy or watch This report 'highlights the importance of rig ful waiting with repeat Papanicolaou smears.5 orously evaluating new technology before its These guidelines seem to reflect practice varia dissemination. As noted by Reid et al,9 "all new tion in the community. The posttest likelihoods diagnostic technologies, before being 'released,' of high-grade lesions associated with a negative (should) receive a standardized assessment, using cervigram might be sufficiently low that clinicians accepted methodological criteria." Improved who currently recommend immediate colposcopy "methodological standards could raise the quality for women with low-grade abnormal cytologic of diagnostic test information, and the careful findings might want to consider a policy of repeat predissemination evaluation of diagnostic tests Papanicolaou smears instead of immediate col could eliminate useless tests before they receive poscopy if the cervigram is negative. For these widespread application." providers, cervicography could be useful as a sec The results of our analysis support these rec ondary triage tool. Offering colposcopy only to ommendations. Given the growing interest in al patients with positive findings on a cervi gram ternative strategies for management of low-grade will decrease the number of colposcopies per cytologic abnormalities and the increasing num formed, and additional cases of high-grade dys ber of providers using cervicography, future stud http://www.jabfm.org/ plasia missed by the index Papanicolaou smear ies on cervicography must employ rigorous might be detected. methodologic standards. For providers who follow up with serial Papan icolaou smears to evaluate low-grade abnormali Conclusions ties, cervicography will result in many false-posi Is cervicography a useful test in the evaluation of tive referrals for colposcopy. Although additional patients for cervical dysplasia? The claims made dysplastic lesions will be detected, whether there on behalf of cervicography are best summarized on 24 September 2021 by guest. Protected copyright. is a clinically meaningful advantage to earlier de by Spitzer et alB: "Because patients are so un tection of such lesions is unclear. Thirty to 50 likely to return for follow-up, we should optimize percent of low-grade lesions will regress, and it is our opportunities for early cancer detection by unlikely that early detection will have an impact using multiple screening techniques where possi on outcome.39-41 For high-grade lesions it is less ble rather than relying on follow-up smears at a clear whether more immediate detection directed later date." The available evidence indicates that by a positive cervi gram will result in improved the potential usefulness of cervicography is heav outcomes. ily dependent on the management strategy cho sen by the provider. Whether patients with minor Cervkograpby tIS lin Initial Screening Test cytologic abnormalities should undergo immedi Only one study addressed cervicography as an ate colposcopy or repeat Papanicolaou smears is initial screening test.29 Cervicography had a not resolved by a cervigram. Additional, well-de higher sensitivity than cervical cytology (0.89 and signed studies are needed to evaluate this new 0.52, respectively) in this study. The specificity of technology as both a screening test and a sec-
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ondary triage test before its appropriate use can I<~ Hertens D, et al. Is tllere a role for cervicography be defined. Such studies must address the defi in the detection of premalignant lesions of thc ccrvix utcri? BrJ Cancer 1994;70:125-8. ciencies of previous research, including verifica 15. Ferris DG, Payne P, Frisch LE, Milner Fll, diPaola tion bias, appropriate selection and description of FM, Petry LJ. Cervicography: adjunctive cervical the population to be studied, the impact of inter cancer screening hy primary care clinicians. J Fam observer variability, technical problems with Pract 1993;37:158-64. cervi gram interpretation, applicability in differ 16. Ferris DG, Payne P, Frisch LE. Cervicography: an ent age and risk groups, and impact on the costs intermediate triage test for the evaluation of cervical of cervical cancer screening. atypia.J Fam Pract 1993;37:463-8. 17. Ferris DG. Cervical carcinoma in situ undetected by Papanicolaou smear but identified by cervicography. 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Ob lomavirus and cervical intraepithelial neoplasia. Aust stet Gynecol Clin North Am 1993;20:13-29. N ZJ Obstet GynaecoI1993;33:176-9. 5. Kurman RJ, Henson DE, Herbst AL, Noller KL, 21. Rehder KE, Blythe JG. Cytology and cervicography Schiffman MH. Interim guidelines for manage compared to cytology alone for human papilloma ment of abnormal cervical cytology. The 1992 N a virus detection. Colposcopy Gynecol Laser Surg tional Cancer Institute Workshop.]AMA 1994;271: 1988;4: 1-7. 1866-9. 22. Reid R, Greenberg MD, Lorincz A, Jenson AB, 6. Prendiville W, Walker P. Every woman with an Laverty CR, Husain M, et a!. Should cervical cyto abnormal cervical smear should not be referred for logic testing be augmented by cervicography or colposcopy: debate. Clin Obstet Gynecol 1995;38: human papillomavirus deoxyribonucleic acid de 592-9. tection? Am J Obstet Gynecol 1991;164(6 Pt I): 7. FlanneIIy G, Kitchener H. 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ABFP Announcement Certificate of Added Qualifications (CAQ) in Geriatric Medicine Examination Date: Wednesday, November 4, 1998 http://www.jabfm.org/
Applications are available after February 1, 1998, and must be postmarked for rerum to the ABFP by July 1, 1998. Requirements for Certification in Geriatric Medicine Requirements for the examination include current certification in family practice; valid, full, and unrestricted licensure in the United States or Canada; and completion of 12 months of clinical train ing in an ACGME-accredited geriatric medicine fellowship program. The examination fee is $750. on 24 September 2021 by guest. Protected copyright. The certificate is time-limited, requiring recertification in 10 years. RESERVE YOUR APPLICATION TODAY
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Cervicography 397