 |
|
Characteristics and Quality of Papanicolaou Smears Obtained by Primary Care Clinicians Using a Single Commercial Laboratory
Peter Curtis, MD;
Melanie Mintzer, MD;
Daphne Morrell, MSPH;
Jacqueline C. Resnick, BS;
Selinde Hendrix, BA;
Bahjat F. Qaqish, PhD
Arch Fam Med. 1999;8:407-413.
ABSTRACT
| |
Background Few data are available on factors associated with the quality of Papanicolaou smears performed in primary care.
Objective To identify the patterns and proficiency of cervical cancer screening among different primary care specialties.
Materials and Methods Clinical and cytologic data from 21,833 Papanicolaou smears, submitted to a single large commercial laboratory by 176 clinicians during a 7-month period, were correlated with individual clinician and specialty characteristics according to indexes of specimen quality.
Results Obstetrician-gynecologists, nurse practitioners, and physician assistants provided screening to a younger population of women compared with family physicians, internists, and general practitioners. Factors positively associated with a greater probability of a "satisfactory" smear or the presence of endocervical cells (as a marker of adequate sampling) were increasing patient age, use of the cytobrush, and the specialty of the obstetrician-gynecologist. Satisfactory smears were not associated with any increased identification of cytologic abnormalities compared with "limited" smears. In contrast, smears with endocervical cells showed a higher proportion of abnormalities compared with specimens without such cells.
Conclusions Differences in the performance of obtaining Papanicolaou smears exist between primary care specialties, but need further clarification. The use of the cytobrush and the presence of endocervical cells are criteria that reflect clinician proficiency more realistically than the laboratory criterion of satisfactory smear.
INTRODUCTION
ENSURING THE QUALITY of cervical cancer screening is a complicated process, involving issues of access and cost for the patient, a series of procedural and technical steps in obtaining and interpreting the smear, and the effective reporting of the result to clinician and patient.1-3
During the past few years, improvement in the quality of Papanicolaou (Pap) smears has been achieved through the implementation of national standards in laboratory processing and interpretation, widespread acceptance of the Bethesda system for cytologic reporting, the development of better sampling tools, and, more recently, the use of computer-assisted cell pattern recognition to rescreen slides.4-7
Studies8-12 on the quality of cervical cancer screening performed by primary care clinicians have been directed mainly toward compliance with recommended screening intervals. There are few data on sampling proficiency by different primary care disciplines other than studies3, 6, 13-17 on the effectiveness of the new sampling tools in harvesting endocervical cells. Ensuring optimal sampling and preparation of the Pap smear should be a major quality target in any screening program.
As part of a 4-year National Cancer Institute–sponsored research study on clinician performance and cervical cancer screening, we examined the performance of 176 clinicians in primary care practice in obtaining a Pap smear, using a single laboratory. Previous analysis of aggregated data of all clinicians using this laboratory had indicated an overall "satisfactory" Pap smear rate of 65%, a figure below reported norms.2, 14-15,17-18 We report data collected during a 7-month baseline period in 1993, before the subsequent implementation of an intervention to improve clinician performance by individualized feedback.
MATERIALS AND METHODS
In 1992, all clinicians who routinely used the same commercial laboratory for cervical cytologic screening and who had submitted at least 30 Pap smears during the previous 12 months were asked to participate in a quality assurance project for cervical cancer screening. The criterion of 30 Pap smears was selected because (1) this was the minimum number needed to show an intervention effect of at least 10%, (2) this number was a reasonable reflection of cervical cancer screening as an integral part of practice, and (3) this was judged an adequate number of smears on which to provide valid feedback during the intervention. Clinicians were informed that the laboratory would be testing Pap smear reporting formats as part of the project, and they might, therefore, receive a laboratory report that was different from the usual style. Of 465 clinicians contacted, 186 (40.0%), consisting of family physicians, general practitioners, obstetrician-gynecologists, internists, nurse practitioners, and physician assistants, consented to participate in the study. Confidentiality and anonymity were maintained and supported by a Federal Certificate of Confidentiality, and the study was approved by the Committee on the Protection of the Rights of Human Subjects of the School of Medicine at the University of North Carolina at Chapel Hill.
The cytology laboratory provided information associated with each Pap smear performed by participating clinicians, including universal physician identification number; clinician name, address, and telephone number; clinical data, including patient age, reproductive status, hormonal therapy status, menopause status, hysterectomy status, sampling methods, and previous cytologic results; interpretation of Pap smear adequacy; endocervical cell counts; and cytologic findings.
Because of the recent introduction by the Bethesda system of specific adequacy assessment, the cytotechnologists at the laboratory were specially trained to evaluate Pap smear adequacy to ensure uniform Pap smear interpretation.5 This was in addition to usual quality assurance procedures dictated by national laboratory standards and the Clinical Laboratory Improvement Act Amendment regulations.4, 17 After assigning standardized explanatory computer codes to describe the technical adequacy of smears, cytotechnologists determined the overall quality of each Pap smear using criteria based on the new Bethesda system recommendations.5 These were "satisfactory," "satisfactory with limitations," and "unsatisfactory." However, more rigorous criteria were used for endocervical cells, requiring a minimum of 25 for a satisfactory smear, compared with 10 cells reported in the Bethesda guidelines.5, 19
Limited and unsatisfactory categories comprised either sampling (clinician dependent) and/or preparation (clinician or nurse dependent) errors identified and coded by the cytotechnologist. However, a satisfactory interpretation could be made despite the presence of limiting factors in certain clinical situations, such as severe atrophy in women undergoing menopause.5 Based on published criteria,3, 6, 15, 17 clinicians whose proportion of satisfactory smears was below 60% during the entire 7-month period were judged to have low proficiency. Abnormal cytologic results consisted of squamous intraepithelial lesions categorized into either low- or high-grade lesions.
Shortly before the study started, the cytology laboratory had disseminated to all clinicians performing Pap smears a description of the Bethesda terminology and criteria for Pap smear adequacy, as well as instructions on optimal sampling techniques.5 The cytobrush was offered to clinicians, on request, at no extra cost.
After recruitment into the study was completed, and during the data collection period, clinicians received no further communication regarding the project.
A conceptual model of factors affecting Pap smear adequacy was constructed (Figure 1). We assumed there would be only small variability in the laboratory factors (based on the special training of cytotechnologists and previously reported3, 16 low error rates). The clinicians obtaining the Pap smears were not observed, so the proportions of sampling and preparation errors were assumed to be a proxy for their technical skills. However, smear preparation might include assistance in specimen fixation by an assistant or a chaperone.
|
|
|
|
Factors affecting Papanicolaou smear adequacy.
|
|
|
Using a computer system (SAS; SAS Institute Inc, Cary, NC) for data management, we report frequency and comparison statistics on patterns of Pap smear testing by specialty, sex, years in practice, and cervical sampling technique. Using logistic regression, with satisfactory smears and the presence of endocervical cells as dependent variables, we assessed which factors, such as specialty, age of patient, sex of clinician, years in practice, and use of cytobrush, contributed to achieving a satisfactory Pap smear or a smear with endocervical cells present. Exchangeable correlation was used as the working correlation structure. Intracluster correlation (within-clinician and within-practice similarities in obtaining Pap smears) was taken into account for descriptive and logistic statistics using the generalized estimation equations approach.20 In addition, we assessed the probability (odds ratios [ORs]) with which either a satisfactory smear or the presence of endocervical cells would detect abnormal cytologic results (low- and high-grade squamous intraepithelial lesions).
RESULTS
The original study population included 186 office-based primary care providers (146 physicians and 40 nurse practitioners or physician assistants). Most (75.1%) were located in North Carolina, while 24.9% practiced in neighboring states. The laboratory used by these clinicians was a major provider of cytologic services to health professionals in the southeast region of the country. Ten providers were excluded from the present analysis because they did not regularly submit Pap smears to the laboratory throughout the study period. A total of 21,833 Pap smears were obtained by the study population during the 7-month baseline period. Table 1 shows the specialty distribution of the study population (n=176) compared with the 465 eligible clinicians using the laboratory originally and with 5181 office-based clinicians in North Carolina of the same disciplines.21 There was some overrepresentation of internists and underrepresentation of obstetrician-gynecologists in the study group compared with the eligible population. Nurse practitioners or physician assistants and family physicians or general practitioners were overrepresented relative to their numbers among North Carolina clinicians.
|
|
|
|
Table 1. Comparison of the Study Population With Eligible Clinicians Using the Same Laboratory and Primary Care Clinicians in North Carolina*
|
|
|
The proportion of female clinicians was similar among all the specialty groups, except for nurse practitioners, who were all women, and general practitioners, who were all men. More than half (60.8%) of the clinicians had been in practice for 10 years or longer. Female clinicians were more likely to have practiced for 10 years or less compared with male clinicians (P<.001).
SCREENING ACTIVITY OF CLINICIANS
Obstetrician-gynecologists performed Pap smears at an average rate of 67 per month compared with much lower rates (P<.001) in the other disciplines (Table 2). Overall, 94 clinicians (53.4%) performed less than 10 Pap smears per month, and 22 (12.5%) performed 30 or more smears per month.
|
|
|
|
Table 2. Provider Specialty and Characteristics of Screening Activity (N = 21,833 Papanicolaou Smears)
|
|
|
Just more than one third of all Pap smears were performed on women who were no longer reproductive and had either undergone a hysterectomy (16.6%) or were undergoing menopause (20.4%). Family physicians, general practitioners, and internists performed significantly more Pap smears on women undergoing menopause (P<.001) or on women who had undergone a hysterectomy (P<.001) than the other clinician groups, and significantly fewer on women in the reproductive years (pregnant and other hormonal categories) (P<.001). Close to 50% of Pap smears obtained by family physicians, general practitioners, and internists involved patients older than 50 years compared with less than 20% by the other clinician groups (P<.001). Provider sex (P=.30), years in practice (P=.12), and use of the cytobrush (P=.40) had no significant relationship to the number of Pap smears performed. More female clinicians (95.0%) used the cytobrush than male clinicians (82.7%) (P=.03). Of the clinicians using the cytobrush, 71.8% used it in combination with the spatula to scrape the ectocervix. The highest users of the cytobrush were physician assistants (98.3%), obstetrician-gynecologists (85.1%), and nurse practitioners (75.0%), with less use by family physicians (71.1%) and internists (47.1%).
QUALITY OF PAP SMEARS
The overall proportion of satisfactory smears was 71.8%, but ranged from 25% to 100% for individual clinicians. During the 7-month period, 30 clinicians (17.0%) had satisfactory slides in less than 60% of their Pap smears. All specialties were evenly represented in the "low" performance group. Nurse practitioners showed the highest percentage of satisfactory smears (892 [77.8%] of 1147), while general practitioners (237 [61.6%] of 385) had the lowest proportion (P<.02) . There was no correlation between the frequency of performing Pap smears and the proportion of satisfactory smears.
Sampling error (such as a lack of endocervical or metaplastic cells) was the most common reason for limitation of adequacy, occurring in 83.9% of "limited for interpretation" smears. Sampling error caused by vaginal infection or inflammation occurred among clinician groups in the following proportions (excluding the slides of patients who had undergone a hysterectomy): obstetrician-gynecologists, 15.1%; family physicians, 13.9%; physician assistants, 13.4%; internists, 12.4%; and nurse practitioners, 10.1%. Fixation error occurred in only 4% of limited quality Pap smears. Excluding patients who had undergone a hysterectomy, endocervical cells were noted in 49.3% of limited smears and 90.0% of satisfactory smears (P=.02). Although the presence of endocervical cells was reported in more than 80% of women younger than 50 years, this proportion (excluding smears from women who had undergone a hysterectomy) declined for the 50- to 59-year-old group to 73.4%, and for the 60- to 69-year-old group to 59.6%. Endocervical cells were reported in 60.1% of Pap smears obtained by internists compared with more than 80% for nurse practitioners, physician assistants, and obstetrician-gynecologists (P=.009) (Table 2). Family physicians obtained endocervical cells in 74.5% of their smears.
Smears obtained by obstetrician-gynecologist, general practitioner, and physician assistant groups each showed significantly (P<.001) (OR, 3.2; 95% confidence interval [CI], 1.8-5.9) higher frequencies of cytologic abnormalities than those obtained by family physicians, internists, or nurse practitioners (Table 2). During the study period, cytologic abnormalities were found in 0.23% of all smears from women undergoing or past menopause and in 1.6% of all smears from women in the reproductive phase.
To evaluate the correlation between the quality of the Pap smear and the likelihood of identifying abnormalities, we analyzed the relationship between the frequency of abnormalities and the overall quality of smears in the satisfactory and limited categories (Table 3). Unsatisfactory smears were excluded from this analysis because they were not interpreted by the laboratory that routinely requested a second specimen from the clinician. No difference was found between smears reported as either satisfactory or limited in the proportions of cytologic abnormalities detected by the laboratory.
|
|
|
|
Table 3. Proportions of Abnormal Papanicolaou Smears Associated With Adequacy Assessment (N = 21,833)
|
|
|
After excluding the potentially confounding effects of smears from women who had undergone a hysterectomy (usually reported as satisfactory, and with rare incidence of abnormalities) and smears from women who were undergoing or past menopause (often reported as satisfactory despite scanty cellular elements), there remained for analysis 13,863 smears from "reproductive" women. Again, no difference in the proportion of cytologic abnormalities was found between satisfactory and limited quality smears. A satisfactory smear did not convey any advantage in detecting an abnormality compared with a smear reported as limited (Table 3).
When analyzing specific quality factors subsumed under the global adequacy categories (satisfactory, limited, or unsatisfactory), the presence or absence of sampling problems had no effect on the rate of detecting abnormalities. On the other hand, the occurrence of smear preparation problems was positively associated with the detection of abnormal cells. Similarly, the presence of endocervical cells was positively associated with the detection of abnormal cells in all women with an intact cervix.
Using the performance of obstetrician-gynecologists as the standard, with satisfactory smear as the dependent variable, multivariate logistic regression was undertaken, including the variables of specialty, years in practice, clinician sex, use of the cytobrush, patient age, hormonal status, and the presence of hysterectomy or menopause. The only variables positively associated with a higher probability of a satisfactory smear were use of the cytobrush by the clinician (OR,1.6; 95% CI, 1.1-2.2) (P=.02), older patient age (OR, 1.1; 95% CI, 1.0-1.1) (P<.001), or having undergone a hysterectomy (OR, 4.1; 95% CI, 3.5-4.9) (P=.001). Pregnancy was negatively associated with a satisfactory smear (OR, 0.4; 95% CI, 0.3-0.5) (P<.001).
However, it was apparent that the dependent variable describing the adequacy of the smear as satisfactory for interpretation was confounded by the smears obtained from women who had undergone a hysterectomy, which could not yield endocervical and ectocervical cells usually found in other Pap smears. In addition, the small numbers of Pap smears performed by nurse practitioners, physician assistants, and general practitioners could not be incorporated meaningfully into the logistic model. Therefore, after excluding smears obtained from women who had undergone a hysterectomy and clinicians performing only small numbers of Pap smears, we compared obstetrician-gynecologists with family practice and internal medicine groups using either "satisfactory" or "presence of endocervical cells" as dependent variables, adjusting for sex, use of cytobrush recorded for each smear and reported in the clinician questionnaire, years in practice, patient age, and pregnancy status (Table 4).
|
|
|
|
Table 4. Selected Clinician and Patient Characteristics Associated With a "Satisfactory" Papanicolaou Smear and the Presence of Endocervical Cells (N = 16,070)*
|
|
|
For these clinician groups, use of the cytobrush was positively associated with a satisfactory smear. Pregnancy was negatively associated. Compared with obstetrician-gynecologists, family physicians and internists were less likely to obtain a satisfactory smear. The regression model was repeated for the dependent variable (presence of endocervical cells), and the same differences between the clinician groups became even more marked (Table 4). Increasing patient age was positively associated with a satisfactory smear and negatively associated with the presence of endocervical cells.
COMMENT
As might be expected, obstetrician-gynecologists, nurse practitioners, and physician assistants provided cervical cancer screening to a relatively young population of women compared with the other office-based clinician groups. Just less than half of all Pap smears in the 7-month study were obtained by obstetrician-gynecologists, and just less than a third by family physicians, compared with national data reporting that 71.6% of Pap smears are collected by obstetrician-gynecologists.10 This translated into an average of 67 Pap smears per month for each obstetrician-gynecologist and approximately 12 per month for each family physician.
Even after adjusting for provider and patient variables, obstetrician-gynecologists obtained more adequate smears using the criteria of either satisfactory for interpretation or endocervical cells present than family physicians, who, in turn, performed somewhat better than internists (Table 4). Similar differences have been suggested by 2 other studies.22-23 This may be the result of greater experience or better overall training and knowledge among obstetrician-gynecologists. Our data showed a significant (P=.001) reduction in cellular harvesting from the cervix with increasing patient age, yet studies5, 12-13 of the effectiveness of the cytobrush show that age is not usually an adverse factor in obtaining a sample if the instrument is used appropriately and the smear is not severely atrophic.
In addition to differences in specialty performance, there were low performers in each of the clinician groups. Laboratory identification of these clinicians for remediation would be feasible provided certain circumstances prevailed. These include (1) a method for tracking individuals (and not just physicians) rather than just the practice group, (2) implementation of a regular and frequent summative reporting mechanism describing adequacy patterns and the proportion of smears with adequate endocervical cells, (3) practice stability of at least 12 months for clinicians using the laboratory, (4) acceptable limits of variability in the laboratory evaluation of Pap smear adequacy, (5) confidentiality of the data, and (6) acceptance by clinicians and the laboratory that remedial education could be triggered by performance data. Although there is some evidence that feedback on Pap smear performance leads to some improvement in academic settings or in population-based cervical screening systems, few data exist to support its general value for primary care practice.24-26
The frequency of cytologic abnormalities (squamous intraepithelial lesions) varied between some specialties. These differences were not related to the presence of inflammatory changes on the smear. The younger patient age group and the likelihood of receiving referrals from other clinicians were probable factors contributing to the higher proportion of abnormalities detected by obstetrician-gynecologists. However, it was not possible to correlate performance of the Pap test and its direct effect on identifying abnormalities from data in this study.
The frequency of identifying abnormalities was unrelated to the overall quality of Pap smears using the adequacy criteria of the Bethesda system, even when adjusting for hysterectomy and menopause status. However, our data did confirm the findings of other researchers13, 15, 23 that the presence of endocervical cells was positively associated with cytologic abnormalities. We conclude that the presence of endocervical cells in a Pap smear is a valid indicator of adequacy and clinician performance. We also confirmed the findings by Buntinx and Browers15 that Pap smear preparation errors (particularly air drying) were significantly (P=.01) associated with cytologic abnormalities. The proposed reason for this paradoxical association is that air drying can cause cells to appear abnormal.
Managed care organizations are beginning to use the reporting of cervical screening rates and Pap smear adequacy as a performance indicator of care for their patients (S. W. Warburton, MD, oral communication, 1994).27 Are these process measures of cervical cancer screening reasonable? It seems that the use of the cytobrush in combination with the spatula, in women in the reproductive phase with an intact cervix, is clearly an indicator of quality since it improves cervical cell harvesting and greater detection of abnormalities.15, 28-29 However, the use of any stated proportion of either satisfactory or inadequate smears as an indicator of effective cervical cancer prevention is confounded by the routine incorporation into this measure of atrophic smears and smears obtained from women who had undergone a hysterectomy and, therefore, should not be used as a performance measure unless adjusted for reproductive status and patient age.30
Although this study is limited by its regionality and some potential biases in the representativeness of the study group compared with all eligible clinicians using the laboratory, to our knowledge, there are no other studies against which this combination of clinician groups, patient population, and Pap smear analysis can be compared.
There is evidence that "performance" or "report card" comparisons in managed care settings and between specialties are on the increase, and there is considerable variation in health care provided to women.31-35 There is also competitive marketing of cervical screening services that uses quality indicators to sell the product.36 Cervical screening offers accessible data for quality measurement from medical record, billing, and laboratory systems, which, on first glance, should provide a fairly straightforward reflection of proficiency. However, developing performance profiles for clinicians involved in cervical cancer screening must be done carefully and with a clear sense of the various factors that can potentially confound the findings and lead to erroneous conclusions.27
AUTHOR INFORMATION
Accepted for publication September 8, 1998.
This study was supported by grant 5-R18-CA52748 from the National Cancer Institute, Bethesda, Md (Drs Curtis and Mintzer).
We thank all the clinicians who participated in the study for their cooperation and support; Tiea Kesler, CT, and Darlene Butler, CT, supervisors of the Cytology Unit, LABCORP, Burlington, NC, for their close collaboration; management and staff at LABCORP (previously Roche Biomedical Laboratories, Inc), Burlington, NC; and Wesley Fowler, MD, and Richard Shermer, MD, for providing valuable advice.
Corresponding author: Peter Curtis, MD, Department of Family Medicine, Campus Box 7595, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514 (e-mail: fmcurtis{at}med.unc.edu).
From the Department of Family Medicine (Drs Curtis and Mintzer); the Departments of Maternal and Child Health (Mss Morrell and Hendrix) and Biostatistics (Dr Qaqish), School of Public Health; and the Office of the Vice Provost for Graduate Studies and Research (Ms Resnick), University of North Carolina at Chapel Hill.
REFERENCES
| |
1. Garlinghouse CJ. Ensuring quality. Cancer. 1993;72:1119-1124.
FULL TEXT
|
ISI
| PUBMED
2. Shingleton HM, Patrick RL, Johnson WIN, Smith RA. The current status of the Papanicolaou smear. CA Cancer J Clin. 1995;45:305-320.
ABSTRACT
3. Curtis P, Mintzer M, Resnick JC, Morrell D, Hendrix S, Qaqish B. The quality of Pap smears: a primary care perspective. Am J Med Qual. 1996;11:11-18.
4. Medicare, Clinical Laboratory Improvement Amendments of 1988: final rule, 57 Federal Register 7001 (1992).
5. Kurman RJ, Solomon D. The Bethesda System for Reporting Cervical/Vaginal Cytologic Diagnoses. New York, NY: Springer-Verlag NY Inc; 1993.
6. Boon M, Guillond J, Rectveld W. Analysis of five sampling methods for the preparation of cervical smears. Acta Cytol. 1989;33:843-848.
ISI
| PUBMED
7. Koss LG, Lin E, Schreiber K, Elgert P, Margo L. Evaluation of the PAPNET cytologic screening system for quality control of cervical smears. Am J Clin Pathol. 1994;101:220-229.
ISI
| PUBMED
8. Hall JA, Palmer RH, Orav EJ, Hargraves JL, Wright EA, Louis TA. Performance quality, gender, and professional role: a study of physicians and non-physicians in 16 ambulatory care practices. Med Care. 1990;28:489-501.
ISI
| PUBMED
9. Carney PA, Dietrich AJ, Freeman DH, Mott LA. The periodic health examination provided to asymptomatic older women: an assessment using standardized patients. Ann Intern Med. 1993;119:129-135.
FREE FULL TEXT
10. Franks P, Clancy CM. Physician gender bias in clinical decision making: screening for cancer in primary care. Med Care. 1993;31:213-218.
ISI
| PUBMED
11. Osborn E, Bird J, McPhee S, Rodnick J, Fordham D. Cancer screening by primary care physicians: can we explain the differences? J Fam Pract. 1991;32:465-471.
ISI
| PUBMED
12. Goldman DA, Simpson DM. Survey of El Paso physicians' breast and cervical cancer screening attitudes and practices. J Community Health. 1994;19:75-85.
FULL TEXT
| PUBMED
13. Murata PJ, Johnson RA, McNicoll KE. Controlled evaluation of implementing the cytobrush technique to improve Papanicolaou smear quality. Obstet Gynecol. 1990;75:690-695.
ISI
| PUBMED
14. Germain M, Heaton R, Erickson D, Henry M, Nash J, O'Connor D. A comparison of the three most common Papanicolaou smear collection techniques. Obstet Gynecol. 1994;84:168-173.
ISI
| PUBMED
15. Buntinx F, Browers M. Relation between sampling device and detection of abnormality in cervical smears: a meta-analysis of randomized and quasi-randomized studies. BMJ. 1996;313:1285-1290.
FREE FULL TEXT
16. Van der Graaf Y, Voojis GP, Guillaard HLJ, et al. Screening errors in cervical cytology. Acta Cytol. 1987;31:434-435.
ISI
| PUBMED
17. Council on Scientific Affairs, American Medical Association. Quality assurance for cervical cytology: the Papanicolaou smear. JAMA. 1989;262:1672-1679.
FREE FULL TEXT
18. Morrell D, Curtis P, Mintzer M, Resnick JC, Hendrix S, Qaqish BF. Perceptions and opinions on the performance of Pap smears: a survey of clinicians using a commercial laboratory. Am J Prev Med. 1996;12:271-276.
ISI
| PUBMED
19. Dotters D, Carney C, Droegmuller W. Nylon brush improves collection of cervical cytologic specimens. Am J Obstet Gynecol. 1988;159:814-819.
ISI
| PUBMED
20. Liang KY, Zegar SL. Longitudinal data analysis using generalized linear models. Biometrika. 1986;73:13-22.
FREE FULL TEXT
21. Health Services Research Center Data Source: Sheps Center for Health Services Research Chapel Hill: University of North Carolina; 1993.
22. Klassan AC, Celentano DD, Brookmeyer R. Variation in the duration of protection given by screening using the Pap test for cervical cancer. J Clin Epidemiol. 1989;42:1003-1011.
FULL TEXT
|
ISI
| PUBMED
23. Buntinx F, Knotterus JA, Crebolder HFJM, Essed GGM. Afnamekwaliteit van cervixuitsrijkjes: een beschrijvend onderzoek. Huis Weten. 1991;34:457-461.
24. Curtis P, Skinner B, Varenholt JJ, Addison L, Resnick J, Kebede M. Papanicolaou smear quality assurance: providing feedback to physicians. J Fam Pract. 1993;36:309-312.
ISI
| PUBMED
25. Pachciarz JA, Abbott MI, Gorman B, Henneman CE, Kuhl M. Continuous quality improvement of Pap smears in an ambulatory care facility. Qual Rev Bull. July 1992:229-235.
26. Buntinx F, Knotterus JA, Crebolder HFJM, Seegers T, Essed GGM, Schouten H. Does feedback improve the quality of cervical smears? a randomized controlled trial. Br J Gen Pract. 1993;43:194-198.
ISI
| PUBMED
27. Epstein A. Performance reports on quality: prototypes, problems and prospects [Sounding Board]. N Engl J Med. 1995;333:57-61.
FREE FULL TEXT
28. Buntinx F, Knotterus JA, Crebholder HFJM, et al. Relation between quality of cervical smears and probability of abnormal results. BMJ. 1992;304:1224.
29. Luzzato R, Boon ME. Contribution of the endocervical cytobrush sample to the diagnosis of cervical lesions. Acta Cytol. 1996;40:1143-1147.
ISI
| PUBMED
30. Dey P, Collins S, Desai M, et al. Adequacy of cytology sampling with the Cervex brush and the Aylesbury spatula: a population based randomized controlled trial. BMJ. 1996;313:721-723.
FREE FULL TEXT
31. Harris JM. Papanicolaou smear recommendations, patient complaints, and patient satisfaction in managed care medical organizations. Med Care. 1995;33:272-279.
FULL TEXT
|
ISI
| PUBMED
32. Brook RH, Kamberg CJ, McGlyn EA. Health system reform and quality. JAMA. 1996;276:476-480.
FREE FULL TEXT
33. Kassirer JP. The use and abuse of practice profiles. N Engl J Med. 1994;330:634-636.
FREE FULL TEXT
34. Dauphinee WD. Assessing clinical performance: where do we stand and what might we expect? JAMA. 1995;274:741-743.
FREE FULL TEXT
35. The smart Pap: how to wage a successful "smear" campaign to improve the accuracy of your results. Prevention. October 1966:82-85, 155-159.
36. Bartman BA, Weiss KB. Women's primary care in the United States: a study of practice variation among physician specialties. J Womens Health. 1993;2:261-269.
RELATED ARTICLES
The Archives of Family Medicine Continuing Medical Education Program
Arch Fam Med. 1999;8(5):383-385.
FULL TEXT
Quality Papanicolaou Smears
Marjorie A. Bowman
Arch Fam Med. 1999;8(5):413.
FULL TEXT
|
