Experience in mass Papanicolaou screening and cytologic observations of teen-age girls CHARLES FIELDS, M.D. t RAYMOND M. RESTIVO, B.S.Ao. MURRAY C. BROWN, M.D.
Chicago, Illinois
This report is based on a seven-year retrospective analysis of computerized data available from the Chicago Board of Health's Cancer Control Section and its Cytology Laboratory. All patients included were medically indigent. The cytologic specimens were obtained by the VCE technique; all Papanicolaou smears were classified with both the numerical and descriptive systems for abnormal cytology. The study cohort was composed of 33,641 teen-age patients through age 19; 58 (1.7/1,000) had abnormal cytology (Class Ill, IV, or V). In Chicago, from 1962 through 1969, approximately 25 per cent of the total patient load were teen-agers under the age of 19 with an extremely low yield of suspect cytology: Class Ill 1.6 per month; Class IV = 0.1 per month; Class V 0.0 per month. The Chicago Board of Health has reduced the number of Papanicolaou smears taken on young women under the age of 19; however, this conceptual approach does not exclude women under age 19 who epidemiologically and/or clinically warrant the implementation of a Papanicolaou smear with the use of Friedell's "biologic age of the cPruix" formula.
INVASIVE CERVICAL carcinoma in the teen-age girl is a rare occurrence. Pollack and Taylor8 stated that despite the occasional occurrence of uterine cancer in young women its presence in those below 20 years of age must be classified as exceedingly rare. Speert 7 said that, "So rare is carcinoma of tbe cervix in minors that such cases constitute gynecologic curiosities." Bowing and McCullough, 6 in reviewing 3,000 invasive carcinomas of the cervix at the Mayo Clinic, found one patient under 20 years of age. Additionally, they reviewed the literature and found only 25 cases since 1862, of carcinoma of the cervix in girls 20 years of age or younger. Koblanck reviewed 6,354 cases of invasive
carcinoma of the cervix and found two cases in patients under 20 years of age. Huffman, 9 in his textbook The Gynecology of Childhood and Adolescence, stated that cervical carcinoma rarely occurs in girls under 17 years old, and, in several thousand patients examined at Children's Memorial Hospital and in private offices, no abnormal cytology was found. Yet he recommends that vaginal cytologic smears should be taken and examined for tumor cells in all adolescents, especially those who are believed to have had coitus. He also reviewed the literature since 1888, and found 32 authentic reports of cervical carcinoma in teen-agers. Despite the rarity of the disease in teen-agers, with the establishment of cytology as an important diagnostic tool, reports began to appear in the literature on cytology in the teen-ager. Papers reflecting extreme divergence of experience have been published. Ferguson' reported that his experience strongly supported the opinion that teen-age female patients should not be denied a cancer smear during a routine pelvic examination. Of 77 positive cytologic smears in girls under 20 years old (a projected rate of 30 per thousand) 10 patients had carcinoma in situ. No cases of invasive carcinoma was found. He concluded that if a girl is old enough to have a vaginal examination she is old enough to have a cervical cytologic examination.
From the Chicago Board of Health, Division of Adult Health and Aging, Cancer Control Section. The State of Illinois Department of Public Health has supported a portion of the Cancer Control Program of the Division of Adult Health and Aging for over a decade. Received for publication May 8, 1975. Accepted May 14, 1975. Reprint requests: Cancer Control Program, Division of Adult Health and Aging, DepartTTUJnt of Health, City of Chicago, Civic Center, Room U-139, Chicago, Illinois 60602. tDeceased.
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Mass cytologic screening of teen-age girls 731
Volume 124 Number 7
Table I. Cytology by classes for groups 19 years old, from the Cancer Control Program, Division of Adult Health and Aging. This retrospective analysis is from january 1, 1962, to May 31, 1969. Class 0 1 2 3 4 5 Race and age unknown
187 3,532 92 6
Total
3,817
Cumulative
Total black patients
Total white patients 49 925 24 1.6
1,386 27 ,Ill 1,275 48 4
29,824
46 909 43 1.6 0.1
Ratet
1,573 30,643 1,367 54 4
45 868 39 1.5 0.1
1,651
47
47 911 41 1.6 0.1
35,292* (33,641 t)
*Including race and age unknown. tExcluding race and age unknown.
Christopherson,3 in 1965, stated that the prevalence of positive cancer smears in teen-age girls examined in his clinic differed extremely from that in Ferguson's report, and he believed it was important to record this conflicting experience and place the relative risk in its proper perspective. In a study of 5,061 girls 19 years of age or less, the results of cell studies revealed neither carcinoma in situ nor invasive carcinoma. A rate of significantly abnormal findings of 1.2 per 1,000 in teen-age girls was observed. In addition, Christopherson quoted Fidler's experience showing a single carcinoma in situ and no invasive carcinoma from 7,17 5 teen-age girls in British Columbia. Christopherson concluded that, "Screening for cervical cancer in teen-agers is not a very rewarding endeavor even in the lower socioeconomic segment of the population. It is important to identify the high risk groups and give priority to effort where it will do most good. Until more data are accumulated, we shall continue to screen all women for cervical cancer regardless of age. At the same time, we will continue to suggest that one should concentrate on the high risk groups with teen-age girls having a very low priority." In two papers ( 1965 and 1970), Kaufman and associates2· 5 reported their observations of 10,246 teen-age patients. In this group there were 296 inconclusive and six positive smears. Three hysterectomies were performed for reasons other than anticipated cervical disease. Their statistics revealed one carcinoma in situ per 2,000 women screened and one per 1,000 with severe dysplasia. Fifty-eight patients were found to have changes suggestive of either severe dysplasia or carcinoma in situ. This represents 5.6 cases per 1,000 girls screened. When 17 5 patients with a cytologic diagnosis of moderate dysplasia were included, 23 patients per 1,000 screened were found to have some degree of significant cervical atypia. They concluded that their findings strongly confirm the advisability of obtaining
cervical-vaginal smears on all gynecologic and obstetric patients regardless of age. This is especially true in the parous and nonvirginal patient. Friedell/ commenting on the need for routinely examining smears from teen-age girls as implied by the report of Ferguson, stated, "Perhaps the best solution would be to consider the biologic age of the cervix in the individual girl, and not the chronologie age of the girl." He further stated, "that perhaps we might simplify the decision-making process for the clinician by using the following equation with KF as the constant: Biologic Age of Cervix = Age of Girl + KF (number of years of active sex life prior to age 20) In this equation Biologic Age of Cervix = Age of Girl plus number of years of active sex life before reaching age 20. This equation is derived by assuming that an active sex life is associated with the development of cervical cancer, and that an average of five (5) years will elapse between the onset of this type of life and the onset of invasive cervical cancer. From available data this five (5) year period would seem to be a rather conservative estimate, and ten (10) years would probably come closer to the truth. Therefore when KF = 5 or more, a smear must be taken. When Kr = less than 5, a smear need not be taken. With this formula it seems likely that cervical smears would be required from a relatively small number of teen-age girls." The ongoing controversy, as evidenced by the aforestated scientific literature excerpts, established the need and set the background for a retrospective analysis of the cytology studies accomplished by the Cancer Control Section of the Chicago Board of Health.
732
Fields, Restivo, and Brown Am.
J.
April 1. 1976 Obstet. Gynecol.
13.6
14
5.57
0 '- · L . . . . - - - - - - - - - - - - - - - - j - - - -
TOTAL O&$EllVAnONS
Fig. I. Rate per 1,000 of Classes 3, 4, and 5 Papanicolaou smears combined, for groups s 19 to 2: 65 years old, from the Cancer Control Program, Division of Adult Health and Aging. This retrospective analysis is from January !, !962, to May 3!, !969.
I RATE/1,000
·~ 2~ 319
~
300
250
~
45-
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~
20-44 YEARS
~
S. /9
YEA~S
"'"1 \ \ '>
150
..,
'"""
I
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AGE GROUP(.YEARS)
i
45- ~65 20-44 :SI9
J
~ \
21
\
----~
1.6
.
5 •.3
0.8 0.1
0.8 0.0 0.0
CLA&5 2 CLA56.31CLASS4 CLASS 5 34 .. 4er 51.5 80 5 4.762. 0 1,367 .54 I 4 NUMBER OF OCCURRENCES
Is-
-ir-
TOTAL OBSE.RVJit.TIO~
5 •.330 87.&95 33,641
'
I I
Fig. 2. Rate per 1,000 of Classes 2, 3, 4, and 5 Papanicolaou smears, for groups :s 19~ 20 ro 44, and 45 to 2: 65 years old, from the Cancer Control Program, Division of Adult Health and Aging. This retrospective analysis is from January 1, 1962, to May 31, 1969.
Methods and material The specimens were obtained by the VCE technique. These smears were obtained from patients artending the Chicago Board of Health Clinics and consisted of Prenatal Clinics, Family Planning Clinics, Model Cities and Federally sponsored Community Health Centers, and other programs. Patients whose cytologic evaluations were found to be abnormal, which in our category included Classes III, IV, and V, were instructed to have: (I) A repeat Papanicolaou smear, (2) treatment and repeat Papanicolaou smear, and (3) referral for a histologic verification. Classification of smears. A variety of authors have written about the desirability of dropping the old
numerical classification system and designating all smears descriptively. In practice, however, it is quite difficuh to undo the famiiiarity of working for two decades with a numerical system. Therefore, we have routinely used both the numerical and descriptive systems to classify abnormal smears. The numerical system is the basis for computer input. Since the onset of the program, we have obtained data regarding treatment and follow-up of patients with abnormal cytology.
Results and follow-up This report is based on a retrospective analysis of computerized data avaiiabie from january i, 1962, through May 31, 1969. All patients included in this
Mass cytologic screening of teen-age girls
Volume 124 Number 7
NUMBER
2015-
CLASS
m
CLASS
Dr
-
NON-WHITE
WHITE
25-
~
1111 8•R£PeAT PAP SMEAR INDICATED E3 C•TREAT AND REPEAT 6\'J D•HISTOL06Y REQUIRED
-
.~
mm
10~
5-
0'-------"'E=l=-wlffijjjjJ......_ 14
IS
16
17
18
19
F3
mmm
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IS
I 1 I ~l l l l 16
17
18
19
AGE
Fig. 3. Cytology distribution of 58 patients with abnormal smears by class, age, and race, from January 1, 1962, to May 9.1
..J.t,
10~0
1-JU;J.
study were considered to be medically indigent, and the population screened originated from the more densely populated and underprivileged socioeconomic clusters within the city of Chicago. The study cohort was composed of 33,641 teen-age patients through age 19; 3,817 were white, and 29,824 were nonwhite. Of this group, 58 patients had abnormal cytology; six white patients had Class III smears, a rate of 1.6 per thousand. Forty-eight nonwhite patients had Class III smears, a rate of 1.6 per thousand. It is interesting to note that the rate per thousand is identical for this age group. The cumulative total Class III smears for white and nonwhite patients was 54, a rate of 1.6 per thousand. Four nonwhite patients were included '.vi thin the Class IV category, or 0.1 per thousand. There were no Class V smears in this study group. The 58 patients represent a combined rate for Classes III and IV of 1.7 per thousand (Table I and Figs. I and 2). Evaluation of the 58 abnormal smears observed in these teen-age patients revealed the data which are detailed in Fig. 3. It is significant that 45 (76 per cent) of these patients were 18 and 19 years old. Repeat smears were requested on all patients. Some were difficult to obtain because the postpartum patients had visited the Chicago Board of Health Clinics for the first time while in the third trimesteL Twenty of the 58 patients were referred to hospitals for histologic verification. The results of these referrals are detailed as follows: Of the 20 patients referred, seven had cytologic studies only; four smears were Class I and three were Class II. Two patients had biopsies only; five had biopsy and conization, three had conization only; three had conization and curettage. These procedures yielded two benign lesions and seven dysplasias. Of the four patients with carcinoma in situ, one had a vaginal hysterectomy with residual carcinoma in situ in the surgicai specimen. She was i8 years old (gravida 6, para 3).
733
Of 38 nonreferred patients, 25 were lost to followup, nine '";ere uncooperative, three \vere treated and had repeat cytology, and one had a smear which reverted to Class I. Of the 58 abnormal cases, 47 (79 per cent) were either pregnant or postpartum. The gravidity and parity of this group are detailed as follows: Of the 58 patients, 47 had a gravidity range of one through six. Of this group of 4 7 patients, 35 had a parity range of one through five. The parity and gravidity for II of the 58 patients were classified as "unknown." One hundred and thirty-nine Papanicolaou smears were recorded for these 58 abnormai cases by the Board of Health Cytology Laboratory and 23 smears were taken by referral hospital cytology laboratories. This is a composite total of 162 cytology smears.
Conclusion and summary When establishing criteria for the implementation of a mass cytology screening program in a specific target population, one of the most important considerations should be age grouping. The Chicago Board of Health has reduced the number of Papanicolaou smears taken on young women under the age of 19. However, this approach does not exclude women under age 19 who epidemiologically and/or clinically warrant the implementation of a Papanicolaou smear. In Chicago, from 1962 through 1969, approximately 25 per cent of the total patient load were teen-agers under the age of 19 vvho 'vere being screened annually in Chicago Board of Health Clinics. These data and our experience with the female teen-age population utilizing the Chicago Board of Health Clinics suggest that our efforts should be concentrated in the higher risk age population for Papanicolaou smear screening. The Chicago experience reinforces the concept that epidemiologic selection of populations to be mass screened is an imperative course of action if fiscal effectiveness and responsibility are considered major objectives. It is obvious that epidemiologic factors such as degree of risk, racial and ethnic medical anitudes, socioeconomic stratification, and other demographic characteristics should be considered as important variables in determining the selective populations for all public health Papanicolaou screening programs. It is our consensus that cervical Papanicolaou screening efforts should be focused on "high-risk" populations. This concept in no way excludes any teen-age girl from having a cervical Papanicolaou smear taken when epidemiologically and/or clinically warranted, with the use of Friedeirs bioiogic age of cervix formula.
734
Fields, Restivo, and Brown
We would like to express grateful appreciation to Eric Oldberg, M.D., President, Chicago Board of Health, Jack Zackler, M.D., Assistant Commissioner of Health, and Edward F. King, R.S .. Assistant Commissioner of Health. We acknowledge the cooperation and support of Mr. Henry Stanton, Director, Registration and Statistical Services, Diana K. Dietz, Chief Cytotechnologist, L. Steven Medgyesy, M.D., and Bashir Khan, M.D., Pathologists, and the staff of the
April I. 1976 Am. J Obstet. Gvn<'col.
Chicago Board of Health, Cancer Control ProgramCytology Laboratory. We also gratefully express our appreciation for the preparation of illustrations and tables to Thomas Whipple, Sidney Stern, Vincent Saunders, and Jack Skillman. We extend a special note of thanks to Donald Bratkovic, Editorial Consultant, and to our key stenographic personneL Gail Pacelli and Eva Smolin, who made this report a realitv with dedicated labor.
REFERENCES I. Ferguson. J. H.: Positive cancer smears in teenage girls. .J. A.M. A. 178: 365, 1961. 2. Kaufman, R. H., Spjut, H. J., and Carrig, S.: Cervicovaginal cytology in the teenage patient, A.S.C.P .. Acta Cytol. 9: 314, 1965. 3. Christopherson, W. M.: The risk of cervical cancer in teen-aged girls, J. A. M. A. 194: 176, 1965. 4. Friedell, G. H.: Cancer of the cervix-A selective review, Pathol. Ann. 1: 48, 1966. 5. Kaufman. R. H., Burmeister, R. E., and Spjut, H. J.: Cervical cytology in the teen-age patient, AM. J. OssTET. GYNECOL. 108: 515. 1970.
6. Bowing, H. H., and McCullough, ]. A. L.: Carcinoma of the cervic uteri in childhood and adolescence, Am . .J. Roentgenol. 45: 819, 1941. 7. Speert, H.: Cervical carcinoma in young girls, AM . .J. 0BSTET. GYNECOL. 54: 982, 1947. 8. Pollack, R. S.. and Taylor, H. C .. Jr.: Carcinoma of the cervix during the two decades of life, AM. J. 0BSTET. GYNECOL. 53:135,1947. 9. Huffman, J. W.: The Gynecology of Childhood and Adolescence, Philadelphia, 1968, W. B. Saunders Companv.