CERVIX CANCER CONTROL IN LOUISVILLE, KENTUCKY

WILLIAM M. CHRISTOPHERSON, MD,* WINIFRED M. MENDEZ, RN, BS,f ELIZABETH M. AHU JA, MSc,+ FRANK E. LUNDIN, JR., MD, DRPH,+ AND

JAMES E. PARKER, MD"

The results of 12 years of mass cytologic screening of a community for protec- tion from uterine cancer are reported, and the effects upon incidence rates of the various component cancers are analyzed. A preceding 3-year period during which no screening was performed was used to calculate the expected rates. Total cancers of the uterus, including carcinoma in-situ, had an average annual rate of 125.5 per 100,000 women 20 years of age and older during the 15-year period. During the last 3-year period, carcinoma of the cervix was diagnosed a t an earlier stage, and the rates decreased by one third. Carcinoma in-situ in- creased in proportion to screening activity. There was an increase in the rate for endometrial carcinoma. The greatest response to screening was in women under 50 years of age. This group showed the greatest decrease in rates and was, for the most part, diagnosed at an earlier stage of the disease. On the other hand, older women were less inclined to avail themselves of cytologic screening.

CONTINUING PROGRAM OF POPULATION A screening for the early detection of cer- vix cancer has been in operation in Jefferson County, Ky. since 1956. Prior to the establish- ment of this program, essentially no cervical cytology was performed. After a modest be- ginning of examination of 7,652 women in 1956, there has been an impressive growth each year; by the end of 1967, preliminary data indicated that the equivalent of over 90% of the adult female population had been screened at least once. Table 1 shows the num- ber of annual cytologic examinations done by all laboratories in Louisville, Ky. These in- clude rescreenings as well as examinations on nonresidents. The female population, 20 years of age and over, increased from 188,789 in 1956, the first test year, to 213,178 in 1967, the last year of the study period, with a yearly average of 201,227. Currently, attempts are being made to estimate the movement of the population in and out of Jefferson County in

Supported, in part, by contract number PH-43-63- 1155, National Institutes of Health, Public Health Ser- vice, and by Grant PHS-33065, from the Cancer Con- trol Program, Division of Chronic Disease Programs, Regional Medical Programs Service, USPHS.

* Department of Pathology, University of Louisville School of Medicine, Louisville, Ky.

t Occupational Studies Unit, National Institute of Environmental Health Sciences, National Institutes of Health, Bethesda, Md.

Received for publication January 20, 1970.

order to describe more accurately the screened population: these results will be published in another report.

It was hoped that cervical carcinoma would be treated in Stage 0, thus decreasing the in- cidence of invasive carcinoma, and that inva- sive carcinoma would be detected at an early, preferably asymptomatic, stage. These 2 ac- complishments would of necessity eventually reduce the mortality rate from cancer of the cervix. Other benefits would be the detection of other tumors of the uterus and the identifi- cation of cellular abnormalities that might precede cervical cancer.

The results of this continuing study through 1963 have been previously publishedlo; this communication presents the data through 1967. The data are divided into five 3-year pe- riods. The first period represents precytology years and forms the basis for the expected rates used in this report.

METHODS

Details of the methods used in obtaining data have previously been published.lO In brief, the cases were identified through the cooperation of all hospitals and pathology laboratories in the county. Detailed case ab- stracts were made by medical students trained for the project. When any question concern-

29

30 CANCER July 1970 Vol. 26

TABLE 1. Number of Cytologic Screenings* Done in All Laboratories of Louisville and Jefferson County, Ky.

by Year, 1956-1968

Year Number of screenings

1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968

7,652 38,913 42,194 47,238 46,519 50,339 56,800 60,018 63,601 73,770 79,704 89,203 96,737

TOTAL 752,688 ~

* Includes rescreenings as well as examinations done on nonresidents. Average female population 20 years old and over: 201,227.

ing a particular case arose, or when data were missing from the hospital records, the ab- stracts were completed through direct contact with the community pathologists or with the patients’ physicians. Mortality records at the State Board of Health were reviewed annually.

Population data were grouped into socio- economic areas on the basis of census tracts inside the 1950 city limits of Louisville. For each census tract, estimates of the median in- come for families and unrelated individuals and of the total population were made for January 1, 1958, by straight line interpolation between the 1950 and 1960 census.ll9 l2 Then the tracts were ranked from lowest (SEA I) to highest (SEA IV) median income and were grouped into areas containing approximately 25% of the total population. Since census in- formation available did not allow computa- tion of the socioeconomic areas for the county, these data are given separately. The median family income of the county residents, how- ever, was greater than for the residents in the highest socioeconomic area of the city. Dur- ing the years studied, the economic setting of the region has greatly improved. The total population of the county has increased, and there has been a notable migration of people from the lower socioeconomic areas of the city to the more affluent suburbs (Table 2).

It was estimsted that 181,707 women, 20 years old and over, lived in Louisville and Jefferson County at the beginning of the study, and 213,718 during 1967, the final year. In

the 15-year study period, there were 2,966,923 woman-years at risk. T h e non-Caucasian pop- ulation which is almost entirely Negro, com- prised an average of 12.9yo of the population of women 20 years of age and older through- out the study. Rates used are for women 20 years of age and over; there was no cancer under the age of 20.

RESULTS

During the 15-year period, 3,723 cases of uterine cancer were registered; of these, 97.74% were histologically proved. Four cases of uterine cancer of unspecified site were ex- cluded. In the last period, 1965-67, 99.6% were histologically proved. Table 3 gives the breakdown of the total lesions by method of diagnosis.

Since the elimination of squamous cell carcinoma in-situ would not be expected tQ have the same subsequent effect on the rates for adenocarcinoma or mixed carci- noma of the cervix as i t would on invasive squamous cancer, primary interest is focused on the latter. The rates for other types and histologically unproved cases of cervix cancer are occasionally included, however, to pro- vide completeness and comparability among time periods and with other studies.

Table 4 shows an increase in rates during the early years of cytologic screening attrib- utable to the detection of asymptomatic cases, followed by a decrease in rates. For invasive squamous cell carcinoma, the decrease was 33.9%, and for all cervix cancer, including his- tologically unproved cases, 32.1%. When we compare the observed rates for 1967 with the rates expected, the decrease is 37.3% for squa- mous cell carcinoma and 37.1% for all cervix cancer, including unproved cases. The age- adjusted rate for proved invasive squamous cervix cancer during the last 3-year period is down 38.0y0.

The decrease in cervix cancer during the

TABLE 2. Change in Total Population and in Socioeconomic Areas between 1953 and 1967

SEA I - 41.2% SEA I1 - 19.6% SEA 111 - 13.5% SEA IV -I- 6.1%

*COUNTY +105.8% TOTAL + 17.3%

* Refers to population outside Louisville city limits.

No. 1 CERVIX CANCER CONTROL IN LOUISVILLE - Christopherson et al. 31

TABLE 3. Number of Newly Diagnosed Cases of Uterine Cancer by Site, Method of Diagnosis, and Histologic Type, Louisville, Jefferson County, Ky., 1953-1967

Histologically Clinica! Death certificate confirmed diagnosis only Total

CERVIX - - Invasive squarnous carcinoma 1324 Adenocarcinoma 95 Other carcinoma* 15

13 23 I n-si tu 1339 Total cervix 2773 13 23 CORPUS

- - - -

Malignancy unspecified+ -

- -

- - Adenocarcinoma of endometrium 707 Other cancer of corpus uteri 111 Malignancy of corpus

unspecified' -

- -

8 40 - - In-situ endometrium 48

TOTAL CORPUS 866 8 40 914 TOTAL UTERINE CANCERS 3639 21 63 3723

2809

97.74% histologically proved. * Includes anaplastic and mixed. + Clinical diagnosis and death certificate cannot be further classified.

last 3 years of the study was more pronounced in women under 50 years of age for both races than for those 50 years and older (Table 5) . Table 6 gives the same breakdown for invasive squamous carcinoma alone.

The lowest income group, SEA I, had the highest base rates of invasive squamous can- cer of the cervix. The rates were lowest in the most affluent groups, SEA IV and the county residents. Because of the great shift of popula- tion to higher socioeconomic areas and to the county (Table 2), it is difficult to interpret the rate decreases according to socioeconomic areas. Fig. 1 is presented, however, to show that there was a drop in all 4 socioeconomic areas and in the county.

Socioeconomic status is an important mea- sure of risk for cervix cancer. During the con- trol years, the lowest income area of the city had a risk over 2y2 times the affluent area and 3 times that of the county women. The vast

majority of Negroes lived in SEA I during the years 1953 to 1955. We have previously shown, however, that it is not race per se but socioeconomic status that most closely measures risk.3~

I t seems evident that a major problem in cervix cancer control is persuading older women to be screened. From age 40 on, they not only have a high incidence rate, but the percent of cases with Stage I disease decreases with each decade reaching a low of 15'% for those 70 years of age or older. Table 7 shows the influence of age on rates and stage of dis- ease. It also shows that in addition to a de- crease in cervix cancer rates, there has been a remarkable increase in early diagnosis over the years. Only a therapeutic nihilist would deny, given these 2 facts, that death rates from the disease must decrease following an inten- sive cytologic screening of the population.

Age is an important factor in risk. There

TABLE 4. Observed Number of Newly Diagnosed Cases and Annual Rates of Cancer of the Uterine Cervix Per 100,000 Women* in Louisville-Jefferson County, Ky., by 3-Year Periods,

Type and Method of Diagnosis Clinical Death

Squamous Carcinoma Other Carcinoma Diagnosis Only Certificate Only Total

No. Rate No. Rate No. Rate No. Rate No. Rate 3 .4 6 1 . 1 13 2.4 286 51.6 1953-1955 248 44.9 19

1956-1958 32 1 56.0 23 4 .0 1 0.2 5 0 .9 350** 61.0 1959-1961 318 53.5 21 3.5 5 0 .8 2 0 .3 346 58.2 1962-1964 249 40.6 16 2.6 0 0.0 1 0 . 2 266 43.3

1 0.2 2 0 .3 222 35.1 1965-1967 188 29.7 31 4.9

* 20 years old or older. ** The difference between this figure and published data is due to review of cases.

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No. 1 CERVIX CANCER CONTROL IN LOUISVILLE Chistopherson et al. 33

was no cancer of the uterus before the age of 20. Table 8 gives rates for the precytology years compared to the last 3 years by decade of age, by race, and for combined races. The ratio of cervix cancer rates, Caucasians to Negroes, was 1:1.7 in the first period as com- pared to 1:l.S during the last one.

Table 8 also shows the changes in rates by decade for these 2 time periods. Examination of the difference in rates during the 2 periods for the women aged 70 years and over reveals that success in reducing the rates did not oc- cur in this age group, particularly among non-Caucasians who experienced an in- crease in incidence. For women under 50 years of age, the decrease in rates was 43.1y0 compared to 27.6y0 for those over 50 years of age.

It is of interest to examine the characteris- tics of the 13 Negro patients in the 70 and over age group. Ten of the 13 had not had a cyto- logic examination of the cervix prior to the time they reported symptoms to a physician and a lesion was observed. Two were said to have Stage I carcinoma at the time of initial examination; one of these was dead within 2 months and the other one was dead within 17 months. Two were in Stage 11; one was dead within 6 months and the status of the other one is unknown. Four were in Stage 111; they all died within 13 months. Two were in Stage IV, one died after 4 months and, in the other, the cancer was diagnosed at autopsy.

The remaining 3 patients had cytologic tests before diagnosis. One had positive cy- tology 4 years before diagnosis but had refused treatment. She had Stage 111 disease at the time of tissue confirmation. Another was di- agnosed 45 months after a negative cytologic

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I N V A S I V E SQUAMOUS CARCINOMA OF T H E CERVIX BY SOCIOECONOMIC AREA

1953-55 a n d 1965-67

1953-55

1965-67

Puortite I II m ISI County

FIG. 1. The base rates (1953-55) are ahown by the light bar. The last 3 years’ average rates are repre- sented by the solid bar. Although there is a decrease in rates in all socioeconomic areas, movement of pop- ulation into more affluent areas has the effect of altering the total picture.

examination and died within a month. The third had one negative cytologic examina- tion followed 10 years and 3 months later by a biopsy diagnosis. She had Stage I11 disease and died 6 months later. I t is quite obvious that this older group of women present a problem. They seem recalcitrant to screening, usually

TABLE 7. Number of Cases, Rates, and Percent of Cases in Stage I by .Age. Includes Only Proved Invasive Sauamous Carcinoma of the Cervix in 1953-1955 and 1965-1967

Total Cases Stage I

1953-1955 1965-1967 1953-1955 1965-1967

Age No. Rate No. Rate No. Percent S o . Percent

20-29 10 7.9 8 6.2 5 50.0 8 100.0 30-39 47 37.4 23 18.4 23 48.9 1 7 73.9 40-49 69 63.9 46 36.2 22 31.9 Z i 58.7 50-59 67 79.6 54 50.7 18 26.9 33 61, 1 60-69 35 58.2 26 33.5 8 22.9 13 50.0 70 & Over 20 41.6 31 45.4 3 15.0 9 29.0

188 29.7 79 31.9 107 56.9 Age-adjusted* rate 29.5 18.3

TOTAL 248 44.9

* Age adjusted to U. S. population, 1950.

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No. 1 CERVIX CANCER CONTROL IN LOUISVILLE - Christopherson et al. 35 TABLE 9. Change in Average Age of Newly Diagnosed Cases with Invasive Squamous Cell Carcinorna of

Cervix According to Race and to Socioeconomic Area for Years 1965-1967

Caucasian Non-Caucasian SEA I SEA I1 SEA I11 SEA IV County Total

Expected* 49.6 50.9 49.5 49.0 52.8 49.4 4 8 7 49.8 Observed 52.8 56.1 53.7 52.2 56.4 55.5 52.1 53.5 Increase in average

age over expected 3 . 2 5 .2 4 . 2 3.2 3 . 6 6 . 1 3 . 4 3 . 7

* Average for cases in precytology years, 1953-1955.

have advanced disease, and, consequently, con- tribute appreciably to the difficulty in obtain- ing a dramatic drop in death rate.

For Caucasian women 70 years of age and over the trend was similar but not quite so disappointing as with the Negroes. Eight of the 27 patients in this group never had cyto- logic examinations, and an additional 7 had their cytology simultaneous with the biopsy. Only one third had Stage I disease, and 15 are already dead. The average survival time of those dead of disease was only 10.5 months, with 8 patients surviving less than 2 months.

A further indication that we failed to screen older women is seen in Table 9. The average age at time of diagnosis of invasive squamous carcinoma of the cervix increased 3.7 years during the last time period compared to the control years. The increase in average age was greater in Negro women.

CARCINOMA IN-SITU

With the increased utilization of cytologic screening of asymptomatic women, one would expect an increase in the rates for car- cinoma in-situ. Table 10 shows such an in- crease, over sixfold. Fig. 2 illustrates the in- crease in the proportion of in-situ carcinoma compared to invasive squamous cell carci- noma by 3-year periods.

Fig. 3 shows an abrupt increase in combined invasive and in-situ carcinoma rates coinci- dent with screening activity. Since 1959, there

TABLE 10. Number of Cases of Newly Diagnosed Carcinoma In-Situ of the Cervix and Annual Rates

Per 100,000 Women by 3-Year Periods, Louisville, Jefferson County, Ky., 1953-1967

Number Rate/100,000

1953-1955 52 9 .4 1956-1958 2 74 47.8 1959-1961 300 50.5 1962-1964 338 55.1 1965-1967 375 59.2

has been a decrease in the combined rate de- spite a continual increase in carcinoma in- situ.

Unlike invasive carcinoma, carcinoma in- situ has boundaries of diagnosis that are, to an extent, debatable and largely subjective. It was pointed out earlier that while epide- miologic data for the 2 lesions show similar trends, they are not as clear-cut in carcinoma in-situ.5 This is most likely due to the inclu- sion of lesions which, although histologically disturbing, are not biologically malignant.

The rates in a given time period in a socio- economic area is to a large extent a function of screening activity. T h e total picture of 1,339 cases diagnosed in a number of labora- tories by different pathologists shows a trend similar to invasive cervix cancer according to socioeconomic status, with the exception of the county (Table 11). There is evidence that cytologic screening of county residents was greater than in any other group, which seems to be a plausible explanation for higher rates for in-situ carcinoma in the county.9

Table 12 demonstrates the importance of age

Per Cent of Total Cases Per Three Year Period Corcinoma i n Silu YS. lnvorive Squamous Cancer

Carcinoma in sit" I lnvasive Sqvomous Cancer

1953 - '55 I 1956 - '58 b

I I I I

90 80 70 60 10 +O 30 20 10 0 10 20 W 40 SO 80 70 80 90 Par cent

FIG. 2. There has been a steady increase in the overaIl proportion of carcinoma in-situ to total carci- noma. The period 1953-55 represents the precytology years.

36

100

90

80

CANCER July 1970

- P-*-------. 2.2.- parison of rates by 3-year periods is shown in Table 13. During the last 3 years, the rates for - /

- /* endometrial carcinoma approached the rates --.- .I* .--.-.-

Vol. 26

O L I I 1953-55 1956-58 1959-61 1962-64 1965-67

FIG. 3. The effect of screening is shown by an abrupt increase in carcinoma in-situ with the begin- ning of the program, and a less marked but steady increase as the volume of examinations increased. The concomitant decrease in invasive cancer has resulted in a dccrease in total cases over the years.

as a risk factor for carcinoma in-situ. It also shows a smaller difference in rates by race than was found for invasive squamous carci- noma. It is emphasized that these figures do not represent true incidence rates, but rather a discovery rate based on screening activity and interpretation of histologic material.

In this study, the average age of patients with carcinoma in-situ at time of diagnosis was 39. I years. This compared with an average age of 49.9 years for invasive cancer during the control years and 53.5 years for invasive can- cer during the last 3 years of the study.

There now appears to be an increase of 26.3% in the rate for endometrial carcinoma in our population, 20 years of age and older. After age adjustment to the population of the 1950 U.S. census, the rate for the first period is 13.2 per 100,000 females compared to 15.3 per 100,000 in the last period, an increase of 15.9%. Thus, some of the increase is not due to aging of the population. An actual decrease of 12.7y0 occurred in the women 70 years of age and over. Furthermore, the greatest in- crease, l00%, was in women 30 to 39 years of age. If the somewhat controversial cases of en- dometrial carcinoma in-situ had been in- cluded, the increase would have been even more pronounced.

Other cancers of the uterus contribute ap- preciably to total morbidity from cancer of the body of the uterus. During the 15-year pe- riod, they comprised 18.4% of the total cases and added significantly to the death rates.

DISCUSSION

ENDOMETRIAL CARCINOMA AND It is a well-documented fact that the risk of OTHER UTERINE CANCER cervix cancer among certain identifiable

groups of women is much greater than among the total population. In certain groups, the risk can be extraordinarily high. Women aged

Although not directly relevant to the main purpose of this study, endometrial carcinoma

TABLE 11. Number of Cases of Carcinoma In-Situ of Cervix, and Annual Rates Per 100,000 Women by 3-Year Periods and Socioeconomic Area, Louisville, Jefferson County, Ky., 1953-1967

SEA I SEA I1 SEA 111 SEA IV County Total

No. Rate No. Rate No. Rate No. Rate No. Rate No. Rate

1953-1955 7 7 . 3 11 11.1 10 10.2 9 9 .7 15 9 .0 52 9 . 4 1956-1958 40 45.7 36 38.5 42 44.7 42 44.4 114 55.9 274 47.8 1959-1961 63 79 8 48 54 5 34 37.6 29 30.1 126 52.4 300 50.5 1962-1964 56 79.9 44 51.7 50 56.7 42 43.3 146 53.4 338 55.1 1965-1967 47 76.8 67 81.4 44 50.1 34 34.9 183 59.8 375 59.2

TOTAL 213 54.0 206 46.0 180 39.4 156 32.6 584 49.1 1339 45.1

No. 1 CERVIX CANCER CONTROL IN LOUISVILLE * Christopherson et al. 37 TABLE 12. Number of Cases of Carcinoma In-Situ and Rates by Age and by Race Louisville,

Jefferson County, Ky., 1953-1967

Caucasian Non-Caucasian Combined Races

Age No. Rate No. Rate No. Rate

20-29 212 38.5 44 30-39 464 82.6 83 40-49 284 56.4 34 50-59 120 29.1 19 60-69 47 15.8 8 70 & Over 14 5 . 4 10

TOTAL 1141 44.2 198 Age-adjusted* rate 30.2

* Age adjusted to U. S. population, 1950.

58.5 256 40.9 98.3 547 84.6 42.6 318 54.5 29.4 139 29.2 17.3 55 16.0 30.6 24 8.2 51.7 1339 45.1 35.3 30.8

40 and over in the lowest socioeconomic class, who married or were pregnant in their teens, appear to be at greatest risk.5, On the other hand, women who remain celibate and live a cloistered life are at relatively little risk.8 There appears to be good evidence from this study that routine cytologic population screening can greatly alter the risk of invasive cervical cancer. Using socioeconomic area of residence as the single criteria, 17.4% of women accounted for 31.9% of cervix cancer. At the other extreme, 30.1% of women con- tributed only 17.3% of the cervix cancers.

Race does not appear to be an important fac- tor when correction is made for socioeco- nomic status.1Q On the other hand, at the present time, this group of women-non- Caucasian, living in low socioeconomic areas -is at greater risk than are Caucasians, in general.

Age is of tremendous importance in deter- mining risk. This is magnified by cytologic screening, since younger women are much more apt to receive the protection cytology of- fers than are older women. We recently found that 4G74, of our screening effort in the low-in-

come group was expended on screening women below the age of 30, where the risk of cervix cancer is very low.6

The program in Jefferson County was de- signed to screen all women. I t is somewhat unique in that the response of the low-income population was as good as was that of the more affluent groups. Success of a program must rest in the rescreening of women. Whereas younger women are more easily re- cruited for initial examination, the older groups are more apt to return for rescreening once they have been recruited.

With the elimination of so many cases of carcinoma in-situ, one would expect the de- crease in invasive squamous carcinoma to be greater than 34%. Two factors help explain this apparent paradox. The average duration of carcinoma in-situ appears to he from 10 to 14 years. The cases designated as carcinoma in-situ contain an unknown number of le- sions that were obviously not biological can- cers. Furthermore, progression rates are based on age. There are a certain number which would not become invasive during the life span of the patient.

TABLE 13. Number of Newly Diagnosed Cases of Carcinoma of the Endometrium, Other Uterine Cancers, and Annual Rates Per 100,000 Women by 3-Year Periods, 1953-1967

~~ ~

In-situ carcinoma Endometrial carcinoma of endometrium Other cancers*

Number Rate Number Rate Number Rate

1953-1955 113 20 5 2 0 4 30 5 4 1956- 19% 120 20 9 6 1 0 39 6 8 1959-1961 156 26 2 10 1 7 39 6 6 1962-1964 154 25 1 16 2 6 36 5 7 1965-1967 164 25 9 14 2 2 19 3 0

To rAL 707 23 8 48 1 6 163 5 5

* Includes: 103 sarcomas, 8 choriocarcinomas, 8 clinical diagnosis only, 40 death certificate only, and 4 uterine cancer of unspecified site.

38 CANCER July 1970 Vol. 26

We would again emphasize to critics of mass cytologic screening, that with yearly incidence rates down one third and with the percent of cases diagnosed in Stage I greatly increased, that the death rates must of necessity decrease, provided the accepted dictum that Stage I car- cinoma is more curable than advanced dis- ease is true.

Bryans et al.1 were able to separate their clinical from microinvasive and occult carci- nomas. They demonstrated a dramatic de-

crease in clinically evident cervical cancers. Since our cases were diagnosed in several lab- oratories, we were not able to make this dis- tinction. We have previously pointed out that the diagnosis of microinvasive carcinoma can- not be made with less than serial blocks and step sections of the entire cervix or on an ade- quate cone ~pec imen .~ We agree with Fidler and Boyd7 that it is important to identify microinvasive carcinoma, since its treatment and prognosis are similar to carcinoma in-situ.

REFERENCES

1. Bryans, F. E., Boyes, D. A., and Fidler, H. K.: T h e inflnence of a cytologic screening program upon the incidence of invasive squamous cell carcinoma of the cervix in British Columbia. Amer. J. Obstet. Gynec. 88:898-906, 1964.

2. Christopherson, W. M., Mendez, W. M., Lundin, F. E., Jr., and Parker, J. E.: A ten-year study of en- dometrial carcinoma in Louisville, Kentucky. Cancer

3. Christopherson, W. M., and Parker, J. E.: A study of the relative frequency of carcinoma of the cervix in the Negro. C a n m 13:711-713, 1960.

4. - . and ___ : Microinvasive carcinoma of

18:554-558, 1965.

thc uterine- cervix. A clinical pathological study. Can- cer 17:1123-1131, 1964.

5. ~ , and -: Relation of cervical cancer to earlv marriage and childbearing. New Eng. J . Med.

6 . __ , and ___ : Control of cervix cancer i n 273~235-239, 1965.

women of low income in a community. Cancer 24:64- 70, 1969.

7. Fidler, H. K., and Boyd, J. R.: Occult invasive squamous carcinoma of the cervix. Cancer 13:764-771, 1960.

8. Gagnon, F.: Contribution to the study of the etiology and prevention of cancer of the cervix of the uterus. Amer. J. Obstet. Gynec. 60516-522, 1950.

9. Lundin, F. E., Jr.: Unpublished data. 10. ___ , Christopberson, W. M., Mendez, W. M.,

and Parker, J. E.: Morbidity from cervical cancer: Effects of cervical cytology and socioeconomic status. J. Nut. Cancer Inst. 35:1015-1025, 1965.

11. U.S. Bureau of the Census. U.S. Census of Population: 1950, vol. 3, Census Tract Statistics, Chap. 29. U.S. Govt. Print. Office, Washington, D.C., 1952.

12. U.S. Bureau of the Census. U.S. Census of Population and Housing: 1960. Census tracts. Final Report PHC (1)-83, U.S. Govt. Print. Office, Washing- ton, D.C., 1962.