Cancer Patterns and Risk Factors in the African Population...

Vol. 3, 537-547, October/November 1994 Cancer Epidemiology, Biomarkers & Prevention 537

Cancer Patterns and Risk Factors in the African Population ofSouthwestern Zimbabwe, 1963-1977

D. M. Parkin,’ A. P. Vizcaino, M. E. G. Skinner,and A. Ndhlovu

Unit of Descriptive Epidemiology, International Agency for Research onCancer 1 50, cours Albert Thomas, F-69372 Lyon Cedex 08, France ID. M.

P., A. P. V.]; 89, Kruger Gardens, Admiralty Way, Summerstrand, PortElizabeth 6001, South Africa IM. E. G. S.]; and 7/237 Lupopama(Mpopama(, Bulawayo, Zimbabwe IA. N.l

Abstrad

The incidence of cancer and the importance of someseleded risk fadors in its etiology were estimated fromthe data collected in the cancer registry of Bulawayo,Zimbabwe, during the period 1 963-1 977. Cancer caseswere interviewed with a standard questionnaire, andmore than 71 % of these were complete. In men, themost frequent cancer sites were liver, esophagus, andlung, while in women, cervical cancer was the dominantmalignant tumor, followed by cancers of the liver,breast, and bladder.

Risk factors of cancer cases were estimated by case-control analysis in which other cancers (excludingtobacco-related cancers in men and hormone-relatedcancers in women) were considered as controls. In men,tobacco smoking was associated with increased risk oflung cancer (odds ratio OR2, 5.2) and esophagus cancer(OR, 5.6) in the highest consumption category (1 5 g oftobacco per day) compared to nonsmokers. Copper (OR,1 .5), gold (OR, 1 .5), and nickel (OR, 2.6) miners had anincreased risk of lung cancer, but no increase was foundamong asbestos miners (OR, 0.7). There was noindependent effed of alcohol consumption on the risk ofesophagus cancer. The presence of schistosomiasis wasassociated with a significantly increased risk of bladdercancer (OR, 3.9).

The risk of invasive cervical cancer increased withnumber of children-the estimated odds ratio was 1 .8 inwomen with six or more births-but no consistentassociation was found for first intercourse. Inpostmenopausal women, the risk of breast cancerincreased with age at first pregnancy (but not in thehighly fertile) and decreased with high parity, if age atfirst pregnancy was 1 9 or more.

Introdudion

Information about cancer in Africa is rather sparse, althoughthanks to the dedicated work ofciinicians, pathologists, andepidemiologists who have established and maintained can-

Received 4/26/94; revised 7/19/94; accepted 7/19/94.1 To whom requests for reprints should be addressed.2 The abbreviations used are: OR, odds ratio; CI, confidence interval.

cer registries in different parts of the continent, often withvery minimal resources, some information about the gen-eral pattern of cancer has emerged. There are even fewerstudies on the importance of different etiological factors formany of the major cancers, with the exception of associa-tions of particular interest to external researchers (hepatitisviruses and aflatoxin and liver cancer; Epstein-Barr Virus,and Burkitt’s lymphoma). in this article, we provide a sum-mary of the results obtained from the Bulawayo cancerregistry, which for a 1 5-year period in the 1 960s and 1 970srecorded information on over 1 0,000 African cancer pa-tients, including personal interviews on occupational andlifestyle factors in almost 8,000. Despite the age ofthe data,the findings provide a unique insight into the patterns and

causes ofthe major cancers in what was an essentially ruralpopulation of southern Africa. The full results are availablein the form of a monograph (1).

Materials and Methods

Sources of Data

The cancer registry of Bulawayo (Zimbabwe) was foundedin 1963 and functioned for 1 5 years. It was located in theMpilo Central Hospital which, in addition to providing theonly hospital service to the black African population of thecity of Bulawayo, also acted as the referral center for cancercases from the southwestern part of Zimbabwe (until 1980,Rhodesia), including the provinces of Matabeleland (Northand South), Masvingo (formerly Victoria) and Midlands (Fig.1). New cases of cancer were notified from all hospitalwards and departments; case notes with a diagnosis ofcancer or suspected cancer were sent to the registry ondischarge or death. Copies of all histology and autopsy

reports mentioning cancer were scrutinized monthly by theregistrar. Since death certification before burial was man-datory in the city of Bulawayo, persons who died outsidehospital were brought for autopsy prior to certification.This, together with the very high autopsy rate within thehospital, meant that, for the great majority of cases regis-tered, histological information of diagnosis was available.

An attempt was made to interview all cases notified; ifthe individuals themselves could not be questioned, therelatives were interviewed. The information recorded oneach case included demographic data (name, residence,age, sex, birthplace, occupation, education level), history ofmining (type of mine, duration of employment), tobaccohabits (cigarettes, pipe, snuff, chewing tobacco), alcoholintake (local and European beer), and medical history (in-cluding history of biiharzia and hematuria). For women,sexual and reproductive history were also recorded (age atmenarche, age at menopause, age at first intercourse, age atfirst pregnancy, number of pregnancies). Neopiasm site wascoded according to the 7th and 8th revisions of the lCD,and histological code according to MOTNAC (2); these

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IIZIMBABW�]

.3.

.3..3.

‘3.

‘3.

.3.

.3.

‘3.-3

-3

.3.

3-

Fig. 1. Geographic situation and provinces of Zimbabwe (preindependence boundaries).

538 Cancer in Southwestern Zimbabwe

were recoded to the 9th revision of the lCD for presentation.Validation of the. records was carried out by checking forincompatible sex-site, site-histology, and age-site codecombinations. The list of errors and queries was carefullychecked against hospital records, and corrections weremade when necessary.

The data set analyzed comprised 10,678 cases of can-cer (malignant tumors only) registered during the years1963-1977 (excluding 243 cases in nonresidents of Zim-babwe). These were separated into residents of Buiawayo(individuals with a minimum period of residence of threemonths in the defined urban area), 21 80 cases, and others.

Population

The estimated population of Bulawayo in 1 965 (based onthe census of 1 962 and a demographic sample survey in1965) was 95,885 males and 69,226 females. Accurate agedetermination for elderly Africans was found to be difficult,and the final estimate had an apparent deficit ofthe elderly,particularly females. The census of 1969 showed a popu-lation of 1 1 1 ,470 males and 75,800 females. Linear inter-polation by sex and age class was used to estimate thepopulation at risk for each year (1963-1972). The averageannual population at risk for this period is shown in Fig. 2.The unilateral declaration of independence by the colony ofRhodesia in 1965, and the gradually intensifying civil warin the country which followed, resulted in major undocu-mented shifts of population; no attempt was therefore madeto estimate population at risk for the final quinquennium of

registration (1973-1 977).

Statistical Methods

Average annual incidence rates were calculated for the

Buiawayo population only, for the period 1963-1972. Be-cause of uncertainty about the accuracy of statements of ageamong the elderly, and lack of precision in the population

estimates, the upper age group for calculation of rates is60+ years.

Age standardization of incidence rates was carried by

calculation of the cumulative rates (to age 60), and by thedirect method, using the world standard population (3).

For the more important cancer sites, a study of the

etiological significance of the various factors included inthe questionnaire was undertaken. The data set comprisedall cancer cases in Zimbabwe residents, and the method-ology used was that of the case-control study where, foreach cancer site, the distribution of risk factors was corn-pared with that in a control group comprising other cancercases. The control group was either “all other cancers”registered or all cancers with specified exclusions, for ex-ample, tobacco-related sites. Odds ratios were calculatedby nonconditional logistic regression, by means of the corn-puter package GLIM (4), and presented as point estimates,with 95% confidence limits, and the significance of thedifference from the reference category (= 1 .0). P values fortrend were calculated by categorizing and scoring the ex-posure variable and treating it as continuous. Table 1 showsthe variables studied, with the levels or categories used inthe model.

Not all of the patients (or their relatives) could beinterviewed, and in some who were, the questionnaire was



20 15 10 5

Males (%)5 10 15 20

Females (%)

Cancer Epidemiology, Biomarkers & Prevention 539

1304

1913

3010

5285

7703

9582

12385

13444

11420

8620

8102

10900

11962

05630

60+

55-

50-

45-

40-

35-

30-

25-

20-

15-

10-

5-

0-

0 0

Fig. 2. Average annual population at risk, Bulawayo, 1963-1 972.

562

489

916

1809

3013

4617

6676

8496

8773

7285

8102

10480

12119

73337

not always completed. Overall, 86.7% of subjects could beinterviewed; however, many of the interviews wereincomplete, so that only 71% of cases had completeinformation on lifestyle, with an additional 5.1 % having anoccupational and educational history.

Results

During the first 1 0-year period (1 963-1 972), 1 282 cancerswere registered among the residents of Bulawayo, 992cases in men (corresponding to a crude annual incidence of93.9 per 100,000) and 290 cases in women (39.5 per1 00,000). Table 2 shows the numbers and age-standardizedincidence rates by cancer site. Three cancers dominate thepicture in men: liver; esophagus; and lung, the preciseranking depending upon the index chosen. Thus, with theage-standardized (world) rate, esophagus cancer is first inimportance, although the high rate (58.6) is strongly influ-enced by 51 cases in the oldest age-group (60+), so thatwith the cumulative rate (0-59), liver cancer emerges asnumber one. Moderately high rates are observed also forcancers of the prostate and bladder. In women, cervicalcancer is the dominant malignant tumor, followed by can-cers of the liver, breast, bladder, and esophagus. There is avery high proportion of cancer cases with histologicalverification of diagnosis, 94% overall.

In Table 3, the cumulative incidence rates (0-59) re-

corded in Bulawayo (1 963-1 972) are compared with con-temporaneous results from other cancer registries in Africa,and with incidence rates from the U.S. (white and blackpopulations).

For several of the major cancers the information avail-able through the questionnaire did not permit investigationof the more important etiological factors. Thus, for livercancer (the major cancer of men, and second in importance

in women), there were no data on markers of infection withhepatitis B or C. Similarly, the questionnaire did not touchupon dietary habits (likely to be of importance in some ofthe gastrointestinal cancers), nor upon possible factors rel-evant to prostate cancer. The results for three cancers inmen (esophagus, lung, and bladder) and two in women

(cervix and breast) are presented in more detail.

Esophagus Cancer (Men). Eight hundred twenty-six caseswere registered; 90% of these with a histological diagnosiswere squamous cell carcinomas. The control group (3007cases) for comparison excluded cancer sites known to berelated to alcohol and tobacco consumption in studies in

western countries (oral cavity, pharynx, liver, larynx, lung,and bladder). Table 4 shows the distribution of cases andcontrols by residence, and history of tobacco and alcoholconsumption, together with the crude and adjusted oddsratios. There is a marked geographical variation in risk, withMatabeleland North showing a significantly higher oddsratio than the other provinces. The effect of tobacco smok-ing is also clear, with an apparent dose-response effect(although reported ex-smokers appear to have risks similarto light smokers, <15 cigarettes per day). Adjustment forpossible confounding variables (including consumption ofthe major type of alcoholic beverage, local beer) appears tohave little effect on the results. The unadjusted odds ratiosshow a small effect of alcohol consumption (this is princi-pally locally produced beer), but this is due to the con-founding effect oftobacco smoking, as shown by the lack ofsignificant effect in the adjusted odds ratios.

Lung Cancer (Men). There were 877 lung cancer cases inmen; the control group comprised 4434 other cancers,exclud i ng major tobacco-related sites (esophagus, bladder,and larynx). The risk of lung cancer in relation to smoking(Table 5) shows the expected relationship; taking all forms




Table 1 Variables studied in the case-control studies

Males and Females

Age group (yr)

Time period

Birthplace

Province

Education

Cigarettes (bought)

Home-made cigarettes

All tol)acco

Local beer

European beer

All alcohol

History of mining

Type of mine and duration of exposure

Reported history of bilharzia

Females only

Age at menarche (yr)

Age at menopause (yr)

Age at first intercourse (yr)

Age at first pregnancy (yr)

No. ot full-term pregnancies

0-34, 35-44, 45-54, 55-64, 65+, unknown

1963-1967, 1968-1972, 1973-1977

Zimbabwe, other, unknown

Matabeleland North, Matabeleland South, Victoria, Midlands, other, unknown

Illiterate, literate without schooling, schooling (primary, secondary or higher), unknown

Nonsmoker, ex-smoker, <1 5 daily, �1 5 daily, not specified, unknown

As above

Derived from cigarette consumption (1 cigarette = 1 g tobacco) and pipe smoking (1 pipeful = 0.63 g

tobacco) nonsmoker, ex-smoker, <15 g daily, �15 g daily, not specified, unknown

None, occasionally, weekly, daily, not specified, unknown

As above

Same categories as above, if any type of alcohol, including wine and spirits, had been consumed

Never worked in a mine, ever worked in a mine, unknown

Asbestos: never, ever, 0-6 yr, >6 years

Chrome: never, ever, 0-6 yr, >6 years

Coal: never, ever, 0-6 yr, >6 years

Copper: never, ever, 0-6 yr, >6 years

Gold: never, ever, 0-6 yr. >6 years

Nickel: never, ever, 0-6 yr, >6 years

Tin: never, ever, 0-6 yr, >6 years

Other: never, ever, 0-6 yr, >6 years

None, present, past, unknown

�12, 13, 14, 15, �16, unknown

�42, 43-47, 48-52, �53, unknown

�16, 17, 18, �19, unknown

es17, 18, 19-20, �20, unknown

None, 1-2, 3-6, �7, unknown

of tobacco use, the risk of lung cancer in smokers of 1 5 g ormore per day is about 5 times that of lifelong nonsmokers.A self-reported history of ever having worked in a mine wasassociated with an elevated risk of lung cancer (OR2 = 1 .3),but part of this effect was due to confounding, particularlyby tobacco smoking. In the fully adjusted model the risk isno longer significant (1 .2) (Table 6). With respect to specifictypes of mine, miners of coal and chrome appear to be at

normal risk, while the risk for copper and gold miners iselevated (the latter nonsignificant in the adjusted model).Nickel miners have a clear increase in risk of lungcancer (2.6) but there is no dose-response effect with re-ported duration of work in nickel mining. Conversely, mm-ers of asbestos appear to be at rather lower risk (0.7;nonsignificant).

Bladder Cancer (Men). Ofthe 494 cases of bladder cancer,52 were not histologically confirmed, 75 were of ill definedhistology, 257 were squamous cell cancers, 1 05 were tran-sitional cell carcinomas and 5 were sarcomas. The controlgroup comprised all other cancers, excluding esophagus,larynx, and lung (441 2). There is a strong regional variationin risk, with significantly raised odds ratios in residents ofMidlands and Victoria (Masvingo). This distribution corre-lates well with self-reported history of bilharzia amongcontrols (Table 7). Table 8 shows the odds ratios of bladdercancer in relation to a self-report of having had “bilharzia”in the past and with smoking history. There is a significantlyincreased risk in relation to bilharzia (3.9). When the datawere analyzed by cell type, this risk was found to be slightlymore marked for squamous cell cancers (OR, 3.8) thantransitional/adenocarcinoma (OR, 3.3). There was no sig-nificant effect of tobacco smoking, although it was muchmore marked for transitional cell cancers (OR for 1 5 g or

more per day = 2.2 [95% CI, 0.9-5.7]) than for squamous

cell tumors (OR, 1 .1 ) (data not shown).

Cervical Cancer. One thousand two hundred sixty-threecases of invasive carcinoma of cervix were registered. Ofthose with a specified histology, the great majority was

squamous cell carcinoma (86%) and only 3.4% were ade-nocarcinomas. They were compared with 2347 controls,

which were all other cases, excluding cancers of the breast,corpus uteri, and uterus unspecified. The risk of cervicalcancer (Table 9) was somewhat increased in illiteratewomen relative to those who were literate (OR, 1 .3; 95% Cl1 .0-1 .5). Prevalence of tobacco smoking amongst womenwas very low (3% ever smoked), and there was no signifi-

cant increase in risk of cervix cancer in smokers. Alcoholdrinking (mainly home-made beer) was more frequent. Theassociated risks were assessed in three categories: non-drinkers; occasional drinkers; and frequent drinkers (weeklyor more often). There was a small but significant increase inrisk with increasing consumption, even after adjustment forpotential confounding factors. The number of full-termpregnancies showed a strong association with risk of cervixcancer, with the trend in the odds ratio remaining highlysignificant after adjustment for demographic variables andalcohol consumption. Age at first intercourse did not showany association with risk, however.

Breast Cancer. Three hundred forty-four cases of femalebreast cancer were compared with 2347 controls (othercancers, excluding cancers of the uterus). The average ageat diagnosis for breast cancer is low in this population (48.2)and 42% of cases were diagnosed before the age of 45.Table 1 0 shows the odds ratios in respect to various repro-

ductive variables; there is no clear effort of age at menarche




Table 2 Incidence of cancer in Bulawayo re sidents, 1 963-1 972; crude and age -standardized rates per 1 00,000, cumulative (0- 59) rate per 100,000

ICD-9 Site

Male Female

No. /oASR

(WId)

Cum.

(0-59)No.

/�

ASR

(WId)”

Cum.

(0-59)”

HV%

140-149 Oral and pharyngeal 26 (2.6) 2.8 0.26 3 (1.0) 1.0 0.1 1 96

150 Esophagus 164 116.5) 58.6 1.60 10 (3.4) 8.1 0.23 94

151 Stomach 36 (3.6) 10.6 0.39 9 (3.1) 7.3 0.12 93

153, 154 Colon, rectum 28 (2.9) 6.0 0.25 6 (2.11 4.1 0.25 97

155 Liver 261 (26.3) 52.1 2.62 34 (11.7) 20.6 0.67 91

157 Pancreas 23 (2.2) 8.8 0.20 4 (1.4) 2.7 0.07 85

161 Larynx 16 (1.6) 6.2 0.12 3 (1.0) 1.5 0.16 95

162 Lung 121 (12.2) 48.4 1.20 6 (2.1) 3.0 0.31 96

170 Bone 8 (0.8) 0.7 0.04 2 (0.7) 0.2 0.01 90

1 71 Connective tissue 1 1 (1 .1 1 0.9 0.06 4 (1 .4) 0.6 0.05 100

1 72 Melanoma of skin 2 (0.2) 0.1 0.01 2 (0.7) 0.3 0.02 75

173 Otherskin 22 (2.2) 6.5 0.13 9 (3.1) 2.5 0.25 100

74/175 Breast 2 (0.2 0.3 0.03 30 (10.3) 13.4 0.73 91

179 Uterus, NOS 1 (0.3) 0.1 0.01 100

180 Cervix uteri 60 (20.6) 32.0 1.39 97

181 Placenta 14 (4.8) 1.7 0.12 100

182 Corpusuteri 10 (3.4) 7.1 0.33 100

183 Ovary,etc. 11 (3.8) 9.8 0.18 100

185 Prostate 37 (3.7) 21.9 0.27 81

187 Penis,etc. 13 (1.3) 6.1 0.13 100

188 Bladder 64 (6.5) 17.9 0.50 14 (4.8) 9.5 0.15 97

189 Kidney, etc. 14 (1.4) 3.0 0.11 3 (1.0) 0.8 0.07 100

190 Eye 7 (0.71 0.7 0.05 4 (1.4) 0.4 0.02 100

191/192 Nervous system 7 (0.7) 0.9 0.07 9 (3.1) 1.4 0.09 94

193 Thyroid 5 (0.5) 2.0 0.04 6 (2.1) 1.8 0.17 100

201 Hodgkin’s disease 22 (2.2) 2.0 0.16 1 (0.3) 0.1 0.01 100

200/202 Non-Hodgkin’s lymphoma 20 (2.0) 2.4 0.11 6 (2.1) 0.7 0.04 100

203 Myeloma 8 (0.8) 2.5 0.10 3 (1.0) 2.8 0.08 100

204 Lymphoid leukemia 9 (0.9) 3.9 0.05 5 (1.7) 3.5 0.17 100

205 Myeloid leukemia 16 (1.6) 1.1 0.07 9 (3.1) 4.6 0.05 96

206-208 Other leukemia 5 (0.5) 0.5 0.03 1 (0.3) 0.1 0.01 100

Kaposi’s sarcoma 17 (1.7) 2.3 0.13 3 (1.0) 0.3 0.02 100

140-208 All sites 992 277.4 9.02 290 149.4 5.95 94

a Age-standardized (world standard) incidence rate, per 100,000.

bCumulative rate (0-59) per 100.

or menopause. The population in Bulawayo is very fertile,with a mean of 5.3 births in cases and 5.7 in controls. Ageat first pregnancy is low; the average age is 1 9.2 for casesand 18.9 for controls. Neither has a clear effect on risk(Table 1 0). Table 1 1 shows the joint distribution of risk byage at first pregnancy and number of full-term pregnanciesfor women aged under 45 and women aged 45 or more. Inyounger women, neither variable seems to have much of aneffect on risk. In the older women (45 or more), young ageat first pregnancy and increasing parity both appear todecrease risk, although values are nonsignificant. The effectof increasing parity is confined to women with age at firstpregnancy 1 9 or older.

Discussion

There are many difficulties in estimating the incidenceof cancer in developing countries where population-basedregistration often presents problems (5). In the absence ofobjective criteria for comparison, it is difficult to estimatethe completeness of registration. In the early years of theBulawayo registry, extensive sociological studies (6)showed that the likelihood of under-registration, related tonon-use of medical facilities, was greater amongst oldersubjects, particularly women. In addition, during the lastfive years, the completeness of registration probably dete-

riorated because of the political situation. Certainly thepopulation profile was changed by migration, so that cal-culation of incidence rates became impossible. Conversely,the accuracy of the data registered is probably high, with alarge proportion of subjects being interviewed in person,and with a rate of histological confirmation of diagnosis(89%) comparable to that in developed countries.

Although 87% of the subjects registered with cancerwere interviewed, the interview was complete (including all

lifestyle factors) only in some 71 % Even for those subjects

completing the interview, a considerable percentage of re-sponses was recorded as unknown; thus, only 64.5% of thesubjects had a known occupation, and 58.3% gave a fullsmoking history. As a result, a variable proportion of casesand controls (30-50%) had missing values for the lifestylevariables considered. In calculating odds ratios ignoringthese missing cases and controls, the underlying assump-tion made is that whatever selection bias in respect of therisk factors studied was introduced by nonparticipation, itwas similar in the case group and its controls. Since the

controls were other cancers themselves, this assumptionconcerning non-participants may be less insecure than in

most case-control studies where non-cancer controls areused. Nevertheless, it is possible, for example, that the lungcancer cases which were not interviewed had a higher




Table 3 Cumulative (0-59) rate per 1000 in Bulaw ayo (1963-1972) and other selected registries

ZimbabweBulawayo

1963-1972”

South AfricaNatal:

African

1964�1966C

SenegalDakar

� 969-1 974d

Nigeria

Ibadan� 960-1 967

USA (TNCS)1969-i 971�’

White Black

Males

Esophagus 16.0 23.1 0.2 0.7 1.1 6.6

Stomach 3.9 3.3 1.7 4.0 2.6 5.9

Colon/rectum 2.5 1.7 2.0 1.9 9.3 10.2

Liver 26.2 15.6 15.9 6.9 0.6 2.0

Lung 12.0 21.2 0.9 0.6 19.8 33.8

Bladder 5.0 1.6 1.4 1.4 4.6 2.8

Non-Hodgkin lymphoma 1 .1 1 .6 2.0 6.0 2.9 2.4

All sites 90.2 98.5 40.2 40.4 83.6 1 1 1 .3

(No. of cases) (773) (656) (789) (948) (25,404) (3,376)

Females

Esophagus 2.3 4.9 0.2 0.3 0.4 1 .8

Stomach 1.2 2.0 1.1 4.4 1.3 2.1

Colon/rectum 2.5 1.6 1.0 1.7 8.7 9.1

Liver 6.7 2.8 5.9 3.5 0.4 0.4

Breast 7.3 6.0 7.8 8.6 35.6 29.6

Cervix uteri 13.9 28.0 10.8 13.6 8.9 28.0

Corpusuteri 3.3 2.9 0.8 1.2 9.7 3.8

Ovary 1.8 3.4 3.1 4.9 6.7 5.3

Non-Hodgkin’s lymphoma 0.4 1 .0 0.7 5.6 1 .9 1 .7

All sites 59.5 74.7 47.3 66.5 107.3 106.3

(No. of cases) (254) (368) (693) (964) (34,861) (3,851)

.1 Ref. 23; TNCS, Third National Cancer Survey.

“Refs. 16 and 17.

‘ Ref. 16.

‘I Ref. 46.

“Ref. 17.

proportion of nonsmokers than the noninterviewed controlgroup.

The strikingly high incidence of esophageal cancer,particularly in men, has been noted previously in studiesfrom southern Africa (7). The marked variation by place ofresidence in Zimbabwe (at least 2.5-fold) recalls the patternof localized areas of high and low incidence elsewhere insouthern and eastern Africa (8), although it may in partresult from patients with this rather fatal cancer failing to

reach Mpilo Central Hospital for treatment from the moredistant provinces (9). These geographical features have ledto many theories about possible environmental causes, withCook (8) particularly favoring a geographical associationwith maize, and consumption of locally produced maizebeers. In the present study, there was a clear effect ofsmoking, but no association with consumption of alcohol(locally made beer). Earlier studies in hospital populationsin Durban, South Africa (1 0, 1 1 ), and Transkei (1 2, 1 3) hadalso found a clear association between the risk of esopha-gus cancer and tobacco smoking, but no effect of alcoholconsumption when proper adjustment was made for smok-ing, but no effect of alcohol consumption when properadjustment was made for smoking. In contrast, a recentcase-control study in the more urban population of Soweto,South Africa (14), found that both alcohol and tobaccosmoking had independent (and multiplicative) effects onrisk. It is possible that the difference is associated with thepoorer nutritional status of the Soweto population, relatedto the heavy consumption of maize-beer as Segal et a!. (14)suggest; van Rensburg et a!. (1 1 ) had noted that extensiveuse of purchased maize-meal was an important risk factor.However, it is far from certain that the Matabeleland pop-

ulation of the 1960s and 1970s would have had notablyricher diets, and the investigation of other possible etiolog-ical factors in this part of the world, such as fusariurn toxins(1 5), merits consideration.

The incidence of lung cancer in men in Bulawayo isthe highest recorded (in a nonselected population) in Africa,with an age-adjusted (world standard) rate of 48.4 per 1 0�,comparable to that in Connecticut, at the same period (16,1 7). The high risk in black males from southern Africa hasbeen noted previously, with rates in Natal, South Africa, in

the early 1960s much the same as in Bulawayo (16). Thepresent study clearly demonstrates the importance of to-bacco smoking in the etiology of lung cancer in this pop-ulation. Smoking prevalence in males, on the basis of thecontrol population, is moderately high (41% current ciga-rette smokers), although 86% of them consume fewer than1 5 cigarettes per day. On the basis of Table 5, the propor-tion of lung cancer attributable to cigarette smoking can beestimated as 49%, and to all forms of tobacco, 60%.

The occupational risk of lung cancer in miners is wellknown, and particularly marked in hematite and uraniummining and in miners exposed to arsenic compounds, andwith occupational exposure to asbestos. The risks in coalminers are more uncertain and may largely be related to

smoking habits. In the present study, mining history wasobtained by self-report, so there is considerable opportunityfor misclassification. Nevertheless, there are some surpris-ing findings. In particular, the lack of increased risk inasbestos miners was unexpected, although the only minesin Zimbabwe are of chrysotile asbestos, and previous stud-ies in the country also failed to identify an excess of cancercases (1 8, 1 9). The rather higher risk of lung cancer in gold




Table 4 Risk fact ors for esop hagus cancer i n men

Cases

(826)

ControIs�

(3007)OR d b(cru e)

OR (adj.Y� Cl)

Province

Matabeleland N. 448 1202 1

Matabeleland S. 1 69 654 0.7 (0.6-0.9)’�

Victoria 49 337 0.4’s’ 0.5 (0.3-0.6)�’

Midlands 151 749 0.5’�#{176} 0.6 (0.4�0.7)***

Other 9 61 0.4 0.4 (0.2-0.9)

All cigarettes

Non-smoker 1 48 1 026 1 1

Ex-smoker 21 37 3.23*3 3.2 (1.8-5.9)’’

<15 daily 277 496 3.3 (2.5�4.2)***

>1 5 daily 49 71 45*5* 4.6 (2.9-7.2)”

Not specified 47 75 3.9” 3.3 (2.0-5.4)”

Trendtest P<0.001 P<0.001

Total tobacco

Non-smoker 1 20 947 1 1

Ex-smoker 21 38 3.5” 3.5 (1.9-6.4)”

<15 gr. daily 279 524 3.3” 3.7 (2.8-4.7)”

�15 gr. daily 71 91 5.4” 5.6 (3.7-8.5)”

Not specified 56 1 1 6 3.2” 2.7 (1 .8-4.2)”

Trend test P< 0.001 P < 0.001

Local beer

None 132 637 1 1

Occasionally 43 194 0.9 0.6 (0.4-0.9)’

Weekly 120 378 1.1 0.8 (0.6-1.1)

Daily 21 1 535 1 .4’ 0.9 (0.6-1 .2)

Not specified 54 106 1.9’ 1.3 (0.8-2.1)

Total alcohol

None 144 654 1 1

Occasionally 44 206 0.8 0.6 (0.4-0.9)’

Weekly 121 387 1.1 0.8 (0.6-1.1)

Daily 212 539 1.1 0.8(0.6-1.1)

Notspecified 41 68 2.1” 1.6(0.9-2.5)

a Excluding cancers of the oral cavity and pharynx (lCD 140-149), liver

(155), larynx (161), lung (162), and bladder (188).b Adjusted for age group only.

( Adjusted for age group, time period, province, education, drinking habits,

smoking habits, and history of mining.

C p< 0.05.*3 p< o.oi.*3* p< o.ooi.

miners is no longer significant after adjustment for smoking.An early study in Matabeleland (1 8) showed a highproportion of lung cancer among cancers found at autopsyin the hospital serving the gold-mining community, al-though a cohort study in South African gold miners foundthat most of the excess risk (SMR 1 61 ) was due to smoking(20). Finally, the elevated risk in those working in nickelmines is of considerable interest. The ore extracted at thecopper/nickel deposits at Filabusi in Matabeleland is con-vetted locally to a matte form in furnaces before transportelsewhere for refining. This process has been associated

with an increased risk of lung cancer in studies elsewhere(2 1 ). The ores contain varying amounts of arsenic. Exposureto arsenic by workers engaged in copper smelting has beenassociated with increases in the risk of lung cancer (22).

The high incidence of bladder cancer (similar to therates in North America and Europe) in men is accompaniedby a high proportion of squamous cell cancers: 70% ofhistologically typed cases, compared with 9.8% of cases inthe black population of the United States in 1969-1971

(23). The association of squamous cell tumors and schisto-

Table 5 Lung ca ncer and to bacco smoking

Cases(877)

Controlsa(4434) OR (crude)

OR (adj.(’

� CI)

Cigarettes

Nonsmoker 1 54 1 359 1 1

Ex-smoker 26 59 3.1 “ 2.8 (1 .6-4.7)”

<1 5 daily 286 749 3.0” 3.0 (2.4-3.8)”

�15 daily 60 125 4.0” 4.0 (2.7-5.9)”#{176}

Not specified 42 1 23 2.6” 3.0 (1 .9-4.7)”

Trend test P < 0.001 P < 0.001

All tobacco (including pipe)

Non-smoker 1 07 1 248 1 1

Ex-smoker 26 61 3.8” 3.4 (1.9-5.8)”

<15 g daily 314 818 3.8” 3.9 (3.0-5.0)”

�1 5 g daily 61 1 28 5.0” 5.2 (3.5-7.7)”

Not specified 65 178 3.4” 3.7 (2.4-5.3)”

Trend test P < 0.001 P < 0.001

., Excluding cancers ofthe esophagus (lCD 150), larynx (161), and bladder

(188).1; Adjusted for age only.(� Adjusted for age, time period, birthplace, education, alcohol consumption,

and history of mining (ever/never).

5*’ p< o.ooi.

somiasis has been recognized for many years (24). In thepresent study, the presence of urinary schistosomiasis wasevaluated simply from a question on a history of bilharzia or

hematuria. Although there was probably some confusionbetween such a history and recent hematuria due to thepresence of a tumor (as suggested by a higher odds ratio forrecent rather than past bilharzia/hematuria), the differentialmisclassification would have to have been extreme (61 % ofthe positive responses in cases incorrect) to produce theobserved odds ratio (3.9). In a previous study in Zimbabwe(Rhodesia), Gelfand et a!. (25) compared 33 bladder cancercases with age/sex-matched controls and found a relativerisk for bladder calcification on x-ray (indicative of pastschistosomiasis) of 15.0. The strong regional variation inrisk observed in the present study coincides closely with thegeographical differences in the prevalence of schistosomi-asis, as noted in another recent study (26).

The failure to find an association between bladdercancer and tobacco smoking was probably the result of thehigh proportion of squamous cell tumors, for which noexcess risk in smokers was observed. Kantor eta!. (27) in theU.S. found that squamous cell carcinomas of the bladderhad much the same association with tobacco smoking astransitional cell tumors, although the study was small, andconfidence limits on the estimated relative risks were wide.

Cervix cancer is the dominant cancer of women, as itis elsewhere in sub-Saharan Africa, with the rates in Bula-wayo being typical of other African series. Prevalence ofsmoking in women in Bulawayo was very low, and there isno apparent excess risk in smokers. In contrast, the findingof an association with alcohol intake is surprising. This hasrarely been reported as an independent risk factor for cervixcancer. However, in an earlier study in Lesotho (28), com-paring 257 cervix cancer cases with controls (matchedfor age, parity, and residence), there was a significantlyincreased risk (RR = 3.2) for consumption of indigenousalcohol (frequent versus never) and European alcohols(RR =1 .3) (each adjusted for the other, and for tobaccoconsumption). In a survey in Johannesburg residents withcancer, undertaken in 1 953-1 955, Oettle (29) also found a




Table 6 Lung canc er and histo ry of working in mines

Cases(877)

Controls’(4434)

,,OR (crude)

OR (adj.)c� Cl)

History of mining

Never 270 1104 1 1

Ever 268 668 1 .3” 1 .2 (0.9, 1 .4)

Type of mine

Asbestos

Ever 56 224 0.8 0.7 (0.5, 1 .0)

�6 yr 34 1 58 0.7 0.7 (0.4, 1.0)

>6 yr 20 82 0.8 0.7 (0.4, 1.2)

Not specified 2 4

Chrome

Ever 42 118 1.2 1.1 (0.7, 1.7)

�6yr 18 61 1.0 0.9(0.7,2.1)

>6 yr 22 56 1.3 1.2 (0.7, 2.1)

Not specified 2 1

Coal

Ever 51 158 1.1 1.1 (0.8, 1.6)

�6 yr 25 76 1 .2 1 .1 (0.7, 1 .9)

>6 yr 26 75 1 .1 1 .0 (0.6, 1 .7)

Not specified 0 7

Copper

Ever 55 106 1.7” 1.5(1.0,2.2)’

�6yr 23 46 1.7’ 1.2 (0.7, 2.1)

>6 yr 27 56 1 .6’ 1 .5 (0.9, 2.6)

Not specified 5 4

Gold

Ever 48 78 2.0” 1 .5 (0.9, 2.3)

�6yr 25 35 2.3” 1.8(0.9,3.2)

>6yr 23 39 1.8’ 1.3(0.7,2.2)

Not specified 0 4

Nickel

Ever 42 59 2.4” 2.6 (1 .6, 4.2)”

�6 yr 20 29 2.4” 2.2 (1 .2, 4.3)’

>6yr 18 28 2.2’ 2.1 (1.1,4.2)’

Not specified 4 2

.1 Excluding cancers of the esophagus (lCD 1 50), larynx (1 61), and bladder(188).

hAdjustedfor age only.( Adjusted for time period, birthplace, education, alcohol consumption, andsmoking habits.S p< 0.05; “ P< 0.01; “ P< 0.001.

higher proportion of cervix cancer cases giving a history oflocal beer drinking; when compared to age-matched othercancers (excluding breast and genital sites), the relative riskwas 3.0.

The importance of reproductive and sexual variables inthe risk of cervix cancer has been the subject of a vastnumber of studies. Of the two major risk factors, age at firstintercourse and number of sexual partners, the latter ap-pears to be the more important determinant (30, 31). Earlystudies demonstrated a higher risk for cervix cancers inassociation with high parity. Subsequently, this associationwas dismissed as being indirect, with high parity merelyreflecting key sexual variables. Recent studies which con-trol for sexual and reproductive variables do, however,suggest that multiparity may have an independent effect(32-34).

There are, however, few studies in Africa on the effectof sexual and reproductive variables on risk. In an earlystudy ofJohannesburg residents (29) that compared cervicalcancer cases with other cancers (age-matched) as controls

Table 7 Odds ratios of bladder cancer and prevalence of self-reported

history of bilharzia, in relation to province of residence (males)

Prevalencec. Cases Controls b of reported

Province OR (95 /o Cl) . .(494) (4412) bilharzta

(%)

Matabeleland N. 1 80 1 929 1 1 0 In = 959)

Matabeleland S. 81 936 0.9 (0.7-1 .2) 1 0 In = 459)

Midlands 1 41 1 041 1 .5 (1 .2-1 .8)” 1 6 In = 391)

Victoria 85 420 2.3 (1 .7-3.0)” 22 In = 227)

Other 7 80 0.9 (0.4-2.0) 1 2 In = 42)

a Excluding cancers of the esophagus (lCD 1 50), larynx (1 61 I and lung (162).

‘3 OR adjusted for age group.C Prevalence of bilharzia in control group (excluding ‘unknown’).

5* p< 0.01; “ P< 0.001.

Table 8 Odds ratios of bladder cancer associated with a history of

bilharzia and tobacco consumption

Cases(494)

ControIs�’(4412)

OR 95#{176}!CI b� #{176}

History of bilharziaor hematuria

No 199 1818 1

Yes 101 260 3.9 (2.9-5.2)”

Tobacco�

Non-smoker 142 1236 1

<1 5 g daily

�15 g daily

Not specified

98

25

1 9

782

160

1 75

1 .0 10.7-1 .3)

1.4 10.9-2.3)

1 .1 (0.7-1 .9)

a Excluding cancers ofthe esophagus (lCD 1 50), larynx 11 61 ), and lung (1 62).b OR adjusted for age group, time period, province, bilharzia, education,

drinking and smoking habits.C Excludes ex-smoker category.

*3* p< o.ooi.

(excluding breast and female genital sites), there was almostno difference between the iwo groups in age at menarche orin parity (slightly fewer pregnancies or births to cervix can-cer cases), but age at marriage and age at birth of first childwere lower for cervix cancer cases (not significant, howev-er). In a later study in Africans of Durban (35), cervix cancercases had a significantly earlier age at first intercourse (1 8.2years), age at first pregnancy, and higher parity than con-trols. There was no difference in age at menarche. Finally,Freedman, et a!. (36) compared 48 cervix cancers patientsfrom Baragwanath Hospital (Johannesburg) with age-matched (± 1 0 years) controls from the same hospital. Al-though results are not clearly presented, there appear to beno significant differences between cases and controls ineducation level, mean age at first coitus (1 6.2 in bothgroups), average number of sexual partners (2.4 in cases;2.8 in controls), and age at menarche. There was a sugges-tion of higher parity in the cases than the controls.

In the present study, age at first intercourse has hardlyany effect on risk, although the range of ages given wasnarrow, with half of the cases reporting age 1 7 or 1 8. Themedian age (18.3) was relatively high, as in the earlier

studies summarized above. The number of sexual partnerswas not investigated in the present study, but high parityand early age at pregnancy both appear as risk factors. Theeffect of age at first pregnancy is reduced when adjustmentis made for number of pregnancies, and parity appears to be



Table 9 Risk factors for invasive carcinoma of the cervix Table 10 Risk factors for breast cancer in women

Cases Controls” OR (crude)” OR )adj.)’

1344) 12347) )95%� Cl)

61 227

134 525

51 225

0 113

26 100

68 278

15 43

123 614

1 1

0.9 0.9 (0.6-1 .3)

0.9 0.8 (0.5-1 .2)

1 1

0.9 0.9 10.5-1 .5)

1.3 1.410.7-3.1)

Age at menarche (yr)

<14

14

>14

Not applicable

Age at menopause (yr)

<48

48-52

>52

Not applicable

Age at first pregnancy lyr)

<18

18

19-20

>20

Not applicable

No. of full-term pregnancies

<3

3-4

5-6

>6

Not applicable

48 199

55 194

53 234

85 370

14 165

a Excluding cancers of the breast (lCD 1 74), endometrium (1 82), and uterus

NOS (179).b OR adjusted for age group only.

C OR adjusted for age group, time period, province, education, drinking

habits, age at first intercourse, and number of full-term pregnancies.

*P< 0.05; “ P< 0.001.

a Excluding cancers of the uterus (lCD codes 1 79, 1 80, 1 82).b OR adjusted for age group only.C OR adjusted for age group, time period, province, education, drinking

habits, age at first pregnancy, and number of full-term pregnancies.


Cases Controls’

(12631 (2347)b

OR Icrude)

OR Iadj.)c

(95% CI)

Education

Illiterate 625 747 1 1

Literate 283 466 0.8’ 0.9 (0.7-1 .0)

Smoking habits

Never 776 1 078 1 1

Ever 30 48 0.8 1 .0 (0.6-1 .7)

Alcohol intake

Never 376 702 1 1

Occasional 169 185 1.6” 1.4 11.1-1.8)’

Frequent 367 348 1 .9” 1 .6 (1 .3-1 .9)”

Trendtest P<0.001 P<0.001

Age at first intercourse

>18 194 233 1 1

18 303 328 1.1 1.1 (0.8-1.4)

17 140 130 1.3 1.2 (0.9-1.7)

<1 7 262 278 1 .1 1 .0 (0.8-1 .3)

Not applicable 0 139

No. of full-term pregnancies

<3 142 199 1 1

3-6 361 428 2.0” 1 .3 (1 .0-1 .7)’

>6 424 370 2.6” 1 .8 (1 .3-2.3)”

Not applicable 9 165

Trend test P < 0.001 P < 0.001

the major determinant of risk. It has been suggested thattrauma to the cervix through multiple childbearing, partic-ularly at young ages, in some way increases the risk ofneoplastic change, or that hormonal or nutritional influ-ences of pregnancy are responsible. If so, high fertility mayprovide part ofthe explanation for the elevated incidence ofcervix cancer in this part of Africa, although the proportionofcases attributable to high parity (more than three full-termpregnancies) estimated from the results in Table 9, is quitelow at about 30%.

The incidence of breast cancer, as elsewhere in sub-Saharan Africa, is low, less than one quarter of that in theU.S. black population (Table 3). The results suggest that, asdo many studies (37), a late age of menarche and early ageat menopause may be associated with reduced risk of breastcancer, although the effect is small and not statisticallysignificant in either case. This may be a consequence of therather narrow range of values in the population studied, aswell as the inevitable uncertainty about exact age in anAfrican female population (6) giving rise to the misclassifi-cation between categories.

Early age at first full-term pregnancy and, independentof this, the total number of pregnancies have also beenobserved to be associated with a low risk of breast cancer inmany studies (38, 39). It is now generally agreed that preg-nancy has a dual effect on breast cancer risk, an initialincrease in risk (due to hormonal promotion of early ma-lignant tissue) being followed by a reduction due to “ter-minal differentiation” of breast tissue. This would explainthe increased risk in relation to late age at last birth (40) andthe observation of increased risk with high parity in young

51 256 1 1

57 223 1 .3 1 .2 (0.8-1 .9)

78 282 1.5 1.5 (0.9-2.2)

44 163 1.2 1.1 (0.7-1.7)

15 168

1 1

1 .2 1 .3 (0.8-2.0)

0.9 0.9 10.6-1 .4)

0.8 0.8 (0.5-1 .3)

women (41 , 42). In young women with high parity, the mostrecent birth will generally have occurred relatively shortlybefore the diagnosis. The results in Bulawayo are coherentwith these observations. Parity and age at first pregnancyappear to influence risk only in women over 45 at diagnosis(although none of the estimated risks are significant). In-creasing parity seems to reduce risk only in women whosefirst pregnancy was at age 1 9 or older, and age at firstpregnancy is unrelated to risk in the highly parous group (six

or more full-term pregnancies). The population studied inBulawayo has a much lower average age at first pregnancy(1 8.7) and number offull-term pregnancies (5.6) than in thewestern populations which have been the subject of thegreat majority of previous studies. There appear to be nopublished studies of breast cancer risk in relation to repro-ductive variables in an African setting, although popula-tions with high fertility have been investigated in S#{227}oPaulo,Brazil (43), Burma (44), and Costa Rica (45). In this latterstudy, the population had a mean parity of 5.1 , a mean ageat first birth of 22.1 and, as in Bulawayo, there was no effectof parity in women with first birth before age 20, but asignificant decline in risk with increasing parity for womenwith their first birth aged 20 or more. An association withage at first birth was only observed in women over 45, andwomen with first birth age 20-24 were at higher risk thanthose in the group younger than 20 years of age.

Conclusions

The cancer pattern in Bulawayo shows, on the one hand,characteristics typical of developing countries (high mci-dence rates of esophagus cancer, liver cancer, and cervicalcancer), but also patterns more familiar in the so-calleddeveloped world, particularly the high incidence of lung




Table 1 1 Odds ratios (age-adjusted ) for breast cancer according to par ity and age at first pregnancy, and age (le ss than 45, 45 and over)

ParityAge at first pregnancy (yr)

�18 19+ All

Young women (0-44 yrl

0-2 1�’ 0.87 (0.31-2.46) 1”

3-5 1 .36 (0.54-3.341 1 .59 (0.27-9.57) 1 .66 (0.87-3.14)

6+ 0.97 (0.38-2.47) 0.96 (0.1 7-5.63) 1 .05 (0.53-2.08)

All 1 a 1 .07 (0.66-1 .74)

Older women (45+ yr)

0-2 1’ 2.30 (0.88-6.04) i.’

3-5 1 .09 (0.41 -2.89) 1 .62 (0.25-9.20) 0.85 (0.47-1.52)

6+ 1.07 (0.46-2.50) 1.16 (0.22-6.21) 0.70 (0.41-1 .18)

All 1’ 1.32 (0.90-1 .9S)

.1 Reference category.

cancer in men. Tobacco smoking emerges as an importantfactor in the etiology of lung cancer and esophagus cancerin this population. Copper, gold, and nickel miners had anincreased risk of lung cancer; no risk was found amongasbestos miners. Schistosomiasis is an important risk factorfor bladder cancer, while tobacco smoking had a weakeffect.

For the reproductive variables in the women, we foundthat the risk of cervix cancer increased with childbearing,while for breast cancer in post-menopausal women (al-though not in the highly fertile with six or more pregnan-cies) risk increases with age at first pregnancy and decreaseswith high parity (although not ifthe first pregnancy occurredyounger than 19 years of age).

AcknowledgmentsWe wish to acknowledge the contributions of Professor W. Fraser Ross and

Dr. D. A. Parker at Mpilo Central Hospital, of Dr. W. Castle at the Depart-ment of Community Medicine and of Hilary Flegg Mitchell to the sociolog-cal surveys. Professor A. G. R. Stewart (University of Zimbabwe) arranged

the transfer of the registry files to computer medium, and Dr. R. T. Mossopprovided useful information concerning the history of mining in Rhodesia!Zimbabwe. We thank Allan Bieber for his work on checking and correcting

the data file and Iacques Ferlay for estimating the incidence rates. Theanalyses of these data were undertaken during the tenure of Ana Paloma

Vizcaino’s fellowship from the Medical and Health Research programme of

the European Communities.

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