Tobacco attributable deaths in South Africa
In mid 1998, a question "Was the deceased a smoker five years ago?" was introduced on the newly revised South African death notification form. A total of 16,230 new death notification forms from 1998 have been coded, and comparison of the prevalence of smoking among those who died of different causes was used to estimate, by case-control comparisons, tobacco attributed mortality in South Africa. Cases comprised deaths from causes known (from other studies) to be causally associated with smoking, and controls comprised deaths from medical conditions expected to be unrelated to smoking. Those who died from external causes, and from diseases strongly related to alcohol consumption, were excluded. Reports were available from 5340 deceased adults (age 25+), whose smoking status was given by a family member. Significantly increased risks were found for deaths from tuberculosis (odds ratio (OR) 1.61, 95% confidence interval (CI) 1.23 to 2.11), chronic obstructive pulmonary disease (COPD) (OR 2.5, 95% CI 1.9 to 3.4), lung cancer (OR 4.8, 95% CI 2.9 to 8.0), other upper aerodigestive cancer (OR 3.0, 95% CI 1.9 to 4.9) and ischaemic heart disease (OR 1.7, 95% CI 1.2 to 2.3). If smokers had the same death rate as non-smokers, 58% of lung cancer deaths, 37% of COPD deaths, 20% of tuberculosis deaths, and 23% of vascular deaths would have been avoided. About 8% of all adult deaths in South Africa (more than 20 000 deaths a year) were caused by smoking.
Tobacco attributable deaths in South Africa
F Sitas, M Urban, D Bradshaw, D Kielkowski, S Bah, R Peto
See end of article for
A Professor Freddy Sitas,
the Cancer Council New
South Wales, P.O. Box
572, Kings Cross, NSW,
2011, Australia. Email:
Accepted 4 June 2004
Tobacco Control 2004;13:396–399. doi: 10.1136/tc.2004.007682
Background: In mid 1998, a question ‘‘Was the deceased a smoker five years ago?’’ was introduced on
the newly revised South African death notification form.
Design: A total of 16 230 new death notification forms from 1998 have been coded, and comparison of
the prevalence of smoking among those who died of different causes was used to estimate, by case–control
comparisons, tobacco attributed mortality in South Africa. Cases comprised deaths from causes known
(from other studies) to be causally associated with smoking, and controls comprised deaths from medical
conditions expected to be unrelated to smoking. Those who died from external causes, and from diseases
strongly related to alcohol consumption, were excluded.
Subjects: Reports were available from 5340 deceased adults (age 25+), whose smoking status was given
by a family member.
Results: Significantly increased risks were found for deaths from tuberculosis (odds ratio (OR) 1.61, 95%
confidence interval (CI) 1.23 to 2.11), chronic obstructive pulmonary disease (COPD) (OR 2.5, 95% CI 1.9
to 3.4), lung cancer (OR 4.8, 95% CI 2.9 to 8.0), other upper aerodigestive cancer (OR 3.0, 95% CI 1.9 to
4.9) and ischaemic heart disease (OR 1.7, 95% CI 1.2 to 2.3).
Conclusion: If smokers had the same death rate as non-smokers, 58% of lung cancer deaths, 37% of COPD
deaths, 20% of tuberculosis deaths, and 23% of vascular deaths would have been avoided. About 8% of all
adult deaths in South Africa (more than 20 000 deaths a year) were caused by smoking.
outh Africa is a middle-income country of approximately
45 million people. The population is heterogeneous and
using the population groups defined by the most recent
census (2001) shows that about 77% are of African origin,
10% are whites of European origin, 9% are coloured (of mixed
origin), and 2.5% are Asian, most of whom are of Indian
In 1992 it was found that a third of the adults (> 18 years)
in South Africa were smokers (52% male, 17% female).
Smoking was prevalent among men of all population groups
(53% in African, 43% in white, 58% in coloured, and 48% in
Asian/Indian), and it is noteworthy that smoking rates
among Africans exceeded those of whites. Only 10% of
African women were smokers compared with 27% of white
and 59% of coloured women. Average annual consumption of
manufactured cigarettes per adult (15 years and older) rose
from 1340 in 1970–72 to 1720 in 1990–92.
From about 200
billion cigarettes consumed in 1991, consumption declined to
70 billion in 2001.
Methods of estimating tobacco attributed mortality that
are appropriate for Western developed countries may not be
One way to estimate tobacco attributed
mortality in developing populations is to study retrospectively
a large number of people who have recently died, ascertain-
ing their previous smoking habits by interviewing the family,
and recording the underlying disease that caused death. This
has been done in China
where the next of kin of
the deceased individuals were visited by research teams and
answered questions about their own smoking status and
about the smoking status of their deceased relative.
Comparisons of smoking could then be made either between
people who had died of different diseases (as in the present
report) or between those who had died and those who had
not (using the surviving relatives as unmatched controls).
In South Africa death registration is compulsory. A new
death notification form was introduced in 1998 in an
extensive effort by the South African government to improve
coverage and to conform to international standards regarding
both medical and non-medical cause of death notification.
The incorporation of former black homelands into a unitary
state has now increased the proportion of adult deaths that
are certified to over 90%.
The new death notification form
(and, for the first time, an instruction manual on how to
) was introduced in June 1998. The cause of
death details are recorded using the World Health
Organization recommended format ( International classification
of diseases, 10th revision (ICD-10)) to enable identification of
the underlying cause. Further demographic details about the
deceased are also included—for example, level of education,
population group, and usual residence. In addition, the
question ‘‘Was the deceased a smoker five years ago? (Yes/
No/Not applicable/Minor)’’ has been introduced to provide a
direct estimate of tobacco attributed mortality
national death notification system.
The South African death notification system was used to
gather this information. A doctor or nurse ascertained
whether a death was natural or suspicious and filled the
medical section of the death notification form accordingly.
Forms are passed on to the local Department of Home Affairs
who check the identity of the deceased and of the next of kin.
Deaths that may be due to an external cause are dealt with by
a pathologist, who may perform a necropsy, before releasing
the body for burial. Once such investigations are complete,
the Department of Home Affairs issues a burial order and a
death certificate to the next-of-kin. These notification forms
are centrally microfiched and the paper original sent to
Statistics South Africa for coding and statistical reporting.
As data processing by the Vital Statistics Section of
Statistics South Africa has a lag of a minimum of about five
years, a sample of 16 230 new forms (approximately 5%) was
gathered by asking all local Department of Home Affairs
offices to submit copies to Statistics South Africa of the first
200 death notifications, starting three months after imple-
mentation (that is, from October 1998) to a cut-off of
December 1998. Trained nosologists, from the Vital Statistics
section of Statistics South Africa, coded the underlying cause
of death using the medical information on the new
notification form which is more detailed than previously;
thereafter the whole form was captured on computer.
A case–control analysis was used to estimate tobacco
attributed mortality. ‘‘Cases’’ comprised deaths from diseases
known from studies elsewhere to be potentially related to
smoking, and ‘‘controls’’ comprised deaths from other
defined medical conditions expected to be largely unrelated
to smoking. Specifically, cases comprised adults (age 25+)
with death attributable to tuberculosis, other lung infection,
chronic obstructive pulmonary disease (COPD), lung cancer,
and cancers of the nose, oral cavity, larynx, pharynx,
oesophagus, stomach, liver, bile duct, pancreas, bladder,
kidney, and cervix uteri (all combined into two categories
due to small sample sizes), ischaemic heart disease, and
stroke and other vascular disease (excluding rheumatic heart
The controls comprised adults with deaths caused by other
infectious diseases (A00–A09, A20–B99, n = 410); benign
neoplasms (D00–D89, n = 103); endocrine diseases (E00–
E89, n = 264); diseases of the nervous system (G00–G99,
n = 81); female breast and genital cancers (other than
cervix) (C50–C52, C54–C58, n = 52); male genital cancers
(C60–C63, n = 33); colorectal cancer (C18–C21, n = 32);
cancers of the bone, skin, connective and soft tissue (C40–
C49, n = 22); haematological cancers (C81–C96, n = 20);
diseases of the genitourinary system (N00–N99, n = 81),
diseases of the digestive system excluding varices (K35–K66,
n = 40); obstetric conditions (O00–O99, n = 12); musculo-
skeletal conditions (M00–M99, n = 8); cancers of the eye,
central nervous system, (C69; n = 1); endocrine glands
(C69–C75, n = 2); congenital malformations (Q00–Q93,
n = 2); eye disorders (H00–H99, n = 2), and diseases of
the skin (L00–L99, n = 2).
We excluded from the case–control comparison persons
with ill defined causes of death (as we did not know whether
they should be cases or controls), persons dying from
diseases strongly associated with alcohol (cirrhosis, pancrea-
titis, peptic ulcer, and oesophageal varices) and persons dying
from external causes, who, from other studies,
expected to include a non-causal excess of smokers.
Data were analysed using unmatched unconditional
logistic regression to estimate odds ratios (OR), standardised
for age (25–34, 35–44, 45–54, 55–64, 65–74, and 75+ years),
education (none, primary (up to seven years)), secondary or
tertiary, and unknown), population group (black, white,
Asian, coloured, unknown), and by sex, where appropriate.
Attributable risks and fractions were estimated in the usual
way as P 6 (OR 2 1)/(P 6 OR) + (1 2 P), where P is the
prevalence of smokers in the control group.
This study was
approved by the University of Witwatersrand human research
ethics committee (medical).
Of the 16 230 death notifications included, almost all of
which recorded sex and age, 12 959 were from persons of a
known sex and over 25 years of age. Of this group 9085 death
notification forms had informants who were a close family
member (son, daughter, parent, or spouse). This analysis is
based on the data from these 2946 men and 2394 women
with close family informants who had smoking status
After standardisation for age, sex, education, ethnicity, and
disease, there was no significant difference in the response
rate for the question on the smoking status of the deceased
reported by different family members (x
= 5.08, 3 df,
p = 0.166). Likewise, the education level of the informant
= 6.6, 3 df, p = 0.086), and the age group of the
= 5.38, 5 df, p = 0.372), did not affect the
responses on smoking, giving some assurance that relatives
of those with tobacco related diseases were not likely to
differentially report the smoking status of their deceased
relatives (table 1). Further quality control indices of the new
death notification form have been published elsewhere.
The prevalence of smoking in the controls was 54.9% in males
(298/543) and 15.8% in females (92/581). This is similar to
prevalence rates found in other national population based
surveys conducted in 1995 (52% male, 17% female).
Significantly increased risks (OR) were found for deaths
from causes already known, or thought to be associated with
tobacco (table 2). These are tuberculosis (OR 1.61, 95%
confidence interval (CI) 1.23 to 2.11), COPD (OR 2.53, 95% CI
1.90 to 3.38), lung cancer (OR 4.79, 95% CI 2.86 to 8.01),
upper aerodigestive cancer (OR 3.04, 95% CI 1.89 to 4.89),
and ischaemic heart disease (OR 1.69, 95% CI 1.24 to 2.33).
Significant excesses of smokers’ increases in risk were also
found for causes of death previously thought to be
confounded by smoking, these being cirrhosis of the liver
and other alcohol related conditions (OR 1.58, 95% CI 1.11 to
2.28), and external causes (OR 1.37, 95% CI 1.09 to 1.73).
The relative risk of death from lung cancer in smokers are
lower than those found in two other South African case–
control studies among Africans only (OR 10.7 and 5.5 for
male and female smokers
in a mainly rural setting of the
Northern province, and 9.8 in males and 13.5 in females in
). This may be partly because metas-
tases to the lung from other anatomic sites may be mis-
certified as lung cancer in routine death records; partly
because in the present study some recent or ex-smokers may
have been reported as non-smokers; partly because some of
the controls may in fact have been killed by tobacco; partly
due to occupational factors; but chiefly because those who
now smoke may not have smoked intensively for long
enough to suffer the full risks of persistent cigarette use.
Nevertheless, even with all these limitations and sources of
dilution (which would also apply to other causes of death), at
least 60% of lung cancers would be attributed to tobacco.
Ischaemic heart disease comprised about a third of all
vascular deaths and the effect of tobacco on vascular disease
appears, at this stage of the epidemic, to be lower than that
expected from western countries. Nevertheless 20% of all
Table 1 Proportions reporting unknown smoking status
among cases and controls
n = 4295
n = 1952
Age group (years) (%) (%)
25–34 45.7 47.7
35–44 49.5 44.0
45–54 43.1 42.9
55–64 40.7 38.6
65–74 36.6 40.2
75+ 35.5 38.2
None 19.4 18.5
Primary 19.4 19.0
Secondary/tertiary 16.6 13.1
Unknown 66.2 70.1
Relationship of informant to deceased
Parent 42.8 54.4
Spouse 38.4 40.6
Son/daughter 36.7 41.2
Other relative 44.9 42.5
Tobacco attributable deaths in South Africa 397
Table 2 Tobacco attributed mortality in South Africa
Males Females Both sexes
Smokers Non-smokers OR AF % n* Smokers Non-smokers OR AF % n* OR 95% CI AF% n*
Tuberculosis A15–A19 185 78 1.7 28 73 31 120 1.5 7 11 1.61 1.23 to 2.11 20 84
Other lung infection J00–J39 103 71 1.2 10 17 26 128 1.3 5 7 1.32 0.98 to 1.75 7 24
COPD I26–I28; J40–J49 134 55 2.6 47 88 52 96 3.0 24 36 2.53 1.90 to 3.38 37 124
Lung cancer C33–C34 57 16 3.9 61 5 17 11 6.8 48 13 4.79 2.86 to 8.01 58 58
C00–C14; C15, C30–C32 52 19 3.1 53 38 10 19 3.5 28 8 3.04 1.89 to 4.29 46 46
C16–C26; C53; C64–C68 46 43 1.1 5 5 25 75 1.7 10 10 1.31 0.89 to 1.91 8 15
I20–I25 85 75 1.4 18 29 43 97 2.4 18 25 1.69 1.24 to 2.33 18 54
Stroke & other
I10–I15; I30–I45; I47–I49;
161 166 1.1 5 17 75 381 1.3 5 21 1.18 0.93 to 1.49 5 38
Total (cases) (823) (523) 1.5 10.6 (312) (279) (927) 1.7 5.5 (131) 1.6 1.34 to 1.90 8.3 (443)
Total (controls) (298) (245) 1.0 – (92) (489) 1.0 – 1.00 – –
Cirrhosis, etc K20–K22; K25–K31; F00–F19 77 45 1.4 – 16 47 1.9 – 1.58 1.11 to 2.28 –
Ill defined medical I46; I50; J95–J99; K90–K92;
P00–P99; O00–O99; R60–R99
178 170 1.0 – 61 328 1.1 – 1.06 0.84 to 1.33 –
External causes V00–V99; W00–W99 372 215 1.2 – 38 117 1.7 – 1.37 1.09 to 1.73 –
Total (exclusions) (627) (430) (115) (492)
All deaths 1748 1198 486 1908
Odds ratios (OR) and 95% confidence intervals (CI) are adjusted for age, sex (where relevant), population group, and education.
*n, Number of tobacco attributed deaths (zero for ‘‘exclusions’’, because of possible confounding, and for controls).
Includes cirrhosis, peptic, and oesophageal ulcers, pancreatitis and rheumatic heart disease (which is not included with vascular disease).
398 Sitas, Urban, Bradshaw, et al
vascular deaths would be attributed to smoking, if the
observed excess were causal.
South Africa has a high incidence of tuberculosis and this
rate has been increasing dramatically as a result of the HIV
Notably, about 20% of deaths caused by tubercu-
losis would be avoided if smokers had the same death rates as
non-smokers. Studies in China,
and the UK
also found smokers to have higher age standardised death
rates from tuberculosis than non-smokers. Given the high
local prevalence of latent tuberculosis and the ability of
smoking to damage the lung, this excess may well be largely
or wholly causal, making smoking a cause of one out of five
deaths from tuberculosis. This finding may be particularly
relevant to the mixed race (coloured) population of South
Africa where smoking rates are 58% in males and 59% in
and tuberculosis rates in this population are
Latent tuberculous infection can be activated by HIV and
some may hypothesise that, as in some western countries,
persons infected with HIV smoke more than uninfected
individuals. However, in a study of 2910 black cancer and
vascular disease patients mainly from Johannesburg and
Soweto, South Africa (Sitas et al, unpublished data), the age
adjusted prevalence of HIV was 5.3% in non-smokers, 6.6% in
ex-smokers, and 5.7% in current smokers (p = 0.4), so at
least, in an urban South African setting, smoking does not
seem to be associated with lifestyles leading to an increased
risk of HIV.
More smoking attributed deaths would involve COPD
(n = 124), tuberculosis (n = 87), and vascular disease
(n = 92) than lung cancer (n = 57). If the smoking
associated proportions in table 2 are typical of South Africa
as a whole, then in 1998 about 8% of adult deaths (21 500
deaths per year) in South Africa could be attributed to
smoking. These estimates are quite close to those derived for
South Africa from indirect methods.
Similar proportions of
adult deaths attributed to tobacco have been found—for
example, in China (13%)
and Mexico (15%)
proportions are likely to increase. In countries like the USA
and UK about 25% of deaths are attributed to smoking.
The advantage of this simple methodology is that once
further data are accumulated, better estimates can be derived
by subgroups like population group, and by province, and as
the system settles down it will help monitor the national and
local trends in this epidemic, whose effects in Africa or other
countries have been little studied. More countries should
consider including questions about the smoking status of the
deceased on their death notification forms, allowing compar-
isons between places with different tobacco control strate-
F Sitas, M Urban, National Health Laboratory Service, and
Witwatersrand University, South Africa
D Bradshaw, Burden of Disease Research Unit, Medical Research
Council of South Africa
D Kielkowski, National Centre for Occupational Health, National Health
Laboratory Service and Witwatersrand University
S Bah, Statistics South Africa
R Peto, Clinical Trial Service Unit, University of Oxford, Oxford, UK
Supported by: South African Medical Rese arch Council, Cancer
Association of South Africa, National Health Laboratory Service,
University of the Witwatersrand, Swiss-RE Southern Africa, Health
Systems Trust, University of Oxford Clinical Trial Service Unit (CTSU),
Yvonne Klugman Memorial Fund and National Health Information
System, Department of Health; and assisted by S Khotu, M Cassim, A
Mogkabudi, E Kritzinger, Y Saloojee, N Mavimbela, D Yach, AD Lopez,
R Pacella-Norman and J Boreham.
Conflict of interest: None.
1 Statistics South Africa. Census 2001: Census in brief. Pretoria: Statistics South
Africa, 2003, www.statssa.gov.za [Accessed 8 July 2003].
2 Reddy P, Meyer-Weitz A, Yach D. Smoking status, knowledge of health effects
and attitudes towards tobacco control in South Africa. South African Med J
3 World Health Organization. Tobacco or health: a global status report.
Geneva: WHO, 1997.
4 (South African) National Council Against Smoking. South African Cigarette
Tax vs Consumption. www.againstsmoking.org [Accessed 18 May 2004].
5 Peto R, Lopez A, Boreham J, et al. Mortality from smoki ng in developed
countries 1950–2000. Oxford: ICRF/WHO, Oxford University Press, 1994.
6 Liu B-Q, Peto R, Chen Z-M, et al. Emerging tobacco hazards in China: 1.
Retrospective proportional mortality study of one million deaths. BMJ
7 Lam TH, Ho SY, Hedley AJ, et al. Mortality and smoking in Hong Kong: case-
control study of all adult deaths in 1998. BMJ 2001;323:361–2.
8 Gajalakshmi V , Peto R, Kanaka TS, et al. Smoking and mortality from
tuberculosis and other diseases in India. Retrospective study of 43000 adult
male deaths and 35000 controls. Lancet 2003;362:507–15.
9 Bradshaw D, Kielkowski D, Sitas F. New birth and death registration forms-a
foundation for the future, a challenge to health workers? South African Med J
10 Dorrington R, Bourne D, Bradshaw D, et al. The impact of HIV/Aids on adult
mortality. MRC Technical Report. MRC: Cape Town, 2001. ISBN: 1-919809-
14-7. www.mrc.ac.za/bod/bod.htm [Accessed 18 July 2003].
11 Republic of South Africa. Department of Health. National Health Information
System. Training Manual for the Death Notification Form (BI 1663). Pretoria,
1999. http://www.doh.gov.za/nhis/index.html [Accessed 6 Nov 2003].
12 Sitas F, Pacella-Norman R, Peto R, et al. Why do we need a large study on
tobacco-attributed mortality in South Africa? South African Med J
13 Doll R, Peto R, Wheatley K, et al. Mortality in relation to smoking: 40 years’
observations on British male doctors. BMJ 1994;309:901–11.
14 Breslow NE , Day NE. Statistical methods in cancer research. Vol 1. The
analysis of case-control studies. IARC Scientific Publication 32 Lyon, 1980.
15 Republic of South Africa. Department of Health. National Health Information
System. Evaluation of the new Death Notification form B1663, Pretoria, 2001
http://www.doh.gov.za/nhis/index.html [Accessed 6 Nov 2003].
16 Mzileni O, Sitas F, Steyn K, et al. Lung cancer, tobacco and environmental
factors in the African population of the Northern Province, South Africa.
Tobacco Control 1999;8:398–401.
17 Pacella-Norman R, Urban MI, Sitas F, et al. Risk factors for oesophageal,
lung, oral and laryngeal cancers in black South Africans. Br J Cancer
18 Centers for Disease Control. Smoking attributable mortality – Mexico, 1992.
MMWR Morb Mortal Wkly Rep 1995;44:372–81.
19 Ezzati M, Lopez AD. Measuring the accumulated hazards of smoking: global
and regional estimates for 2000. Tobacco Control 2003;12:79–85.
What this paper adds
We believe this study describes the first attempt to include a
question on smoking on a revised official death notification
form for routine monitoring of the evolution of the tobacco
epidemic. Using a case–control methodology, we were able
to demonstrate that the results are reliable, and concordant to
what may be expected from indirect calculations of the
burden of tobacco related disease. Data on the effect of
tobacco are largely lacking in Africa. This initiative may
provide useful and, up to a point, generalisable data for the
continent. We also hope that by publishing this paper, other
countries (even those with limited death registration systems)
may consider altering their death notification system to
incorporate useful questions on smoking.
Tobacco attributable deaths in South Africa 399