You are on page 1of 20

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/10792612

Management of chronic respiratory and allergic diseases in developing


countries. Focus on Sub-Saharan Africa

Article in Allergy · May 2003


DOI: 10.1034/j.1398-9995.2003.02005.x · Source: PubMed

CITATIONS READS

64 1,199

5 authors, including:

Jean Bousquet Magatte Ndiaye


Centre Hospitalier Universitaire de Montpellier Cheikh Anta Diop University, Dakar
2,034 PUBLICATIONS 128,479 CITATIONS 247 PUBLICATIONS 2,002 CITATIONS

SEE PROFILE SEE PROFILE

Nadia ait khaled


International Union Against Tuberculosis and Lung Disease (The Union)
108 PUBLICATIONS 16,794 CITATIONS

SEE PROFILE

All content following this page was uploaded by Nadia ait khaled on 24 May 2019.

The user has requested enhancement of the downloaded file.


Allergy 2003: 58: 265–283 Copyright  Blackwell Munksgaard 2003
Printed in UK. All rights reserved ALLERGY
ISSN 0105-4538

Allergy Review Series VIII: Allergy: a global problem

Management of chronic respiratory and allergic diseases


in developing countries. Focus on sub-Saharan Africa

J. Bousquet1,2, M. Ndiaye1,3,
N. At-Khaled4, I. Annesi-Maesano5,
A.-M. Vignola6
1
Service des Maladies Respiratoires and INSERM
U454, CHU Montpellier; 2Centre d'Allergologie,
Institut Pasteur, Paris, France; 3H$pital Fann, Dakar,
S'n'gal; 4Chief International Union Against
Tuberculosis and Lung Diseases (IUATLD) Asthma
Divisison, Paris; 5INSERM U472, Villejuif, France;
6
Department of Internal Medicine and Pneumology
and Istituto di Fisiopatologia Respiratoria, Palermo,
Italy

Prof. Jean Bousquet, MD, PhD


Centre d'Allergologie
Institut Pasteur
25–28 rue du Docteur Roux
75015 Paris
France

Accepted for publication 26 July 2002

‘‘Chronic respiratory diseases (CRD) which include years, particularly in developing countries. Evidence also
asthma and chronic obstructive pulmonary diseases indicates that in many countries people with common
(COPD) comprise a major cause of death and disability CRD have no access to acceptable standards of health care;
for all age groups and regions in the world. In the absence health systems may also provide inappropriate care due to
of effective interventions, risk factors such as smoking, air misdiagnosis arising from respiratory symptoms which
pollution, allergen exposure, severe childhood respiratory are often common for acute and chronic illnesses.’’ (1)
infection and TB are expected to cause a further rise in In low and middle-income countries, the capacity of
the magnitude of these health problems in the coming health professionals should be expanded to address CRD.
Sub-Saharan Africa appears to be an important region of
the world that could be used to assess how the CRD
Abbreviations. ARIA: Allergic Rhinitis and its Impact on Asthma; program can be modeled and implemented.
BTS: British Thoracic Society; CD: communicable disease; COPD: In these countries, CRD (including allergic diseases)
chronic obstructive pulmonary diseases; CRD: chronic respiratory
represent only one type of major disease, and in many ins-
diseases; DALE: disability-adjusted life expectancy; DALYs:
disability-adjusted life years; DFLE: disability-free life expectancy; tances are not the main disease burden. Thus, it is import-
GBD: global burden of disease; GINA: Global Initiative for ant to propose an integrated management of disease that
Asthma; GOLD: Global Initiative for Obstructive Lung Diseases; covers communicable and noncommunicable diseases.
ISAAC: International Study on Asthma and Allergy in Childhood;
IUATLD: International Union Against Tuberculosis and Lung
Diseases; NCD: non-communicable disease; QALYs: quality-
adjusted life years; QOL: quality-of-life; SORDSA: Surveillance of Needs for equity in health around the world
Work-related and Occupational Diseases in South Africa; TB:
tuberculosis; WHO: World Health Organization; WTO: World Equity in health and healthcare has become a priority for
Trade Organization; YLD: years lived with disability; YLL: years of developed and developing countries. If the efforts at
life lost. achieving equity are to have any basis in evidence

265
Bousquet et al.

concerning which strategies are likely to work, a research countries, some Asian–Pacific areas, and the Caribbean
agenda is necessary. An adequate research agenda needs area. Such grouping has already been carried out
to (2): successfully when the GINA (Global Initiative for
Asthma) guidelines were applied to the Caribbean with
1. assess the magnitude of the problem and the burden
participants from English-, Spanish- and French-speak-
of the disease;
ing countries (4).
2. understand the genesis and correlates of the problem;
In sub-Saharan Africa, little information is available
3. propose methods to measure these correlates;
concerning the prevalence, morbidity and mortality in-
4. rigorously test alternative explanations and inter-
curred by CRD, but the limited available data and clinical
ventions.
practice suggest that chronic obstructive pulmonary dis-
Recognition of the need for integrated approaches has eases (COPD) and asthma are important— at least in some
re-emerged but the capacity to conduct appropriate populations (5). Moreover, risk factors such as tobacco
research in developing countries is weak and these smoking, air pollution, and respiratory infections are also
countries have relied on importing both researchers and very common. Finally, asthma and COPD guidelines are
their methods. While qualitative methods are needed (and rarely (and sometimes not at all) implemented in most sub-
used) in developing countries, their use will increase only Saharan African countries except for South Africa (6, 7),
if appropriate training initiatives are undertaken (3). which is the wealthiest sub-Saharan country and can be
The document entitled ‘‘Macroeconomics and Health: classified in the middle-income country group.
Investing in Health for Economic Development’’ (WHO,
December 20, 2001; bookorder@who.int) highlights a
strong and clear message for the ‘‘central task of raising Global burden of disease
the health of the poor’’. This commission was established
Disability-adjusted life years and related outcomes
in order to assess the place of health and to promote
global economic development, especially for the world’s Information on nonfatal health outcomes of disease and
poorest countries. Although this report is targeted at the injury has been largely neglected in health planning
low-income countries where communicable diseases because of the conceptual and definitional complexity of
(CDs) are the most important cause of death and measuring morbidity and disability in populations. Dis-
disability, it is also aimed at reducing the economic ability adjusted life years (DALYs) have been launched
burden of noncommunicable diseases (NCDs). by the World Bank and backed by the WHO as a measure
of the global burden on disease (GBD) combining
morbidity and mortality (8). Just like quality adjusted
life years (QALYs) (9), DALYs combine information
Reasons for the focus on sub-Saharan African countries
about morbidity and mortality in numbers of healthy
in the current document
years lost. The calculation of disease-specific health loss
A great diversity exists between developing countries. in DALYs is the sum of years of life lost (YLLs) and
Within a developing country there is a large heterogeneity years lived with disability (YLDs) weighted for severity.
of the populations. Usually, a small number of inhabit- In the DALYs approach, each state of health is assigned a
ants have a (very) high income, a large part of the disability weighting by an expert panel on a scale from 0
population has a moderate-to-low income, and often the (perfect health) to 1 (death). To calculate the burden of a
largest proportion of the population is below the poverty certain disease, the disability weighting is multiplied by
limit. These differences are increased by cultural and the number of years lived in that health state and is added
social barriers. Healthcare systems should consider all of to the number of years lost due to that disease. Future
these factors to implement a program and to achieve burdens are discounted at a rate of 3% per year, and the
equity in health. value of the lifetime is weighted so that years of life in
Extremely large developing countries like China or childhood and old age are counted less.
India, within which there is a great diversity, should be New formulae for measuring DALYs have been
studied separately and may even need subgrouping. proposed (10) and have found that the global burden of
There are also clusters of countries with a similar diseases and injuries as previously reported in the GBD
cultural, social and economic status, and similar health study (11) may therefore be underestimated. The differ-
problems. These countries may be studied more globally. ence is greatest for diseases of short duration (e.g.
Sub-Saharan African countries represent a relatively infectious diseases). Although the approach is of interest,
homogeneous group of developing countries with similar there are several criticisms (12, 13) (Table 1).
health problems. Although there are significant differ- Regional patterns of disability-free life expectancy
ences in terms of their economic situations, cultures, and (DFLE) and disability-adjusted life expectancy (DALE)
health systems, as well as linguistic differences, they may were examined by the GBD study (11). Published and
be grouped. Other groupings of countries may include unpublished data were systematically reviewed to esti-
the Maghreb, some Spanish-speaking South American mate the incidence, prevalence and duration of 483

266
CRD and allergy in sub-Saharan Africa

Table 1. Criticisms of the DALY (disability-adjusted life years) studies and 15 years ranges from 22.0% in sub-Saharan Africa to
1.1% in the established market economies. Probabilities
The DALY approach explicitly presupposes that the lives of disabled people have
less value than lives of people with disabilities.
of death between 15 and 60 years range from 7.2% for
The method assumes that disabled people are less entitled to healthcare resources women in established market economies to 39.1% for
for interventions that would extend their lives. men in sub-Saharan Africa. The probability of a man or
These assumptions may be in contrast with basic principles of the World Health woman dying from noncommunicable diseases is higher
Organization (12). in sub-Saharan Africa and other developing regions than
DALYs have been used as an outcome indicator in microeconomic evaluations as in established market economies. The leading causes of
well as sectoral prioritization exercises using league tables of cost-effectiveness.
death in 1990 were ischaemic heart disease (6.3 million
However, many of the current analyses are not comparable or transferable
because either the assumptions used differ or are unclear, and because results deaths), cerebrovascular accidents (4.4 million), lower
are not presented in a way that allows researchers or policy-makers to respiratory infections (4.3 million), diarrhoeal diseases
recalculate and reinterpret findings for use in an alternative context (170). (2.9 million), perinatal disorders (2.4 million), COPD
There are different ways of measuring DALYs (171). Incidence-based DALYs are (2.2 million), tuberculosis (2.0 million), measles (1.1 mil-
appropriate where the means of reducing the burden of disease is by prevention; lion), road-traffic accidents (1.0 million), and lung cancer
prevalence-based DALYs are appropriate when a disease cannot be prevented (0.9 million). In 1990, noncommunicable diseases were
but effective treatment is available.
therefore already major public health challenges in all
regions.
Information on cause of death among adults in sub-
disabling sequelae of 107 diseases and injuries. Prevalence Saharan Africa is essentially nonexistent (15) because
of most disability classes is highest in sub-Saharan Africa death certificates are not issued for most people. Scarce
and lowest in established market economies. Low-severity published sources provide statistics on both cause-specific
disabilities (class I and class II) are the most common. and overall rates of mortality, but closer examination
The expectation at birth of class I disability ranges from reveals that these data consist mostly of extrapolations
6.5 years in established market economies to 14.7 years in and outright guesses (16). Noncommunicable diseases
sub-Saharan Africa, and for class II disabilities, from 8.5 account for a significant portion of adult deaths in sub-
to 18.4 years. DFLE varies significantly among regions: Saharan Africa, yet the empiric bases for public health
DFLE for class I disabilities at birth ranges from policies and interventions are essentially absent. Meas-
9.9 years in sub-Saharan Africa to 47.7 years in estab- urement of the local burden of disease in sub-Saharan
lished market economies for women and DFLE for Africa may be done using years of life lost (YLL) (17).
class V disabilities ranges from 43.4 years for men in sub-
Saharan Africa to 74.8 years for women in established
Morbidity and mortality incurred by respiratory diseases
market economies. In high-income regions, nearly 90% of
in sub-Saharan Africa
expected disability is due to NCDs and most of the
remainder to injuries. In poorer regions, almost half of Chronic respiratory diseases impose an enormous burden
expected disability is due to CDs and injuries. on the Society. According to the WHO World Health
Report 2000, the top five respiratory diseases account for
17.4% of all deaths and 13.3% of DALYs.
Mortality
Reliable information on causes of death is essential to the
Chronic obstructive pulmonary disease (COPD)
development of national and international health policies
for the prevention and control of disease and injury. DALYs for COPD, based on incidence and prevalence
Medically certified information is available for less than rates from 1990, that are adjusted to 2000 mortality rates
30% of the estimated 50.5 million deaths that occur each and applied to 2000 population data, show an increase of
year worldwide. However, other data sources can be used DALYs across all regions for men and across most
to develop cause-of-death estimates for populations. To regions for women (1). It is estimated that mortality
be useful, estimates must be internally consistent, plaus- for COPD will continue to increase within the next
ible, and reflect epidemiological characteristics suggested 10–20 years (18, 19) due, in particular, to tobacco
by community-level data. smoking, and possibly air pollution (20).
The GBD study used various data sources and made The recent review published on COPD in Africa (5)
corrections for the miscoding of important diseases (e.g. explained the reasons of the paucity of data in this region
ischaemic heart disease) in order to estimate worldwide of the world and gave the results of several studies
and regional cause-of-death patterns in 1990 for 14 conducted on the prevalence of chronic bronchitis in this
age–sex groups in eight regions, for 107 causes (14). region. These studies were generally conducted among
Ninety-eight percent of all deaths in children younger men in occupational settings in whom smoking was
than 15 years are in the developing world; 83% and 59% common. In the nonexposed control group, the preval-
of deaths at 15–59 and 70 years, respectively, are in the ence of chronic bronchitis obtained by questionnaire is
developing world. The probability of death between birth lower than in the exposed group and varies between 3.5%

267
Bousquet et al.

in Annaba (Algeria) to 11% in Cape Town (South ISAAC study, it was found that a very high percentage of
Africa). children were suspected of presenting rhinitis in sub-
In sub-Saharan Africa, air pollution is a result of Saharan Africa with prevalences (assessed by question-
tobacco smoking, industrialization, domestic pollution, naire) of up to 50% (29, and personal communication
and vehicular fuel combustion. Risk factors for COPD from Aı̈t-Khaled,) (Figs 1 and 2). The reasons explaining
such as tobacco smoking and occupational agents are these very high prevalences of rhinitis are unclear and
well known. The role of indoor-air pollution appears to may be related to the children misunderstanding the
be of importance in places like China (21), but little is questionnaire.
known about sub-Saharan Africa and more research is Systematic international comparisons of the preva-
needed (22). Cooking fuels (wood, charcoal, electricity, lences of asthma and other allergic disorders in children
and liquefied petroleum gas) were found to increase acute are needed for a better understanding of their global
respiratory infections in sub-Saharan Africa (23, 24). epidemiology, to generate new hypotheses, and to assess
existing hypotheses of possible causes. The worldwide
prevalence of asthma, allergic rhinoconjunctivitis
Asthma
(Fig. 3), and atopic eczema, was investigated by ques-
The assessment of the burden of asthma is more tionnaire in the ISAAC study; 257 800 children aged
difficult. Mortality is important in asthma and it is 6–7 years from 91 centers in 38 countries, and 463 801
estimated that 180 000 asthmatics die every year children aged 13–14 years were studied in 155 collabor-
(WHO, 1999). Deaths have also been recorded in sub- ating centers in 56 countries (30). The centers with the
Saharan Africa (25). The assessment of the burden of lowest rhinitis prevalences were similar to those for
asthma is also challenging (1). Even when using the asthma symptoms. In the past year, the prevalence of
same research protocol, reports on asthma prevalence rhinitis with itchy, watery eyes (‘‘rhinoconjunctivitis’’)
have shown huge variations for children and adoles- varied across centers from 0.8% to 14.9% in the 6–7-
cents within and among countries. Less variable data year-olds and from 1.4% to 39.7% in the 13–14-year-olds
were shown for adults. To make country-specific (29). Some sub-Saharan African studies have been
estimates of asthma for the GBD 2000, comparable published (31).
data are needed.
In African migrants, such as Ethiopian migrants in Prevalence of asthma in rural and urban areas in sub-
Israel, asthma may be extremely common (26). Saharan Africa. Asthma appears to be a growing but
neglected public health problem in Sub-Saharan Africa
ISAAC study. Rhinitis is usually present in asthma and (32–44). Urbanization was shown to increase asthma
constitutes a risk factor for asthma (27, 28), at least in prevalence in South Africa (45) and other parts of sub-
developed countries and in occupational asthma. In the Saharan Africa (33–38, 43, 44) (Table 2).

Figure 1. Prevalence of self-reported rhinitis in Africa (source: Aı̈t-Khaled).

268
CRD and allergy in sub-Saharan Africa

Figure 2. Prevalence of self-reported asthma in Africa (source: Aı̈t-Khaled).

It appears that asthma is uncommon in rural areas and adoption of an urbanized ‘‘western’’ lifestyle as suggested
more common in urban areas (38). In developing coun- by a study carried out in southwest Ethiopia (37).
tries, asthma and allergy may be associated with the Asthma was reported by 3.6% of the children in the
urban group and was absent in the rural group. Atopy
was a strong risk factor for asthma in urban Jimma.
In the rural areas, skin sensitivity to mixed threshings
was only slightly less common than in urban Jimma,
whereas sensitivity to Dermatophagoides pteronyssinus
was significantly more common. Wheeze or sensitivity to
D. pteronyssinus were positively associated with housing
style, bedding materials, and with use of malathion
insecticide, but no single factor accounted for the urban–
rural differences.

Links between asthma and allergy in sub-Saharan


Africa. The links between asthma and environmental
allergens have been recently questioned in developed
countries (46), but in these countries most asthmatics
are also atopic (47). In sub-Saharan Africa, little is
known concerning allergy sensitization, and the relation-
ship between allergy and asthma may present some
specificity.
In sub-Saharan Africa, aeroallergens have been iden-
tified (48, 49), but the exposure differs between developed
countries and sub-Saharan Africa. The frequency of cat
and/or dog ownership in Ghana is comparable to that in
the UK (approximately 50%). However, in Ghanaian
communities pets are predominantly kept outdoors.
Levels of pet allergens in Ghanaian homes with pets
Figure 3. Worldwide prevalence of allergic rhinitis (ISAAC were between 75-fold (dog) and 275-fold (cat) lower than
questionnaire) (28). levels in homes with dogs and cats in the UK, and were

269
Bousquet et al.

Table 2. Urban and rural differences in the prevalence of asthma

Prevalence rate (%) Atopy (%)

Reference Country Age group Outcome measure Urban Rural Urban Rural

Godfrey 1975 (34) Gambia School children Diagnosed asthma Present None
Van Niekerk 1979 (35) South Africa Children Exercise challenge 3.17 0.14
Addo-Yobo 1997 (36) Ghana 9–16 years Exercise challenge 4.7* 1.4 6.55** 2.9
Ng'Ang'A 1997 (37) Kenya 8–17 years Exercise challenge 22.9 13.2 30.1 11.1
Yemaneberhan 1997 (38) Ethiopia Wheeze 13.3 4.35 11.0 7.6
Asthma 18.95 6.4
Odhiambo 1998 (39) Kenya Asthma 9.5 2.8 26 10.9
Rhinitis 9.7 1.5
Nyan 2001 (44) Gambia Wheeze 4.4 3.5 35.3 22.5
Walvaren 2001 (45) Gambia ‡15 years Wheeze 4.1 3.3 7.5 3.8
Diagnosed asthma 3.6 0.7
Chronic bronchitis 0.6 1.2

* Urban rich.
** Urban poor.

also lower than or comparable to levels in homes without Ethiopia of intestinal parasite (hookworm) infection and
pets in the UK (50). domestic allergen exposure with risk of wheeze. This
Sensitization to dust-mite and cockroach allergens, suggests that a high degree of parasite infection might
inner-city residence, and low position in sib-ship were prevent asthma symptoms in atopic individuals (58). The
found to be independent risk factors for asthma in differences in these studies may, however, be related to
Ghanaian children (51). the parasite concerned.
In a recent study in East Africa (52), it was found that Th2 responses without atopy may be associated with
although most patients were atopic, few were asthmatics, immunoregulation in chronic helminth infections and
and there was no correlation between atopy and asthma. reduced allergic disease (59). The increase of allergic
The study suggests that in tropical areas where parasites diseases in the industrialized world has often been
are endemic, the relationship between asthma and immu- explained by a decline in infections during childhood
noglobulin E (IgE) is different from that of areas without (60). The immunological explanation has been put into
major parasitic disease. However, in this study, atopy was the context of the functional T cell subsets, known as Th1
defined ‘‘as any specific IgE over 0.35 kU/L’’ and this and Th2, which display polarized cytokine profiles. This
definition may raise some problems (53). Levels of specific notion is contradicted by observations that the prevalence
IgE between 0.35 and 0.70 kU/l are positive using the CAP of Th1-autoimmune diseases is also increasing and that
system (Pharmacia, Uppsala, Sweden) but may be consid- Th2-skewed parasitic worm (helminth) infections are not
ered as borderline in allergic patients, and even more so in associated with allergy. More recently, elevations of
people with very high IgE levels. In the study, over 30% of antiinflammatory cytokines, such as interleukin (IL)-10,
subjects had total IgE > 2000 kU/l and over 60% had which occur during long-term helminth infections, have
total IgE > 1000 kU/l. Although the CAP system is a very been shown to be inversely correlated with allergy (61, 62).
reliable test, which does not appear to be influenced by The induction of a robust antiinflammatory regulatory
total IgE levels (54), it is possible that extremely high total network by persistent immune challenge offers a unifying
IgE levels may induce some nonspecific binding. explanation for the observed inverse association of many
Many local allergens may not yet be identified. Nonal- infections with allergic disorders (Fig. 4) (63). A high
lergic triggers may be more important than in developed degree of parasite infection may prevent asthma symp-
countries. Indoor- and outdoor-air pollution, including toms in atopic individuals (58). Some studies suggest that
tobacco smoke, is an important cofactor for asthma. in tropical areas where parasites are endemic the rela-
tionship between asthma and IgE is different from that in
Links between asthma, allergy, and parasitosis in sub- areas without major parasitic disease (52, 64–66).
Saharan Africa. Parasitic diseases may be a confounding The lack of cross-reactivity between parasite and
factor. Early studies suggested that parasitic diseases inhalant allergen antigens has been discussed (67). It has
prevent the onset of asthma (33, 55, 56). On the other been shown that Dermatophagoides and cockroaches
hand, different studies suggested that groups of patients share common allergens with some unrelated allergens
who respond immunogenically to Ascaris infestation such as snails (68), crustaceae, or Anisakis (69). Both
might be predisposed to allergic diseases such as asthma parasites and house-dust mites contain cysteine proteases
(57). Recent studies have confirmed independent effects in (70, 71) which may cross react.

270
CRD and allergy in sub-Saharan Africa

Figure 4. Divergent outcome of Th2 responses in industrialized and developing countries (63). Depending on the nature of the signals
they receive from the microenvironement, dendritic cells (DC) develop into distinct subpopulations and direct T cell differentiation
into polarized subsets (Th1 and Th2). When uncontrolled, strong Th1 or Th2 responses can lead to autoimmunity or allergy. High
pathogen burden can change the physiology of the microenvironment that endow dendritic cells to induce T regulatory cells (Tr),
which produce immunosuppressive molecules interleukin (IL)-10 and transforming growth factor (TGF)-b.

king, and possibly tuberculosis, were found to be


Occupational lung diseases
confounding factors.
For several years, miners and founders have been known A large nationwide surveillance study is now available
to suffer from pneumoconiosis, often associated with in the region. The Surveillance of Work-related and
tuberculosis and tobacco smoking (72–75). Occupational Respiratory Diseases in South Africa
More recently, asthma, COPD, chronic cough, and/or (SORDSA) was established in 1996 to provide systematic
rhinitis induced by occupational exposure have been information on occupational respiratory diseases (86, 87).
identified in developing countries (76–83). They represent In the first 2 years of the program (ending October 1998),
a major burden for many workers. In the world’s poorest 3285 cases of occupational respiratory disease were
countries, technologies that are obsolete or banned in reported to SORDSA by 203 doctors and 97 occupational
industrialized countries are still largely used (84). Result- health nurses. After pneumoconiosis, occupational
ing occupational illnesses are also generally less visible asthma was the second most commonly reported disease
and not adequately recognized as a problem in low- (6.9%). The average annual incidence for occupational
income countries (85). People outside the workplace can asthma in South Africa was 13.1 per million employed
also be affected through, for example, work-related people. Latex was the most frequently reported agent for
environmental pollution. occupational asthma, followed by isocyanates and plat-
The same agents are found in developed and develop- inum salts. Low-molecular-weight agents accounted for
ing countries (86, 87), but some agents are specific to 59.6% of the cases of occupational asthma. Such a
developing countries, and the levels of exposure are not comprehensive program may be used in other developing
usually controlled, making the diseases more prevalent countries to assess the prevalence of occupational CRD
and severe than in developed countries. Tobacco smo- and to develop prevention and intervention programs.

271
Bousquet et al.

However, in sub-Saharan Africa, occupational diseases tious and parasitic diseases of childhood remain a
are not usually compensated, and patients continue to priority. At the same time, noncommunicable diseases,
work with lung diseases of increasing severity. including CRD, are emerging as a serious problem in
countries at intermediate stages of the epidemiological
transition (100). Noncommunicable diseases will
Other chronic respiratory diseases
undoubtedly represent tomorrow’s pandemics in devel-
Other CRD are of great importance in sub-Saharan oping countries (101). There is already evidence that the
Africa and should also be taken into account for a global prevalence of certain noncommunicable diseases, such as
program. Some of these are important and include: diabetes, asthma, COPD, epilepsy, and hypertension, is
increasing rapidly in some parts of sub-Saharan Africa
1. Sequelae of tuberculosis and of acute pulmonary in-
(102, 103). However, in many sub-Saharan African
fections in the form of bronchiectasis, pachypleuritis,
countries such as Zambia, there is no obvious policy on
aspergillosis, and/or fibrothorax (88–91). In sub-Saha-
noncommunicable diseases and no accurate information
ran Africa, HIV infection represents a very important
about their burden (104). Tobacco smoking is a critical
risk factor for recurrence of tuberculosis (92).
problem to be dealt with urgently (105).
2. Tropical pulmonary eosinophilia results from a
Concern has been expressed that the available
hypersensitivity reaction to lymphatic filarial para-
resources to deal with communicable diseases would be
sites and may lead to long-term sequelae of
reduced by increasing the emphasis on noncommunicable
pulmonary fibrosis with chronic respiratory fail-
diseases. The latter, however, already present a substan-
ure (93).
tial burden because their overall age-specific rates are
3. Two forms of pulmonary involvement in schistosomi-
currently higher in adults in sub-Saharan Africa than in
asis can be observed. The acute form usually occurs
populations in established market economies (102). To
about 6 weeks after the infection (Katayama syn-
ignore the noncommunicable diseases would inevitably
drome) and seems related to an allergic manifesta-
lead to an increase in their burden; the provision of health
tion to the presence of worms or eggs. The chronic
services would be largely undirected by issues of clinical
involvement is in the form of pulmonary hyperten-
and cost-effectiveness, and their treatment and prevention
sion with cor pulmonale, pulmonary granulomatous
would be left to the mercy of local and global commercial
schistosomiasis, and pulmonary arteriovenous fistu-
interests (102).
las (94–96). These chronic pulmonary complications
Health systems should have short-, medium- and
usually occur in less than 5% of infections (94) but
long-term policies. The management and prevention of
some limited data suggest a prevalence of up to 25%
noncommunicable diseases should be considered in con-
of infected people (97).
junction with those of communicable diseases with which
they often interact.
Improved surveillance of all diseases within sub-Saha-
Prioritization of health programs in developing countries
ran Africa is needed in order to place noncommunicable
and importance of the CRD program
diseases properly within the context of the overall burden
Importance of noncommunicable diseases in developing countries of disease. Research is needed to guide improvements in
the clinical and cost-effectiveness of resources currently
There is no doubt that, for the next 10–20 years,
committed to the care of patients with noncommunicable
communicable diseases will remain the predominant
diseases, and to direct and evaluate preventive measures
health problem for the populations in sub-Saharan
(102).
Africa, even for adults. In sub-Saharan Africa, there is
a high childhood and maternal mortality and relatively
short life expectancy. Mortality in childhood is mainly Importance and diversity of CRD in developing countries
due to diseases like malaria, measles, poliomyelitis,
In developing countries, CRD represent a challenge to
tetanus, diarrhea, and acute respiratory tract infections.
public health because of their frequency, severity, pro-
Diseases like filariasis, schistosomiasis, and leprosy,
jected trends, and economic impact. Healthcare planners
which are now readily controlled by drugs, still cause
are faced with a dramatic increase in tobacco use and
considerable morbidity. In adults, tuberculosis and
must establish priorities for the allocation of limited
malaria will remain the highest priorities among public
resources. Major CRD in both developed and developing
health problems during the next two decades.
countries include COPD (21) and asthma (106). Thus,
Economic transition is the term used to describe the
smoking prevention and standardized management pro-
change in disease patterns associated with economic
grams for asthma and COPD should be implemented in
development (98, 99). Health systems in developing
developing countries whenever possible (107). However,
countries faced major challenges in the 1990s and beyond
other CRD should be taken into account (see Other
because of a growing epidemiological diversity, rapid
chronic respiratory diseases).
economic development and declining fertility. The infec-

272
CRD and allergy in sub-Saharan Africa

The CRD program should be applied together with the WHO Global Report, in 1990–92, the overall
other health programs. There is need for concerted efforts consumption in Africa is estimated at 600 cigarettes/
on the part of African governments, health administra- adult/year. The richest countries of Africa show the
tors and health workers to ensure that necessary attention highest consumption. In low-income countries, smoking
is given to multidisciplinary research on the subject so and other uses of tobacco indicate a relative increase in
that meaningful control measures can be formulated, wealth (112). Currently, Mauritius, South Africa, and
thereby ensuring clean air for the people to breathe. As an Botswana have consumption rates similar to those in
example, several recent initiatives by nongovernment developed countries. Consumption in middle-income
organizations (NGOs) and the WHO have highlighted countries such as Cameroon and Senegal is around
the need for concerted approaches to lung health that 800/adult/year (113). While consumption rates have
require addressing two major threats, tuberculosis and declined slightly in developed countries, rates are increas-
tobacco smoking (108). ing throughout the developing world. The Food and
Agriculture Organization (FAO) estimates that the level
of consumption in Africa will be one of the highest in the
world if nothing is done to stop this rate of growth (112).
Features of developing countries: social and economic
The aggressive marketing campaigns of international
vulnerability and barriers
tobacco companies are encouraging young men and boys
Low-income developing countries can be characterized by in particular to spend their precious disposable income on
social and economic vulnerability that induce cultural cigarettes, which can be bought one at a time (114).
barriers to CRD management (1, 109, 110). Women in Africa and Asia, whose smoking rates are low,
are the next market to be targeted by the tobacco industry
(115).
Generic barriers
Pollution is another well-identified barrier that appears
There are several generic barriers, of which heavy debts to be of great importance, but precise information is
and poverty represent major problems. Poverty is wide- unavailable for sub-Saharan Africa. Automobile pol-
spread among rural Africans and increase in elderly (111); lution is often extensive in urban and suburban areas
it is associated with poor health and unsatisfactory access since most cars and diesel vehicles are old and poorly
to healthcare. In sub-Saharan Africa, a large part of the maintained, emitting far more pollutants than in devel-
population is rural, consisting of farmers and breeders. oped countries. Occupational pollution is also important
They live in small communities with a heavy workload. (see 3,4). Indoor-air pollution is another poorly under-
Rural exodus is explained by the dryness and the spread stood problem related to indoor cooking fuel. The effects
of the desert, and by poverty, causing overpopulation of of indoor pollution are worsened by poor living condi-
the towns, and development of shantytowns in so-called tions.
‘‘suburban’’ areas. Poor nutrition is common in sub-Saharan Africa
This vulnerability (over half of these populations live (116–118). It was felt that urbanization of the popula-
below the poverty threshold) is going to cause an tion would lead to improved nutrition (119) but
important disparity in the different methods of financing economic problems and structural reforms have had
healthcare. dire effects on urban populations. Today, increasing
There are many other barriers including poor educa- poverty and the effects of globalization are again
tion, illiteracy of many people, lack of sanitation, and increasing nutritional problems for the suburban areas
poor infrastructure. (120).

Environmental barriers Drug availability and accessibility: from the Bamako Initiative
to the Doha declaration
Tobacco smoking is a common environmental barrier
throughout the world, particularly so in some parts of There is increasing pressure on developing countries to
sub-Saharan Africa. In many countries, the recently improve the social, political, and economic status of their
decreed anti-tobacco-smoking legislation has been people. Despite the Bamako Initiative (121, 122) there
adversely affected by successful advertising of the multi- remain situations where drugs are unavailable or there is
national tobacco companies. Aware of their economic poor access to drugs; efforts must be made to ensure that
weight and importance, they have reinforced their pro- essential drugs are available to all (123), particularly
motional policies in these countries, promoting tobacco inhaled corticosteroids (124) and, b2-agonists. The non-
in terms of modernity, liberation, and well-being. availability of drugs most needed for healthcare and
These ill-founded ideas are sure to have an effect on disease control in sub-Saharan Africa is not only due to
smoking habits, with an increase in the number of insufficient funding, but also due to the use of limited
smokers, especially in young adults, and more smoking funds for expensive drugs that have little bearing on the
in public places (both passive and active). According to disease pattern.

273
Bousquet et al.

The Bamako Initiative in the African region of the In the rural and suburban areas, the organization of
World Health Organization was designed to ensure healthcare services has common major drawbacks
regular availability of drugs, especially to primary (Table 4 and Fig. 5). In rural areas, most resources are
healthcare facilities. Seed drugs are provided to the used for the management of acute infectious or parasitic
health institutions either by the National Government or diseases, and for prevention of maternal and perinatal
through external aid. These are sold to patients for a mortality.
small profit. The proceeds are used to replenish stocks
and the small profit is used to improve services in the
Patient barriers
health center. The introduction of these programs to
countries like Nigeria, Gambia, Guinea, and Senegal has Patient barriers are also of major importance, such as
improved considerably the availability of drugs over the associated languages (131), and religious and cultural
past couple of years and should soon start to yield beliefs and taboos. For example, in Senegal, hematuria is
measurable improvements in the health situation considered a sign of virility within the Soninké ethnic
(125–129). Like any other form of financing health group where schistosomiasis is highly prevalent.
service, the Bamako Initiative is not free of difficulty The number of elderly people in sub-Saharan Africa is
(130). Moreover, many people cannot use Bamako growing rapidly, and there is an increase in life expect-
Initiative Health Centers for financial reasons. ancy; at the same time the proportion of children is
The members of the World Trade Organization (WTO) declining (132). This has several implications, such as the
issued an historic Ministerial Declaration in Doha stating erosion of social support by extended families, dramatic
that the Agreement on Trade-Related Aspects of Intel-
lectual Property Rights (TRIPS) should be interpreted
Table 4. Major drawbacks in the organization of healthcare services in the rural
and implemented so as to protect public health and
and suburban areas
promote access to medicines for all. WHO welcomed this
declaration and looks forward to working together with Inaccessibility of healthcare facilities (distance, nonexistence, lack of application)
WTO and others to achieve these objectives (Statement Disparity in the establishment and implantation of healthcare facilities
WHO/18, November 15, 2001). Poor and insufficient technical support
International agencies should define the essential drugs, Lack or nonexistence of qualified personnel: the health posts are usually run by
nurses. Training is not similar between the different countries
and encourage the use of generic drugs, particularly for
inhaled corticosteroids. For such programs to be effect-
ive, producers of high-quality generics will need to be
identified, and the medications added to national lists of
essential drugs and included in procurement procedures
(107). communicable
diseases
Organization of healthcare services
Economic and cultural barriers in sub-Saharan Africa
usually result in at least three distinct groups of medical
care: people living in urban areas, suburban areas, and non-communicable
rural areas. These groups need to be addressed separately diseases
for the management of CRD (Table 3). In sub-Saharan
Africa, a minority of people are in the first category; the
majority are in rural areas.

Table 3. Distinct groups of medical care in Sub Saharan Africa low-income middle-income high-income
country country country
People living in urban areas with a high income and with a settled and sedentary
lifestyle. These include: Figure 5. Coexistence of communicable and noncommunicable
rich people who can afford expensive investigations and treatments diseases in the same country. Communicable and noncommu-
government workers who are compensated for investigations and treatments nicable diseases coexist within the same country. In low-income
workers of industry, agriculture, or the third sector who are compensated for countries, communicable diseases are more common than non-
investigations and treatments communicable diseases. In high-income countries, the inverse
People living in urban areas who are jobless or have limited financial resources, and relationship exists. However, within a single country there are
people living in the poor so-called ``suburban'' areas. These usually have similar
differences such as those found in urban (communicable diseases
healthcare management and will be in the document ascribed to ``suburban
and noncommunicable), suburban (communicable diseases >
areas''
noncommunicable) and rural (communicable diseases >>>
Poor people living in rural areas
noncommunicable) areas of sub-Saharan Africa.

274
CRD and allergy in sub-Saharan Africa

changes in disease patterns, and increases in rates of same principles, a strategy for COPD management in
cancer and noncommunicable diseases, in particular Africa has been recently proposed by IUATLD (5, 107).
CRDs. The relevance of guidelines in developing countries is
difficult to assess and differences largely depend on the
area of the country. It is clear that in sub-Saharan Africa,
Parallel medicine
guidelines are inapplicable for the majority of the
In sub-Saharan Africa, parallel medicine is extremely population.
important with many traditional healers. This is usually It has been proposed that it may not be desirable to
the first step in the management of diseases due to merge all guidelines, but it does seem that a patient-
cultural beliefs and taboos, the inaccessibility of health- targeted approach is required, and since there is much
care, and drug costs. The theory behind traditional overlapping among CRD, the merging of guidelines in an
medicine in the several black ethnic groups of Africa is integrated approach may be needed (1). Most asthmatics,
essentially similar. Disease is a supernatural phenomenon if not all, have rhinitis (28) and in many patients, COPD
governed by a hierarchy of vital powers beginning with a and asthma are difficult to distinguish (21). Many
most powerful deity followed by lesser spiritual entities, asthmatics smoke and are exposed to indoor- and
ancestral spirits, living persons, animals, plants, and other outdoor-air pollutants that can induce COPD. Finally,
objects. These powers can interact, and they can reduce it will be necessary to merge certain key elements from
or enhance the power of a person. Disharmony in these each guideline document into an algorithm for use at the
vital powers can cause illness. Thus, ancestral spirits can first point of contact of a respiratory patient with the
make a person ill. Ingredients obtained from animals, health service. Such an approach has been discussed in
plants, and other objects can restore the decreased power the CRD consultation document (1).
in a sick person and therefore have medicinal properties. Existing guidelines are usually comprehensive and have
Traditional healers are enshrined in the minds of the been developed using the evidence-based model. For
people and respected in their community, and they are asthma, three updates have being finalized or are in the
often opinion leaders. Unfortunately, there have been no process of being finalized: the GINA (137), the BTS
studies on the efficacy of traditional remedies (133). They (British Thoracic Society) and the IUATLD guidelines.
are believed to be effective in diarrhea, headache, and
other pains, as well as for sedation. Success in treating
psychological problems is well known and often recog-
Requirements and aims for CRD management in developing
nized. Traditional medicine has been confronted by the
countries
quest for new sources of legitimation (134) that has not
been proven. In many places, traditional medicine and In a recent paper, Unwin et al. (138) proposed the
modern medicine have tended to work in tandem (135). following characteristics to implement a program in a
In South Africa, traditional healers have flourished in developing country:
the face of competition from modern medicine. In 1995, it
1. The disease is chronic.
was thought that about 200 000 traditional healers were
2. Effective measures exist for controlling symptoms
practicing in South Africa, compared with 25 000 doctors
and preventing complications.
of modern medicine; 80% of the black population use the
3. These measures need to be delivered to the patients
services of traditional healers (133).
over long periods.
4. They require well-organized healthcare systems for
this to be done effectively.
Gaps, relevance and the integration of different guidelines
There are several objectives of a strategy for the
in developing countries
effective control and prevention of common CRD within
The CRD working group identified several gaps in the sub-Saharan Africa (Table 5) (107,138).
current CRD guidelines (1). Moreover, GINA (Global In order to implement the program, outcome measures
Initiative for Asthma) (106) and GOLD (Global Initiative should be used. They will necessarily differ from those used
for COPD) (21) are not patient-oriented guidelines, in developed countries.
whereas ARIA (Allergic Rhinitis and its Impact on
Asthma) tends to be more global for patients with asthma
and rhinitis (28). GINA and GOLD are not targeted Outcome measures for CRD in developing countries
towards their application to developing countries whereas
Classical outcome measures
ARIA has a specific section. Asthma management for
developing countries was proposed in the IUATLD Assessment of interventions of the CRD program must
(International Union Against Tuberculosis and Lung use outcome measures that are appropriate for develop-
Diseases) asthma guide (136). It considers affordability ing countries (139). Outcome measures used in developed
and availability of drugs and local needs. Based on the countries are often poorly applicable to developing

275
Bousquet et al.

Table 5. Objectives for a strategy for the effective control and prevention of Table 6. Problems with measurements of FEV1 (forced expiratory volume in 1 s) in
common chronic respiratory disorders (CRD) (107) sub-Saharan Africa

Develop guidelines that are adapted to local contexts The reference values for lung function parameters have been published in some
Evaluate the adapted guidelines, including guideline review criteria and quality populations (172–174) but may not apply to all the ethnic groups
standards FEV1 cannot be used at present for the vast majority of the population and a special
Ensure their distribution for the treatment of CRD at primary-care level in effort should be made to increase the availability of the test. However, it is clear
sub-Saharan African countries that spirometry will not be possible in the near future in all parts of developing
Develop and assess rapid evaluation methods for assessing the quality of CRD countries
care at a health district or country level Peak expiratory flows (PEF) can be used more easily everywhere. Although PEF may
Upgrade equipment at district level not be as accurate as FEV1, reversibility of the airflow obstruction may be done
Purchase high-quality drugs at low prices easily. In this case, the validity of the PEF measurement should be monitored by
Provide routine training and supervision of health service personnel specific studies in pilot trials
Develop and implement a protocol for assessing current policy and opportunities Training of healthcare personnel should be carried out
for health promotion at a national level for the different CRD
Through baseline prevalence surveys, provide new knowledge on the epidemiology
of CRD and major risk factors for these conditions, and on current national These outcome measures are usually less responsive
policies for the prevention of noncommunicable diseases within the countries
than in asthma (142–145) and should be applied for
longer times than for asthma (at least 1 year).
Thus, very few responsive outcome measures may be
applied to assess intervention for COPD in developing
countries; moreover, race, ethnicity, or culture may countries.
influence asthma outcomes (140).
Lung function measurement
Asthma. For asthma, outcome measures include lung
function measurements, symptoms, rescue medication Measurement of lung function using simple and inexpen-
needs, control of asthma, exacerbations, hospitalization sive methods is a major issue for the CRD program.
rate, and quality-of-life (QOL) measures (141). These FEV1 and other lung function parameters can be studied
measures are usually not applicable to most parts of in all countries but only in reference hospitals (146,147)
developing countries, and QOL is mostly inapplicable or eventually in occupational settings (76,78–82). In the
because there are social and cultural problems that are middle-income countries of Africa (at least in Algeria,
not taken into consideration in these measures. Morocco, Tunisia, and South Africa), the spirometry is or
Hospitalization rates cannot usually be used since there may be available at district level. In these countries, the
are very few ICU or hospital beds in central hospitals or progressive development of health structure at district
university hospitals, and they may not exist elsewhere. In level will be directly linked with the political involvement
most African countries, there is one hospital per district, for the management of CDR. The choice and the
but in rural areas this is devoted to CD and national maintenance of equipment will be essential for the
health programs. CRD are not yet listed as a national sustainability of eventual national intervention on
health program in sub-Saharan African countries. More- CDR. Moreover, there are problems with FEV1 meas-
over, there is no register to account for hospitalization urements in low-income countries (Table 6).
rates. These registers were found to be of paramount There are some other outcome measures used for all
importance for the assessment of tuberculosis prevalence diseases that may be used by the CRD program. They
and its management in district hospitals. The IUATLD include mortality rates, the assessment of the burden of
guide proposed the same information system as for the disease, and the assessment and follow up of
tuberculosis with a register for persistent asthma. A occupational lung diseases.
routine evaluation of patient outcomes will be possible
using a quarterly report based on the register. This
Global burden of disease measures
evaluation is likely to be the cornerstone of a manage-
ment program for asthma in developing countries. Global burden of disease (GBD) measures seem to be
applicable to developing countries. DALY studies have
COPD. For COPD, outcome measures are even more confirmed the efficacy and cost-effectiveness of many
difficult to use since most treatments are not very effective interventions in middle-income countries for AIDS (148)
in preventing the alteration of lung function, and studies or in low-income developing countries, such as Sri Lanka,
should be carried out over long periods. Usual outcome where the highest burden was due to noncommunicable
measures used in trials include symptoms, exacerbations, diseases, as their duration and degree of disability are
hospitalizations, forced expiratory volume in 1 s (FEV1), high (149). In Africa, DALYs supported the environ-
other functional parameters, and QOL. Hospitalization mental management for malaria control (150). In Japan,
rates cannot usually be used for the same reasons as for DALYs was used to assess the deleterious effects attrib-
asthma. utable to tobacco (151).

276
CRD and allergy in sub-Saharan Africa

A methodology should be developed to assess the


efficacy of interventions in populations. Trials similar to
those used to assess practice interventions may be
Tertiary Hospital designed. These trials randomize practices instead of
referral patients and need some specific statistical methods
(153,154). In developing countries, a trial may compare
Secondary communities or villages in which an intervention has been
referral Low level of initiated with others in which there has been no
equipment intervention. Randomization will not be based on the
Health-care patient’s characteristics but on the features of the site.
There may be baseline imbalances between sites and these
workers
need careful understanding and evaluation. The choice of
the units of analysis (outcome measures) will be most
important where there are large numbers of patients
Patients recruited from each site and/or a high degree of variab-
ility within patients (153,154).
Figure 6. Referral of patients in developing countries. In order to select the units (outcome measures) to be
used, the goal(s) of the program should be clearly stated.
New formulas for measuring DALYs have been As an example, the Roll Back Malaria (RBM) WHO
proposed (10) and have found that the global burden of initiative, started in 1998, had the ambitious goal of
diseases and injuries, as previously reported in the GDB halving the malaria burden by the year 2010, and halving
study (11), may be underestimated. The difference is it again in the next 5 years. Such goals are easier to
greatest for diseases of short duration (e.g. infectious propose and implement for parasitic and infectious
diseases). diseases than for noncommunicable diseases.
Reliable information on causes of death is essential to Some models can be used such as the inner-city asthma
the development of national and international health program (P15). Some studies have already assessed
policies for the prevention and control of disease and differences in asthma management between white Euro-
injury. Mortality data can be used in COPD but not in pean and Indian-subcontinent ethnic groups living in
asthma because the numbers are too low. Moreover, socioeconomically deprived areas in the Birmingham
information on the cause of death among adults in sub- (UK) conurbation (155). However, this study and the
Saharan Africa is essentially nonexistent (15). In the National Cooperative Inner-City Asthma Study (NCI-
absence of accurate and comprehensive registries of vital CAS) implemented in the USA (156,157), dealt with
events for the majority of the region’s inhabitants, health resources which were far more advanced than in
longitudinal studies of defined population-based cohorts the suburban areas of sub-Saharan Africa.
represent the only realistic strategy to fill this void in basic
public health information. Years of life lost (YLL) can be
used in sub-Saharan Africa (17).
Cost-effectiveness trials

Assessment and follow-up of occupational respiratory diseases Cost-effectiveness analyses should be included in all trials;
analyses using a decision-analysis model linking epidemi-
In places where longitudinal studies can be carried out, ological data with economic information have been
the serial measurement of lung function and the assess- proposed for AIDS (158), meningitis (159), and tubercu-
ment of symptoms should be carried out. A comprehen- losis (160,161). DALYs can be used for cost-effectiveness
sive program like the nationwide SORDSA surveillance analyses and were found useful for parasitic diseases such
may be used in other developing countries to assess the as malaria (150,162,163) and AIDS (164,165). Since data
prevalence of occupational CRD and to develop preven- are scarce, even for a disease such as malaria, models that
tion and intervention programs. include probabilistic sensitivity analyses have been pro-
posed to calculate DALYs, averted for each intervention
by economic strata (162).
Trials to assess efficacy of interventions in developing Some projects have already started to tackle the
countries emerging pandemic of noncommunicable diseases in
sub-Saharan Africa. Methods are being developed and
Double-blind, placebo-controlled, randomized controlled piloted in urban and rural Tanzania and Cameroon for a
trials (DBPC-RCT) can be performed in Africa (152) but community-based program on high blood pressure (166).
such trials do not seem necessary to evaluate the CRD A project, funded by the Department for International
program and do not make it possible to assess cost- Development of the British Government aims to provide
effectiveness of interventions. costed and evaluated treatment packages for use at a

277
Bousquet et al.

primary healthcare level, methods and materials for Table 7. Aims of an algorithm model developed for the application of the chronic
evaluating the quality of noncommunicable disease care, respiratory disease (CRD) program in rural areas
and a protocol for the assessment of national opportun- Assessment of the prevalence and burden (GBD) of CRD in urban, suburban,
ities for the prevention of hypertension, diabetes, asthma, and rural areas since it seems that CRD are largely underestimated
and epilepsy in Tanzania and Cameroon (138). Assessment of risk factors
Propose and evaluate a simple management scheme which will be tested
further for applicability and cost-effectiveness
For this purpose there is a need for:
Prioritization within the CRD program improvement of availability of effective generic drugs
(e.g. inhaled salbutamol and beclomethasone)
Economic and cultural barriers in sub-Saharan Africa making peak flow measurements possible at each site. However, peak flow
usually result in at least three distinct groups of medical monitoring may be available only in the health centers
care (urban, suburban, and rural). These groups must be Education of healthcare workers
addressed separately for the management of CRD.
However, this categorization may not always be easy to
use since the health strategy is not always followed. It is
anticipated that patients in rural areas will consult nurses increasingly severe and may persist even after exposure
in the vicinity. Then, depending on the severity of the eviction (168). Symptoms of rhinoconjunctivitis are often
disease, patients will optimally be sent to intermediate associated with occupational asthma (169). In many
structures run by physicians and eventually to referral patients, rhinitis appears earlier than asthma. Occupa-
centers. People living in rural areas often try to have tional rhinitis can be used as an early predictor of asthma,
direct access to the referral centers with the help of their as patients can be removed from exposure in order to
family members living in the cities. However, many poor prevent persistent asthma.
people cannot access healthcare centers since they die For the management of CRD in rural areas, a new
before any action has been taken. model should be used. The model should be based on a
It seems that tobacco control is probably the highest simple symptom algorithm, which will guide the health-
priority of the program because a reduction of smoking care worker (or physician) towards the accurate diagno-
will be associated with a decrease in COPD and other sis of CRD and propose the treatment of symptoms. In
tobacco-related diseases. This program is probably the this model, acute and chronic respiratory symptoms
most important in urban and suburban areas, even should be combined to make an optimal diagnosis of
though it is difficult to measure changes in smoking tuberculosis, pneumonia, asthma, or COPD exacerba-
habits (167). tion, and other possible CRD. Only patients with severe
There is limited epidemiological data and clinical symptoms are likely to need treatment and the algorithm
experience about asthma; it is relatively common and should make it possible to differentiate accurately
may be severe at least in urban and suburban areas. The between the diseases and propose treatment for acute
burden of asthma in rural areas is not generally known. symptoms. Such a model using algorithms is currently
In central or university hospitals, which have well-trained being tested in Marrocco and Peru. The model should
personnel and which are sufficiently well equipped, have several aims (Table 7).
guidelines may be tested with some local adaptations From the limited epidemiological data and clinical
using generic drugs. A program adapted from the experience, COPD is known to be relatively common and
National Cooperative Inner-City Asthma Study (NCI- can be very severe. The DALY model and related
CAS) (156,157) may be of interest. measures can be used. However, the best and simplest
Occupational diseases represent a major problem in outcome measure is decrease in FEV1, which is not easily
sub-Saharan Africa. There is an urgent need for improved accessible to the vast majority of people living in sub-
control of occupational pollutants and sensitizers in Saharan Africa.
factories in the developing world. Patients excluded from
work are skilled individuals needed by the country for
economic development. Patients with occupational asth-
Conclusion
ma or COPD working in large companies with a
compensation plan can be followed up after work Due to limited resources and the importance of commu-
cessation and/or treatment. Patients with severe occupa- nicable and noncommunicable diseases in sub-Saharan
tional asthma or COPD working in smaller companies Africa, priorities should be targeted at public health
without a compensation plan are much more difficult to problems that need to be decided at national levels.
manage. In occupational asthma, if people are removed It is clear that tobacco control is the highest priority
from exposure to the substance causing their asthma as whichever country is considered. The management of
soon as they start to develop symptoms, they are likely to asthma using cheap and effective generic drugs and peak
make a complete recovery (http://www.hse.gov.uk/ flows is another priority. The prevention of occupational
condocs/). If exposure continues, symptoms become diseases is equally important since it also has an economic

278
CRD and allergy in sub-Saharan Africa

benefit. However, this may only be a high priority for effective and the priority is probably lower, especially in
middle-income countries. For COPD, besides tobacco low-income countries. The education of healthcare work-
and indoor-pollution control, most measures are not very ers should be an essential part of the program.

References
1. World Health Organization. WHO 11. Murray CJ, Lopez AD. Regional 22. Tanimowo MO. Air pollution and
consultation on the development of a patterns of disability-free life respiratory health in Africa: a review.
comprehensive approach for the pre- expectancy and disability-adjusted life East Afr Med J 2000;77:71–75.
vention and control of chronic respir- expectancy: Global Burden of Disease 23. Ellegard A. Cooking fuel smoke and
atory diseases. January 11–13, 2001. Study. Lancet 1997;349:1347–1352. respiratory symptoms among women
Management of Noncommunicable 12. Arnesen T, Nord E. The value of in low-income areas in Maputo. Envi-
Diseases Department. Chronic Respir- DALY life: problems with ethics and ron Health Persp 1996;104:980–985.
atory Diseases and Arthritis. WHO/ validity of disability adjusted life years. 24. Ezzati M, Kammen D. Indoor air
NMH/CRA/01.1. Geneva: WHO, Bmj 1999;319:1423–1425. pollution from biomass combustion
2001. 13. Cohen J. The Global Burden of and acute respiratory infections in
2. Starfield B. Improving equity in Disease Study: a useful projection of Kenya: an exposure-response study.
health: a research agenda. Int J Health future global health? J Public Health Lancet 2001;358:619–624.
Serv 2001;31:545–566. Med 2000;22:518–524. 25. Bandele EO. A ten-year review of
3. Yach D. The use and value of qualit- 14. Murray CJ, Lopez AD. Mortality by asthma deaths at the Lagos University
ative methods in health research in cause for eight regions of the world. Teaching Hospital. Afr J Med Med Sci
developing countries. Soc Sci Med Global Burden Dis Study Lancet 1996;25:389–392.
1992;35:603–612. 1997;349:1269–1276. 26. Rosenberg R, Vinker S, Zakut H,
4. CCMRC/GINA. Workshop on asthma 15. Cooper RS, Rotimi C, Kaufman J, Kizner F, Nakar S, Kitai E. An
management and prevention in the Lawoyin T. Mortality data for sub- unusually high prevalence of asthma in
Caribbean July 1–3, 1997. Trinidad. Saharan Africa. Lancet 1998;351: Ethiopian immigrants to Israel. Fam
Commonwealth Caribbean Medical 1739–1740. Med 1999;31:276–279.
Research Council. Global Initiative for 16. Kaufman JS, Asuzu MC, Rotimi CN, 27. Wright AL, Holberg CJ, Martinez
Asthma. West Indian Med J Johnson OO, Owoaje EE, Cooper RS. FD, Halonen M, Morgan W,
1998;47:133–152. The absence of adult mortality data for Taussig LM. Epidemiology of physi-
5. Aı̈t-Khaled N, Chaulet P, Enarsson sub-Saharan Africa: a practical solu- cian-diagnosed allergic rhinitis in
D, Slama K. Epidemiology and man- tion. Bull World Health Org childhood. Pediatrics 1994;94:895–901.
agement of stable chronic obstructive 1997;75:389–395. 28. Bousquet J, van Cauwenberge P,
pulmonary disease in Africa. In: 17. Wurthwein R, Gbangou A, Khaltaev N. Allergic rhinitis and its
Similowski, T, Derenne, P, editors. Sauerborn R, Schmidt CM. Measur- impact on asthma. J Allergy Clin
Clinical Management of Chronic ing the local burden of disease. A study Immunol 2001;108:S147–S334.
Obstructive Pulmonary Disease. New of years of life lost in sub-Saharan 29. Strachan D, Sibbald B, Weiland S,
York: Marcel Dekker 2002, 1007–1030. Africa. Int J Epidemiol 2001;30:501–508. et al. Worldwide variations in preval-
6. Lalloo UG, Bateman ED, Feldman 18. Hurd S. The impact of COPD on lung ence of symptoms of allergic rhino-
C, et al. South African Pulmonology health worldwide: epidemiology and conjunctivitis in children: the
Society Adult Asthma Working incidence. Chest 2000;117:1S–4S. International Study of Asthma and
Group. Guideline for the management 19. Gulsvik A. The global burden and Allergies in Childhood (ISAAC).
of chronic asthma in adults—2000 impact of chronic obstructive pulmon- Pediatr Allergy Immunol 1997;8:161–
update. S Afr Med J 2000;90:544–552. ary disease worldwide. Monaldi Arch 176.
7. Motala C, Kling S, Gie R, et al. Chest Dis 2001;56:261–264. 30. The International Study of Asthma
Allergy Society of South Africa 20. Rahman Q, Nettesheim P, Smith KR, and Allergies in Childhood
Working Group. Guideline for the Seth PK, Selkirk J. International (ISAAC) Steering Committee.
management of chronic asthma in conference on environmental and Worldwide variation in prevalence of
children—2000 update. S Afr Medical J occupational lung diseases. Environ symptoms of asthma, allergic rhino-
2000;90:524–528, 530, 532. Health Persp 2001;109:425–431. conjunctivitis, and atopic eczema (see
8. Murray CJ. Quantifying the burden 21. Pauwels RA, Buist AS, Calverley comments). Lancet 1998;351:1225–
of disease: the technical basis for dis- PM, Jenkins CR, Hurd SS. Global 1232.
ability-adjusted life years. Bull World strategy for the diagnosis, manage- 31. Falade AG, Olawuyi F, Osinusi K,
Health Org 1994;72:429–445. ment, and prevention of chronic Onadeko BO. Prevalence and severity
9. Loomes G, McKenzie L. The use of obstructive pulmonary disease. of symptoms of asthma, allergic rhino-
QALYs in health care decision making. NHLBI/WHO Global Initiative for conjunctivitis and atopic eczema in
Soc Sci Med 1989;28:299–308. Chronic Obstructive Lung Disease secondary school children in Ibadan,
10. Elbasha EH. Discrete time represen- (GOLD) Workshop summary. Nigeria. East Afr Med J 1998;75:695–
tation of the formula for calculating Am J Respir Crit Care Med 2001;163: 698.
DALYs. Health Econ 2000;9:353–365. 1256–1276.

279
Bousquet et al.

32. Nriagu J, Robins T, Gary L, et al. 44. Walraven GE, Nyan OA, van der 58. Scrivener S, Yemaneberhan H,
Prevalence of asthma and respiratory Sande MA, et al. Asthma, smoking Zebenigus M, et al. Independent
symptoms in south-central Durban, and chronic cough in rural and urban effects of intestinal parasite infection
South Africa. Eur J Epidemiol adult communities in The Gambia. and domestic allergen exposure on risk
1999;15:747–755. Clin Exp Allergy 2001;31:1679–1685. of wheeze in Ethiopia: a nested case-
33. Godfrey RC. Asthma and IgE levels 45. MacIntyre UE, de Villiers FP, control study. Lancet 2001;358:1493–
in rural and urban communities of The Owange-Iraka JW. Increase in child- 1499.
Gambia. Clin Allergy 1975;5:201–207. hood asthma admissions in an urban- 59. Yazdanbakhsh M, van den
34. van Niekerk CH, Weinberg EG, ising population. S Afr Med J Biggelaar A, Maizels RM. Th2
Shore SC, Heese HV, van Schalk- 2001;91:667–672. responses without atopy: immunoreg-
wyk J. Prevalence of asthma: a com- 46. Pearce N, Douwes J, Beasley R. Is ulation in chronic helminth infections
parative study of urban and rural allergen exposure the major primary and reduced allergic disease. Trends
Xhosa children. Clin Allergy cause of asthma? Thorax 2000;55:424– Immunol 2001;22:372–377.
1979;9:319–314. 431. 60. Holt PG, Sly PD. Interactions be-
35. Addo-Yobo EO, Custovic A, Tag- 47. Peat JK. The epidemiology of asthma. tween respiratory tract infections and
gart SC, Asafo-Agyei AP, Wood- Curr Opin Pulm Med 1996;2:7–15. atopy in the aetiology of asthma. Eur
cock A. Exercise induced 48. Kambarami RA, Marechera F, Respir J 2002;19:538–545.
bronchospasm in Ghana: differences in Sibanda EN, Chitiyo ME. Aero-al- 61. van den Biggelaar AH, van Ree R,
prevalence between urban and rural lergen sensitisation patterns amongst Rodrigues LC, et al. Decreased atopy
schoolchildren. Thorax 1997;52:161– atopic Zimbabwean children. Cent Afr in children infected with Schistosoma
165. J Med 1999;45:144–147. haematobium: a role for parasite-in-
36. Ng’ang’a LW, Odhiambo JA, Omwega 49. Cadman A, Prescott R, Potter PC. duced interleukin-10. Lancet
MJ, et al. Exercise-induced broncho- Year-round housedust mite levels on 2000;356:1723–1727.
spasm: a pilot survey in Nairobi school the Highveld. S Afr Med J 62. Holt PG. Parasites, atopy, and the
children. East Afr Med J 1997;74:694– 1998;88:1580–1582. hygiene hypothesis: resolution of a
698. 50. Woodcock A, Addo-Yobo EO, paradox? Lancet 2000;356:1699–1701.
37. Yemaneberhan H, Bekele Z, Venn A, Taggart SC, Craven M, Custovic A. 63. Yazdanbakhsh M, Kremsner PG,
Lewis S, Parry E, Britton J. Preval- Pet allergen levels in homes in Ghana van Ree R. Allergy, parasites, and the
ence of wheeze and asthma and rela- and the United Kingdom. J Allergy hygiene hypothesis. Science
tion to atopy in urban and rural Clin Immunol 2001;108:463–465. 2002;296:490–494.
Ethiopia. Lancet 1997;350:85–90. 51. Addo-Yobo EO, Custovic A, 64. Scrivener S, Britton J. Immuno-
38. Odhiambo JA, Ng’ang’a LW, Taggart SC, Craven M, Bonnie B, globulin E and allergic disease in
Mungai MW, et al. Urban-rural dif- Woodcock A. Risk factors for asthma Africa. Clin Exp Allergy 2000;30:304–
ferences in questionnaire-derived in urban Ghana. J Allergy Clin 307.
markers of asthma in Kenyan school Immunol 2001;108:363–368. 65. Borkow G, Leng Q, Weisman Z, et al.
children. Eur Respir J 1998;12:1105– 52. Sunyer J, Torregrosa J, Anto J, et al. Chronic immune activation associated
1112. The association between atopy and with intestinal helminth infections
39. de Almeida MM, Pinto JR. Bronchial asthma in a semirural area of Tanzania results in impaired signal transduction
asthma in children: clinical and epi- (East Africa). Allergy 2000;55:762–767. and anergy. J Clin Invest
demiologic approach in different Por- 53. Bousquet J. Atopy and allergy in East 2000;106:1053–1060.
tuguese speaking countries. Pediatr Africa. Allergy 2001;56:189. 66. Selassie FG, Stevens RH, Cullinan
Pulmonol Suppl 1999;18:49–53. 54. Costongs GM, Janson PC, Hermans P, et al. Total and specific IgE (house
40. Weinberg EG. Urbanization and WJ, van Oers RJ, Leerkes B. Evalu- dust mite and intestinal helminths) in
childhood asthma: an African per- ation of performance characteristics of asthmatics and controls from Gondar.
spective. J Allergy Clin Immunol automated measurement systems for Ethiopia Clin Exp Allergy
2000;105:224–231. allergy testing. Eur J Clin Chem Clin 2000;30:356–358.
41. Koffi N, Kouassi B, Ngom A, Aka- Biochem 1995;33:295–305. 67. van den Biggelaar AH, Lopuhaa C,
Dangui E. Value of a video question- 55. Warrell DA, Fawcett IW, van Ree R, et al. The prevalence of
naire in the evaluation of the preval- Harrison BD, et al. Bronchial asthma parasite infestation and house dust
ence of asthma in Africa. Med Trop in the Nigerian savanna region. A mite sensitization in Gabonese school-
2000;60:412–413. clinical and laboratory study of 106 children. Int Arch Allergy Immunol
42. Kayantao D, Toloba Y, Kamissoko patients with a review of the literature 2001;126:231–238.
M, et al. Epidemiological, clinical and on asthma in the tropics. Q J Med 68. van Ree R, Antonicelli L,
progressive aspects of asthma observed 1975;44:325–347. Akkerdaas JH, et al. Asthma after
at Bamako, Mali. Sante 2001;11:101– 56. Macfarlane JT, Bachelor M, consumption of snails in house-dust-
103. Ridyard JB, Ball PA. Asthma, IgE mite-allergic patients: a case of IgE
43. Nyan OA, Walraven GE, Banya and environment in northern Nigeria. cross-reactivity. Allergy 1996;51:387–
WA, et al. Atopy, intestinal helminth Clin Allergy 1979;9:333–337. 393.
infection and total serum IgE in rural 57. Joubert JR, de Klerk HC, Malan C. 69. Pascual C, Crespo J, San-Martin S,
and urban adult Gambian communi- Ascaris lumbricoides and allergic asth- et al. Cross-reactivity between
ties. Clin Exp Allergy 2001;31:1672– ma: a new perspective. S Afr Med J IgE-binding proteins from Anisakis,
1678. 1979;56:599–602. German cockroach, and chironomids.
Allergy 1997;52:514–520.

280
CRD and allergy in sub-Saharan Africa

70. Chua KY, Stewart GA, Thomas WR, 82. Mengesha YA, Bekele A. Relative 95. Bethlem EP, Schettino G, Carvalho
et al. Sequence analysis of cDNA chronic effects of different occupa- CR. Pulmonary schistosomiasis. Curr
coding for a major house dust mite tional dusts on respiratory indices and Opin Pulm Med 1997;3:361–365.
allergen, Der, p. 1. Homology with health of workers in three Ethiopian 96. Lambertucci JR, Serufo JC,
cysteine proteases. J Exp Med factories. Am J Ind Med 1998;34:373– Gerspacher-Lara R, et al. Schistoso-
1988;167:175–182. 380. ma mansoni: assessment of morbidity
71. Michel A, Ghoneim H, Resto M, 83. Rees D, Nelson G, Kielkowski D, before and after control. Acta Trop
Klinkert MQ, Kunz W. Sequence, Wasserfall C, da Costa A. Respir- 2000;77:101–109.
characterization and localization of a atory health and immunological profile 97. Barbosa MM, Lamounier JA,
cysteine proteinase cathepsin L in of poultry workers. S Afr Med J Oliveira EC, et al. Pulmonary hyper-
Schistosoma mansoni. Mol Biochem 1998;88:1110–1117. tension in Schistosoma mansoni. Trans
Parasitol 1995;73:7–18. 84. Loewenson R. Globalization and R Soc Trop Med Hyg 1996;90:663–665.
72. van Sprundel MP. Pneumoconioses: occupational health: a perspective from 98. Omran AR. The epidemiologic trans-
the situation in developing countries. southern Africa. Bull World Health ition. A theory of the epidemiology of
Exp Lung Res 1990;16:5–13. Org 2001;79:863–868. population change 1971. Bull World
73. Rees D, Weiner R. Dust and pneu- 85. Ndiaye M, Fall C, Ndir M, et al. Health Org 2001;79:161–170.
moconiosis in the South African foun- Occupational asthma in a Senegalese 99. Caldwell JC. Population health in
dry industry. S Afr Med J 1994;84:851– car sprayer. Diagnostic and medico-le- transition. Bull World Health Org
855. gal problems. Rev Mal Respir 2001;79:159–160.
74. Loewenson R. Assessment of the 1999;16:199–203. 100. Jamison DT, Mosley WH. Disease
health impact of occupational risk in 86. Esterhuizen TM, Hnizdo E, Rees D, control priorities in developing coun-
Africa: current situation and meth- et al. Occupational respiratory diseases tries: health policy responses to epide-
odological issues. Epidemiology in South Africa—results from SOR- miological change. Am J Public Health
1999;10:632–639. DSA, 1997–99. S Afr Med J 1991;81:15–22.
75. Davies JC. Silicosis and tuberculosis 2001;91:502–508. 101. Alberti G. Noncommunicable
among South African goldminers—an 87. Hnizdo E, Esterhuizen TM, Rees D, diseases: tomorrow’s pandemics. Bull
overview of recent studies and current Lalloo UG. Occupational asthma as World Health Org 2001;79:907.
issues. S Afr Med J 2001;91:562–566. identified by the Surveillance of Work- 102. Unwin N, Setel P, Rashid S, et al.
76. Yach D, Myers J, Bradshaw D, related and Occupational Respiratory Noncommunicable diseases in sub-Sa-
Benatar SR. A respiratory epidemio- Diseases programme in South Africa. haran Africa: where do they feature in
logic survey of grain mill workers in Clin Exp Allergy 2001;31:32–39. the health research agenda? Bull World
Cape Town, South Africa. Am Rev 88. Tiendrebeogo H, Sangare SI, Health Org 2001;79:947–953.
Respir Dis 1985;131:505–510. Roudaut M, Schmidt D, Assale N. 103. Gill GV, Scott B, Beeching NJ,
77. Fatusi A, Erhabor G. Occupational One hundred and one cases of pul- Wilkinson D, Ismail AA. Enumer-
health status of sawmill workers in monary aspergillosis in Ivory Coast ation of non-communicable disease in
Nigeria. J R Soc Health 1996;116:232– (author’s translation). Med Trop rural South Africa by electronic data
236. (Mars) 1982;42:47–52. linkage and capture-recapture tech-
78. Ige OM, Onadeko OB. Respiratory 89. Mushegera CK, Mbuyi-Muamba JM, niques. Trop Med Int Health
symptoms and ventilatory function of Kabemba MJ. Indications and results 2001;6:435–441.
the sawmillers in Ibadan, Nigeria. Afr J of pleuropulmonary decortications in 104. Yikona J. Non-communicable disease
Med Med Sci 2000;29:101–104. the University hospital of Kinshasa. in sub-Saharan Africa. Lancet
79. Hnizdo E, Murray J, Davison A. Acta Chir Belg 1996;96:217–222. 2001;357:74.
Correlation between autopsy findings 90. Desai G, Amadi W. Three years’ 105. Yach D. Tobacco control. From con-
for chronic obstructive airways disease experience of empyema thoracis in cern for the lung to global political
and in-life disability in South African association with HIV infection. Trop action. Thorax 2001;56:247–248.
gold miners. Int Arch Occup Environ Doct 2001;31:106–107. 106. World Health Organizaton. Global
Health 2000;73:235–244. 91. Souilamas R, Riquet M, Barthes FP, strategy for asthma management and
80. Osim EE, Tandayi M, Chinyanga Chehab A, Capuani A, Faure E. prevention. WHO/NHLBI Workshop
HM, Matarira HT, Mudambo KK, Surgical treatment of active and Report. Publication Number 95–3659.
Musabayane CT. Lung function, sequelar forms of pulmonary tubercu- Bethesda: National Institutes of
blood gases, pH and serum electrolytes losis. Ann Thorac Surg 2001;71:443– Health, National Heart, Lung and.
of small-scale miners exposed to 447. Blood Institute, 1995.
chrome ore dust on the Great Dyke in 92. Mallory KF, Churchyard GJ, 107. Ait-Khaled N, Enarson D,
Zimbabwe. Trop Med Int Health Kleinschmidt I, de Cock KM, Bousquet J. Chronic respiratory dis-
1999;4:621–628. Corbett EL. The impact of HIV in- eases in developing countries. the bur-
81. Osim EE, Musabayane CT, Mufunda fection on recurrence of tuberculosis in den and strategies for prevention and
J. Lung function of Zimbabwean farm South African gold miners. Int J management. Bull World Health Org
workers exposed to flue curing and Tubercul Lung Dis 2000;4:455–462. 2001;79:971–979.
stacking of tobacco leaves. S Afr Med J 93. Ong RK, Doyle RL. Tropical pul- 108. Yach D. Partnering for better lung
1998;88:1127–1131. monary eosinophilia. Chest health: improving tobacco and tuber-
1998;113:1673–1679. culosis control. Int J Tubercul Lung
94. Morris W, Knauer CM. Cardiopul- Dis 2000;4:693–697.
monary manifestations of schistosomi- 109. Enarson DA, Ait-Khaled N. Cul-
asis. Semin Respir Infect 1997;12:159– tural barriers to asthma management.
170. Pediatr Pulmonol 1999;28:297–300.

281
Bousquet et al.

110. Green RJ, Greenblatt MM, Plit M, 126. Knippenberg R, Alihonou E, Soucat 139. Ait-Khaled N, Enarson DA,
Jones S, Adam B. Asthma manage- A, et al. Implementation of the Bam- Behbehani N, Yeung MC, Irisen E.
ment and perceptions in rural South ako Initiative; Strategies in Benin and The Asthma Workshop. Report of a
Africa. Ann Allergy Asthma Immunol Guinea. Int J Health Plan Manag workshop organised by the Interna-
2001;86:343–347. 1997;12:S29–S47. tional Union Against Tuberculosis and
111. Oranga HM. Ageing and poverty in 127. Soucat A, Levy-Bruhl D, dE Beth- Lung Disease, Paris, 15–16 December
rural Kenya: community perception. une X, et al. Affordability, cost-ef- 2000. Int J Tubercul Lung Dis
East Afr Med J 1997;74:611–613. fectiveness and efficiency of primary 2001;5:973–977.
112. Yach D. Tobacco in Africa. World health care: the Bamako Initiative 140. Partridge MR, Fabbri LM, Chung
Health Forum 1996;17:29–36. experience in Benin and Guinea. Int J KF. Delivering effective asthma car-
113. World Health Organization. Health Plan Manag 1997;12:S81–S108. e—how do we implement asthma
Tobacco or Health: a Global Status 128. Knippenberg R, Soucat A, Oyegbite guidelines? Eur Respir J 2000;15:235–
Report. Geneva: WHO, 1997. K, et al. Sustainability of primary 237.
114. Mackay J, Crofton J. Tobacco and health care including expanded pro- 141. Holgate ST, Bousquet J, Chung KF,
the developing world. Br Med Bull gram of immunizations in Bamako Bisgaard H, Pauwels R, Fabbri L,
1996;52:206–221. Initiative programs in West Africa: an et al. Recommendations for the design
115. Amos A. Women and smoking. Br assessment of 5 years’ field experience of clinical trials and the registration of
Med Bull 1996;52:74–89. in Benin and Guinea. Int J Health Plan drugs used in the treatment of asthma.
116. Stephenson LS, Latham MC, Manag 1997;12:S9–S28. Group for the Respect of Ethics and
Ottesen EA. Global malnutrition. 129. Diallo I, Molouba R, Sarr LC. Pri- Excellence in Science (GREES). Int J
Parasitology 2000;121:S5–S22. mary health care: from aspiration to Pharm Med 2002;16:115–127.
117. Walker AR. Nutritionally related achievement. World Health Forum 142. Pauwels RA, Lofdahl CG, Laitinen
disorders/diseases in Africans. High- 1993;14:349–355. LA, et al. Long-term treatment with
lights of half a century of research with 130. Ceesay N, Kalliecharan RV. Sus- inhaled budesonide in persons with
special reference to unexpected phe- taining the Bamako Initiative in the mild chronic obstructive pulmonary
nomena. Adv Exp Med Biol Gambia—some management implica- disease who continue smoking. Euro-
1997;427:1–14. tions. World Hosp Health Serv pean Respiratory Society Study on
118. Marek T, Diallo I, Ndiaye B, 1994;30:10–14. Chronic Obstructive Pulmonary
Rakotosalama J. Successful contract- 131. Napoles-Springer A, Perez-Stable Disease. N Engl J Med 1999;340:
ing of prevention services. Fighting EJ. The role of culture and language in 1948–1953.
malnutrition in Senegal and Madagas- determining best practices. J General 143. Burge PS, Calverley PM, Jones PW,
car. Health Policy Plan 1999;14:382– Intern Med 2001;16:493–495. Spencer S, Anderson JA, Maslen
389. 132. Nordberg E. Health and the elderly in TK. Randomised, double blind, pla-
119. Vorster HH, Bourne LT, Venter CS, developing countries with special ref- cebo controlled study of fluticasone
Oosthuizen W. Contribution of nutri- erence to sub-Saharan Africa. East Afr propionate in patients with moderate
tion to the health transition in devel- Med J 1997;74:629–633. to severe chronic obstructive pulmon-
oping countries. a framework for 133. Kale R. Traditional healers in South ary disease: the ISOLDE trial. BMJ
research and intervention. Nutr Rev Africa: a parallel health care system. 2000;320:1297–1303.
1999;57:341–349. BMJ 1995;310:1182–1185. 144. Effect of inhaled triamcinolone on the
120. Martin-Prevel Y, Maire B, Del- 134. Fassin D, Fassin E. Traditional medi- decline in pulmonary function in
peuch F. Nutrition, urbanization and cine and the stakes of legitimation in chronic obstructive pulmonary disease.
poverty in subsaharan Africa. Med Senegal. Soc Sci Med 1988;27:353–357. N Engl J Med 2000;343:1902–1909.
Trop 2000;60:179–191. 135. Pretorius E. Traditional and modern 145. Spencer S, Calverley PM, Sherwood
121. The Bamako initiative. Lancet medicine working in tandem. Curat- Burge P, Jones PW. Health status
1988;2:1177–1178. ionis 1991;14:10–13. deterioration in patients with chronic
122. Chabot J. The Bamako initiative. 136. Ait-Khaled N, Enarson D. Manage- obstructive pulmonary disease. Am J
Lancet 1988;2:1366–1367. ment of asthma guidelines. Guide for Respir Crit Care Med 2001;163:122–
123. Velasquez G, Boulet P. Essential Low Income Countries. IUATLD. 128.
drugs in the new international econo- Frankfurt am Main, Moskau, Senwald, 146. Ait-Khaled N, Hamadache M, Byles
mic environment. Bull World Health Wien: pmi-Verl Gruppe, 1996. KB. Analysis of demand for pulmon-
Org 1999;77:288–292. 137. Global strategy for asthma manage- ary function testing for obstructive
124. Ait-Khaled N, Auregan G, Ben- ment and prevention. www.ginasth- airway disease in an Algerian laborat-
charif N, et al. Affordability of ma.com 2002 (revised 2002). ory. Bull Int Union Tubercul Lung Dis
inhaled corticosteroids as a potential 138. Unwin N, Mugusi F, Aspray T, et al. 1990;65:39–41.
barrier to treatment of asthma in some Tackling the emerging pandemic of 147. Muzembo Ndundu J, Nkakudulu
developing countries. Int J Tubercul non-communicable diseases in sub-Sa- Bikuku H, Frans A. Respiratory
Lung Dis 2000;4:268–271. haran Africa: the essential NCD health rehabilitation in patients with bron-
125. Gbedonou P, Moussa Y, Floury B, intervention project. Public Health chial asthma and chronic obstructive
Josse R, Ndiaye JM, Diallo S. The 1999;113:141–146. pulmonary disease (COPD) in Kins-
Bamako initiative: hope or illusion? hasa. Rev Pneumol Clin 2001;57:209–
Observations on the Benin experience. 218.
Sante 1994;4:281–288.

282
CRD and allergy in sub-Saharan Africa

148. Wilkinson D, Floyd K, Gilks CF. 157. Mitchell H, Senturia Y, Gergen P, 166. Pobee JO. Community-based high
National and provincial estimated et al. Design and methods of the blood pressure programs in sub-Saha-
costs and cost effectiveness of a pro- National Cooperative Inner-City ran Africa. Ethn Dis 1993;3:S38–S45.
gramme to reduce mother-to-child HIV Asthma Study. Pediatr Pulmonol 167. Rashid S, Aspray TJ, Edwards R,
transmission in South Africa. S Afr 1997;24:237–252. et al. Essential NCD Health Inter-
Med J 2000;90:794–798. 158. Kahn JG, Marseille E. Fighting glo- vention Project Team. The pitfalls of
149. Wijewardene K, Spohr M. An bal AIDS. The value of cost-effective- measuring changes in smoking habits.
attempt to measure burden of disease ness analysis. Aids 2000;14:2609–2610. Trop Doc 2000;30:160–161.
using disability adjusted life years for 159. Parent du Chatelet I, Gessner BD, 168. Chan-Yeung M, MacLean L, Paggi-
Sri Lanka. Ceylon Med J 2000;45:110– da Silva A. Comparison of cost-ef- aro PL. Follow-up study of 232
115. fectiveness of preventive and reactive patients with occupational asthma
150. Utzinger J, Tozan Y, Singer BH. mass immunization campaigns against caused by western red cedar (Thuja
Efficacy and cost-effectiveness of envi- meningococcal meningitis in West plicata). J Allergy Clin Immunol
ronmental management for malaria Africa: a theoretical modeling analysis. 1987;79:792–796.
control. Trop Med Int Health Vaccine 2001;19:3420–3431. 169. Malo JL, Lemiere C, Desjardins A,
2001;6:677–687. 160. Maher D, van Gorkom JL, Gondrie Cartier A. Prevalence and intensity of
151. Shibuya K. Recent trends in mortality, PC, Raviglione M. Community con- rhinoconjunctivitis in subjects with
years of life lost (YLLs), and disability- tribution to tuberculosis care in coun- occupational asthma. Eur Respir J
adjusted life years (DALYs) attribut- tries with high tuberculosis prevalence: 1997;10:1513–1515.
able to tobacco in Japan. Nippon past, present and future. Int J Tubercul 170. Fox-Rushby JA, Hanson K. Calcula-
Eiseigaku Zasshi 2001;56:484–491. Lung Dis 1999;3:762–768. ting and presenting disability adjusted
152. Schellenberg D, Menendez C, 161. Nuwaha F. Chemoprophylaxis for life years (DALYs) in cost-effectiveness
Kahigwa E, et al. Intermittent treat- tuberculosis in HIV-infected individu- analysis. Health Policy Plan
ment for malaria and anaemia control als in sub-Saharan Africa. East Afr 2001;16:326–331.
at time of routine vaccinations in Med J 1998;75:520–527. 171. Hollinghurst S, Bevan G, Bowie C.
Tanzanian infants: a randomised, pla- 162. Goodman CA, Coleman PG, Mills Estimating the ÔavoidableÕ burden of
cebo-controlled trial. Lancet AJ. Cost-effectiveness of malaria con- disease by Disability Adjusted Life
2001;357:1471–1477. trol in sub-Saharan Africa. Lancet Years (DALYs). Health Care Manag
153. Kerry SM, Bland JM. Trials which 1999;354:378–385. Sci 2000;3:9–21.
randomize practices. I. How should 163. Alonzo Gonzalez M, Menendez C, 172. Peters EJ, Esin RA, Immananagha
they be analysed? Fam Pract Font F, et al. Cost-effectiveness of iron KK, Siziya S, Osim EE. Lung function
1998;15:80–83. supplementation and malaria chemo- status of some Nigerian men and
154. Kerry SM, Bland JM. Trials which prophylaxis in the prevention of anae- women chronically exposed to fish
randomize practices. II. Sample size. mia and malaria among Tanzanian drying using burning firewood. Cent
Fam Pract 1998;15:84–87. infants. Bull World Health Org Afr J Med 1999;45:119–124.
155. Moudgil H, Honeybourne D. Dif- 2000;78:97–107. 173. Orie NN. Comparison of normal res-
ferences in asthma management be- 164. Bos JM, Postma MJ. The economics of piratory function values in young
tween white European and Indian HIV vaccines: projecting the impact of Kenyans with those of other Africans
subcontinent ethnic groups living in HIV vaccination of infants in sub-Sa- and Caucasians. East Afr Med J
socioeconomically deprived areas in haran Africa. Pharmacoeconomics 1999;76:31–34.
the Birmingham (UK) conurbation. 2001;19:937–946. 174. Hnizdo E, Churchyard G, Dowde-
Thorax 1998;53:490–494. 165. Sweat M, Gregorich S, Sangiwa G, swel R. Lung function prediction
156. Kattan M, Mitchell H, Eggleston et al. Cost-effectiveness of voluntary equations derived from healthy South
P, et al. Characteristics of inner-city HIV-1 counselling and testing in redu- African gold miners. Occupat Environ
children with asthma: the National cing sexual transmission of HIV-1 in Med 2000;57:698–705.
Cooperative Inner-City Asthma Study. Kenya and Tanzania. Lancet
Pediatr Pulmonol 1997;24:253–262. 2000;356:113–121.

283

View publication stats

You might also like