A sub-Saharan African perspective of diabetes
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- Gill, G.V., Mbanya, JC., Ramaiya, K.L. et al. Diabetologia (2009) 52: 8. doi:10.1007/s00125-008-1167-9
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Diabetes mellitus is an important and increasing cause of morbidity and mortality in sub-Saharan Africa. Accurate epidemiological studies are often logistically and financially difficult, but processes of rural–urban migration and epidemiological transition are certainly increasing the prevalence of type 2 diabetes. Type 1 disease is relatively rare, although this may be related to high mortality. This diabetic subgroup appears to present at a later age (by about a decade) than in Western countries. Variant forms of diabetes are also described in the continent; notably ‘atypical, ketosis-prone’ diabetes, and malnutrition-related diabetes mellitus. These types sometimes make the distinction between type 1 and type 2 diabetes difficult. Interestingly, this is also a current experience in the developed world. As more detailed and reliable complication studies emerge, it is increasingly apparent that African diabetes is associated with a high complication burden, which is both difficult to treat and prevent. More optimistically, a number of intervention studies and twinning projects are showing real benefits in varying locations. Future improvements depend on practical and sustainable support, coupled with local acceptance of diabetes as a major threat to the future health and quality of life of sub-Saharan Africans.
KeywordsAfrica Atypical diabetes Diabetes mellitus Diabetic complications Healthcare delivery Malnutrition-related diabetes mellitus Mortality Type 1 diabetes Type 2 diabetes
coronary artery disease
fibrocalculous pancreatic diabetes
hyperosmolar non-ketotic coma
islet cell antibodies
International Diabetes Federation
malnutrition-modulated diabetes mellitus
malnutrition-related diabetes mellitus
Diabetes mellitus in the African continent is hugely affected by epidemiological factors and issues of healthcare economics. A major factor increasing diabetes prevalence in Africa is urbanisation . There continues to be an increasing number of people moving into urban areas from rural environments, particularly in sub-Saharan Africa. This migration is inevitably associated with a shift in lifestyle from a relatively healthy traditional pattern, to the urban scenario of increased food quantity and reduced quality, low levels of exercise, smoking and increased alcohol availability . This rapid and dramatic epidemiological transition is driving the emergence of high and increasing prevalence rates of type 2 diabetes and hypertension , with growing mortality implications. Indeed, even though at present infective diseases such as HIV infection, tuberculosis and malaria dominate mortality in sub-Saharan Africa, it is predicted that by 2020, non-communicable diseases will proportionately overtake infections as the major cause of mortality . The burden of non-communicable diseases in Africa is already proportionately greater than that in Western countries .
As well as quantitative issues, diabetes epidemiology in Africa also involves a number of qualitative peculiarities. Type 1 disease appears rarer than in Western countries , and ‘malnutrition-related’ and ‘atypical’ forms of type 2 diabetes have been described. With the migration of many African people to Europe and America, some of these unusual diabetic subgroups may now be seen in developed countries. Indeed, a recent study of atypical type 2 diabetes (discussed later) has used a cohort of African patients now resident in France .
The diabetes care delivery agenda in Africa is dominated by poverty, especially in sub-Saharan Africa, where 33 out of the 40 (82%) of the world’s most heavily indebted poor countries are situated . Also, in the African continent, diabetes management costs have to compete with health issues such as anti-retroviral drugs, tuberculosis treatment and malarial control programmes. As a continent heavily dependent on the developed world for aid, it is important that health problems in Africa are understood by the rest of the world. Diabetes is a good example, as the epidemiology of this disease and care systems in place for its treatment are very different in Africa from those in Western countries. In this article, we will try to emphasise unique perspectives of diabetes in sub-Saharan Africa, as well as aspects that can perhaps provide lessons elsewhere.
Problems of numbers, classification and diagnosis
Atypical African diabetes
An atypical presentation of diabetes was first described in the late 1960s by researchers working in Africa [11, 12, 13, 14, 15, 16]. Subsequent reports from Nigeria described patients who could switch from insulin therapy to oral hypoglycaemic agents or vice versa [15, 16], as well as those with ketoacidosis but without islet cell antibodies (ICA) [13, 14]. In 1985, Ahren and Corrigan , working in northern Tanzania, described this atypical diabetes with phasic insulin-requiring profiles in the absence of obvious precipitating factors for ketosis. It has now become apparent that there are other forms of atypical presentations of diabetes, with predominance in populations of African ancestry that do not easily fit the criteria defining the main known types. The most often reported atypical form of diabetes is characterised by an initial clinical presentation of apparent type 1 diabetes with severe hyperglycaemia and ketosis, and subsequent long-term remission with or without relapses or a clinical course compatible with type 2 diabetes.
The term ‘ketosis-prone atypical diabetes mellitus’ was first described in African-American children in 1987 [17, 18]. The first reports of well-phenotyped African-American adults came from New York in 1990 and 1994, in which ‘Flatbush’ diabetes, with the same characteristics as ketosis-prone atypical diabetes, was described [19, 20]. Unlike patients with true young-onset type 1 diabetes , both the GAD antibodies (GADA) and ICA are an exceptional finding in patients with this form of acute-onset ketotic diabetes [14, 20, 21, 22]. A syndrome similar or identical to the US descriptions has been described more recently in West Africa . Children presenting with atypical diabetes are mostly African or of African ancestry, obese, have an age of onset around 14 years and a strong positive family history of type 2 diabetes approaching 100%; there is a male preponderance of up to 3:1 [17, 18, 21, 23]. The age at diagnosis in adults varies from 35 to 46 years. Adults with atypical diabetes are less often obese than children (depending on the population studied, obesity is present in not more than 56%). The initial presentation is usually acute with polyuria, polydipsia and weight loss. The result of a random blood glucose test is very high (often above 30 mmol/l), ketones are present in the urine and there may be ketoacidosis with low pH and serum bicarbonate [12, 17, 22, 24]. Thus, the initial presentation requires insulin treatment with appropriate fluid and electrolyte management as necessary. A recent interesting and exciting development in the aetiology of ketosis-prone atypical diabetes has come from work by Sobngwi et al. . Antibodies to the human herpesvirus 8 (HHV-8) were found in 88% of patients with atypical diabetes but in only 15% of patients with classical type 2 diabetes (p < 0.001). This may explain the abrupt onset of the disease and its subsequent benign clinical course, sometimes with glycaemic remission.
Malnutrition-related diabetes mellitus
Summarised features of ‘atypical’ and ‘malnutrition-related diabetes’ in Africa
Children or young adults
3:1 Male excess
2:1 Male excess
Islet autoimmunity rare
Occasional ‘type 1’ HLA pattern
Often strong family history
Past or present malnutrition
Steatorrhoea in some areas
Type 1 diabetes
In Africa, the presence of atypical forms of diabetes makes it difficult to classify patients as having type 1 and type 2 diabetes based on usual clinical criteria [29, 30, 31, 32]. Interestingly, there is currently debate in Europe over whether type 1 and type 2 diabetes may share some common aetiologies—the so-called accelerator hypothesis [33, 34]. The difficulty in classifying and diagnosing some forms of diabetes in Africa may explain why approximately half (42–64%) of African patients initially treated with insulin do not have classical type 1 diabetes and may enter prolonged remission [30, 35]. It is widely believed that classical type 1 diabetes is less common in Africa than in Europe or North America, and this is certainly common clinical experience. However, early out-of-hospital mortality may confound this impression, and the question remains open. Epidemiological studies of type 1 diabetes are few and are difficult to conduct because of problems in finding cases as well as enumeration of the background population. Incidence rates of 10 per 100,000 per year have been reported from Sudan , and 1.5 per 100,000 per year from Tanzania . Both are certainly lower than expected Western rates. One interesting and unexplained feature of African type 1 diabetes is that the age of onset is about 10 years later than elsewhere. In a unique study from Johannesburg, South Africa, it was found that the mean age of presentation was 23 years for black African type 1 patients compared with 13 years for white African type 1 patients . This contrasts with the falling age of onset of type 1 diabetes in Europe . Immunological studies in black African patients with clinically diagnosed type 1 diabetes have been hampered by cohorts with varying disease duration and variable and sometimes dated laboratory methodology. Early studies reported low rates of ICA positivity [40, 41]. More recently, 44% of recently diagnosed (within 1 year of presentation) black South African type 1 patients were found to be GADA-positive . A further study from South Africa measured GADA in 43 black and 17 white type 1 patients presenting in ketoacidosis. The rate of GADA positivity was 32% in black and 67% in white patients (p = 0.03) , although diabetes duration was not exactly matched. Results such as these have led some workers to surmise that non-autoimmune factors may be a major determinant of type 1 diabetes in black sub-Saharan Africans .
Other diagnostic and classification issues
The clinical combination of weight loss, polyuria and sepsis has led to the erroneous diagnosis of AIDS in diabetic patients, and contributed to the delay in seeking medical care in Africa, where HIV/AIDS is now endemic . Now that anti-retroviral drugs are being widely used in African patients with AIDS, the metabolic syndrome and type 2 diabetes may soon occur as an adverse effect. Furthermore, there are socioeconomic inequalities in health that can be attributed to inadequate access to healthcare and other inequalities in material circumstances. These are intermediate factors that may lead to a misdiagnosis or a delay in diagnosis of diabetes. Cultural factors and health beliefs differ in sub-Saharan Africa, where under-nutrition and opulence coexist; food remains a daily challenge and overweight can be subsequently perceived as a sign of wealth. Indeed, being obese is a deeply rooted status symbol. Obviously, there are wide geographical variations in these perceptions, in addition to differences between urban and rural environments. However, in a continent where there is an underdeveloped healthcare system with poor diagnostic facilities, and where poverty can be considered a disease, the atypical presentations of diabetes, health beliefs and the endemic HIV/AIDS epidemic can lead to difficulties in the classification and diagnosis of diabetes.
Complications and mortality
Selected chronic complication prevalence studies of diabetes in Africa
The relatively high frequency of neuropathy leads, as may be expected, to a significant problem of foot ulceration . The majority of diabetes-related foot ulcers (>80%) in Africa are neuropathic rather than ischaemic, presentation may be late and the outcome often poor . A further problem is that in many African societies there are strong cultural objections to amputation—loss of a limb may be considered worse than loss of life . Diabetes-related large vessel disease syndromes are generally less common than in developed countries (particularly in sub-Saharan areas of the continent) . Following detailed studies in the Copperbelt of Zambia, Rolfe found only 12 out of 600 participants had possible coronary artery disease (CAD; according to ECG diagnosis only), seven had past strokes and ten had peripheral vascular disease . It was calculated that large vessel disease was uncommon, in spite of the high prevalence of hypertension. Similar observations were made at around the same time in Ethiopia, where Lester and Keen reported that macrovascular disease was not common among middle-aged Ethiopian diabetic patients . Even in 2000, definite CAD was considered rare enough among Nigerian diabetic patients for two cases to be reported in the literature .
The acute metabolic complications of diabetic ketoacidosis, hyperosmolar non-ketotic coma and hypoglycaemia all commonly occur in Africa, and have a worse prognosis than in developed countries. Severe diabetes-related infections can also perhaps be considered an acute complication of the disease. Diabetic ketoacidosis may have a mortality rate of 10–30% [9, 61], and is often due to a lack of insulin or delayed presentation (related to both the patient attending traditional healers initially, but also to misdiagnosis when attending clinics or hospitals) . One of the few outcome studies of hyperosmolar non-ketotic coma in Africa was from Johannesburg, South Africa, and reported a mortality rate of 41% . Hypoglycaemia as a cause of hospital admission is more frequently related to sulfonylurea drugs (33% of hypoglycaemic admissions in one study)  than in developed countries, and such hypoglycaemia may be severe and prolonged. Acute diabetes-related infections include foot sepsis of course, but also unusual problems such as severe hand infections  and, occasionally, mucormycosis. Tuberculosis is also more common and more severe in patients with diabetes .
Diabetes mortality studies in Africa
Mixed—most type 2
41% had died at the 6-year follow-up
Most due to DKA, HNK, hypoglycaemia and infection
Mixed—most type 2
5-year mortality: 18% if not on insulin; 34% on insulin
Metabolic and infections. Some cardiovascular causes in type 2 patients
All type 1
Mortality rate16% at 10 years, 43% at 20 years
About half of deaths were nephropathic, others were due to DKA and hypoglycaemia
In Soweto, South Africa, a long-term follow-up of a type 1 cohort reported mortality rates at 10  and 20  years from recruitment. There were originally 88 in the cohort, all with definite type 1 disease (confirmed by C-peptide testing), followed from 1982. At the 10-year follow-up (1992) , 16% had died; half of the deaths were due to nephropathy and the rest due to diabetic ketoacidosis or hypoglycaemia. At 20 years, the crude mortality rate was 43% , with a Kaplan–Meier calculated mortality hazard rate of 33%. Renal failure owing to nephropathy was again the main mortality cause (43%). Other causes were hypoglycaemia (29%), diabetic ketoacidosis (10%) and infection (10%). Although the overall 20-year mortality figures were in excess of those reported in developed countries, interestingly, they were similar to figures from equivalent Afro-Caribbean type 1 patients in the USA .
Overall, the outcome of African diabetes remains poor, but there is evidence of improvement in the recent past. Metabolic and infective causes of death remain important, but nephropathic renal failure is an increasing problem. Large vessel disease syndromes as causes of mortality are also probably emerging [69, 73].
Delivering care: existing problems and potential solutions
Economic factors remain an important barrier to adequate diabetes care delivery in Africa. Insulin, in particular, is a relatively expensive drug in resource-limited countries. In 1992, in Tanzania, Chale et al.  calculated that those in the country on insulin treatment (0.2%) were consuming 8% of the national healthcare budget. This well-known chronic ‘insulin dilemma’ has been revisited in detail by Beran and colleagues of the International Insulin Foundation [75, 76]. They have carried out in-depth studies of the insulin supply problem in specific African countries, using a newly introduced Rapid Assessment Protocol for Insulin Access (RAPIA) system of enquiry, operating at various levels, from health ministry to patient. Problems identified included poor quantification of need, high insulin cost, erratic peripheral delivery and, sometimes, failure to take advantage of cheaper insulin alternatives.
There have been scattered reports of successful attempts to improve diabetes care delivery and outcome, but sadly these have largely been initiated either by local hospitals or by external funding and support. In Soweto, during the 1980s, hyperglycaemic emergency admission rates and mortality were reduced by a package of measures, which included patient and staff education and formalised treatment protocols . A team-based restructuring of care in Ghana, including, in particular, nurse-led patient education, resulted in reduced diabetes-related admission rates and in-patient mortality . Both of these studies were from city teaching hospitals, and the Soweto project was internally organised and cost-neutral. The Ghana initiative was aided by an external non-governmental organisation, namely, the Tropical Health and Education Trust (THET). This trust has also been active in the Jimura area of Ethiopia, promoting a devolved system of non-communicable disease (including diabetes) care in rural health centres . Although this has proved highly successful, hard outcome indicators have not been assessed, and high levels of staff turnover have been a problem. In rural KwaZulu-Natal in South Africa, a previous successful non-communicable disease delivery programme  has been used as the basis for a nurse-only approach to deliver protocol-based diabetes care and structured patient education to a scattered community at the primary health clinic level . Significant falls in glycated haemoglobin (HbA1c) levels were seen over 18 months of follow-up. This project was supported by the Rhodes Trust and the Liverpool School of Tropical Medicine, but is currently self-sustaining . Finally, in Eritrea , a US team made three visits to the country over a 2-year period to support and educate local diabetes health workers. A subsequent significant fall in mean patient HbA1c levels was demonstrated. The project was funded by the USA, and although clearly of value, there are issues concerning long-term sustainability. As well as those evidence-based interventions, there are a number of other support projects and initiatives ongoing in the continent. These include a twinning project between Diabetes UK and the Mozambique Diabetes Association, and the introduction of a National Diabetes Programme in Tanzania .
The lessons appear to be that real improvements in diabetes care and outcome in Africa are achievable. However, although external support, local health facilities, support groups and diabetes associations all have a role to play, national government health departments need to take the responsibility of instigating widespread permanent change and improvement. The costs need not be great, as patient education (one of the least expensive of diabetes treatments) has been shown to be a major and effective part of all the currently described care delivery packages [80, 81, 82, 83, 84, 85, 86]. The integration of traditional healers should also be considered as part of these reforms, since, to the everyday African, they are very much a part of illness management.
The complication and mortality burden of diabetes in Africa is high and increasing. With increasing urbanisation and transitional lifestyles, CAD and the metabolic syndrome are now significantly emerging problems  that require urgent attention. In 1977, Morley et al.  from Baragwanath Hospital in Soweto, South Africa, wrote, ‘we do not underestimate the difficulties of providing a proper service for diabetics, but we should be able to do better’. Over 30 years later, one would have to conclude that more should have been achieved.
We are grateful for the helpful assistance of A. K. Ramaiya and T. V. Mathew (University of Waterloo, Waterloo, ON, Canada).
Duality of interest
The authors declare that there is no duality of interest associated with this manuscript.