Diabetologia

, 52:8 | Cite as

A sub-Saharan African perspective of diabetes

  • G. V. Gill
  • J.-C. Mbanya
  • K. L. Ramaiya
  • S. Tesfaye
Review

Abstract

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.

Keywords

Africa Atypical diabetes Diabetes mellitus Diabetic complications Healthcare delivery Malnutrition-related diabetes mellitus Mortality Type 1 diabetes Type 2 diabetes 

Abbreviations

CAD

coronary artery disease

FCPD

fibrocalculous pancreatic diabetes

GADA

GAD antibodies

HNK

hyperosmolar non-ketotic coma

ICA

islet cell antibodies

IDF

International Diabetes Federation

MMDM

malnutrition-modulated diabetes mellitus

MRDM

malnutrition-related diabetes mellitus

Introduction

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 [1]. 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 [2]. This rapid and dramatic epidemiological transition is driving the emergence of high and increasing prevalence rates of type 2 diabetes and hypertension [3], 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 [4]. The burden of non-communicable diseases in Africa is already proportionately greater than that in Western countries [5].

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 [6], 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 [7].

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 [8]. 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

As observed elsewhere in the world, the majority of diabetic patients in Africa have type 2 disease. Drawing information from the separate African continent, the International Diabetes Federation (IDF) estimates a current overall prevalence of 2.4% [9]. Good epidemiological studies are difficult in sub-Saharan Africa; they are expensive, labour intensive and populations are often mobile and poorly enumerated. Figure 1 shows a map of the area with recent adult diabetes prevalence estimates by country. The figures are from cohort studies (using glucose tolerance tests) and derived projected data from known population structure (rural/urban distribution and age). It was compiled by the IDF in 2003 (included in [9, 10]). Generally speaking, prevalence is significantly higher in urban compared with rural communities, and is particularly high in particular ethnic groups, notably the descendants of Asian migrants. As well as these epidemiological issues, there are classification difficulties in Africa (see Textbox: Epidemiological issues in African diabetes), discussed below.
Fig. 1

Map of Africa showing estimated adult prevalence rates in different countries. Darker shading indicates sub-Saharan countries. Localised areas of much higher prevalence also exist, e.g. 10.8% in the ‘Cape-coloured’ population of Capetown, South Africa; and 9.8% among Asian immigrant descendants in Dar es Salaam, Tanzania. (IDF figures, 2003, adapted from [9, 10])

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 [12], 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 [20], 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 [23]. 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. [7]. 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

This syndrome was previously known as ‘tropical diabetes’ or ‘tropical pancreatic diabetes’ and is characterised by early-onset non-ketotic diabetes in underweight patients, with very high subsequent insulin requirements [25]. The acute onset with very high glycaemic levels, and sometimes ketosis or ketoacidosis is compatible with type 1 diabetes, but the non-insulin dependent clinical course is more likely to mimic type 2 diabetes. This atypical presentation is distinct from true African type 1 diabetes with regard to beta cell autoimmunity [26]. Although the HLA alleles associated with susceptibility to type 1 diabetes are of high frequency in some populations with this form of diabetes [20], there is an absence of markers of pancreatic beta cell autoimmunity [17]. Patients with malnutrition-related diabetes mellitus (MRDM) have been described in geographically distinct areas throughout the tropics, including Africa, and a male predominance has been described (as with atypical diabetes) [27]. Pancreatic calcification is sometimes present (so-called fibrocalculous pancreatic diabetes or FCPD). Without this feature it is known as malnutrition-modulated diabetes mellitus (MMDM). As both names suggest, present or past malnutrition is a feature, although it is uncertain whether this may be causative, or secondary to uncontrolled diabetes and/or exocrine pancreatic deficiency. The nature and even existence of MMDM is, however, uncertain and controversial. Fifteen years ago, the well-known Kenyan diabetologist Tom Johnson described it as ‘a syndrome seeking clarity’ [28], and the same is very much true today. Because of these problems of definition, there are no reliable data on the relative frequency of MRDM (and indeed atypical diabetes). Table 1 summarises the key features of these two diabetes variants.
Table 1

Summarised features of ‘atypical’ and ‘malnutrition-related diabetes’ in Africa

Atypical

Malnutrition-related

Ketotic presentation

Insidious onset

Children or young adults

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

Remission possible

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 [36], and 1.5 per 100,000 per year from Tanzania [37]. 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 [38]. This contrasts with the falling age of onset of type 1 diabetes in Europe [39]. 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 [42]. 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) [43], 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 [8].

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 [44]. 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

Chronic complications

It was traditionally thought that chronic complications of diabetes are rarely seen in Africa as a consequence of the high mortality rate leading to a low mean disease duration in most patients. Although there is some truth in this, there is no doubt that if carefully looked for, chronic diabetic complications are not infrequently seen. Thus, the prevalence of retinopathy has been recorded as 7–52%; cataract, 9–16%; neuropathy, 6–47%; nephropathy, 6–30%; and macroangiopathy, 1–5% [45, 46]. Table 2 summarises the recent complication prevalence studies in various parts of Africa. For each of the complications of retinopathy, neuropathy, nephropathy and microalbuminuria, two separate studies are quoted [47, 48, 49, 50, 51, 52, 53, 54]. The important points from these studies are that the specific complications of diabetes are common in the African continent, but their quoted prevalence varies enormously. This is almost certainly related to wide variations amongst the populations studied, including diabetes duration, glycaemic control, other risk factors (e.g. hypertension, smoking), population studied (hospital or community), diagnostic facilities and possibly ethnic factors.
Table 2

Selected chronic complication prevalence studies of diabetes in Africa

Complication

Location

Year

Prevalence (%)

Retinopathy

  [47]

Cape Town

1997

55

  [48]

Nigeria and Ghana

2003

18

Nephropathy

  [49]

Egypt

2004

14

  [50]

Nigeria

2003

28

Neuropathy

  [51]

Tanzania

2000

25

  [52]

Libya

1999

46

Microalbuminuria

  [53]

Tanzania

2007

11

  [54]

Cameroon

1999

53

The relatively high frequency of neuropathy leads, as may be expected, to a significant problem of foot ulceration [55]. The majority of diabetes-related foot ulcers (>80%) in Africa are neuropathic rather than ischaemic, presentation may be late and the outcome often poor [56]. 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 [55]. Diabetes-related large vessel disease syndromes are generally less common than in developed countries (particularly in sub-Saharan areas of the continent) [57]. 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 [58]. 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 [59]. Even in 2000, definite CAD was considered rare enough among Nigerian diabetic patients for two cases to be reported in the literature [60].

Acute complications

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) [62]. 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% [63]. Hypoglycaemia as a cause of hospital admission is more frequently related to sulfonylurea drugs (33% of hypoglycaemic admissions in one study) [64] 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 [65] and, occasionally, mucormycosis. Tuberculosis is also more common and more severe in patients with diabetes [66].

Metabolic and infective complications have been the major reasons for the high excess mortality associated with diabetes in Africa. Over a hundred years ago, the British missionary doctor in Uganda, Albert Cook, recorded that diabetes was ‘very fatal’ [67]. Sadly, this remains the case, although there is some evidence of improvements in at least some locations over the last 10–20 years. Population mobility, patient tracing and mortality enumeration all make it difficult to conduct reliable outcome studies in Africa. The main reports are summarised in Table 3 [68, 69, 70, 71]. The landmark initial study was by Castle and Wicks in Harare, Zimbabwe, some 30 years ago. They carefully followed a mixed-type cohort of 97 diabetic patients admitted to hospital [68]. With a high level of case tracing, they found that 6 years later, 41% had died—nearly all from metabolic or infective causes. They identified male sex, alcohol abuse and insulin treatment as being particular risk factors. In 1990, McLarty and colleagues from Dar es Salaam, Tanzania, reported on a larger series (again of mixed type) followed between 1981 and 1987 [69]. This was not a single cohort followed from one time point, but calculated 5 year mortality rates showed 66% survival if on insulin, and 82% if on oral agents. The increased risk conferred by insulin treatment described a decade earlier by Castle and Wicks [68] was thus again confirmed, although the overall outcome figures were a little improved. However, compared with European figures, the Tanzanian data was still depressing—McLarty et al. [69] showed that 5 years from presentation, one-third of those on insulin are likely to have died, whereas in Europe, 40% of such patients should survive for 40 years or more [72]. The increased mortality risk associated with insulin treatment may reflect dangers of insulin treatment itself (particularly without self-monitoring of blood glucose), or it may simply reflect that this represents a high-risk diabetic subgroup.
Table 3

Diabetes mortality studies in Africa

Country

Year

Diabetes types

Outcome

Mortality causes

Zimbabwe [68]

1980

Mixed—most type 2

41% had died at the 6-year follow-up

Most due to DKA, HNK, hypoglycaemia and infection

Tanzania [69]

1990

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

South Africa [70, 71]

1995, 2005

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

DKA, diabetic ketoacidosis; HNK, hyperosmolar non-ketotic coma

In Soweto, South Africa, a long-term follow-up of a type 1 cohort reported mortality rates at 10 [70] and 20 [71] 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) [70], 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% [71], 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 [72].

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. [74] 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.

Diabetes is perhaps the index case of a general problem of non-communicable disease healthcare delivery in developing countries.
Chronic disease care is compounded with the higher political priorities of infective diseases, poor supply of drugs and monitoring equipment and, for many people, a reliance on traditional rather than Western medicines [77, 78, 79].

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 [80]. 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 [81]. 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 [82]. 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 [83] 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 [84]. 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 [85]. Finally, in Eritrea [86], 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 [87].

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 [88] that require urgent attention. In 1977, Morley et al. [89] 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.

Notes

Acknowledgements

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.

References

  1. 1.
    Godfrey R, Julien M (2005) Urbanisation and health. Clin Med 5:137–141PubMedGoogle Scholar
  2. 2.
    Beaglehole R, Tack D (2003) Globalisation and the prevention and control of non-communicable disease: the neglected chronic diseases of adults. Lancet 362:903–908PubMedCrossRefGoogle Scholar
  3. 3.
    Aspray TJ, Mugusi F, Rashid S, for the Essential Non-Communicable Disease Health Intervention Project et al (2000) Rural and urban differences in diabetes prevalence in Tanzania: the role of obesity, physical activity and urban living. Trans R Soc Trop Med Hyg 94:637–644PubMedCrossRefGoogle Scholar
  4. 4.
    Murray CJL, Lopez A-D (1997) Mortality by cause of eight regions of the world: Global Burden of Disease Study. Lancet 349:1269–1276PubMedCrossRefGoogle Scholar
  5. 5.
    Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL (2006) Global and regional burden of disease and risk factors 2001: systematic analysis of population health data. Lancet 367:1747–1757PubMedCrossRefGoogle Scholar
  6. 6.
    Elamin A, Omer MI, Zein K, Tuvemo T (1992) Epidemiology of childhood type I diabetes in Sudan, 1987–1990. Diabetes Care 15:1556–1559PubMedCrossRefGoogle Scholar
  7. 7.
    Sobngwi E, Choukem SP, Agbalika F et al (2008) Ketosis-prone type 2 diabetes mellitus and human herpesvirus 8 infection in sub-Saharan Africans. JAMA 299:2770–2776PubMedCrossRefGoogle Scholar
  8. 8.
    WHO (2002) World Health Report 2002—reducing risks, promoting healthy life. WHO, Geneva. Available from http://www.who.int/whr/2002/, accessed 11 August 2008
  9. 9.
    Mbanya J-C, Ramaiya K (2006) Diabetes mellitus. In: Jamison DT, Feachem RG, Makgoba MW (eds) Disease and mortality in sub-Saharan Africa, 2nd edn. The World Bank, Washington, pp 267–287Google Scholar
  10. 10.
    Mbanya J-C, Gill GV (2004) Diabetes mellitus. In: Parry EPO, Godfrey R, Mabey D, Gill GV (eds) Principles of medicine in Africa, 3rd edn. Cambridge University Press, Cambridge, pp 739–767Google Scholar
  11. 11.
    Dodu SR (1967) Diabetes in the tropics. BMJ 2:747–750PubMedGoogle Scholar
  12. 12.
    Ahren B, Corrigan CB (1985) Intermittent need for insulin in a subgroup of diabetic patients in Tanzania. Diabet Med 2:262–264PubMedGoogle Scholar
  13. 13.
    Oli JM (1978) Remittant diabetes mellitus in Nigeria. Trop Geogr Med 30:57–62PubMedGoogle Scholar
  14. 14.
    Oli JM, Bottazzo GF, Doniach D (1981) Islet cell antibodies and diabetes in Nigerians. Trop Geogr Med 33:161–164PubMedGoogle Scholar
  15. 15.
    Adadevoh BK (1968) “Temporary diabetes” in adult Nigerians. Trans R Soc Trop Med Hyg 62:528–530PubMedCrossRefGoogle Scholar
  16. 16.
    Adetuyibi A (1975) Insulin in the management of diabetes mellitus in Nigerians. West Afr J Pharmacol Drug Res 2:97–102PubMedGoogle Scholar
  17. 17.
    Winter WE, Maclaren NK, Riley WJ et al (1987) Maturity-onset diabetes of youth in black Americans. N Engl J Med 316:285–291PubMedGoogle Scholar
  18. 18.
    Rosenbloom AL, Joe JR, Young RS, Winter WE (1999) Emerging epidemic of type 2 diabetes in youth. Diabetes Care 22:345–354PubMedCrossRefGoogle Scholar
  19. 19.
    Banerji MA, Lebovitz HE (1990) Remission in non-insulin-dependent diabetes mellitus: clinical characteristics of remission and relapse in black patients. Medicine (Baltimore) 69:176–185CrossRefGoogle Scholar
  20. 20.
    Banerji MA, Chaiken RL, Huey H et al (1994) GAD antibody negative NIDDM in adult black subjects with diabetic ketoacidosis and increased frequency of human leukocyte antigen DR3 and DR4. Flatbush diabetes. Diabetes 43:741–745PubMedCrossRefGoogle Scholar
  21. 21.
    Pinhas-Hamiel O, Dolan LM, Zeitler PS (1997) Diabetic ketoacidosis among obese African-American adolescents with NIDDM. Diabetes Care 20:484–486PubMedCrossRefGoogle Scholar
  22. 22.
    Yan SH, Sheu WH, Song YM, Tseng LN (2000) The occurrence of diabetic ketoacidosis in adults. Intern Med 39:10–14PubMedCrossRefGoogle Scholar
  23. 23.
    Sobngwi E, Mauvais-Jarvis F, Vexiau P, Mbanya J-C, Gautier J-F (2002) Diabetes in Africans. Part 2: ketosis-prone atypical diabetes mellitus. Diabetes Metab 28:5–12PubMedGoogle Scholar
  24. 24.
    Aizawa T, Funase Y, Katakura M et al (1997) Ketosis-onset diabetes in young adults with subsequent non-insulin-dependency, a link between IDDM and NIDDM? Diabet Med 14:989–991PubMedCrossRefGoogle Scholar
  25. 25.
    Abdulkadir J, Mengesha B, Welde Gebriel Z et al (1990) The clinical and hormonal (C-peptide and glucagon) profile and liability to ketoacidosis during nutritional rehabilitation in Ethiopian patients with malnutrition-related diabetes mellitus. Diabetologia 33:222–227PubMedCrossRefGoogle Scholar
  26. 26.
    Elamin A, Omer MI, Tuvemo T (1992) Islet-cell antibodies and endogenous insulin secretion in Sudanese diabetic children. Diabetes Res Clin Pract 16:91–96PubMedCrossRefGoogle Scholar
  27. 27.
    Habtu E, Gill G, Tesfaye S (1999) Characteristics of insulin-requiring diabetes in rural northern Ethiopia—a possible link with malnutrition? Ethiop Med J 37:263–267PubMedGoogle Scholar
  28. 28.
    Johnson TO (1992) Malnutrition-related diabetes mellitus: a syndrome seeking clarity. IDF Bull 37:3–4Google Scholar
  29. 29.
    Perret JL, Nguemby-Mbina C (1991) Characteristics of the development of insulin need in primary diabetes of adults in Gabon. Ann Soc Belg Med Trop 71:243–249PubMedGoogle Scholar
  30. 30.
    Lokrou A, Assamoi G, Cuisinier JC (1994) Plasma C-peptide levels amongst African diabetic patients from Cote d’Ivoire. Cross-sectional study of 207 cases. Rev Franc Endocrinol Clin 35:227–233 (article in French)Google Scholar
  31. 31.
    Ducorps M, Ndong W, Jupkwo B et al (1996) Diabetes in Cameroon. Classification difficulties in Africa. Med Trop 56:264–270Google Scholar
  32. 32.
    Perret JL, Bifane E, Ngou-Milama E, Moussavou-Kombila JB, Nguemby-Mbina C (1996) Types of sugar diabetes encountered in internal medicine in Gabon. Med Trop 56:55–58Google Scholar
  33. 33.
    Gale EAM (2007) To boldly go—or to go too boldly? The accelerator hypothesis revisited. Diabetologia 50:1571–1575PubMedCrossRefGoogle Scholar
  34. 34.
    Wilkin TJ (2007) Changing perspectives in diabetes: their impact on the classification. Diabetologia 50:1587–1592PubMedCrossRefGoogle Scholar
  35. 35.
    McFarlane SI, Chaiken RL, Hirsch S et al (2001) Near-normoglycaemic remission in African-Americans with type 2 diabetes mellitus is associated with recovery of beta cell function. Diabet Med 18:10–16PubMedCrossRefGoogle Scholar
  36. 36.
    Elamin AMI, Omer K, Tuvemo RT (1992) Epidemiology of childhood type 1 diabetes in Sudan 1987–1990. Diabetes Care 15:1556–1559PubMedCrossRefGoogle Scholar
  37. 37.
    Swai ABM, Lutale J, McLarty DG (1993) Prospective study of incidence of juvenile diabetes mellitus over 10 years in Dar es Salaam, Tanzania. BMJ 306:1570–1572PubMedGoogle Scholar
  38. 38.
    Kalk WJ, Huddle KRL, Raal FJ (1993) The age of onset of insulin-dependent diabetes mellitus in Africans in South Africa. Postgrad Med J 69:552–556PubMedGoogle Scholar
  39. 39.
    Harjutsalo V, Sjoberg L, Tuomilehto J (2008) Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 371:1777–1782PubMedCrossRefGoogle Scholar
  40. 40.
    Omar MAK, Bottazzo GF, Asmal AC (1986) Islet cell antibodies and other autoantibodies in South Africa blacks and Indians with insulin-dependent diabetes mellitus (IDDM). Hormone Metab Res 18:126–128CrossRefGoogle Scholar
  41. 41.
    Oli JM, Bottazzo GF, Doniach D (1980) Islet cell antibodies in Nigerian diabetics. Lancet 1:1090PubMedCrossRefGoogle Scholar
  42. 42.
    Panz VR, Kalk WJ, Zourvanis M, Joffe BI (2000) Distribution of autoantibodies to glutamic acid delarboxylase across the spectrum of diabetes mellitus seen in South Africa. Diabet Med 17:524–527PubMedCrossRefGoogle Scholar
  43. 43.
    Rheeder P, Stolk RP, Grobbee DE (2001) Ethnic differences in C-peptide levels with anti-GAD antibodies in South African patients with diabetic ketoacidosis. Quart Med J 94:39–43Google Scholar
  44. 44.
    Burdon J (1996) Another deadly Zairean disease. BMJ 313:58Google Scholar
  45. 45.
    Mbanya J-C, Sobngwi E (2003) Diabetes, micro-vascular and macrovascular disease in Africa. J Cardiovasc Risk 10:97–102PubMedCrossRefGoogle Scholar
  46. 46.
    Rolfe M (1997) Chronic complications of diabetes. In: Gill GV, Mbanya J-C, Alberti KGMM (eds) Diabetes in Africa. FSG Communications, Cambridge, pp 43–50Google Scholar
  47. 47.
    Levitt NS, Bradshaw D, Zwarenstein MF, Bawa AA, Maphumolo S (1997) Audit of primary diabetes care in Cape Town, South Africa: high prevalence of complications, uncontrolled hyperglycaemia, and hypertension. Diabet Med 14:1073–1077PubMedCrossRefGoogle Scholar
  48. 48.
    Rotini C, Daniel H, Zhou J et al (2003) Prevalence and determinants of diabetic retinopathy and cataracts in West African type 2 diabetes patients. Ethn Dis 13(Suppl 2):S110–S117Google Scholar
  49. 49.
    Afifi A, El-Setouhy M, El Sharkawy M et al (2004) Diabetic nephropathy as a cause of end-stage renal disease in Egypt: six-year study. East Mediterr Health J 10:620–626PubMedGoogle Scholar
  50. 50.
    Alebiosu CO (2003) A clinical review of diabetic nephropathy in Ogun State University Teaching Hospital, Sagamu. West Afr Med J 22:152–155Google Scholar
  51. 51.
    Abbas ZG, Archibald LK (2000) Foot complications in diabetes patients with symptomatic peripheral neuropathy in Dar es Salaam, Tanzania. Diabetes Int 10:52–56Google Scholar
  52. 52.
    Kadiki OA, Roaed RB (1999) Epidemiological and clinical patterns of diabetes mellitus in Benghazi, Libyan Arab Jamahiriya. East Mediterr Health J 5:6–13PubMedGoogle Scholar
  53. 53.
    Lutale J, Thordarson H, Abbas ZG, Vetvik K (2007) Microalbuminuria among type 1 and type 2 diabetic patients of African origin in Dar es Salaam, Tanzania. BMC Nephrol 8:2PubMedCrossRefGoogle Scholar
  54. 54.
    Sobngwi E, Mbanya J-C, Moukouri EN, Ngu KB (1999) Microalbuminuria and retinopathy in a diabetic population of Cameroon. Diabetes Res Clin Pract 44:191–196PubMedCrossRefGoogle Scholar
  55. 55.
    Abbas ZG, Lutale JK, Morbach S, Archibald LK (2002) Clinical outcomes of diabetes patients hospitalised with foot ulcers. Diabet Med 19:575–579CrossRefGoogle Scholar
  56. 56.
    Akanji AO, Adetuyidi A (1990) The pattern of presentation of foot lesions in Nigerian diabetic patients. West Afr J Med 9:1–5PubMedGoogle Scholar
  57. 57.
    Kengne AP, Amoah AG, Mbanya J-C (2005) Cardiovascular complications of diabetes mellitus in sub-Saharan Africa. Circulation 112:3592–3601PubMedCrossRefGoogle Scholar
  58. 58.
    Rolfe M (1988) Macrovascular disease in diabetics in Central Africa. BMJ 296:1522–1528PubMedGoogle Scholar
  59. 59.
    Lester FT, Keen H (1988) Macrovascular disease in middle-aged diabetic patients in Addis Ababa, Ethiopia. Diabetologia 31:361–367PubMedCrossRefGoogle Scholar
  60. 60.
    Danbauchi SS, Onyemelukwe GC (2000) Ischaemic heart disease in Nigerians: report of two cases. Diabetes Int 10:59–60Google Scholar
  61. 61.
    Lester FT (1997) Acute complications of diabetes. In: Gill GV, Mbanya JC, Alberti KGMM (eds) Diabetes in Africa. FSG Communications, Cambridge, pp 35–42Google Scholar
  62. 62.
    Rwiza HT, Swai ABM, McLarty DG (1986) Failure to diagnose diabetic ketoacidosis in Tanzania. Diabet Med 3:181–183PubMedGoogle Scholar
  63. 63.
    Rolfe M, Ephraim GG, Lincoln DC, Huddle KRL (1995) Hyperglycaemic nonketotic coma as a cause of emergency hyperglycaemic admissions in Baragwanath Hospital. S Afr Med J 85:173–176PubMedGoogle Scholar
  64. 64.
    Gill GV, Huddle KRL (1995) Hypoglycaemic admissions among diabetic patients in Soweto, South Africa. Diabet Med 12:546–550PubMedGoogle Scholar
  65. 65.
    Gill GV, Olufunsho O, Famuyiwa O, Rolfe M, Archibald LK (1998) Tropical diabetic hand syndrome. Lancet 351:113–114PubMedCrossRefGoogle Scholar
  66. 66.
    Balde N, Camara A, Camara LM, Diallo MM, Kake A (2006) Associated tuberculosis and diabetes in Conakry, Guinea: prevalence and clinical characteristics. Int J Tuberc Lung Dis 10:1036–1040PubMedGoogle Scholar
  67. 67.
    Cook AR (1901) Notes on the diseases met with in Uganda, Central Africa. J Trop Med 4:175–178Google Scholar
  68. 68.
    Castle WN, Wicks ACB (1980) Follow-up of 93 newly diagnosed African diabetics for 6 years. Diabetologia 18:121–123PubMedCrossRefGoogle Scholar
  69. 69.
    McLarty DG, Kinaabo L, Swai ABM (1990) Diabetes in tropical Africa: a prospective study 1981–7. II course and prognosis. BMJ 300:1107–1110PubMedGoogle Scholar
  70. 70.
    Gill GV, Huddle KR, Rolfe M (1995) Mortality and outcome of insulin-dependent diabetes in Soweto, South Africa. Diabet Med 12:546–550PubMedCrossRefGoogle Scholar
  71. 71.
    Gill GV, Huddle KRL, Monkoe G (2005) Long-term (20 years) outcome and mortality of type 1 diabetes patients in Soweto, South Africa. Diabet Med 22:1642–1646PubMedCrossRefGoogle Scholar
  72. 72.
    Nishimura R, Tajima N, Laporte RE, Becker D, Dornan JS, Orchard TJ (2001) Mortality trends in type 1 diabetes. The Allegheny County (Pennsylvania) Registry 1965–99. Diabetes Care 24:823–827PubMedCrossRefGoogle Scholar
  73. 73.
    McLarty DG, Unwin N, Kitange HM, Alberti KGMM (1996) Diabetes mellitus as a cause of death in sub-Saharan Africa: results of a community-based study in Tanzania. The Adult Morbidity and Mortality Project. Diabet Med 13:990–994PubMedCrossRefGoogle Scholar
  74. 74.
    Chale SS, Swai ABM, Mujinja PGM, McLarty DG (1992) Must diabetes be a fatal disease in Africa? Study of costs of treatment. BMJ 304:1215–1218PubMedCrossRefGoogle Scholar
  75. 75.
    Beren D, Yudkin JS, de Courten M (2005) Access to care for patients with insulin-requiring diabetes in developing countries. Case studies of Mozambique and Zambia. Diabetes Care 28:2136–2140CrossRefGoogle Scholar
  76. 76.
    Beren D, Yudkin JS (2006) Diabetes care in sub-Saharan Africa. Lancet 368:1689–1695CrossRefGoogle Scholar
  77. 77.
    Tanimowo MO (1994) Preliminary observations on the treatment of diabetes by a traditional medical practitioner in Nigeria. Int Diabetes Dig 5:99–101Google Scholar
  78. 78.
    Whiting DR, Hayes L, Unwin NC (2003) Diabetes in Africa. Challenges to health care for diabetes in Africa. J Cardiovasc Risk 10:103–110PubMedCrossRefGoogle Scholar
  79. 79.
    Peltzer K, Kohza LB, Lekhuleni ME et al (2001) Concepts and treatment for diabetes among traditional and faith healers in the northern province, South Africa. Curationis 24:42–47PubMedGoogle Scholar
  80. 80.
    Huddle KRL, Gill GV (1989) Reducing acute hyperglycaemic mortality in African diabetic patients. Diabet Med 6:64–66PubMedGoogle Scholar
  81. 81.
    Acheampong JW, Boateng KA, Eghan BA, Story P, Parry EHO, Tomlinson S (2000) The impact of diabetes nurses in the Komfo Anokye Teaching Hospital, Ghana. Diabetes Int 10:81–93Google Scholar
  82. 82.
    Mamo Y, Seid E, Adams S, Gardiner A, Parry E (2007) A primary health care approach to the management of chronic disease in Ethiopia: an example for other countries. Clin Med 7:228–231PubMedGoogle Scholar
  83. 83.
    Coleman R, Gill G, Wilkinson D (1998) Non-communicable disease management in resource-poor settings: a primary health care model from rural South Africa. Bull World Health Organ 76:633–640PubMedGoogle Scholar
  84. 84.
    Gill GV, Price C, Shandu D, Dedicoat M, Wilkinson D (2008) An effective system of nurse-led diabetes care in rural Africa. Diabet Med 25:606–611PubMedCrossRefGoogle Scholar
  85. 85.
    Gill GV, Price C, Shandu D, Dedicoat M (2007) Diabetes intervention in rural South Africa: long-term results from the Hlabisa Diabetes Project. J Endocrinol Metab Diab South Afr 12:30 (abstract)Google Scholar
  86. 86.
    Windus DW, Ladensun JH, Merrins CK et al (2007) Impact of a multidisciplinary intervention for diabetes in Eritrea. Clin Chem 53:1954–1959PubMedCrossRefGoogle Scholar
  87. 87.
    Ramaiya K (2005) Tanzania and diabetes: a model for developing countries? BMJ 330:679CrossRefGoogle Scholar
  88. 88.
    Ntyintyane LM, Panz VR, Raal FJ, Gill GV (2006) Metabolic syndrome, undiagnosed diabetes mellitus and insulin resistance are highly prevalent in urbanised South African blacks with coronary artery disease. Cardiovasc J South Afr 17:7–12Google Scholar
  89. 89.
    Morley JE, Lowenthal MN, Asvat MS, Kopelowitz W, Klein C, Kokoris N (1977) Problems experienced in a diabetic clinic for blacks. South Afr Med J 52:215–218Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • G. V. Gill
    • 1
  • J.-C. Mbanya
    • 2
  • K. L. Ramaiya
    • 3
  • S. Tesfaye
    • 4
  1. 1.Clinical DivisionLiverpool School of Tropical MedicineLiverpoolUK
  2. 2.Department of Diabetes and EndocrinologyUniversity of YaoundeYaoundeCameroon
  3. 3.Department of MedicineShree Hindu Mandal HospitalDar es SalaamTanzania
  4. 4.Department of Diabetes and EndocrinologyRoyal Hallamshire HospitalSheffieldUK

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