Review Article | Published:

Acting on non-communicable diseases in low- and middle-income tropical countries

Naturevolume 559pages507516 (2018) | Download Citation

Abstract

The classical portrayal of poor health in tropical countries is one of infections and parasites, contrasting with wealthy Western countries, where unhealthy diet and behaviours cause non-communicable diseases (NCDs) such as heart disease and cancer. Using international mortality data, we show that most NCDs cause more deaths at every age in low- and middle-income tropical countries than in high-income Western countries. Causes of NCDs in low- and middle-income countries include poor nutrition and living environment, infections, insufficient taxation and regulation of tobacco and alcohol, and under-resourced and inaccessible healthcare. We identify a comprehensive set of actions across health, social, economic and environmental sectors that could confront NCDs in low- and middle-income tropical countries and reduce global health inequalities.

Main

Poor health in the tropics often brings to mind infectious and parasitic diseases that thrive and spread in hot and humid climates (http://www.who.int/topics/tropical_diseases/en/ and http://www.astmh.org/education-resources/tropical-medicine-q-a/major-tropical-diseases), rather than NCDs like cancers and heart disease, which are considered ailments of wealthy urbanized Western nations1,2. NCDs refer to conditions other than injuries, maternal and perinatal conditions and nutritional deficiencies that do not involve an acute infection or parasite, and hence are not transmittable from person to person.

In the 1970s, Omran proposed3 a theory of epidemiological transition in which, as countries develop economically and ‘modernise’, there is a shift from communicable (infectious) diseases to NCDs. This linear perspective on health development has led the bulk of domestic and international health financing and policy in low- and middle-income countries to focus on infectious diseases and maternal and child health4.

As worldwide data on deaths and disease have become more available, it has become increasingly apparent that NCDs also affect the populations of low- and middle-income nations5,6,7. The growing evidence for the relevance of NCDs as a global health issue led to a United Nations high-level meeting on the prevention and control of NCDs, following which the World Health Organization (WHO) member states committed to reducing premature mortality from four NCDs (cancers, cardiovascular and chronic respiratory diseases, and diabetes in people in the age range 30–69 years) by a quarter relative to their 2010 levels by 2025. NCDs have also been included in the United Nations Sustainable Development Goals (SDGs), with a target of reducing by one-third, relative to their 2015 levels, premature mortality from NCDs and promoting mental health and well-being by 2030; the indicator used to measure progress towards this target is the same as that of the WHO target.

Despite increasing awareness of the importance of NCDs as a global health issue, there is limited evaluation of how similarities and differences in NCD composition between low- and middle-income tropical and high-income countries should influence policies and programmes that aim to reduce their health burden5,8,9. In this Review, we use international data to compare NCDs between low- and middle-income tropical and high-income Western regions (Box 1), and use these comparisons to identify policies and interventions that could reduce their burden. We begin by describing the overall mortality burden and composition of NCDs in tropical regions in comparison to high-income countries. We then evaluate some of the potential causes of regional differences of NCDs, including genetics, infections, nutrition, healthcare and poverty. Finally, we identify a comprehensive set of actions across health, social, economic and environmental sectors aimed at reducing NCDs in low- and middle-income countries.

NCD deaths in the tropics

In 2016, life expectancy at birth in low- and middle-income tropical countries ranged from less than 53 years in Sierra Leone and Central African Republic to above 79 years in some countries in Latin America and the Caribbean, for example Costa Rica and Cuba (Supplementary Fig. 1). With the exception of the USA, in which life expectancy at birth of 78.6 years was similar to that of some better-off low- and middle-income nations, life expectancy was consistently high in high-income Western countries, surpassing 83 years in Switzerland, Spain, France, Canada and Australia.

Of the 25.3 million deaths in the four tropical regions—Africa, India (south Asia), southeast Asia, and Latin America and the Caribbean—in 2016, 8.7 million (34%) were from infectious and parasitic diseases, maternal and perinatal conditions, and nutritional deficiencies, 14.0 million (55%) from NCDs and the remainder from injuries. The share of deaths from NCDs in tropical countries had the same geographical pattern as life expectancy, ranging from below 30% in some African countries to over 80% in parts of southeast Asia and Latin America and the Caribbean, Mauritius and Seychelles (Fig. 1a). Tropical Africa was the only region in which NCDs accounted for fewer deaths than infectious and parasitic diseases, maternal and perinatal conditions, and nutritional deficiencies (33% versus 57%). NCDs accounted for nearly 90% of all deaths in high-income Western countries, higher than their share in all tropical regions, as predicted by the epidemiological transition theory. Crude death rates from NCDs as a whole, and from most individual NCDs, were also higher in high-income Western nations than in low- and middle-income tropical regions.

Fig. 1: NCD mortality in low- and middle-income tropical countries and high-income Western countries.
Fig. 1

a, b, Share of deaths from NCDs (a) and age-standardized death rates from NCDs (b) in low- and middle-income tropical and high-income Western countries in 2016. NCDs include: cancers; cardiovascular diseases; diabetes; endocrine, blood and immune disorders; non-infectious respiratory, digestive (including liver), and genitourinary diseases; neurological conditions; mental and substance-use disorders; congenital anomalies; and sense-organ, skin, musculoskeletal and oral/dental conditions. The mortality and population data were taken from the WHO global health estimates85. All results are for females and males combined. Death rates were age-standardized to the WHO standard population10.

Crude death rates do not take into account that the populations of low- and middle-income countries are younger than in high-income countries (Supplementary Fig. 2). For example, 83% of tropical Africa’s population and 70% of India’s population is younger than 40 years, compared to 49% in high-income Western nations. Many infections disproportionately affect infants and children (such as diarrhoea, malaria and measles) or young and middle-aged adults (such as HIV and tuberculosis). In contrast, deaths from most NCDs increase with age (although there are exceptions such as congenital anomalies and haemoglobinopathies like sickle cell). This combination of distinct age patterns of deaths from NCDs versus infections and different age structures is the main reason for higher crude NCD death rates in high-income countries. In other words, low- and middle-income tropical countries have lower NCD death rates than high-income nations at least partly because their population is younger.

One way to compare the epidemiological (versus demographic) features of NCDs across countries is to fix the age structure to a reference (standard) population, a process known as age-standardization (this is done by taking a weighted average of age-specific death rates, with the weight for each age group being its share of standard population)10. Once this is done, NCDs as a whole, and most individual NCDs, have higher death rates in tropical countries than they do in high-income Western countries (Figs. 1b and 2). The exceptions to this pattern are cancers, mental, neurological and substance-abuse disorders, and endocrine, blood and immune disorders, for which age-standardized death rates are slightly lower or about the same in the tropical regions (Fig. 2). In other words, low- and middle-income tropical countries have a disadvantage in NCDs compared to their high-income Western counterparts, as they do for infectious diseases. The largest absolute disadvantage of tropical regions is that of cardiovascular diseases, followed by chronic respiratory diseases, diabetes, kidney and other genitourinary diseases, and liver cirrhosis and other digestive diseases. In the following sections, we examine the regional patterns of cardiovascular diseases and cancers, which are the largest two groups of NCDs.

Fig. 2: Comparison between low- and middle-income tropical regions and the high-income Western region of age-standardized death rates from NCDs in 2016.
Fig. 2

The mortality and population data were taken from the WHO global health estimates85. Results are for females and males combined. Death rates were age-standardized to the WHO standard population10.

That NCDs have a substantial mortality burden in low- and middle-income countries is consistent with the historical experience of high-income countries11,12,13. For example, in 1900, the ten leading causes of death in the USA included infectious diseases such as respiratory infections, influenza, tuberculosis and diarrhoea as well as heart and kidney diseases, stroke and cancers; by 1930, these latter diseases made up four of the five leading causes of death11,13. As life expectancy increased in high-income countries, age-standardized death rates declined for some NCDs (stroke and possibly kidney disease) but increased for others (cancers)11,12.

Regional inequalities in cardiovascular diseases

Cardiovascular diseases accounted for 5.8 million deaths (23% of all deaths) in the four low- and middle-income tropical regions, with their share ranging from 13% in Africa to 32% in southeast Asia, compared to 2.2 million deaths (30% of all deaths) in high-income Western countries. Age-standardized death rates from cardiovascular diseases as a whole, as well as from most individual cardiovascular diseases, were higher in low- and middle-income tropical regions than in the high-income Western region (Fig. 3).

Fig. 3: Age-standardized cardiovascular disease death rates in low- and middle-income tropical regions and the high-income Western region in 2016.
Fig. 3

A point above the dotted line has a higher death rate in the tropical region than in the high-income Western region, and a point below the dotted line has a lower death rate. Data are for females and males combined. Congenital heart anomalies are not classified as a cardiovascular disease by the international classification of disease system. They are shown here alongside the international classification of disease cardiovascular disease categories to show regional variations in their death rates9. Mortality and population data are taken from the WHO global health estimates85. Death rates were age-standardized to the WHO standard population10.

In relative terms, the largest regional mortality disparity was that of rheumatic heart disease, with death rates in the African and Asian tropical regions many times those in the high-income Western region. Rheumatic heart disease, which is caused by rheumatic fever from group A streptococcal disease, is a classic NCD of poor communities9,14. In 2016, it accounted for nearly 300,000 worldwide deaths, nearly half of which occurred in tropical Africa, India and southeast Asia. However, even in these regions, rheumatic heart disease accounted for no more than 4% of cardiovascular disease deaths in 2016.

Rheumatic heart disease was present at the beginning of the twentieth century in high-income countries, declining sharply and virtually disappearing by the 1970s, except in disadvantaged indigenous communities14,15,16. Much of this decline occurred before the introduction of antibiotics, owing to improvements in housing, hygiene, nutrition and primary healthcare11,14,15. More recent declines in middle-income tropical countries such as Costa Rica and Cuba have benefited from a combination of environmental interventions and antibiotic therapy14. Incidence remains high in sub-Saharan Africa and south Asia, where systematic prevention and treatment programmes are rare9,17. Other cardiovascular diseases associated with infections that are more common in low-income than in high-income countries include endomyocardial fibrosis, pericarditis and cardiomyopathy9,18,19. Like rheumatic heart disease, they accounted for a small share of cardiovascular disease deaths in 2016.

Although the near-disappearance of rheumatic heart disease from high-income nations has, appropriately, put a spotlight on its persistent burden in the poorest countries, the largest absolute mortality inequality between tropical and high-income regions is unequivocally that of stroke and ischaemic heart disease (Fig. 3) because they have a large mortality burden—more than three-quarters of cardiovascular disease deaths in every region. Historical data from high-income countries consistently show a decline in stroke death rates from as early as 1900, driven initially by a sharp decline in haemorrhagic stroke and subsequently by both haemorrhagic and ischaemic subtypes16. Limited data from middle-income countries also show similar trends16. High blood pressure is the single most important risk factor for stroke, especially for haemorrhagic stroke20, and is addressed later in this Review. Some stroke risk factors, such as sickle cell, are nonetheless predominantly tropical21.

How ischaemic heart disease changes during economic and health development is more complex than trends for rheumatic heart disease and stroke, which both tend to decline as overall health improves11,12,16,22. In high-income countries, ischaemic heart disease mortality increased in the first half of the twentieth century and declined subsequently, with similar trends seen today in middle-income countries with longitudinal data including Seychelles, South Africa and parts of Latin America11,16,22 Some studies have found a low prevalence of markers of coronary atherosclerosis, a precursor of ischaemic heart disease, in remote indigenous populations of the tropics—such as the Masai and Samburu in east Africa in the 1960s23,24, the Kalahari Bushmen in the 1970s25 and the Tsimane in South America in the 2010s26—even though diets, including the share of carbohydrates versus animal-source foods, vary substantially among these groups. It is, however, unclear how representative these groups are of the populations of the larger tropical regions where they live, and studies in the same and other tropical regions have found high levels of coronary disease or its precursors24,27. The variations in ischaemic heart disease rates and trends even within low- and middle-income countries may be because the disease has diverse causes, including chronic inflammation, fetal and early life malnutrition and stunted growth, smoking, heavy episodic (binge) alcohol drinking, and low consumption of fruits and vegetables, which are present to varying degrees in low- and middle-income countries. The large burden of ischaemic heart disease and stroke in low- and middle-income countries, and the similarities and differences in their causes compared to high-income countries, necessitate going beyond the simple paradigm of epidemiological transition to identify interventions that effectively address their local causes and health systems that are able to help patients with these conditions.

Diverse regional patterns of cancer mortality

Cancers accounted for 2.4 million deaths in 2016 (9% of all deaths) in the four low- and middle-income tropical regions, with their share ranging from 6% in Africa to 18% in Latin America and the Caribbean, compared to 1.9 million deaths (26% of all deaths) in high-income Western countries. Cancers are a heterogeneous group of diseases, so the regional variations may differ by type of cancer8,28. After age-standardization, death rates from many cancers were lower in the tropical regions than in high-income Western countries, with the difference largest for lung cancer, followed by colorectal and pancreatic cancers (Fig. 4). However, cervical, head and neck, liver, stomach and oesophagus cancers had higher death rates in all or some tropical regions than in the high-income Western region. Prostate cancer death rates were higher in tropical Africa and Latin America and the Caribbean than in high-income countries, but the opposite was true in India and southeast Asia.

Fig. 4: Age-standardized site-specific cancer death rates in tropical regions and the high-income Western region in 2016.
Fig. 4

A point above the dotted line has a higher death rate in the tropical region than in the high-income Western region, and a point below the dotted line has a lower death rate. Mortality and population data were taken from the WHO global health estimates85 Death rates were age-standardized to the WHO standard population10. Kaposi’s sarcoma is not shown as a separate category because its deaths were reported together with those from HIV/AIDS in the WHO global health estimates. See Supplementary Fig. 3 for incidence.

The regional differences in cancer death rates are due to a combination of differences in incidence and survival. Variations in cancer incidence are, in turn, due to different exposures to its major risk factors including smoking and alcohol use, chemicals and radiation in the environment, infections, diet, reproductive and sexual practices, and metabolic and hormonal factors28,29,30,31. Access to and utilization of screening and treatment also matters when precancerous lesions or early-stage cancer can be effectively treated, such as for cervical cancers. The incidence of most cancers in low- and middle-income tropical regions was similar to, or lower than, that in high-income countries, with the difference largest for prostate and breast cancers, followed by lung and colorectal cancers (Supplementary Fig. 3). That prostate and breast cancers had lower incidence but higher death rates in low- and middle-income regions is because of worse cancer survival32. Cervical, liver and stomach cancers were the only cancers with higher age-standardized incidence in all or most low- and middle-income regions. Kaposi’s sarcoma, of which HIV/AIDS is the leading cause, was unfamiliar to many physicians in the early 1980s, and has emerged as a leading cancer in Africa as a result of the HIV/AIDS epidemic, and the single most common cancer in countries such as Zimbabwe and Mozambique.

Almost all cervical cancers are caused by infection with human papillomavirus, which is mostly transmitted via sexual contact, and around 90% of non-cardia stomach cancers (that is, stomach cancer not including the upper stomach) are due to Helicobacter pylori infection (an estimated 70% of all stomach cancers are non-cardia)33,34, a bacterium transmitted via contaminated food and water. Given their main routes of transmission, both infections are strongly related to the hygiene environment and behaviour. Cervical and stomach cancer incidence and deaths have declined steadily in high-income countries and in emerging economies, owing to improvements in water and sanitation, housing, electrification and refrigeration, and access to soap and other basic hygiene necessities, as well as effective screening and treatment programmes for cervical cancer35,36,37,38,39. Poorer countries fare worse in terms of the social, environmental and health-system determinants of these two infection-related cancers. Further, although an effective vaccine for human papillomavirus now exists, most lower-income nations have not introduced human papillomavirus vaccination, partly owing to its cost28,40. As a result, in 2016, nearly two thirds (63%) of worldwide deaths from cervical cancer deaths occurred in the four tropical regions covered in this Review, compared with 7% in high-income Western countries.

Liver cancer, which is also more common in low- and middle-income tropical countries than in high-income countries, has multiple causes, including hepatitis B and C viral infection, mycotoxins, especially aflatoxin from contamination of foods such as maize and groundnuts during storage, liver flukes, which are transmitted by eating infected raw freshwater fish, smoking, alcohol use, adiposity and diabetes28,41,42,43. In high-income countries, hepatitis B virus infection has declined, while adiposity and diabetes have increased43,44,45, and alcohol use and smoking have declined in some countries and increased in others46. Owing to these complex trends, liver cancer declined in the middle decades of the twentieth century in high-income countries, followed by a continued decline in some countries and an increase in others, such as the USA and the UK36. Currently, the highest worldwide hepatitis B infection rates are those in tropical Africa, where hepatitis B virus vaccine coverage, especially for the birth dose, is lowest42. As a result, despite the availability of an effective vaccine, hepatitis B infection, in combination with aflatoxin, remains a key determinant of the large burden of liver cancer in Africa28, especially in west Africa.

Although infections remain an important cause of cancers in low- and middle-income tropical countries, other cancer risk factors are increasingly important. In particular, smoking accounts for about 20% of all cancer deaths in low- and middle-income countries, compared to 30% in high-income countries29. However, smoking is rapidly shifting from high-income to low- and middle-income countries owing to differences in taxes and other tobacco control measures, and fuelled by the tobacco industry’s tactics47. Harmful alcohol use, which accounts for about 5% of all cancer deaths worldwide is also common in Latin America, and rising in Africa and Asia48. The coexistence of cancers that are largely or partly caused by infections and those that are related to smoking and alcohol use means that reducing cancer burden in low- and middle-income countries must include social and environmental improvements such as clean water and sanitation, electrification and refrigeration to reduce the risk of infections, vaccination to protect against infections, and effective tobacco and alcohol control. However, the benefits of some of these actions will take decades to materialize. Therefore, health systems should be equipped to detect and treat precancerous signs or early-stage cancers49.

Causes of NCDs in low- and middle-income countries

The data presented in this Review demonstrate that not only are NCDs present in low- and middle-income tropical countries, but that also, after accounting for differences in age structure, the populations of these countries experience a higher burden of NCDs than high-income Western countries. Beyond a general disadvantage, there are differences in the composition of NCDs across low- and middle-income tropical regions compared to the high-income Western region. Here we examine some of the potential determinants of these regional differences.

Genetics

Genetic variants that increase the risk of NCDs may have different regional frequencies. For example, the sickle haemoglobin gene (HbS), which is protective against malaria, is more frequent in tropical regions, especially in Africa, than in other parts of the world, with three-quarters of children with a haemoglobinopathy born in sub-Saharan Africa50. Within Africa, the frequency of the HbS gene is associated with the historical geographical distribution of malaria, supporting the hypothesis that a classical tropical disease has shaped the geographical distribution of an NCD via genetic selection51,52.

It is possible that genetic susceptibility loci for other NCDs are also over- or under-represented in tropical regions. For example a variant on chromosome 17q21, which is more common in men of African descent than in non-African men, is associated with an increased risk of prostate cancer53,54. How much this single-nucleotide polymorphism accounts for the higher rates of prostate cancer in tropical Africa, however, is unclear because its causal effect is not fully established and its frequency varies across Africa. More broadly, currently known genetic variants do not account for the large regional variations in NCD rates seen earlier or for the fact that disease rates change over periods of years and decades. Nor do genetic variants explain why migrants from the tropics to Western countries tend to converge to disease rates in the host environment within a few generations. Therefore, it is important to evaluate genetics alongside social and environmental determinants in studying worldwide disease patterns.

Obesity and other cardiometabolic risks

One of the factors underlying the claims that NCDs, especially ischaemic heart disease and stroke, are uncommon in lower-income tropical countries is the assumption that diet worsens as societies become more affluent and urbanized, leading to higher rates of obesity and diabetes, and higher blood pressure and lipids1,7,55,56,57,58. However, affluence and urban living can lead to improvements as well as worsening in diet. For example, consumption of fruits, which are beneficial for NCDs, is seasonal in poorer countries, while more affluent populations use food trade, transportation and storage to consume fruits year-round and hence have higher average consumption16,46,59.

Body-mass index (BMI) and associated metabolic conditions also have varied patterns in relation to national income60. BMI is currently lower in tropical Africa and south and southeast Asia than in the high-income Western region, but is about the same in the latter region and Latin America and the Caribbean (Fig. 5)45. In contrast to BMI, diabetes prevalence is about the same, or higher, in most low- and middle-income regions than in the high-income Western region44. The regional discordance between diabetes and elevated BMI, which is an important cause of diabetes, might be partly due to phenotypic variations arising from inadequate fetal and childhood nutrition and growth in low- and middle-income countries as discussed below, leading to earlier onset of β-cell dysfunction. Additionally, the better-resourced health systems in high-income countries can identify people at high risk of diabetes at an earlier stage, and use lifestyle and dietary modification and drugs to delay or prevent its onset.

Fig. 5: Age-standardized cardiovascular disease death rate, mean BMI, mean systolic and diastolic blood pressure, mean serum total cholesterol and diabetes prevalence in low- and middle-income tropical and the high-income Western region.
Fig. 5

For each outcome, the colour shows the ratio for the level in each region to the average of the five regions. The inset text gives the actual level of each outcome. For example, mean BMI in high-income Western countries is 27.4 kg m−2, which is 1.12 times the average of all five regions. Data on deaths are from the WHO global health estimates85 and on risk factors from the NCD Risk Factor Collaboration (http://www.ncdrisc.org)44,45,61,63. Death rates and risk factors were age-standardized to the WHO standard population10.

In an even more extreme form of disadvantage in low- and middle-income regions, the highest worldwide blood pressure levels are those in sub-Saharan Africa, with blood pressure also high in south Asia, whereas high-income nations have some of the lowest blood pressure levels in the world61. Although historically, high as well as low blood pressure levels were observed in tropical countries27, blood pressure levels seem to have increased in Africa and Asia over the past few decades, while declining sharply in high-income countries61,62. Of the cardiometabolic risk factors, only cholesterol reflects the classical epidemiological transition model, and is currently lower in tropical Africa, south Asia, and east and southeast Asia than in high-income Western countries (Fig. 5)63.

Fetal and early-life environment and nutrition

Nutrition and environment during the fetal, childhood and adolescence periods are an important determinant of NCDs. In the second half of the twentieth century, researchers realised that children born or growing during periods of famine, war and economic hardship had a higher risk of some NCDs in adulthood64,65,66. The thrifty phenotype hypothesis67, which summarises these findings, postulates that early-life undernutrition increases the risk of NCDs, especially if followed by rapid or excessive weight gain68. In parallel, nutritionists and social scientists noted that, although there is a strong genetic influence on individual height, changes in height of an entire population are driven by social, environmental and nutritional status during childhood and adolescence69,70,71. Being taller is associated with enhanced longevity, lower risk of cardiovascular and respiratory diseases, and higher risk of some cancers65,72. These studies collectively demonstrate that fetal, childhood and adolescent environment and nutrition influence NCDs, with at least part of the effects mediated by linear growth.

In the early twentieth century, the shortest heights in the world were those in tropical Asia and Andean Latin America72. Asians and Latin Americans grew taller over the course of the twentieth century, with some of the largest worldwide gains in height occurring in east Asia. In India and other south Asian nations, height in adulthood has plateaued at lower levels than those experienced elsewhere72. Adults in sub-Saharan Africa were taller than those in Asia and parts of Latin America in the early twentieth century, but fell behind because Africans born in the last three decades of the twentieth century are shorter than their predecessors72,73. Poor early-life nutrition and stunted growth may be partly responsible for the fact that some NCDs are high in low-income countries, and decline as economies develop, the opposite of what is predicted by a simple epidemiological transition model.

Infections, parasites and mycotoxins

A distinct feature of the NCDs in tropical countries, especially in the lower-income regions of tropical Africa and south Asia, is the importance of diseases with infectious, parasitic and fungal origins (Box 2). As discussed earlier, infection-related NCDs include rheumatic heart disease, liver cirrhosis, cervical, liver and stomach cancers, and Kaposi’s sarcoma. Infections and parasitic diseases also contribute to other NCDs. For example, infectious respiratory diseases increase the risk of chronic obstructive pulmonary disease74, schistosomiasis and other helminth infections increase the risk of genitourinary diseases75, and inflammation as a result of chronic and repeated infections increases the risk of cardiovascular diseases19,76.

Although infections remain an important cause of NCDs in poor countries and communities, the burden of most infection-related NCDs is comparable to or smaller than that of other NCDs. For example, colorectal cancer, which is caused by high consumption of red and processed meat and low intake of dietary fibre now has a comparable burden to liver and stomach cancers in low- and middle-income tropical regions (Fig. 4). Age-standardized death rates from breast cancer are higher than those of cervical cancer in every tropical region except Africa, where their mortality burden is about the same. Similarly, prostate cancer has emerged as an important cause of death among men across low- and middle-income tropical regions, with a higher age-standardized death rate than liver or stomach cancer in some regions. Finally, NCDs with non-infectious origins are not only an important cause of mortality in low- and middle-income countries, but they may increase the risk of infectious diseases (Box 2). This reciprocal relationship should motivate a more integrated response to communicable and non-communicable diseases.

Poverty

More than two-thirds of people in the poorest countries in tropical Africa and about 12% in India live on less than I$1.90 per day (I$, international dollar that is adjusted for purchasing power and inflation; https://data.worldbank.org/indicator/SI.POV.DDAY?). The poor experience higher rates of NCDs partly because many causes of NCDs, including poor nutrition at all stages of life; inadequate housing, water, sanitation and electricity; smoking and elevated blood pressure, tend to be associated with poverty5,9,60,77,78,79. People in poor countries and communities, and those with lower income, also have more limited access to high-quality healthcare, because health infrastructure, personnel and technologies are more restricted or because they cannot afford the out-of-pocket cost of services. Limited primary care leads to low rates of diagnosis and treatment, or late diagnosis. For example, fewer women are screened and treated for cervical cancer and fewer people with hypertension and diabetes are diagnosed and treated in lower-income than in high-income countries5,80,81,82. Late diagnosis, typically when complications arise, coupled with more limited specialist care, worsens the prognosis of NCDs in low- and middle-income countries compared to high-income nations32,52,83. Given its central role in pathogenesis of NCDs, the poverty of individuals and communities, and not inherent features of the tropics, is the most important determinant of the higher NCD rates in the lower-income tropical countries and regions, compared to high-income nations as well as to the better-off region of Latin America and the Caribbean.

Actions to reduce NCDs in low- and middle-income countries

The data presented in this Review demonstrate that NCDs are an important cause of ill health and early death in low- and middle-income tropical countries, and after accounting for differences in age, most NCDs have a higher mortality burden than in high-income Western countries. Therefore, reducing the burden of NCDs is essential for improving health in low- and middle-income tropical countries and reducing global health inequalities.

The causes of NCDs in low- and middle-income tropical countries are diverse and include poor nutrition and living environment, infections, insufficient regulation of tobacco and alcohol, and under-resourced and inaccessible healthcare. Although much of the epidemiological research has focused on the effect of these factors on individual NCDs, they often lead to multiple communicable and NCDs in the same people and communities, leading to multi-morbidity84. Multiple co-occurring diseases and risk factors can have amplifying effects and lead to overall poor health and loss of productivity. At the same time, the shared causes and aetiologies of these conditions, and their overlap, provides an opportunity for systematic integration of public health and healthcare interventions for their prevention and treatment. Doing so requires better data on the patterns of multi-morbidity among communicable and non-communicable diseases and their risk factors in low- and middle-income countries because they may be different from those in high-income countries (Box 3).

Underpinning these proximal determinants is a background of poverty, food insecurity (in terms of both quantity and quality), and insufficiency of infrastructure and services related to housing, water, sanitation, transportation and healthcare that afflict poor countries, communities and families. These challenges are the focus of the SDGs. The SDGs have broadened the development agenda of their predecessor, the Millennium Development Goals, whose health-related goals and targets focused on maternal and child health and infectious diseases. As stated earlier, SDGs have a target related to reducing NCD mortality, although this target excludes some important NCD causes of death in low- and middle-income tropical countries such as kidney, liver and other genitourinary and digestive diseases. Alongside this NCD mortality target, SDGs have targets for reducing tobacco and alcohol use (important causes of NCDs throughout the world), and for increasing universal health coverage (essential for enhancing timely diagnosis and treatment of NCDs and their risk factors in an equitable manner). The momentum generated by the SDGs provides an opportunity to turn political attention to NCDs. To succeed in reducing the large burden of NCDs in low- and middle-income countries and global health inequalities requires (1) identifying interventions and programmes that can be scaled up in resource-limited settings to effectively lower the burden of NCDs (Box 3) and (2) a substantial increase in domestic as well as international financing that supports low- and middle-income countries in sustained actions against NCDs.

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Acknowledgements

We thank R. Beaglehole, S. Blundell, R. Nugent, F. Piel, M. Parkins and M. Thun for comments and recommendation of background literature.

Reviewer information

Nature thanks F. Assah, P. Byass, B. Singer and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Affiliations

  1. Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK

    • Majid Ezzati
    • , Jonathan Pearson-Stuttard
    •  & James E. Bennett
  2. MRC-PHE Centre for Environment and Health, Imperial College London, London, UK

    • Majid Ezzati
    • , Jonathan Pearson-Stuttard
    •  & James E. Bennett
  3. WHO Collaborating Centre on NCD Surveillance and Epidemiology, Imperial College London, London, UK

    • Majid Ezzati
  4. Department of Information, Evidence and Research, World Health Organization, Geneva, Switzerland

    • Colin D. Mathers

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Contributions

M.E. designed the Review concept and wrote the Review with input from J.P.-S., J.E.B. and C.D.M. J.P.-S. contributed to clinical and epidemiological reviews. J.E.B. and C.D.M. analysed data, and J.E.B. prepared figures.

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The authors declare no competing interests.

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Correspondence to Majid Ezzati.

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