This study describes the prevalence of NCDs and NCD risk factors among South African AYLHIV in an urban setting. Previous studies in sub-Saharan Africa have described NCD comorbidities in adults living with HIV [44, 109–112]. Besides mental health [113–121] and lung diseases [122–126], few studies have assessed the prevalence of NCDs and particularly NCD risk factors in AYLHIV in SSA other than as incidental findings [127–134]. Risk behaviour research on AYLHIV in sub-Saharan Africa has predominantly focused on sexual risk behaviour [135]. We therefore set out to investigate NCD risk factors given the emerging NCD epidemic in SSA occurring against a background of a high HIV burden and increased comorbidity risk in PLHIV.
We highlight several key findings. Almost half of our participants faced multiple deprivations of poverty, significant symptoms of depression and psychological distress, and multiple risk factors for NCDs. More than a third were overweight or obese, a third had insufficient levels of weekly physical activity and the majority did not meet dietary guidelines for fruit and vegetable intake. There was low nutritional knowledge, particularly on healthy food choices and diet-disease relationships. Tobacco use and exposure and harmful use of alcohol were highly prevalent with male participants engaging in more substance use than females. An alarming pattern of early initiation of high-risk behaviours including underage and binge drinking, smoking and experimentation with cannabis emerged in the youngest age group. A detailed interpretation of these findings, comparisons to the general population and previous findings in PLHIV as well as implications for integrated prevention are discussed below.
76% of participants were female
More than two-thirds of our respondents were female which is consistent with national laboratory data for adolescents in HIV care [136]. This reflects the gendered nature of the HIV epidemic in South Africa, where almost a quarter of all new HIV infections occur in young women aged 15–24 years [137], and much higher rates of health care-seeking among young women compared to young men [42, 138].
44% of AYLHIV were multidimensionally poor
This is higher than national estimates which indicate that 33,4% of young people aged 15–24 years are MPI poor [139]. Nationally 34% of young people aged 15–24 years were not in education, employment, or training (NEET) in 2019 [140]. An “idle” youth population, not only impacts on the social cohesion and safety of a community, but is also linked to uptake of risk behaviours [141]. Although the proportion of NEETs in this study was lower than the national average with 73% of respondents either in education or engaged in income-generating activities, they experienced other deprivations which may interact to exacerbate vulnerability to NCDs and poor mental health. The highest deprivation was in general health and functioning dimension; with 68% experiencing difficulties with general health and functioning, 35% lived in informal housing, and 38% reported experiencing severe food insecurity.
Previous studies in South Africa have demonstrated that HIV/AIDS-affected and infected youth face multiple deprivations of poverty [60, 119], including poor educational outcomes [142], informal housing, lack of basic necessities like warm clothing, toiletries and school fees [143] and food insecurity [144]. Socioeconomic barriers such as poverty and food insecurity are commonly cited challenges for adolescents receiving HIV treatment and care in SSA [145]. This is concerning because socioeconomic factors like food insecurity impact adherence to ART and retention in HIV care [146], which has implications for viral suppression and chronic disease pathways [64, 147, 148]. These factors also have an impact on mental health and may increase susceptibility to alcohol and substance use [149–152]. Addressing this challenge requires a multi-sectoral approach for NCD prevention with appropriate social protection systems to meet the needs of the most vulnerable [143].
36% overweight or obese and 37% had abdominal obesity
More than a third of our respondents were overweight or obese (36%), with significantly more overweight and centrally obese females compared to males. Although our rates of overweight and obesity are slightly lower than prevalence rates for youth in the Western Cape (31.5% overweight and 11.3% obese) [38], the rates for ALYHIV appear similar to obesity trends in the general population. A previous study in adult patients attending primary health care HIV-clinics in South Africa found that more than half of female patients were overweight or obese compared to 16% of male patients [153]. Obesity in PLHIV is well documented in high-income countries and is emerging as a major challenge in Africa [50] with numerous studies showing increased rates of obesity in PLHIV [153–158]. But few studies in Africa have reported on overweight and obesity levels in AYLHIV other than in the context of ART-associated dyslipidaemia [129, 159, 160].
One study conducted among South African university students living with HIV (the majority aged 20–25 years) found that 21% were overweight and 30% were obese [161]. Findings from the United States Adolescent Trials Network showed that more than 40% of behaviourally HIV-infected young women (14–24 years) were overweight or obese [162] and approximately 36% of perinatally HIV-infected adolescents were overweight or obese [163]. Our results are consistent with these findings and confirm results from a folder review conducted in this same population that reported similar levels of overweight and obesity [66]. Overweight and obesity in AYLHIV may accelerate their lifetime risk of cardiovascular diseases, additional to the effects of HIV-infection and exposure to ART [162]. In our study, obesity co-occurred with hypertension – 35% of those with elevated blood pressure or hypertension were also overweight or obese. By screening for obesity, other related conditions which tend to cluster with obesity can also be detected. Closer monitoring of overweight and obesity profiles in young PLHIV in SSA is needed as they transition into adulthood, especially with prolonged exposure to ART regimens which are linked to obesity, altered glucose metabolism and dyslipidaemia [164].
In addition to BMI, we assessed central obesity using waist and hip circumference indicators. We found that 26% of our respondents with normal BMI had high WHR or WHtR, meeting criteria for central obesity. Another South African study in adults attending three HIV-clinics reported a high prevalence of central obesity, primarily in women – 45% (4% in men) [161]. In contrast, in a study conducted in Brazil, only 2.5% of children and adolescents on ART were overweight or obese based on subscapular skinfold thickness and less than 1% had a high WC [165]. In that study, the authors highlight that they expected a higher prevalence of overweight and obesity, but this was likely influenced by parallel gains in height and weight observed in adolescents [165]. In a comparison of anthropometric measures for predicting cardiometabolic risk in HIV patients in Cameroon, Dimala et al found that markers of adiposity like WC, WHR and WHtR are better than BMI at identifying HIV/AIDS patients with increased cardiometabolic risk [166].
The WHO and the International Diabetes Federation (IDF) recommend monitoring changes in waist circumference in addition to measuring BMI, as this can provide an estimate of increased abdominal fat even without a change in BMI, particularly in HIV-positive populations on ARV medication and in female patients who have a higher prevalence of obesity [79, 167]. Waist circumference and WHtR have been shown to be better predictors of cardiovascular disease risk factors in children and adolescents than BMI [168]. Waist-to-height ratio has the additional merit of not being dependent on age, sex or ethnicity, as the standard cut-off value of 0.5 is indicative of an increased cardiometabolic risk universally [107]. These findings underline the importance of anthropometry beyond BMI, especially in females. Anthropometric measurements and calculations are non-invasive, low-cost and easy-to-use interventions that can be used in primary care to identify AYLHIV who are at increased cardiometabolic risk.
High levels of depression and psychological distress
Almost half our participants reported symptoms of psychological distress, compared to less than a quarter of young people nationally [21]. Only 11% of those with mild, moderate or severe psychological distress reported previously being diagnosed with a mental health condition. Mental health conditions are prevalent in AYLHIV in both high-income and resource-limited settings [169]. Our results are generally consistent with prevalence rates of depression among children and adolescents living with HIV from other African countries which ranged from 18.9% in Malawi [67], 25% in Rwanda [170], 27% in Tanzania [171] and 51.2% prevalence of psychological distress in Uganda [172]. These results are difficult to pool together due to non-uniformity in the methods used for mental health screening [169].
Significantly more female participants reported depressive symptoms compared to males (51% compared to 19%) which is in line with global statistics on depression [173]. After the age of 15, girls and women are twice more likely to be depressed compared to boys and men [174]. Our findings show that only 17% of those identified as having significant depression via CESD-10 reported being previously diagnosed with anxiety or depression. In a previous retrospective review in the same population, mental health conditions were documented in less than 5% of folders reviewed [66]. These findings highlight that there is a missed opportunity for identifying youth with mental health problems before suboptimal ART adherence or other adverse HIV, NCD and mental health outcomes occur.
A recent study conducted amongst AYLHIV aged 9–19 years attending a primary care clinic in Johannesburg found that 8% screened positive for symptoms of depression which is much lower than our findings. However, 60% of those study participants were young adolescents aged 9–12 years and almost all were perinatally-infected (92%) [116]. Older adolescents in that study (aged 16–19) were more likely to screen positive for depression compared to younger adolescents, which is in line with our findings of higher depression scores in older adolescents and young adults. It has been documented that perinatally-infected adolescents may present with less psychological problems compared to behaviourally-infected adolescents [119, 175]. But similar rates of mental health conditions have been reported in HIV-exposed but uninfected youth entering adolescence [176]. The use of inappropriate comparison groups in studies showing higher rates of mental health disorders in AYLHIV, makes it difficult to determine whether these impairments are in fact due to HIV-infection or other social confounding factors. In a recent study conducted in Soweto, South Africa, the authors found similar rates of mental illness in perinatally-infected and uninfected adolescents, suggesting that other contributing social factors prevalent in the community may override the effect of HIV, especially in the era of highly active antiretroviral treatment [177].
Mental health screening is crucial in HIV care due to multiple psychological vulnerabilities associated with living with HIV and high rates of suicide in PLHIV [178–180]. Recommendations calling for integration of mental health services into HIV care have been made for adults [181]. It is important that adolescents are not overlooked in this respect. A study conducted in Johannesburg found that a simple way of identifying youth struggling with mental health problems at primary care level is by asking them about their future aspirations. Those who do not feel like they have control of their future or do not have a dream for the future are more likely to have symptoms of depression, anxiety or PTSD requiring further support [114].
Low nutritional knowledge, especially on healthy food choices
Participants scored less than 40% on general nutrition knowledge questions and particularly had poor knowledge of healthy food choices and associations between diet and diseases. Only 10% recognised that eating thick-cut instead of thin or crinkle cut chips could help reduce the amount of fat in someone’s diet and 22% correctly identified that eating less trans-fats can prevent heart disease. To our knowledge, this is the first study to assess nutrition knowledge in AYLHIV in Africa. A South African study in school-going adolescents aged 15–18 years found that 77.5% scored below average on diet and nutrition knowledge questions [182]. The poor knowledge on nutrition-related NCDs amongst AYLHIV in our study is concerning in a country undergoing nutritional transition [183]. Nutrition knowledge is strongly correlated with dietary intake and is needed for better dietary habits [97]. Although adolescents may lack autonomy in navigating their food environment, this life stage is characterised by increasing independence and as such they need to be informed about the importance of diet and how it can affect their current health status or future adult health [182]. Some practices like healthy cooking methods requiring steaming, roasting or baking can be adopted in their homes with cooperation of parents and caregivers [184]. With adequate knowledge, older adolescents in our study who ate more fast-food and more meals prepared outside the home, could be encouraged to make healthier food choices.
High fast-food and SSB consumption, and low physical activity
Almost three-quarters of AYLHIV did not eat fruit daily and almost half did not eat vegetables daily, falling below recommended dietary guidelines of eating at least five portions of fruit and vegetables daily in order to reduce the risk of NCDs [185]. Female participants ate less fruit and ate more fast-food, deep-fried foods and foods with added sugar daily compared to males. Younger adolescents ate less fruits, vegetables and wholegrains compared to older age groups.
More respondents, particularly females, consumed deep-fried foods and fast-foods daily compared to provincial estimates for youth in the Western Cape, while the proportion who consumed SSB daily was lower (29% compared to 42%) [20]. Our results are comparable to local estimates that one in five school-going youth skip breakfast [38]. A recent study on fast food and carbonated soft drink consumption among adolescents aged 12–15 years in 44 LMICs (not including South Africa) found that 44% of adolescents consumed a carbonated soft drink at least once per day in the past month [186]. A meta-analysis on SSB intake found that individuals who consumed 1–2 servings per day, had a 26% greater risk of developing type 2 diabetes, and a 20% greater risk of metabolic syndrome compared to those who did not consume SSB or had less than one serving/month [187]. In order to promote healthy diet, a multi-sectoral approach that promotes a healthy food environment is required. The South African government has made strides in promoting healthier food environments by implementing mandatory legislation for salt reduction in processed foods in June 2016 [188] and a tax on sugar-sweetened beverages in April 2018 [189]. These measures were introduced in efforts to reduce the prevalence of hypertension, obesity, NCDs and excess salt and sugar consumption [190]. More efforts are needed to translate these measures into action at a community and household level, especially amongst young girls who have higher prevalence of obesity which is likely to persist till adulthood without intervention.
Our results support findings of gender differences in physical activity levels among South African adolescents similar to global reports [191, 192]. Despite more than two-thirds of our respondents using active transport; either walking to and from school or work, fewer than one-third had sufficient levels of physical activity necessary to promote health and prevent chronic diseases. Almost half spent three or more hours per day of their leisure time sedentary. This is similar to physical inactivity levels reported in urban-based South African students [191]. Sedentary behaviour was higher than general population estimates which showed that 30% of youth watched TV or played computer games for over three hours per day [38] and higher than estimates from other LMICs which found that 27.0% of adolescents engaged in three or more hours of sedentary behaviour per day. Our results are consistent with those from a study in Brazil which found that 71% of ALHIV were sedentary with a higher proportion among girls [193]. Another study conducted in Botswana, found that youth living with HIV had significantly lower levels of daily PA compared to uninfected controls [129]. Similarly, a study in Brazil in 10–15-year-old perinatally-infected adolescents and age-sex matched controls also found that participants living with HIV had lower physical activity scores compared to healthy peers [194]. Additional research is needed in this setting to explore the relationship between PA and HIV in adolescents. A study with an age-and sex-matched uninfected control group from the same community would help to elucidate whether this relationship exists in South Africa.
Early initiation of high-risk behaviours (smoking, alcohol, drugs)
The median age at smoking initiation of 16 years found in our study was similar to the national average of 15.8 years for youth aged 15–24 years. However, our findings that 48% of male and 25% of female AYLHIV smoked daily or occasionally was much higher than national estimates for young people aged 15–24 years reported in the 2016 Demographic and Health Survey (29% of males and 5% of females [20]). Furthermore, almost half of those in the youngest age group reported at least occasional cigarette smoking in the past month and used more alternative tobacco products like water-pipes compared to older age groups. Young adolescents in South Africa increasingly use water-pipes (known as hookah pipes) which are often available without restriction [195, 196]. Our results likely reflect trends in the Western Cape – the province with the highest prevalence of tobacco smoking in South Africa– where a quarter of school-going youth are current smokers [38] and the mean age of smoking initiation is significantly lower than the national average at 14.5 years [21]. There are only a few studies, most from high-income settings, that address the prevalence of smoking among AYLHIV [197–199]. These studies report higher rates of smoking among AYLHIV compared to the general population, particularly among those who were behaviourally-infected [200]. Our findings corroborate this and add to the limited literature from low and middle-income settings.
Smoking increases the vulnerability of PLHIV for adverse lung health and multiplies their risk of developing cardiovascular diseases compared to HIV-negative smokers [201–203]. Smoking often co-occurs with other health risk behaviours like alcohol consumption [204]. More than half (58%) of current smokers in our study had also drunk alcohol in the preceding month. Our results also indicate higher rates of current alcohol consumption compared to national estimates for South African youth (41% versus 33%) [38]. A few studies in SSA have reported higher occurrence of alcohol consumption in AYLHIV compared to HIV-negative adolescents [135]. Auvert et al reported that 29% of AYLHIV in a South African mining town drank alcohol at least once a month although this study was conducted almost 20 years ago [134]. Another study conducted in Zimbabwe reported that 5.6% of adolescent females living with HIV drank alcohol in past month, compared to 4.5% of HIV-negative females [133]. Several studies conducted in young people from other regions have reported increased alcohol and drug use especially among male AYLHIV [205]. Our results suggest that this may be the case, but further research is needed in South Africa and SSA to elucidate whether HIV infection is associated with increased alcohol consumption in young people living in settings like South Africa where heavy drinking is endemic [22].
Our respondents reported higher rates of binge drinking in the past month compared to estimates for the general population [20] (21% of females and 37% of males in our study, compared to 5% and 21% nationally). Alarmingly, half of the underage respondents (< 18 years) were current drinkers and 55% of them engaged in recent binge drinking. Males reported significantly more use of illegal drugs or substances to-get-high compared to females. Previous studies on risk behaviour among AYLHIV in SSA report a high prevalence of alcohol and substance use behaviour, especially among males in late adolescence [135, 206]. In a study conducted amongst young people aged 15–26 years in the rural Eastern Cape province of South Africa, 4% of female AYLHIV reported problem alcohol drinking and 5% reported ever using drugs [131], whilst 31% of male AYLHIV reported problem drinking and 54% reported ever using drugs [132]. Alcohol and drug use did not differ from HIV-uninfected young people residing in the same setting [131].
The Western Cape has significant rates of stimulant use such as methamphetamine and cocaine compared to the rest of the country [207]. Approximately 5% of learners in the Western Cape have used methamphetamine within their lifetime [208]. Our findings may indicate a general underlying substance use problem in young people in this setting, not necessarily related to HIV, but which predisposes AYLHIV to more vulnerability. High rates of substance use and implications for brain development, particularly amongst males and younger adolescents, is concerning and warrants targeted intervention. Prevention and early intervention strategies aimed at harm reduction are needed that incorporate environmental factors beyond individual behaviour.
Other NCD comorbidity
Our blood pressure findings are consistent with findings from studies in general adolescents in urban South Africa which have reported hypertension prevalence rates ranging from 8–16% [209] and elevated BP prevalence of 35% [210]. Chatterton-Kirchmeier et al reported a significantly higher prevalence of elevated blood pressure in a cohort of HIV-infected, predominantly African-American adolescents and young adults in the US compared to healthy children [211]. Globally, studies involving HIV-infected adults have demonstrated higher hypertension prevalence than the general population [212] and hypertension has been found to be associated with ART [213, 214]. One in five young adults (18–35 years) attending an HIV clinic in the same setting in Khayelitsha had comorbid hypertension [65]. There is no clear link in the literature between HIV infection and elevated BP in paediatric populations. Nevertheless, routine monitoring of blood pressure in HIV care, even in younger populations, is warranted in settings like South African with a high background prevalence of hypertension, in order to avert future disease. This is especially relevant in light of evidence that blood pressure trajectories in childhood and adolescence predict future elevated BP and cardiovascular risk in adulthood [209, 210, 215].
None of the 25% with self-reported diabetes symptoms in our study had an abnormal measured random blood glucose. In a cohort study of South African youth living with perinatally-acquired HIV, the authors found a high prevalence of insulin resistance but it did not differ from that in uninfected age-matched adolescents [128]. A systematic review and meta-analysis of African studies, recently reported that there was no statistically significant association between HIV infection or ART exposure and type 2 diabetes (T2DM) prevalence in adults [216]. This is in contrast with study findings from European and North American settings that have shown a higher prevalence of T2DM in HIV-infected adults particularly those on ART [217–219]. However, the cumulative incidence of T2DM in patients with HIV across Africa was higher than international incidence data for HIV-infected individuals. The International Diabetes Federation estimates that 60% of people with diabetes in Africa are undiagnosed [220] suggesting that T2DM might be a major, underdiagnosed public health problem in African populations in general due to the presence of traditional risk factors.
Strengths and Limitations
Our study adds to the limited evidence base on NCD prevalence and risk factors in AYLHIV in sub-Saharan Africa. To our knowledge, only four other studies in sub-Saharan Africa have investigated modifiable NCD risk factors besides alcohol and substance use in AYLHIV [127, 129, 161, 221]. While our study provides novel findings for the sub-Saharan African context, the findings should be interpreted within the following limitations. Firstly, participants were recruited using convenience sampling from healthcare facilities in a peri-urban setting. Second, there was an almost 50% non-response rate. The low response rate and lack of random sampling may limit the generalizability of our findings, however sampling from six different facilities across all substructures in the City of Cape Town, proportional to the total numbers of AYLHIV within each substructure) mitigated unmeasured facility-specific effects. Limited participation and low response rates are a major challenge in adolescent research due to the complexities of enrolment and consent procedures [222, 223]. Although we recruited younger adolescents, requiring parental consent may have led to participant bias as the majority enrolled were older adolescents and young adults (aged ≥ 18 years) who could provide independent consent to participate. We therefore conducted an age-stratified analysis of participant characteristics.
Although we were not statistically powered to detect differences by gender or age groups, some clear differences emerged particularly gender differences in physical activity, obesity levels and mental health which have been previously documented. Striking differences in high-risk behaviours were also identified in the younger age group. Due to the cross-sectional design, we were unable to establish temporality and whether NCD risk factors and risky behaviours preceded an HIV diagnosis amongst behaviourally-infected youth. Our study did not include a control group of HIV-uninfected adolescents, neither did we differentiate between perinatally and behaviourally-infected adolescents who may have very different risk profiles [57, 119]. Nevertheless, since young people come from the same communities and access the same HIV services, irrespective of mode of transmission, interventions targeting risk factors generally may be more effective.
We used subjective recall methods of measuring physical activity which may be prone to over-reporting [224, 225], recall bias and cultural misinterpretation [226, 227]. However, self-report methods like the IPAQ have acceptable validity and are most widely used to measure physical activity in PLHIV [51]. The use of point-of-care random blood glucose testing may have underestimated diabetes risk, however, POC methods are better suited for community screening of diabetes, have high specificity (90%) and provide reliable and immediate results [228, 229]. Similarly, the mental health tools used are screening tools– a diagnosis of depression or anxiety was not confirmed using these tools. But they are appropriate for case-finding in primary care and have been validated in HIV-positive populations in South Africa [103, 230]. Despite using a self-administered questionnaire, there remains a possibility that social desirability or other reporting biases may affect reports of mental health and substance use, with potential for underreporting. To minimise this risk, we used tablet computers for data collection which have been found to reduce reporting bias on sensitive questions [231, 232]. Moreover, the reported rates were still significant and if underreported, warrant further attention. Despite these limitations, this study is an important contribution to the limited literature in sub-Saharan Africa.