Predictors of weight loss after HAART initiation among HIV-infected adults in Tanzania
Li, Nana; Spiegelman, Donnab; Drain, Paulc,d; Mwiru, Ramadhani S.a; Mugusi, Ferdinande; Chalamilla, Guerinof; Fawzi, Wafaie W.g
aDepartment of Nutrition
bDepartments of Epidemiology and Biostatistics, School of Public Health, Harvard University
cDivision of Infectious Diseases, Brigham and Women's Hospital
dDivision of Infectious Diseases, Massachusetts General Hospital, Boston, Massachusetts, USA
eDepartment Internal Medicine, Muhimbili University of Health and Allied Sciences
fManagement and Development for Health (MDH), Dar es Salaam, Tanzania
gDepartments of Nutrition and Global Health and Population, School of Public Health, Harvard University, Boston, Massachusetts, USA.
Correspondence to Nan Li, PhD, MHS, Harvard School of Public Health, 1633 Tremont St, Boston, MA 02120, USA. E-mail: email@example.com
Received 24 July, 2011
Revised 3 November, 2011
Accepted 23 November, 2011
Objective: To explore the predictors of weight loss after highly active antiretroviral therapy (HAART) initiation in a large cohort of HIV-infected adults living in Dar es Salaam, Tanzania.
Design: Cross-sectional and longitudinal analysis of a cohort of HIV-infected adults on HAART.
Methods: HIV-infected adults (n = 18 965) were enrolled between November 2004 to December 2009 in Dar es Salaam, Tanzania. Log-binomial regression and Cox proportional hazard regression were used to explore the predictors of short-term (3 months) and long-term significant weight loss (≥5%) after HAART initiation.
Results: At 3 months after HAART initiation, 8% patients lost greater than or equal to 5% weight. Underweight patients at initiation gained more weight than other body mass index (BMI) groups. Younger or older than age group 30–39, lower socioeconomic status (SES), higher BMI, lower hemoglobin, difficulty breathing, loss of appetite, nausea/vomiting at baseline were associated with the risk of significant weight loss at 3 months after initiation. During a median follow-up period of 10 months [interquartile range (IQR) 4–20 months], 31% patients had experienced an initial significant weight loss after HAART initiation. In addition to time-varying CD4 cell count and hemoglobin level, age, sex, baseline BMI and having loss of appetite, and nausea/vomiting at baseline were associated with the risk of long-term significant weight loss.
Conclusion: Our study suggested that a significant percentage of patients continue to lose weight after HAART initiation. Our findings on the effect of socio-demographics, symptoms and diseases, biomedical indicators in relation to weight loss provide important information that has significant practical implications.
Prior to the introduction of HAART, weight loss and/or wasting were among the most frequently occurring AIDS-defining conditions [1,2]. They were also strong predictors of morbidity and mortality in HIV-infected adults . The cause of HIV-related weight loss is multifactorial, and contributing factors include gastrointestinal malabsorption, decreased caloric intake and hypermetabolism.
Gastrointestinal malabsorption, often marked by diarrhea, has been suggested as a major cause of HIV-related weight loss. It is not uncommon for HIV-infected patients to have abnormal D-xylose and C-glycerol-tripalmitin absorption tests [3,4] and one study has shown that malabsorption of D-xylose was associated with BMI in HIV-infected adults . Another study conducted in the US also suggested a relationship between diarrhea and weight loss . Nutrition for Healthy Living (NFHL) was a longitudinal study of HIV-infected adults in the greater Boston area from 1995 until 2005. Their finding suggested that malabsorption may still play a role in weight loss in the era of HAART . The effect of malabsorption on weight loss may depend not only on the severity and duration of malabsorption, but also on caloric intake. Decreased caloric intake appears to be very common among HIV-infected patents and is another cause of weight loss . Many conditions can cause decreased caloric intake, including central nervous system (CNS) infection, neurologic/psychiatric dysfunction, pharyngeal/esophageal disease and anorexia [9–12]. One study found that oral symptoms and difficulty swallowing were associated with weight loss in HIV-infected patients . Several studies have suggested that HIV-infected patients may have increased metabolism, even without an acute infection or neoplasm [14,15]; however, another study was unable to confirm these results . Thus it remains unclear what is the cause of chronic hypermetabolism in HIV-infected patients. Whether or not chronic hypermetabolism occurs, fever and infections associated with HIV disease may result in increased resting energy expenditure (REE) in HIV-infected patients .
Access to HAART for HIV-infected patients has expanded substantially throughout sub-Saharan Africa since 2003 . Following widespread use of HAART, HIV infection has become a chronic, manageable disease. Some studies suggested the incidence of HIV-related weight loss has declined in the HAART era [19,20]. However, other studies demonstrated that HAART does not eliminate weight loss  and may actually increase the 6-month risk of at least 5% weight loss . Despite the benefits of HAART in patients with HIV, weight loss remains an independent predictor of HIV disease progress and death. A study found that as little as 3–5% weight loss was associated with a significant increase in mortality among HIV-infected patients receiving HAART . Another study suggested that patients with weight loss at 3 months after HAART initiation had a higher risk of death during the first year of HAART . However, few studies have explored predictors of weight change after HAART initiation, and some of these studies were only focused on factors associated with weight gain . In addition, most of the studies published have been conducted in developed countries with small sample sizes [13,26]. To fill this gap, we studied predictors of weight loss after HAART initiation in a large cohort of HIV-infected adults living in Dar es Salaam, Tanzania.
Between November 2004 and December 2009, we enrolled 21 987 HIV-infected adults (>15 years) who initiated HAART and were followed up at least for 3 months in HIV Care and Treatment Clinics in Dar es Salaam, Tanzania. These clinics were supported by the US President's Emergency Plan for AIDS Relief (PEPFAR). Patients were initiated on HAART if they met World Health Organization (WHO) stage 4 criteria, WHO stage 3 criteria and had a CD4 T-cell count less than 350 cells/μl, or had a CD4 T-cell count less than 200 cells/μl. We excluded patients who were previously exposed to HAART (n = 1652), pregnant women (n = 1356), and patients without data on BMI or weight (n = 23) at the time of HAART initiation. After these exclusions, our final sample size was 18 956.
After enrollment and HAART initiation, patients visited clinics monthly and were examined by physicians. Anthropometric measures including height, weight, and middle upper circumference (MUAC) were obtained by nurses using standardized techniques . During each visit, the physician and nurse collect demographic, clinical and therapeutic information. Blood samples were collected and immunologic, biochemical, and nutritional tests were performed. A chest X-ray and sputum test for tuberculosis (TB) were performed at initiation for all patients and at any follow-up for patients presenting with symptoms suggestive of TB.
Weight loss greater than or equal to 5% from the weight recorded at HAART initiation was defined as significant weight loss. A BMI less than 18.5 kg/m2 was categorized as underweight, between 18.5 and less than 25.0 kg/m2 was normal weight, between 25.0 and less than 30.0 kg/m2 was overweight, and at least 30.0 kg/m2 was obese. Possible predictors of weight loss at HAART initiation include age (<30, 30–39, 40–49, >50 years), sex, CD4 cell count (<50, 50–99, 100–199, >200 cells/μl), hemoglobin level (<7.0, 7.0–9.9, 10.0–11.9, >12.0 g/dl), WHO HIV stage (I–IV), district of Dar es Salaam [as a proxy for socioeconomic status (SES)], calendar year, and HAART regimen at initiation. People living in the three districts of Dar es Salaam were categorized as belonging to high (Kinondoni), medium (Ilala) and low (Temeke) SES areas .
The primary outcome in our analysis was significant weight loss. Log-binomial regression was used to examine the relative risk of significant weight loss at 3 months after HAART initiation. Cox proportional hazard models were applied to evaluate the association between baseline characteristics, time-varying covariates and time to first significant weight loss. Multivariate models were fit, including all variables that were associated at the level of P less than 0.20 in the bivariate analysis and forcing in age, sex, calendar year and antiretroviral regimen at initiation. Trend tests were performed in which median values of different category were treated as a continuous independent variable in models. A missing indicator was created when there was missing value. Interaction effects between BMI at HAART initiation and other covariates related to the risk of significant weight loss were assessed using a likelihood ratio test. Stratified analysis were conducted to examine the association between baseline characteristics and risk of significant weight loss across different levels of baseline BMI (<18.5.0, 18.5–25.0, and ≥25.0 kg/m2). All statistical tests were two-sided, with P less than 0.05 considered significant, and all statistical analyses were carried out using the statistical software package SAS, Release 9.2 (Cary, North Carolina, USA).
Table 1 presents the characteristics of 18 965 patients at HAART initiation. The median age of the cohort was 36 years [interquartile range (IQR) 31–43] and 67% were women. The proportion of underweight, normal-weight and overweight/obese at HAART initiation were 28, 57 and 15%, respectively. The median weight at initiation was 52 kg (IQR 46–60). Fifty-five percent of patients had CD4 cell count below 200 cells/μl, 5% had hemoglobin below 7.0 g/dl and 85% of patients met WHO HIV stage III or IV criteria.
The median weight change at 3 months following HAART initiation was 2.5 kg (IQR 0.2–5.0). However, 21% of the cohort lost weight at 3 months, and 8% lost greater than or equal to 5% of their baseline weight. Among those who were underweight at initiation, the median weight change was 4.0 kg (IQR 1.0–7.0), which was significantly higher (P < 0.01) than the weight change among normal-weight patients (median 2.0 kg, IQR 0 to 4.5) and among overweight/obese patients (median 2.0 kg, IQR −0.3 to 4.1). Figure 1 suggests that at 3 months underweight patients had a better response to HAART than the normal weight, overweight and obese groups. About 46% of underweight patients gained more than 10% of their baseline weight, whereas this proportion was only 19 and 8% among normal-weight and overweight/obese patients.
Figure 2 presents weight change after HAART initiation stratified by BMI at initiation and suggested that compared with other BMI groups, underweight patients gained more weight consistently during the whole follow-up period. Patients’ body weight increased rapidly in the first 12 months then plateaued or decreased. At 12 months after HAART initiation, weight gain was 10, 6 and 3 kg for patients who were underweight, normal weight and overweight/obese at initiation. Figure 3 presents absolute weight level after HAART initiation. It suggested that underweight patients did not catch up with other BMI groups in term of weight. Although they gained more weight after HAART initiation, it was only a small proportion compared with the difference in weight among BMI groups at initiation.
Table 2 presents the results for predictors of significant (≥5%) weight loss at 3 months after HAART initiation. Multivariate result suggested there was a U-shaped association between age and risk of significant weight loss at 3 months after HAART initiation: middle-aged patients (30–49 years old) had lower risk than people under age 30 and people above 49 (P = 0.03, not shown in the table). After adjusting for other risk factors, patients who enrolled in clinics in district with lower SES were more likely to have significant weight loss at 3 months. BMI at initiation was positively associated with the risk of significant weight loss. Compared with patients with normal BMI at initiation, patients who were underweight had 25% decrease in the risk of significant weight loss, whereas patients who were obese had 25% increase in this risk. Higher hemoglobin level at initiation was associated with lower risk of significant weight loss after 3 months. Patients having difficulty breathing, loss of appetite and nausea/vomiting had a higher risk of significant weight loss at 3 months. All interactions between baseline BMI and other possible predictors of significant weight loss were examined. Only the interaction between BMI and hemoglobin at HAART initiation was significant (P < 0.01). Stratified analysis showed that hemoglobin at HAART initiation was inversely associated with the risk of significant weight loss at 3 months across all BMI strata except those who were underweight (BMI <18.5 kg/m2).
During a median follow-up period of 10 months (IQR 4–20 months), a total of 5889 patients (31%) experienced an initial significant weight loss after HAART initiation. Table 3 presents results from Cox models. In multivariate analyses, age, sex, district, BMI, loss of appetite, nausea/vomiting were independently associated with the risk of significant weight loss. Older age was associated with the higher risk of long-term significant weight loss. Compared with men, women had lower risk of significant weight loss after HAART initiation. Time-varying covariates including CD4 cell count and hemoglobin level were inversely associated with the risk of long-term significant weight loss. Figure 4 presents trajectory of weight by CD4 cell count. It suggested that weight increased rapidly with the increase of CD4 cell count then slowed down after CD4 cell count reached 400 cells/μl. Figure 5 shows a positive association between patients’ weight and hemoglobin level after HAART initiation. No interaction effect was found between BMI and other covariates on the risk of long-term significant weight loss.
In this large cohort of HIV-infected adults living in Tanzania, the median body weight increased at 3 months after HAART initiation, and continued to increase until 12 months. Patients who were underweight at initiation had a better response to the treatment at 3 months and gained more weight than other BMI groups during the follow-up period. Our findings are consistent with other studies conducted in resource-limited settings [29–31]. A study conducted in Botswana  found that the median weight among HIV-infected adults increased by 2.2 kg (IQR 1.0–3.3) at 3 months, and consistently increased until 12 months after initiation when the study was ended. In Haiti, researchers found that HIV-infected adults and adolescents gained a median of 4.0 kg (IQR 0.9–7.7) by 6 months, and 5.5 kg (IQR 1.4–10.5) by 12 months after HAART initiation . Two studies also found that patients with lower baseline BMI gained more weight at 6 months after HAART initiation [25,32].
We found that baseline symptoms including loss of appetite, nausea/vomiting, and difficulty breathing were important independent predictors of weight loss at 3 months after HAART initiation. Other studies have reported similar findings [9,33]. The oral manifestation is one of the earliest and most important indicators of HIV infection. The presence of oral manifestations can limit patients’ ability to chew and swallow food comfortably, which leads to loss of appetite. Oral manifestation may also have a psychological negative impact on patients’ self-image which could also cause loss of appetite. HIV medications may compound the problem through side effects. Nausea and vomiting have been reported as one of the most frequent symptoms in HIV-infected patients and major causes include gastroparesis and drug-induced infectious and psychological conditions .
We also examined the association between socio-demographic characteristics and weight change at 3 months after HAART initiation. Middle-aged patients were less likely to have significant weight loss after HAART initiation, compared with patients younger than 30 and older than 50 years. This may be because they have more favorable socioeconomic conditions compared with younger groups  and more favorable CD4 cell restoration on HAART compared with older groups . Better antiretroviral adherence among middle-aged patients could be another possible explanation here. In our study, patients who enrolled from the district with highest SES were less likely to have significant weight loss. This finding is consistent with a previous study which found that SES was inversely related to wasting among HIV-infected women . Patients with higher SES may have better access to nutrient-rich diets, or they were better educated so they had better hygiene practices.
Our study found that hemoglobin at HAART initiation was inversely associated with the risk of significant weight loss at 3 months across all BMI strata except those who were underweight (BMI <18.5 kg/m2). It is possible that high baseline BMI implies the absence of other severe symptoms or disease, makes the effect of anemia on weight loss more pronounced. Several previous studies found that anemia is an independent predictor of wasting and mortality in HIV patients [33,37]. In resource-limited settings, anemia is also associated with tuberculosis, malnutrition, gastrointestinal Kaposi's sarcoma, narrow suppression and other conditions with clinical implications [38,39].
When we looked at long-term weight loss, being female was associated with a lower risk of long-term weight loss after HAART initiation. The study from CASCADE Cohort showed that before widespread introduction of HAART in 1997, there was no sex difference in the risk of progression to AIDS or mortality among HIV-infected patients, whereas from 1997 onward, women had slower progression and lower mortality than men, despite a similar time on HAART . It is difficult to know whether these advantages observed in women have a biological basis, but findings from CASCADE Cohort suggested that there is a stronger impact of HAART among HIV-infected women than men. Another study conducted in Tanzania found that men had a significantly higher risk of overall mortality and loss to follow-up after at least 6 months of initiating ART than that in women . Previous study also suggested that lipoatrophy pattern was more predominant in male patients and lipoaccumulation forms in female patients .
We also found that CD4 cell count is an independent predictor of long-term significant weight loss. A study conducted in Zimbabwe also found that CD4 cell count was an independent predictor of at least 10% weight loss among HIV-positive women . They suggested that the association between CD4 cell count and weight loss is most likely mediated by the characteristics of advanced HIV infection such as higher risk of opportunistic infections, malabsorption, and abnormal metabolism, which all contribute to weight loss. Our finding also suggested that the association between CD4 cell count and body weight decreased when CD4 cell count was greater than 350 cells/μl.
One strength of our study lies in the large, diverse patient population which was collected in a developing country. Anthropometric measures were obtained by health professionals minimizing errors. Patients who were included in this study were all HAART-naive, avoiding confounding from previous exposure. However, our findings also have some limitations. We considered potential confounders from every domain available in our data, but there was no information on viral load, food availability, and nutrient intake. In addition to missing information mentioned above, we did not include data on individual SES such as income, education that may have influenced patients’ nutrition status.
This study has documented patients’ weight change and explored the baseline and time-varying factors that are associated with short-term and long-term significant weight loss after HAART initiation. In summary, although body weight increased steadily after HAART initiation, there were still about 10% of patients who lost at least 5% body weight at 3 months after initiation. Therefore, even in HAART era, physicians still need to remain vigilant about patients’ weight. Our findings on the effect of socio-demographics, baseline symptoms and diseases, time-varying biomedical indicators in relation to short-term and long-term significant weight loss provide important information that has significant practical implications. Nutrition counseling for higher caloric intake should be included in the care and treatment for patients after HAART initiation. Future studies should be conducted to explore reasons for more weight loss in men than that in women after HAART initiation.
We are grateful to the HIV patients who participated in this study and acknowledge the efforts of field team including physicians, nurses, data clerks, laboratory and administrative staffs in Tanzania. We also thank the Muhimbili University of Health and Allied Sciences (MUHAS) and Dar es Salaam City Council for their institutional support.
Author contributions: N.L.: data analysis, writing, literature search; D.S.: data analysis, editing; P.D.: editing, literature search; R.S.M.: editing; F.M.: editing; G.C.: data collection, editing; W.W.F.: data analysis, editing.
This study is supported by US President's Emergency Plan for AIDS Relief (PEPFAR).
Conflicts of interest
There are no conflicts of interest.
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