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Obesity in HIV-Infection: Dietary Correlates

Department of Community Health and Family Medicine, Tufts University School of Medicine (K.M.H., C.Y.J.)
Friedman School of Nutrition Science and Policy (K.M.H., R.F.H.)
Tufts University, Frances Stem Nutrition Center, New England Medical Center (K.M.H., K.D.W.), Boston, Massachusetts

Address reprint requests to: Kristy Hendricks, DSc, RD, Department of Community Health and Family Medicine, Tufts University School of Medicine, 150 Harrison Avenue, Jaharis 262, Boston MA 02111. E-mail: Kristy.Hendricks{at}tufts.edu

	ABSTRACT

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
Objective: To describe the prevalence of obesity among a cohort of individuals living with HIV infection, and to determine differences in dietary intake among those subjects who are normal weight, overweight, and obese.

Design: A cross-sectional study among participants enrolled in the Nutrition for Healthy Living (NFHL) study.

Setting: Eligible participants included HIV-positive adults living in the greater Boston, MA and Providence, RI, areas.

Subjects and Measures of Outcome: In total, 321 (265 males, 56 females) subjects were studied. Body composition measurements, demographic and health data, and fasting blood samples were analyzed. Dietary intake was assessed by three-day food records. Statistical analyses were performed using Statistical Package for Social Science (SPSS).

Results: 13% of males and 29% females were found to be obese. Energy intake per kilogram decreased by body mass index (BMI) category for both men and women (p <0.05). Although not different between groups, mean total fat and saturated fat intakes were above recommendations for both men and women in all BMI categories, while total grams dietary fiber decreased as BMI increased. Individuals in all BMI groups had micronutrient intakes below the Dietary Reference Intakes. Serum markers of insulin resistance were significantly different by BMI category among men and women, as well as triglycerides and total cholesterol for the males.

Conclusions: Obesity and diet in individuals living with HIV-infection needs to be addressed, as quality of dietary intake may have future implications regarding cardiovascular disease, metabolic syndrome, and other health risks associated with overweight and obesity.

Key words: HIV, nutrition, overweight, obesity, insulin resistance, dietary intake

	INTRODUCTION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
The study of nutritional status in individuals infected with human immunodeficiency virus (HIV) focused initially on HIV-associated wasting. This research found that even mild and moderate weight loss is predictive of decreased survival and development of opportunistic infections [1,2]. Shor-Posner [3] found that body mass index (BMI) is inversely associated with progression to death independent of CD₄ count among HIV-positive drug users.

Due to the advent of antiretroviral drug therapy (ART) and subsequent improved life expectancy, HIV has become a chronic disease. Long-term complications related to diet, overweight, and obesity have gained a new importance. Among the Nutrition For Healthy Living (NFHL) cohort in 1998, 27% of women were overweight and 21% were obese while 33% of men were overweight and 6% were obese [4]. Hodgson found a high prevalence of obesity among HIV patients, with 34% overweight and 9% being obese [5]. More recently, in a large cohort (n = 1669) of individuals living with HIV infection Amorosa et al. reported obesity and overweight to be more prevalent than wasting [6]. The prevalence of overweight was 30% vs 31% for men and women respectively. These investigators found a positive correlation between BMI and total cholesterol, triglycerides, and glucose. Nutritional problems such as lipodystrophy, hyperlipidemia, and insulin resistance have increased in those living with HIV [7]. Shevitz et al concluded that with the improved prognosis for HIV-infected patients, nutritional complications are playing a primary role in the lives of such patients and attention should be paid to dietary factors [4].

To date, there are few studies looking at dietary intake and obesity within HIV-infected populations. Batterham et al showed that dietary fat and total energy intake was high in their HIV-positive population compared to recommendations, yet results failed to show any relationship between fat or total energy intake and fasting lipids, glucose, insulin, or insulin-resistance ratio [8].

The purpose of this study was to describe the prevalence of obesity among an HIV-infected population, and to determine differences in dietary intake among those subjects who are normal weight, overweight, and obese. This study also investigated differences in insulin resistance within normal, overweight, and obese individuals living with HIV, and ascertained any dietary correlates.

	MATERIALS AND METHODS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
We conducted a cross-sectional study among participants enrolled in the Nutrition for Healthy Living (NFHL) study, a longitudinal study begun in 1995, studying the nutritional and metabolic consequences of HIV infection. The details of the NFHL study have been published elsewhere [9]. In brief, eligible participants included HIV-positive adults living in the greater Boston, MA and Providence, RI, areas. Potential participants were excluded for the following factors at the time of enrollment: pregnancy, thyroid disease, or malignancies other than Kaposi’s sarcoma. Semiannual visits consisted of anthropometric and other body composition measurements, 3-day food record, a comprehensive questionnaire on sociodemographic characteristics, quality of life, clinical status, use of recreational drugs, and use of HIV-related medications. Immunological, biochemical, and nutritional testing was conducted on fasting blood samples collected and stored at each visit. The data analyzed were from the most recent visit of the participants actively enrolled in the cohort between 09/21/2000 and 10/27/2003 (n = 458). After excluding individuals who were diabetic, had glucose greater than 126, had not completed a 3 day food record or who had a BMI <20, the final dataset was 321 subjects [10].

Participants were instructed on how to keep a 3-day food record, including one weekend day. To document portion sizes, participants were provided with a food scale (Sunbeam Corporation, Mississauga, Canada) and a ruler. Prior to each 6-month follow-up visit, participants were mailed a 3-day food record one week before the appointment. Analysis of food records was done by the use of Nutrition Data System (NDS) software (versions 4.02, 4.04, 4.06; Nutrition Coordinating Center, University of Minnesota, Minneapolis, MN; 24).

Measures of insulin resistance were estimated by the homeostasis model assessment (HOMA) and the Quantitative Insulin Sensitivity Check Index (QUICKI) [11,12]. [HOMA = fasting insulin (µU/ml) x fasting glucose (mmol/l)/22.5]. QUICKI has been found to be a valid and reliable index of insulin sensitivity obtained from a fasting blood sample that may be useful in research. [QUICKI = 1/[log glucose (mg/dl) + log insulin (µU/ml)] [12]. Indirect calorimetry was measured by oxygen and carbon dioxide exchange using a VMax Series 29n calorimeter (Sensor Medics Corporation, Yorba Linda, CA). Subjects were studied recumbent in a quiet, dimly lit room. REE was calculated from oxygen and carbon dioxide exchange rates using the Weir Equation [13].

Triceps, subscapular and supra-iliac skin fold thickness and measurements of upper arm, waist, and hip circumference were obtained following the standardized methods of Lohman et al [14]. BMI was calculated as weight in kilograms (kg) divided by height² in meters. Waist circumference was measured with the subject standing erect with the abdomen relaxed, using an inelastic tape at the level of the natural waist. The measurement was taken at the end of a normal expiration, directly on the skin but not compressing the skin and recorded to the nearest 0.1 cm. Fat mass and fat-free mass were determined by bioelectrical impedance (BIA) resistance and reactance (BIA-101A, RJL Systems, Clinton Twp., MI, USA). Transverse whole body dual-energy X-ray absorptiometry (DEXA) scans were obtained using QDR 2000 scanner (Hologic) in the array mode as previously described [15].

Statistical analyses were performed using SPSS (Statistical Package for Social Science, SPSS, Inc, Chicago, Illinois) version 11.0.1. Analysis was stratified by gender and by BMI cataogy as follows: Group 1: BMI 20–24.9 (normal weight), Group 2: BMI = 25–29.9 (overweight), or Group 3: BMI >30 (obese). BMI cutoffs for overweight and obese were taken from the National Heart, Lung and Blood Institute (NHLBI) guidelines [17]. Statistical significance was determined by one way ANOVA with post hoc analysis performed using the Bonferroni method. Skewed distributions of micronutrients and HOMA were transformed by natural logs and significance was then determined by Bonferroni. The small number of females (n = 56) impacted the power of the statistical testing and therefore statistical testing could not be performed with accuracy for some variables.

	RESULTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
Table 1 presents demographic characteristics and body composition by BMI category. Of the men in our study, 47.9% were of normal weight, 39.6% were overweight, and 12.5 % were obese. The women were distributed as follows: 37.5% normal weight, 33.9% overweight, and 28.6% obese. Demographics and other characteristics such as smoking status, drug use, antiretroviral drug therapy, mode of transmission, education level, and physical activity were expressed as percentages within BMI group. Overall, the population was a relatively healthy outpatient cohort with few reported opportunistic infections, well preserved CD₄ counts and mean viral load (VL) <2000 (many in the undetectable range <400). Among the men, shorter duration of known HIV seropositive, trying to lose weight, and non-white race were associated with higher BMI (p <0.05). When normal and overweight individuals were combined, these men were significantly more likely to strength train (p <0.05) than obese men. Women in the obese BMI category were more likely to be non-white (p <0.01).

We used self-report of strength training to assess physical activity. Of the eighty-three men who did strength training, forty-five (53%) were of normal weight, thirty-three (40%) were overweight, and only 5 (6%) were obese. The mean number of strength training sessions per week for males in each BMI Group is 3.6 times for normal weight, 3.3 times for overweight, and 2.8 for obese. Among the females, only 5 participated in strength training, with three individuals (60%) of normal weight. Two individuals, comprising 40% of those participating in strength training were from the overweight group. No females in the obese category participated in strength training. Mean quantity of strength training sessions per week in the normal weight category was 3.7, and for the overweight group, 1.5 sessions per week.

Dietary intake, including macronutrients and micronutrients, is compared between the BMI categories in Tables 2 and 3. Macronutrients were reported as mean intake, with the exception of the grams of dietary fiber per 1000 kilocalories (kcals), which was reported as median intake and interquartile ranges (25^th, 75^th percentile). All micronutrients were reported as median and interquartile ranges (IQR), with percentage below dietary reference intakes (DRI) stated.

Table 4 shows the difference in mean lab values between the BMI groups, and percent abnormal for QUICKI, HOMA, triglycerides, and blood lipids (total cholesterol, LDL, HDL). Among males, statistically significant differences with insulin, QUICKI, and HOMA were found between normal weight and overweight groups, and normal weight and obese. Blood pressure was significantly different between normal weight and overweight groups for systolic and between normal weight and obese for diastolic. Triglycerides and total cholesterol were significantly different between normal weight and obese groups. There was a significant difference in QUICKI, HOMA and bilirubin between normal weight and obese women. Statistical significance was not performed on percents abnormal, but the data is shown for reader interest.

	DISCUSSION

 
There is a growing problem of overweight and obesity in HIV infected populations, potentially leading to disease risk factors of hyperlipidemia and insulin resistance. This study reports the rising prevalence of overweight and obesity among an HIV-infected cohort. Since 1998, the prevalence of overweight among NFHL subjects has risen from 33% to 40% percent in men and from 27% to 34% percent in women [4]. During that same time period, the prevalence of obesity has risen from six to thirteen percent in men and from 21% to 29% in women [4]. Obesity among HIV-infected populations may be reflecting current trends among the general population. The Centers for Disease Control and Prevention (CDC) has called obesity the fastest growing health threat in the US [18]. Obesity is strongly associated with several major health risk factors and it has been well documented that obesity among the general population is associated with health complications such as cardiovascular disease, diabetes, some cancers, and increased mortality [19–22]. In one study using data from the Behavioral Risk Factor Surveillance System, Mokdad et al reported that obesity rates in American adults rose from 19.8 to 20.9% between 2000 and 2001, and that diagnosed diabetes in the general population rose from 7.3% to 7.9% during the same time period [19]. 1999–2000 NHANES data indicate that an estimated 65 % of US adults are overweight or obese, with 31% obese [20,21]. Common consensus attributes this rise in obesity to an increase in dietary intake and decrease in physical activity [22,23]. Further studies will be required to determine whether weight reduction strategies recommended for the general population also apply to those infected with HIV [24].

Overall, dietary intakes were not significantly different between individuals based on normal, overweight, or obese BMI classification. The general public is recommended to consume less than approximately 30% of their total calories from fat, and no more than 10% of their calories from saturated fat [25–28]. Looking at trends in dietary intake from our study, the means for both males and females in our study are greater than the recommended percent of total kcal from fat and saturated fat. A high percentage of participants in all BMI groups consume an excessive percentage of calories from fat and saturated fat. This may have implications for risk of cardiovascular disease and health risks associated with overweight and obesity in HIV patients [27,29]. Omega-3 intake was lower as the BMI category increased among women and approached significance between normal weight and obese groups (p-value = 0.050). This suggests differences in the quality of dietary fat and could influence the effect on coronary heart disease [28].

It is also important to note that intake of fiber was consistently lower as BMI category increased among the females, with over 90% of obese women not meeting the recommendation for fiber intake. Along with the large proportion of women not meeting the recommended intake of 20g (67%, 84%, and 94%, respectively, for each BMI group), at least half the men in each BMI group consumed less fiber than recommended. This suggests a lack of dietary quality, as whole grains, fruits and vegetables, nuts and seeds are major sources of fiber. These could in turn have future implications regarding diet and disease risk [29]. It has been shown that higher intakes of whole grains are associated with increased insulin sensitivity [30]. Hadigan et al identified an association between fiber and insulin resistance among HIV infected patients, indicating a possible role for dietary modifications [31]. Insulin resistance is associated with an increased risk of glucose intolerance and diabetes mellitus among the general population. Additionally, markers of insulin resistance and lipid values were significantly different by BMI category.

In addition to diet, other lifestyle factors such as physical activity impact body composition. Our questionnaire is not designed to assess usual physical activity, although it does record self-reported strength training. It was found that individuals in the higher BMI category were less likely to participate in strength training.

The higher BMI groups were more likely to have tried to lose weight. The higher the BMI, the more likely that participants are non-white (94% of obese women were non white). Racial and ethnic differences, particularly in women, in disease prevalence and health outcomes in obesity, diabetes, and cardiovascular disease need to be addressed [32–33]. This may be important in targeting nutritional interventions to overweight or obese HIV-infected individuals.

Energy/kg was consistently lower as BMI category increased for both men and women, and total energy was lower as BMI increased in women. We had expected total energy intake to be higher as BMI increased. Instead, our results show that although women in our study who are obese have higher REE, their self-reported energy intake was lower. REE per kg FFM was not different between BMI groups thus increased REE was most likely secondary to increasing lean body mass. It has been well documented that overweight and obese women may underreport dietary intake [34–40]. Findings from the third NHANES estimated 18% of men and 28% of women to be under-reporters, rates were highest in women, older individuals, and those trying to lose weight (37). In a Belgian population, Zhang et al used biomarkers to classify under and over reporters and found underreporting of energy intake which increased with increasing BMI (39). Heerstrass used biomarkers to estimate the magnitude of underreporting based on BMI tertile and found underreporting of approximately 20–25% over the observed BMI range (40). It was not the purpose of this study to assess underreporting in the NFHL Cohort. However, in women with BMI >30, reported mean energy intake was almost 100 calories less than measured REE. Thus, under-reporting could explain our unexpected results in the women’s total energy intake although other unidentified mechanism cannot be excluded. A decrease in kcal/kg was seen in both men and women as BMI increased. This may be accurate because, as noted, REE is primarily dependent on LBM and if increases in BMI are also a result of increasing body fat, kcal/kg needs would decrease overall when expressed per kilogram of body weight in obesity.

Although Table 4 shows no significant difference of mean intake of micronutrients by BMI category, intake may be skewed due to use of supplements in this specific study population. Those with higher BMI had a larger percentage of subjects falling below DRI for vitamin E, folate, vitamin B12, calcium, iron, and zinc. Deficiency of such micronutrients may also play a role in the development of chronic disease. In particular, females in the obese category were more likely to be lacking in vitamin E than women in the normal or overweight groups. (Sixty-nine % below the DRI in the obese group, as opposed to forty-eight and forty-seven % in normal weight and overweight categories, respectively.)

Percent of participants with insulin resistance were higher as BMI category increased. This has been shown in other investigations, although not specifically individuals living with HIV. Insulin, blood pressure, triglycerides, and total cholesterol for the men, as well as bilirubin for the women were also significantly different by BMI group. Although it is not yet known whether lipid abnormalities occurring during HAART treatment signify an increased risk for cardiovascular disease, it is possible that chronic presence of these risk factors will lead to disease during long-term management of HIV-infected patients [27]. The relationship between obesity, insulin resistance, metabolic syndrome and type 2 diabetes is long-recognized in the general population [41]. With the rise of obesity in HIV infected populations, the prevalence of the metabolic syndrome may be expected to increase, and clinical management of such conditions in HIV-infected individuals may become imperative. In the general population, wide evidence supports the benefits of maintaining normal plasma lipoprotein levels, body weight, and blood pressure for reducing risk of cardiovascular disease [24,26]. Management of dyslipidemia in the general population has formed the basis for recommendations to patients infected with HIV and receiving antiretroviral therapy [27]. Diet will likely have an important role to play in modifying these risk factors in individuals living with HIV-infection.

Limitations of this study include the small number of females (n = 56), which impacted the power of the statistical testing. Consequently, statistical testing could not be performed with accuracy for some variables. Despite the relatively small number of women in our study, this study provides some insight as research on obesity and dietary intake is particularly lacking in HIV-infected women. Additional investigations will be necessary for HIV-infected women.

An additional limitation is if total intake is underreported in the obese group, it is likely that the intakes of micronutrients would be underestimated as well. Therefore, percentage of obese women who are nutrient deficient may be overestimated in our sample. Although there are criticisms in accuracy for all forms of dietary assessment [42], we do not view 3-day food records as a limitation in our study. Food records are often regarded as the "gold standard" when assessing dietary intake [43] and food records were found to be superior to food frequency questionnaires using biomarkers in this cohort [44].

	CONCLUSION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
We are now called to address issues of overweight, obesity, and nutritional implications in individuals living with HIV. As obesity is growing into a common problem among people infected with HIV, this study suggests the need for physicians and nutritionists be consistent with current recommendations for dietary intake of total fat, saturated fat, and fiber. Obesity in this population needs to be addressed, as quality of dietary intake may have future implications regarding cardiovascular disease, metabolic syndrome, and other risks associated with overweight and obesity. Further study in this population would be valuable to establish advantages of nutrition intervention and lifestyle changes to achieve metabolic benefits. Also, as weight loss is a documented predictor of decreased survival, the role of intentional weight loss in overweight and obese HIV infected individuals needs careful study [2]. It is important for health professionals to address dietary implications of this population, as rising trends in obesity in HIV-infected patients may mirror the trend of the general population.

	FOOTNOTES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 
This work was supported by: NIDDK grant #1P01DK45734-06, NIH Supplemental Grant #2P01-DK-45734-06, General Clinical Research Center #M01-RR00054

Received November 14, 2005. Accepted April 12, 2006.

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TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION REFERENCES

 

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