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Clinical Studies |
Neuroendocrine (S.G., C.C., B.M.K.B., E.W., A.K.) Infectious Disease (N.B., H.M.H.) Departments and the General Clinical Research Center (J.H., E.J.A), Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114
Address all correspondence and requests for reprints to: Steven Grinspoon, M.D., Neuroendocrine Unit, Bulfinch 457B, Massachusetts General Hospital, Boston, Massachusetts 02114.
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Abstract |
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Three groups of women were studied to determine body composition and hormonal changes with respect to stage of wasting [nonwasting (NW; weight >90% ideal body weight; weight loss <10% of preillness maximum; n = 12), early wasting (EW; weight >90% ideal body weight; weight loss >10% of preillness maximum; n = 10), and late wasting (LW; weight <90%; n = 9)] and compared with a control group of 12, healthy, age-matched women. Weight loss averaged 6 ± 6% (NW), 15 ± 6% (EW), and 20 ± 8% (LW) in the three groups. Lean, fat, and muscle masses were determined by dual energy x-ray absorptiometry and urinary creatinine excretion.
Subjects were 36 ± 5 yr of age (mean ± SD) with a CD4 cell count of 379 ± 239 cells/mm3. The body mass index was 24.4 ± 2.6 kg/m2 (NW), 22.2 ± 1.2 kg/m2 (EW), 18.2 ± 2.0 kg/m2 (LW), and 24.3 ± 2.6 kg/m2 (controls; P < 0.01, NW vs. EW; P < 0.0001, NW vs. LW). Lean body mass indexed for height was 15.7 ± 2.4 kg/m2 (NW), 14.8 ± 2.0 kg/m2 (EW), and 13.7 ± 1.2 kg/m2 (LW) and was decreased significantly only in the LW group (P < 0.05 vs. NW). Muscle mass was 96% (NW), 94% (EW), and 78% (LW) of that predicted for height (P < 0.05, NW vs. LW). In contrast, fat mass indexed for height was decreased significantly among patients in both the EW and LW groups [8.7 ± 1.9 kg/m2 (NW), 6.5 ± 1.9 kg/m2 (EW), and 3.7 ± 1.4 kg/m2 (LW); P < 0.05, NW vs. EW; P < 0.001, NW vs. LW). Expressed as a percentage of the value in nonwasting HIV-positive controls (NW), the relative loss of fat was greater than the loss of lean mass with progressive degrees of wasting [EW, 25% vs. 6% (fat vs. lean); LW, 58% vs. 13%].
The prevalence of amenorrhea was 20% among study subjects [17% (NW), 10% (EW), and 38% (LW)]. The percent predicted muscle mass was significantly lower in subjects with amenorrhea (74 ± 8%) compared to that in eumenorrheic HIV-positive subjects (94 ± 4%; P < 0.05). Estradiol levels were lower among subjects with amenorrhea (17.6 ± 21.8 pg/mL) compared to eumenorrheic HIV-positive (48.9 ± 33.6 pg/mL) and control (68.3 ± 47.6 pg/mL) subjects and did not correlate with body composition. Mean free testosterone, but not total testosterone, levels were decreased in subjects with EW and LW compared to those in age-matched healthy controls, but not compared with those in NW [0.9 ± 0.6 ng/dL (NW), 0.7 ± 0.4 ng/dL (EW), 0.6 ± 0.3 ng/dL (LW), and 2.0 ± 2.4 ng/dL (controls); P < 0.05, EW vs. controls and LW vs. controls] and correlated with muscle mass (r = 0.37; P < 0.05). The percentages of women with free testosterone levels below the age-adjusted normal range were 33% (NW), 50% (EW), and 66% (LW). Dehydroepiandrosterone sulfate levels were also low in the subjects with LW compared to those in the control group [98 ± 85 µg/dL (NW), 102 ± 53 µg/dL (EW), 55 ± 46 µg/dL (LW), and 132 ± 68 µg/dL (controls); P < 0.05 LW vs. controls] and were correlated highly with free testosterone levels (r = 0.73; P < 0.00001) and also with muscle mass (r = 0.48; P < 0.01).
These data demonstrate that women lose significant lean body and muscle mass in the late stages of wasting. However, in contrast to men, women exhibit a progressive and disproportionate decrease in body fat relative to lean body mass at all stages of wasting, consistent with gender-specific effects in body composition in AIDS wasting. In addition, these data demonstrate that androgen deficiency is common in women with AIDS wasting and may contribute to decreased muscle mass in this population.
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In this study we compared lean, fat, and muscle masses in women with AIDS wasting, age-matched nonwasting HIV-positive women, and normal controls. Hormonal function was characterized by menstrual history, gonadal steroid, sex hormone-binding globulin (SHBG), gonadotropin, dehydroepiandrosterone sulfate (DHEAS), GH, and insulin-like growth factor I (IGF-I) levels. Our findings demonstrate that in contrast to men, women lose fat mass disproportionately to lean mass in the early and late stages of AIDS wasting. Androgen levels are decreased significantly in this population and correlate with decreased muscle mass. These findings demonstrate gender-specific changes in body composition and hormonal function unique to women with AIDS wasting.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Three groups of HIV-positive patients, 1) nonwasting [NW;
weight >90% ideal body weight (IBW); weight loss <10% of preillness
maximum; n = 12], 2) early wasting (EW; weight >90% IBW; weight
loss >10% of preillness maximum; n = 10), and 3) late wasting
(LW; weight <90% of IBW; n = 9), were investigated during a
3-day hospital admission and compared with 12 healthy, age-matched,
premenopausal controls. All of the women in EW and LW groups and 58%
of the women in the NW group had AIDS by the Centers for Disease
Control criteria. Percent IBW was determined from measured weight and
height (8). Weight loss averaged 6 ± 6% (NW), 15 ± 6%
(EW), and 19 ± 9% (LW). Subjects were 36 ± 5 yr of age and
had a mean CD4 count of 379 ± 239 cells/mm3 (Table 1
). Subjects had been free of acute opportunistic
infection for at least 6 weeks before admission. None of the subjects
had been taking Megace, estrogen, ketoconazole, glucocorticoid, or
anabolic agents within 3 months before admission. In addition, none of
the subjects began a new retroviral agent or protease inhibitor within
6 weeks of study initiation, but 75%, 50%, and 56%, respectively, of
the subjects in each group were receiving chronic antiretroviral
therapy. Subjects with severe diarrhea (>6 stools/day), hemoglobin
below 8 g/dL, or creatinine above 2 mg/dL were excluded. Subjects with
regular menses were studied in the early follicular phase. All subjects
gave written consent as approved by the Subcommittee on Human Studies
of the Massachusetts General Hospital.
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Body composition analysis. Fat and lean body mass were determined by dual x-ray absortiometry (DXA) using a Hologic-2000 densitometer (Hologic, Waltham, MA) and indexed for height by dividing by the square of the height in meters to permit a comparison between the groups. The DXA technique has a precision error of 3% for fat and 1.5% for lean body mass (9). Muscle mass was calculated by averaging urinary creatinine excretion over 3 days as an in-patient on a meat-free diet and multiplying by a constant of 18 kg muscle/g urinary creatinine. Expected muscle mass was determined from height (10, 11).
Hormonal assessment and immune function. Gonadal function was assessed by self-report of menstrual history (recall over 3 months) and serum total and free testosterone, estradiol, SHBG, gonadotropin, and DHEAS levels. Subjects who had not had a period within the last 3 months before admission were categorized as amenorrheic. One subject with a known prior history of chemotherapy and elevated FSH was precluded from the analysis. The GH axis was evaluated in three ways: 1) frequent sampling every 20 min from 2000–0800 h, 2) stimulation testing with arginine hydrochloride (0.5 g/kg, iv; maximum dose, 30 g), and 3) serum IGF-I levels. Immune function was determined by CD4 count.
Nutritional assessment. Before study entry, subjects were instructed on completion of a 4-day food record, which was analyzed for total calorie, protein, and carbohydrate contents (version 8A/2.6, Minnesota Nutrition Data Systems, Minneapolis, MN). Subjects were placed on an isocaloric, meat-free, but protein-substituted, diet for 3 days before and during the in-patient protocol. In addition, calorie and protein intakes were monitored on a daily basis and modified to match those reported in the out-patient food records. For each patient, body mass index (BMI) was calculated, serum albumin and prealbumin levels were measured, and resting energy expenditure (REE) was measured by indirect calorimetry with a metabolic cart (EMS/50 Enhanced Metabolic System, Life Energy Systems, Murray, UT) and compared to predicted basal energy expenditure using the Harris-Benedict equation (12). In addition, REE was divided by weight to determine energy expenditure per kg BW.
Normal controls. Data from the study subjects were compared with those obtained in healthy female controls admitted in the follicular phase for overnight DXA scanning, frequent GH sampling, analysis of gonadal steroid levels, and dietary history analyzed by Minnesota Nutrition Data Systems (version 6A/2.4).
Laboratory methods. Serum FSH, LH, and hematocrit were measured using methods previously described (13). Serum IGF-I was measured after an acid-alcohol extraction using a RIA kit with an intraassay coefficient of variation (CV) of 2.4–3.0% (Corning Nichols Institute, San Juan Capistrano, CA). GH was measured by a two-site radioimmunometric assay with an intraassay CV of 2.8–4.2% (Corning Nichols Institute). Serum total and free testosterone levels were measured by a RIA kit (Diagnostics Products Corp., Los Angeles, CA) with an intraassay CV of 5–12% for total testosterone and 3.2–4.3% for free testosterone. Prealbumin was measured by rate nephelometry (MetPath, Cambridge, MA). CD4 cell counts were measured by flow cytometry using FACS Lysing Solution and a FACScan analyzer (Becton Dickinson Immunocytochemistry Systems, San Jose, CA). Estradiol was measured by RIA kit (Diagnostic Systems Laboratories, Webster, TX) with an intraassay CV of 3.2–5.3%. SHBG was measured by a RIA kit (Diagnostics Systems Laboratories) with an intraassay CV of 2.2–3.0%. DHEAS was measured by a RIA kit with an intraassay CV of 6.3–9.4% (Diagnostic Systems Laboratories).
Statistical analysis. Measures of body composition and hormonal function were compared between groups by Student’s t test and analyzed in a linear regression model (JMP Statistical Discovery Software, SAS Institute, Cary, NC).
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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BMI decreased with successive stages of wasting (Fig. 1A). Lean body mass indexed for height was decreased
significantly only among LW subjects compared to normal controls and NW
HIV-positive subjects (Fig. 1B). Similarly, muscle mass was 96% (NW),
94% (EW), and 78% (LW) of the predicted value (P <
0.05, LW vs. NW) and correlated to free testosterone (r
= 0.37; P < 0.05) and DHEAS (r = 0.48;
P < 0.01) levels (see below). In contrast, fat mass
indexed for height was decreased significantly among subjects in the EW
and LW groups (Fig. 1C) compared to that in normal controls and NW
HIV-positive subjects. Expressed as a percentage of the NW control
value, the relative loss of fat was greater than that of lean mass with
progressive degrees of wasting [25% vs. 6% (fat
vs. lean) for subjects in the EW group and 58%
vs. 13% for subjects in the LW group].
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Caloric intake and REE were not different among study groups [REE, 1657 ± 267 Cal/day (NW), 1641 ± 389 Cal/day (EW), 1508 ± 348 Cal/day (LW)]. REE was greater than predicted by the Harris-Benedict equation in 82% of the patients [percentage of predicted REE, 117 ± 17% (NW), 121 ± 30% (EW), and 118 ± 25% (LW); mean, 119 ± 23%] and was matched by caloric intake in all but 1 of the 31 subjects. Expressed as kilocalories of energy expended per kg wt, energy expenditure tended to increase with the severity of wasting, but these changes did not reach statistical significance [25.4 ± 3.6 Cal/kg (NW), 28.0 ± 6.4 Cal/kg (EW), and 29.5 ± 6.5 Cal/kg (LW); P = 0.1, NW vs. LW]. Albumin and prealbumin levels were relatively low, but were not different among the groups [albumin: 3.4 ± 0.4 g/dL (NW), 3.3 ± 0.5 g/dL (EW), and 3.4 ± 0.6 g/dL (LW); normal range, 3.1–4.3 g/dL; prealbumin: 24.8 ± 18.4 mg/dL (NW), 20.2 ± 7.9 mg/dL (EW), and 20.7 ± 5.4 mg/dL (LW); normal range, 19.5–35.8 mg/dL].
Hormonal function
The prevalence of amenorrhea was 20% among study subjects [17%
(NW), 10% (EW), and 38% (LW)]. Percent predicted muscle mass, but
not BMI or fat mass, was significantly lower in subjects with
amenorrhea (74±8%) compared to that in eumenorrheic HIV-positive
subjects (94 ± 4%; P < 0.05; Fig. 2). Estradiol levels were lower among subjects with
amenorrhea (17.6 ± 21.8 pg/mL) compared to eumenorrheic (48.9 ±
33.6 pg/mL) and control (68.3 ± 47.6 pg/mL) subjects and were not
correlated with body composition. SHBG levels were increased among
HIV-positive subjects compared to controls [64 ± 18 nmol/L (NW),
61 ± 17 nmol/L (EW), 76 ± 22 nmol/L (LW), and 40 ± 15
nmol/L (control); P < 0.001, NW vs. C;
P < 0.01, EW vs. C; P <
0.0001, LW vs. C], but were not different by menstrual
status. Total testosterone levels tended to be lower in the amenorrheic
than in the eumenorrheic subjects (22.3 ± 10.6 vs.
13.8 ± 5.8; P = 0.07). Gonadotropin levels were
not different by wasting category or menstrual status (Table 1
).
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) were
decreased significantly in subjects with early and late wasting
compared to those in age-matched healthy controls (Fig. 3). Thirty-three percent of NW, 50% of EW, and 66% of
LW patients, but none of the control subjects, had free testosterone
levels below the age-adjusted normal range for the assay (0.6–3.1
ng/dL). DHEAS levels were also low in the subjects with LW compared to
controls [98 ± 85 µg/dL (NW), 102 ± 53 µg/dL (EW),
55 ± 46 µg/dL (LW), and 132 ± 68 µg/dL (control);
P < 0.05, LW vs. C] and were correlated
highly with free testosterone levels (r = 0.73; P
< 0.00001). Free testosterone and DHEAS correlated with muscle mass
(r = 0.37; P < 0.05 for free testosterone and
r = 0.48; P < 0.01 for DHEAS). No significant
differences in mean overnight GH levels or GH response to arginine or
IGF-I were observed by wasting category or in comparison with the
control group (Table 1).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In contrast to data from Kotler et al. (14) and in agreement with data from Grunfeld et al. in men (15), we found that ambulatory HIV-infected women, free of acute opportunistic infection, had increased REE compared to that predicted by the Harris-Benedict equation. There was no significant difference in REE between the groups by stage of wasting, but energy expended per kg wt tended to increase, rather than decrease, as expected with increased severity of wasting (16). These data suggest that REE is increased in HIV-infected women, increasing the likelihood of weight loss during secondary infections when caloric intake is decreased (15).
The changes in body composition in women with AIDS wasting are similar to those seen in simple starvation, with loss of fat more than lean (17). This is in contrast to the data previously reported in men with AIDS wasting, in whom the loss of lean is more significant than that of fat (1, 18). One potential explanation for this finding is that normal women have a relatively higher percentage of body fat at baseline than men (19) and, therefore, lose fat preferentially with weight loss, as suggested by Forbes et al. in non HIV-infected women (20). In addition, there may be other gender-specific hormonal and/or metabolic differences that account for such changes. Finally, chronic diarrhea and microsporidiosis were prevalent in prior studies of body composition in men with AIDS wasting (1, 2) and may contribute to the disproportionate loss of lean body mass in this population.
The prevalence of amenorrhea among the subjects studied was 20% overall, 22% among subjects with any weight loss, and 38% among subjects with weight less than 90% IBW. There was no difference in CD4 count or BMI in the eu-menorrheic vs. amenorrheic subjects. These data contrast with those reported by Chirgwin et al. that showed a 5% prevalence of amenorrhea in HIV-positive women without weight loss (21) and are in agreement with data from Ellerbrock et al. demonstrating that menstrual patterns do not differ between HIV-positive and -negative women by CD4 count (22). In contrast, amenorrhea was reported in 17% of women with AIDS by Widi Wirski et al. (23). These data suggest that the overall prevalence of amenorrhea in women infected with HIV disease is relatively higher among patients with weight loss than in previous reports of asymptomatic women with HIV disease. Furthermore, we found that amenorrhea is associated with a decreased muscle mass independent of weight or CD4 count, suggesting that gonadal dysfunction may be a factor in the critical loss of lean body mass in late stage wasting. Decreased testosterone levels among the amenorrheic patients may have contributed in part to the lower muscle mass in this group.
In addition, we investigated the GH axis to determine whether gender-specific differences in GH secretion might in part explain body composition changes in women with AIDS wasting. For example, increased GH secretion in women compared to men may be related to estrogen effects on the hypothalamic release of somatostatin (5, 6, 7, 24). However, we show no correlation between estrogen levels and overnight GH secretion, GH responses to arginine, or IGF-I levels in this study. Furthermore, there were no differences in these parameters between the amenorrheic and eumenorrheic patients, and no correlation between GH and body composition. Of note, we did not observe a significant difference in GH or IGF-I levels in women with advanced wasting compared to aged-matched healthy controls. In contrast, GH levels are elevated, and serum IGF-I levels and IGF-I responses to GH decreased in men with AIDS wasting (25, 26, 27), suggesting a pattern of acquired GH resistance similar to that seen in non-HIV-infected patients with protein-calorie malnutrition (28, 29). These data suggest that the relative degree of acquired GH resistance as a function of weight loss is less severe in women than men, and this may explain in part why fat mass is lost disproportionately to lean mass in women with AIDS wasting. Additional studies comparing directly GH secretory dynamics between men and women with AIDS wasting are necessary to further investigate the clinical significance of this observation.
These data demonstrate that women with AIDS wasting are androgen deficient compared to age-matched controls and suggest that androgen deficiency may contribute to the loss of muscle mass in this population. The mechanisms of decreased free testosterone levels in our subjects are not clear. Eumenorrheic subjects were studied in the early follicular phase. In healthy ovulating women, there is a small cyclicity in androgen levels during the menstrual cycle, but this is less than the variation in estrogen (30). Moreover, androgen levels were low compared to those in an age-matched healthy control population and were below the age-expected normal range in 58% of women with wasting, suggesting true androgen deficiency in this population. SHBG levels were significantly increased compared to control values, suggesting that sex steroid binding levels are increased in women with AIDS. These data suggest a similar pattern of increased SHBG levels in men with AIDS (25, 31, 32) and demonstrate that the free or unbound level is a better index of androgen function in HIV-infected women.
One potential explanation for the observation of decreased androgen levels in this population is the effect of chronic illness on gonadal function (31). Subjects in this study were not taking Megace or other medication and had no known conditions other than HIV that may have predisposed them to decreased androgen levels (33). In addition, subjects with acute opportunistic infection or on a new retroviral agent were excluded. Gonadotropin levels were low, consistent with hypogonadotropic hypogonadism and an effect of illness on the hypothalamic-pituitary-gonadal axis. Furthermore, serum total, but not free, testosterone levels decreased with severity of wasting and tended to correlate with CD4 count (r = 0.35; P = 0.07). Alternatively, decreased adrenal androgen function might contribute to decreased free testosterone levels in this population. DHEAS levels were decreased significantly among subjects with advanced wasting and were highly correlated with free testosterone levels.
The significance of decreased androgen levels with respect to changes in body composition in women with AIDS wasting has not previously been investigated. In this study, we demonstrate a significant correlation between muscle mass and free testosterone levels and between muscle mass and DHEAS levels in women with AIDS wasting, suggesting that physiological androgen deficiency may contribute to body composition changes with wasting in this population. In addition, decreased androgen levels among the patients with wasting suggest a critical level of testosterone below which wasting may occur. These data are in agreement with limited data in other populations which suggest that androgens play a role in the maintenance of lean body mass in women as well as men. For example, in postmenopausal women, androgen levels are correlated with muscle mass and strength (34), and improve with exogenous androgen treatment (35). A similar relationship between androgen levels and lean body mass was recently reported by our group in hypogonadal men with AIDS wasting (25). Taken together, these data are the first to suggest that physiological androgen deficiency occurs in women as well as men with AIDS wasting and suggest that this deficiency may have clinical relevance with respect to the loss of muscle mass seen in the later stages of wasting. In contrast to androgens, estrogen levels were not correlated with indexes of body composition in our patients, consistent with the known effects of androgens, but not estrogens, to mediate changes in lean body mass and whole body proteolysis in other populations (36).
These data suggest that women with AIDS wasting, like men, lose a critical amount of lean body and muscle mass with advanced disease. In contrast to men, however, loss of fat mass is disproportionately greater than loss of lean mass in women and is evident even at the early stages of wasting. These are the first data to demonstrate that androgen deficiency is common among women with AIDS wasting and may contribute to the critical loss of muscle mass in this population. In addition, these data demonstrate that muscle mass is lower among amenorrheic than eumenorrheic women with AIDS wasting, suggesting a heretofore unrecognized association between gonadal function and body composition in this population. Additional longitudinal cohort studies are needed to investigate further the mechanisms and clinical significance of gender-specific changes in body composition and to investigate the potential utility of physiological androgen replacement to build lean body and muscle mass in women with AIDS wasting.
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Acknowledgments |
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Footnotes |
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Received December 3, 1996.
Revised January 22, 1997.
Accepted January 29, 1997.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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F. R. Sattler, S. V. Jaque, E. T. Schroeder, C. Olson, M. P. Dube, C. Martinez, W. Briggs, R. Horton, and S. Azen Effects of Pharmacological Doses of Nandrolone Decanoate and Progressive Resistance Training in Immunodeficient Patients Infected with Human Immunodeficiency Virus J. Clin. Endocrinol. Metab., April 1, 1999; 84(4): 1268 - 1276. [Abstract] [Full Text]
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, P < 0.01, EW vs. NW; §,
P < 0.0001, LW vs. controls, NW, and
EW. For lean body mass: *, P < 0.05, LW
vs. controls and NW. For fat mass: *, P
< 0.05, EW vs. controls and NW; 
, P < 0.001, LW
vs. controls and nonwasting.
