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Differences between men and women as regards the effects of protein-energy malnutrition on the hypothalamic-pituitary-gonadal axis

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Differences between men and women as regards the effects of protein-energy malnutrition on the hypothalamic-pituitary-gonadal axis
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  APPLIED NUTRITIONAL INVESTIGATION  Nutrition  Vol. 15, No. 5, 1999 Differences Between Men and Women asRegards the Effects of Protein-EnergyMalnutrition on the Hypothalamic-Pituitary-Gonadal Axis JOAQUIN LADO-ABEAL, MD, PHD,* DANIEL PRIETO, MD,† MONICA LORENZO, MD,*SANTIAGO LOJO, PHD,‡ MANUEL FEBRERO, PHD,§ EMMA CAMARERO, MD,* ANDJ. CABEZAS-CERRATO, MD, PHD* From the *Endocrinology and Nutrition Service, †General Surgery Service, ‡Central Laboratory Service, GalicianGeneral Hospital, Complejo Hospitalario Universitario de Santiago de Compostela (CHUS), and the §School of  Medicine, Department of Statistics, University of Santiago de Compostela, Santiago de Compostela, Spain Date accepted: 8 July 1998 ABSTRACT Although protein-energy malnutrition (PEM) affects 50% of hospitalized patients, its effects on the hypothalamic-pituitary-gonadal (HPG) axis have not been extensively investigated. To investigate the effects of PEM on the HPG axis in hospitalizedpatients, 62 inpatients ages 18–91 y (35 men and 27 women) had a nutritional and hormonal evaluation. Hormones weredetermined in blood samples obtained between 0700 and 1200 h. Patients were divided into two subgroups: those with body massindex (BMI)  18.5 kg/m 2 (low body mass index [LBMI]; 16 men, 13 women) and those with BMI  20 kg/m 2 (normal-highbody mass index [NHBMI]; 19 men, 14 women). The nutritional parameters of LBMI patients were inferior to those of NHBMIpatients. Total and free testosterone levels were subnormal, 31.4% and 17.2% respectively, in all men; free testosterone wassubnormal in 31.25% of LBMI versus 5.3% of NHBMI male patients and total testosterone concentration was subnormal in43.8% of LBMI versus 21.1% of NHBMI male patients. Luteinizing hormone (LH) level was higher in LBMI men than inNHBMI men, whereas the reverse was the case for women, for whom follicle-stimulating hormone (FSH) also was lower in theLBMI group than the NHBMI group. The HPG axis hormones which best discriminated between the LBMI and NHBMI groupswere free testosterone for men and LH and FSH for women, which were all lower in the LBMI than in the NHBMI group. LHwas correlated with BMI and midupper arm muscle circumference (AMC) (women positively and men negatively) but not withtriceps skin-fold thickness (TSF). Total testosterone level was positively correlated with AMC and free testosterone with TSF.Hypogonadism is common among hospitalized patients with PEM. Men with PEM have low testosterone levels with normal orhigh gonadotropin levels, which suggests impairment of Leydig cell function. Women with PEM suffer hypogonadotropichypogonadism. AMC correlates positively with total serum testosterone concentration in men and with LH levels in women,suggesting that satisfactory function of the HPG axis requires a functional (protein) reserve as well as an energy (fat)reserve.  Nutrition  1999;15:351–358. ©Elsevier Science Inc. 1999Key words: malnutrition, hypogonadism, humans, disease, sex differences INTRODUCTION In women, protein-energy malnutrition (PEM) is frequentlyassociated with amenorrhea 1,2 and with a depression of gonado-tropin levels of hypothalamic srcin. 3,4 According to the Frischhypothesis, 5 the maintenance of menstrual cycles depends on thepossession of a minimum weight for given height and, in partic-ular, on possession of a minimum amount of fat. In spite of numerous criticisms, 6–9 this hypothesis, as such, still stands. Correspondence to: Joaquin Lado-Abeal, MD, PhD, Department of Medicine, Hospital General de Galicia, University of Santiago de Compostela c/ Galerass/n, 15705 Santiago de Compostela, Spain. E-mail: joaquin@cif.esNutrition 15:351–358, 1999©Elsevier Science Inc. 1999 0899-9007/99/$20.00Printed in the USA. All rights reserved. PII S0899-9007(99)00051-9  There has been less research on the effects of PEM on the malehypothalamic-pituitary-gonadal (HPG) axis. Hypogonadotropichypogonadism has been reported in men with anorexia nervosa, 10 but in 25–50% of anorexia nervosa patients, depressed gonado-tropin secretion is not due to malnutrition. 11,12 Smith et al. 13 foundthat a group of male Hindus with severe PEM and clinical hypo-gonadism had subnormal testosterone levels but above-normalgonadotropin levels, both abnormalities disappearing upon ade-quate food intake. Smith et al. accordingly suggested that dys-function of the Leydig cell is the primary cause of hypogonadismin men with PEM. Chlebowski and Heber 14 obtained similarresults in patients with metastatic cancer: The patients with thegreatest percentage of weight deficit relative to their ideal weighthad lower levels of free and total testosterone than the others, eventhough their serum luteinizing hormone (LH) levels were normalor above normal. It therefore seems that the effects of PEM onmen differ from the effects on women.In the work reported here, we studied the HPG axis in patientswith and without PEM, with the aim of determining possiblesex-related differences. The results showed that men with PEMhad low testosterone levels and normal or high LH levels, whereasthe women with PEM had depressed gonadotropin levels, proba-bly due to decreased production of gonadotropin-releasing hor-mone (GnRH) by the hypothalamus. MATERIALS AND METHODS Subjects Between January 1, 1995 and January 1, 1997, we studied 62inpatients in our hospital (35 men and 27 women). The malesubjects’ ages ranged from 20 to 65 y, and those of the femalesubjects from 18 to 91 y. Reasons for hospitalization are given inTABLE I. DIAGNOSIS IN MALE PATIENTSLBMI groupPatients DiagnosisAL Crohn’s diseaseBC Gastric cancerBR Tracheoesophageal fistulaCP Pancreatic pseudocyst, pancreatectomyCGE Diabetes mellitus type IICGM Gastric ulcer, gastrectomyGM Esophageal cancerGJ AIDS disease, pulmonary tuberculosisIP Chronic pancreatitis, diabetes mellitus secondaryMC Caustic esophagitisPP Gastric cancer, peritonitisPS Small cell lung cancer, pulmonary tuberculosisRN Non-small cell lung cancerRL Tracheoesophageal fistulaVF Chronic pancreatitis, diabetes mellitus secondaryVR Esophageal cancerNHBMI groupPatients DiagnosisAH Tuberculosis pleural effusionCF T-cell lymphomaCP Lymph nodal tuberculosisCG Esophageal cancerCC Colon cancerChF Esophageal cancerDC Facial traumaFG Urinary bladder cancerGR Gastric cancerGrC Non-small cell lung cancerHB Diabetes mellitus type I, debutID Colon cancerOF Non-small cell lung cancerPB AIDS disease,  Staphylococcus aureus  sepsisPR Laryngeal cancerPS Indolent non-Hodgkin’s lymphomaRS Gastric cancerRV Colonic polyposis, enterocutaneous fistula, dilatedcardiomyopathyLBMI, low body mass index (  18.5 kg/m 2 ); NHBMI, normal-highbody mass index (  20 kg/m 2 ). TABLE II. DIAGNOSIS IN FEMALE PATIENTSLBMI groupPatients DiagnosisAS Gastric ulcerCV Tuberculosis pleural effusionFL Disorder of intestinal transit (uncertain diagnosis)GG Gastric cancerGG Fever of unknown originGR Pulmonary abscessGS Colon cancerMB PneumoniaMF Pancreatic pseudocystRS Esophageal cancerTG Gluten intoleranceVM Diabetes mellitus type IIVS Miliary tuberculosisNHBMI groupPatients DiagnosisAS Bone metastasis of unknown originAM Esophageal cancerBG Aggressive non-Hodgkin’s lymphomaBlG Colon cancerCI Renal adenocarcinomaCS Gastric ulcer, gastrointestinal hemorrhageFB Hodgkin’s disease, nodular esclerosisFP Non-small cell lung cancerGC Diabetes mellitus type IIGS Cholangiocarcinoma, cholangitisMM Hodgkin’s disease, nodular esclerosisMR Diabetes mellitus type IISG Gastric cancerSG Cervix carcinoma, pulmonary metastasisLBMI, low body mass index (  18.5 kg/m 2 ); NHBMI, normal-highbody mass index (  20 kg/m 2 ). MALNUTRITION AND GONADAL AXIS352  Tables I and II. None were suffering from anorexia nervosa,known brain disease, moderate or severe kidney failure, livercirrhosis, or acute liver failure; none had previously suffered fromany endocrine disorder other than diabetes mellitus, or had beenalcoholic in the preceding 5 y; none were in the intensive care unit,or were receiving or had ever received oncologic chemotherapy orradiotherapy; none were being treated with morphine derivatives,glucocorticoids, catecholamines, ketoconazole, anabolic steroids,amiodarone, spironolactone, flutamide, or replacement estrogens,and none were taking oral steroid contraceptives. Patients wereproperly informed of the aim of the study, which was approved bythe hospital ethics committee. Protocol Nutritional evaluation 15 comprised determination of weight(W, in kg), height (H, in m), body mass index (BMI, in kg/m 2 ),triceps skin-fold thickness (TSF, in mm), midupper arm musclecircumference (AMC, in cm), creatinine height index (CHI, %),serum albumin (Alb, in g/dL) and transferrin (Tf, in mg/dL), andtotal serum lymphocyte count (TLC, in   L  1 ). Anthropometrywas always performed by the same two persons, and subjects wereweighed wearing underclothes and no shoes. TSF and midupperarm circumference (AC) were measured as per Blackburn et al. 15 ;TSF was the mean of three measurements taken with a John Bullcaliper (British Indicators Ltd., England), and AMC was calcu-lated as AC  0.134 TSF. Creatinine in 24-h urine was determinedby colorimetry (Jaffe´’s endpoint method, using a Sys 3 BM/ Hitachi 737 analyzer and Boehringer Mannheim reagents), andCHI (%) was calculated relative to the values published byWalser. 16 Serum albumin was determined by colorimetry (BCGmethod, using a Sys 3 BM/Hitachi 737 analyzer and BoehringerMannheim reagents), and serum transferrin by immunoturbidim-etry (Cobas-Bio kit, Roche, Switzerland). TLC was determinedwith a Bayer Technicon H-3 automatic cell counter.For determination of serum hormone concentrations, bloodsamples were taken between 0700 h and 1200 h after the patienthad been in hospital for at least 3 d with a daily energy intake of at least 600 kcal. LH (U/L), follicle stimulating hormone (FSH)(U/L), total testosterone (TT, nmol/L), estradiol (E 2 , pmol/L),prolactin (PRL, mU/L), cortisol (Cp, nmol/L), growth hormone(GH, mU/L), thyroid-stimulating hormone (TSH) (mU/L), freethyroxine (FT 4 , pmol/L), free 3,5,3  -triiodothyronine (FT 3 ,pmol/L) and sex hormone-binding globulin (SHBG, nmol/L) weredetermined in all subjects; additionally, free testosterone (FT,pmol/L) was determined in all men and progesterone (Pg, nmol/L)in all women. In six women with low gonadotropin levels, pitu-itary reserve and response were tested by determination of gonad-otropins in blood samples taken immediately before and 20 and 60min after intravenous bolus injection of 100  g of GnRH (Luforan500, Serono, Madrid, Spain).Ciba Corning kits (Ciba Corning Diagnostics SA, Spain) wereused to determine by chemoluminescence LH (within-run CV  4.5%, between-run CV    6.5%), FSH (within-run CV    4.5%,between-run CV  8.33%), TT (within-run CV  5.6%, between-run CV  6.6%), E 2  (within-run CV  16.6%, between-run CV  17.5%), PRL (within-run CV  3.8%, between-run CV  4.5%),TSH (within-run CV    4.7%, between-run CV    6.25%), FT 3 (within-run CV    3.8%, between-run CV    6.2%) and FT 4 (within-run CV  3.26%, between-run CV  4.95%). Immulite-DPC kits (Diagnostic Products Corp., Los Angeles, CA, USA)were used to determine Cp (within-run CV    7%, between-runCV    10.3%), GH (within-run CV    4.8%, between-run CV   5%) and SHBG (within-run CV  8%, between-run CV  13%).FT was determined with a radioimmunoassay kit (Coat-A-Count,TABLE III. NUTRITIONAL PROFILES OF LOW-BMI AND NORMAL-HIGH-BMI MALE HOSPITAL PATIENTSVariableLBMI ( n    16) NHBMI ( n  19)Mean  SD(median) RangeMean  SD(median) RangeAge (y) 48.7  12.7 (50) 44.9  16.7 (53) NS26–63 20–65BMI (kg/m 2 ) 16.6  1.5 (16.9) 23.5  3.0 (22.9)  P  0.00113–18.4 20.1–31.3TSF (mm) 5.5  2.5 (5) 9.4  3.2 (10)  P  0.013–13 4–15AMC (cm) 19.6  1.6 (19.5) 25.1  3.1 (24.3)  P  0.00116.9–23.4 20.7–32.4CH I (%) 70.9  34.5 (58.5) 114.9  40.5 (110)  P  0.0526.7–136.8 56.5–185.4Albumin(mg/dL)3.1  0.5 (3.1) 3.8  0.6 (3.7)  P  0.052.1–3.9 2.9–5Transferrin(mg/dL)180.2  58.7 (185) 234.6  87.1 (213) NS76–261 130–399Lymphocite 1470  801 (1600) 1750  817 (1800) NS100–3200 500–3700AMC, midupper arm muscle circumference; BMI, body mass index; CHI, creatinine height index; NS, not significant; TSF, triceps skin-foldthickness. TABLE IV. NUTRITIONAL PROFILES OF LOW-BMI AND NORMAL-HIGH-BMI FEMALE HOSPITAL INPATIENTSVariableLBMI ( n    13) NHBMI ( n    14)Mean  SD(median) RangeMean  SD(median) RangeAge (y) 58.8  23.6 (67) 61.7  19.8 (65.5) NS18–87 19–91BMI (kg/m 2 ) 15.9  1.6 (16.3) 23.7  2.1 (23.7)  P  0.00112.9–18.4 20.8–28.1TSF (mm) 6.9  2.7 (6.5) 12.6  4.1 (12.5)  P  0.0013–12 6–20AMC (cm) 17.4  1.8 (17.2) 21.9  4.6 (21.9)  P  0.00114.1–20.3 10.6–28.8CH I (%) 59.5  27.2 (62.0) 113.9  28.6 (117.4)  P  0.0112.5–108.4 57.8–161.1Albumin(mg/dL)2.9  0.6 (2.9) 3.7  0.8 (3.8)  P  0.052.2–4.8 2.4–4.6Transferrin(mg/dL)175.3  74.3 (169.5) 254.2  88.3 (275) NS64–269 117–369Lymphocite 1314  532 (1400) 1666  578 (1630) NS600–2000 700–2500AMC, midupper arm muscle circumference; BMI, body mass index; CHI, creatinine height index; NS, not significant; TSF, triceps skin-foldthickness. MALNUTRITION AND GONADAL AXIS 353  Diagnostic Products Corp., Los Angeles, CA, USA) with a within-run CV  4.3% and a between-run CV  5.5%.Subjects with PEM were identified as those with BMI  18.5kg/m 2 17,18 ; these 16 men and 13 women are hereinafter referred toas the low BMI group (LBMI), and the others (19 men and 14women with BMI    20 kg/m 2 ) as the normal-high BMI group(NHBMI). Statistical Analysis Comparisons between groups were performed by one-wayanalysis of variance (ANOVA) with post hoc comparisons by theBonferroni test. Correlations were evaluated in terms of Pearson’scoefficient. Linear discriminant analysis 19 was used to determinewhich hormones discriminated best between subjects with LBMIand subjects with NHBMI. RESULTS Within each sex, the LBMI and NHBMI groups did not differsignificantly in age, but NHBMI men were younger than NHBMIwomen, with a median age of 53 as against 65.5 y.The nutritional profiles of each sex in each group are shown inTables III and IV. The nutritional parameters of the LBMI groupwere significantly inferior to those of the NHBMI group, except asregards transferrin and total lymphocyte count. In the NHBMIgroup, men and women differed significantly as regards TSF(median, 10 mm men versus 12.5 mm women,  P    0.05) andAMC (median, 24.3 cm men versus 21.9 cm women,  P  0.05).In the LBMI group, the sexes only differed significantly in AMC(median 19.5 cm men versus 17.2 cm women,  P    0.05).Hormone values are shown in Tables V and VI. LBMI men hadsignificantly higher LH and GH levels, and significantly lower freetestosterone levels than NHBMI men (Fig. 1). LBMI women hadsignificantly lower LH and FSH levels than NHBMI women (Fig.2) and like LBMI men had higher GH levels than their NHBMIcounterparts, although the difference was not statistically signifi-cant ( P    0.07).Within the LBMI group, men had significantly higher levels of LH and lower SHBG than women (median LH 5.2 IU/L menversus 1.6 IU/L women,  P    0.05; SHBG 42.5 nmol/L menversus 77.7 nmol/L women,  P    0.05). Within the NHBMIgroup, men had significantly lower levels of LH, FSH, and SHBGthan women (median LH 4.1 IU/L men versus 23.5 IU/L women, P    0.001; FSH 3.1 IU/L men versus 43.4 IU/L female,  P   0.001; SHBG 32 nmol/L men versus 62.9 nmol/L women,  P   0.05). None of the four subgroups differed significantly from anyother as regards PRL, thyroid hormones, and serum cortisol levels.The proportion of men with subnormal total testosterone con-centration was 31.4% (20% LBMI and 11.4% NHBMI), and theproportion with subnormal free testosterone concentration was17.2% (14.3% LBMI and 2.9% NHBMI). Total testosterone con-centration was subnormal in a greater proportion of LBMI menthan NHBMI men (43.8% as against 21.1%), and the same wastrue of free testosterone levels (31.25% as against 5.3%).TABLE V. HORMONE PROFILES OF LOW-BMI AND NORMAL-HIGH-BMIMALE HOSPITAL INPATIENTSVariable(normal range)LBMI ( n    16) NHBMI ( n    19)Mean  SD(median) RangeMean  SD(median) RangeLH (U/L) 6.4  3.5 (5.2) 4.5  1.7 (4.1)  P  0.05(2.4–5.9) 1.6–12.6 1.6–9.5FSH (U/L) 6.6  5.4 (4.3) 4.4  3.8 (3.1) NS(0.9–15) 1.4–18.8 1.3–17.2TT (nmol/L) 10.8  7.6 (10) 14.4  5.6 (13.3) NS(9–47) 1–22.6 5.8–25.9FT (pmol/L) 40.9  18.2 (37.4) 78.2  42.9 (62.8)  P  0.01(31.2–162.9) 16.5–89.2 26.4–196.9PRL (mU/L) 291  165 (264) 225  116 (198) NS(  600) 102–590 70–520Estradiol (pmol/L) 140  72 (130) 170  108 (133) NS(  270) 58–259 0–331TSH (mU/L) 2.1  1.2 (2.1) 1.99  1.02 (1.79) NS(0.35–5.5) 0.7–5.5 0.4–4.3FT 4  (pmol/L) 14.2  2.9 (14.4) 15.2  2.7 (15.5) NS(10.3–23.2) 7.7–19.7 9–20FT 3  (pmol/L) 3.7  1.1 (3.4) 3.9  0.6 (4.1) NS(3.5–6.5) 2.6–6.2 2.8–5GH (mU/L) 6.7  6.9 (4) 2.2  2.3 (1.2)  P  0.05(  17) 0.6–28 0.2–8.4Cortisol (nmol/L) 582  97 (552) 607  196 (552) NS(140–700) 414–773 331–1214SHBG (nmol/L) 46.76  28.56 (42.50) 37.17  23.24 (32) NS(10–70) 12–97 14–102FT 3 , free 3,5,3  -triiodothyronine; FT 4 , free thyroxine; FSH, follicle-stimulating hormone; LH, luteinizing hormone; NS, not significant;PRL, prolactin; TSH, thyroid-stimulating hormone. TABLE VI. HORMONE PROFILES OF LOW-BMI AND NORMAL-HIGH-BMIWOMEN HOSPITAL INPATIENTSVariable(normal range)LBMI ( n    13) NHBMI ( n    14)Mean  SD(median) RangeMean  SD(median) RangeLH (U/L) 4.9  7.9 (1.6) 23.1  14.5 (23.5)  P  0.01(0.8–104) 0–23.7 5.4–53.4FSH (U/L) 14.8  18.3 (8.5) 41.7  30.5 (43.4)  P  0.05(0.8–96) 0.1–53.2 3.2–114.1PRL (mU/L) 380  279 (340) 272  231 (226) NS(  540) 96–1040 80–874Estradiol (pmol/L) 95  54 (97) 135  110 (153) NS(  1600) 3.6–187 3.6–350TSH (mU/L) 1.7  1.2 (1.2) 1.8  1.6 (1.8) NS(0.35–5.5) 0.03–3.9 0.2–5.8FT 4  (pmol/L) 14.8  3 (15.2) 16.9  4.4 (15.9) NS(10.3–23.2) 10.1–19.6 10.7–26.2FT 3  (pmol/L) 3.5  0.9 (3.2) 4.45  0.9 (4.5) NS(3.5–6.5) 2.4–5.2 2.8–6.1GH (mU/L) 6.9  5.7 (5.2) 3.3  3.2 (2) NS(  17) 0.8–18.4 0.4–11.2Cortisol (nmol/L) 692  241 (607) 693  187 (690) NS(140–700) 442–1132 386–994SHBG (nmol/L) 81.5  27.8 (77.7) 61.5  24.7 (62.9) NS(20–100) 47–125 36–105FT 3 , free 3,5,3  -triiodothyronine; FT 4 , free thyroxine; FSH, follicle-stimulating hormone; GH, growth hormone; LH, luteinizing hormone;NS, not significant; PRL, prolactin; SHBG, sex hormone-binding globu-line; TSH, thyroid-stimulating hormone. MALNUTRITION AND GONADAL AXIS354  The hormones best discriminating between LBMI men andNHBMI men were GH and free testosterone, with discriminantfunction coefficients of 0.56 and   0.49 respectively (sign con-vention: hormones with higher levels in the LBMI than theNHBMI group have positive coefficients). The hormones bestdiscriminating between LBMI women and NHBMI women wereLH, FSH, and GH, with discriminant coefficients of    0.76,  0.60, and 0.33 respectively. The hormones that discriminatedworst between the LBMI and NHBMI groups were, for men,cortisol, prolactin, and FSH, and for women cortisol, FT 4 , andprolactin.LH was significantly correlated with BMI among men, women,and the whole sample, but the correlation was positive amongwomen but negative among men (Fig. 3A). In the case of corre-lation between LH and AMC, the same difference between menand women (positive correlation among men, negative amongwomen) sufficed to prevent significant correlation in the wholesample (Fig. 3B). Total testosterone correlated with AMC ( r    0.45,  P    0.01) and free testosterone correlated with TSF ( r    0.41,  P    0.05).In the GnRH test study of six of the female subjects, themedian levels of LH were 0.7, 3.6, and 11.9 IU/L after 0, 20, and60 min respectively, while the median levels of FSH at the sametimes were respectively 5.7, 7.5, and 12.9 IU/L. DISCUSSION Although the assessment of nutritional status is the subject of some controversy 15,20–23 it has been estimated that about 50% of hospital inpatients suffer PEM. 23,24 The criterion used to identifyPEM in this study was low BMI, which has been criticized as amarker of nutritional status 25 but has nevertheless been recom-mended as an initial marker of chronic energy deficiency. 17,18 Theassumption that patients with low BMI are more protein/energy-deficient is supported in this study by the LBMI group also havingbeen inferior to the NHBMI group as regards other indices of nutritional status (specifically, the anthropometric parametersAMC and TSF, the biochemical parameter albumin, and the CHI[%]).The effects of PEM on the HPG axis have been studiedextensively only in anorexia nervosa patients. This may, in part, bebecause it is sometimes difficult to distinguish between the effectsof malnutrition and the effects of underlying disease and/or med-ication. It is well known that critical illness causes hypogonado-tropic hypogonadism in both men 26–31 and women, 32–34 and thatmorphine derivatives 35 and large doses of glucocorticoids 36 block gonadotropin secretion, which is also potentially subject to alter-ation by catecholamines. 37 Severe hepatic disease (cirrhosis oracute liver failure) alters gonadal steroid metabolism, 38 and mod-erate or severe kidney failure affects the clearance of a variety of hormones. 38 All patients with these possible sources of confusionbetween the effects of PEM and underlying disease or treatmentwere excluded from the study, as were those taking drugs knownto affect the HPG axis (see  MATERIALS AND METHODS ). Thus,although the pathologies suffered by the patients studied cannotdefinitively be said not to have affected the HPG axis, none of the FIG. 1. Free testosterone and growth hormone (GH) serum levels in male patients with low body mass index (LBMI) and without normal high body massindex (NHBMI) malnutrition. In each group, the continuous dark line represents the mean value. MALNUTRITION AND GONADAL AXIS 355
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