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INT J TUBERC LUNG DIS 8(2):211217

2004 IUATLD

Malnutrition and the severity of lung diseasein adults with pulmonary tuberculosis in Malawi

M. Van Lettow,* J. J. Kumwenda, A. D. Harries, C. C. Whalen, T. E. Taha,* N. Kumwenda,*

C. Kangombe, R. D. Semba*

* Johns Hopkins Medical Institutions, Baltimore, Maryland, USA; College of Medicine, University of Malawi, Blantyre, Malawi National TB Control Programme, Lilongwe, Malawi; Department of Medicine, Case Western Reserve

S U M M A R Y

University, Cleveland, Ohio, USA

SETTING: Zomba Central Hospital, Zomba, Malawi.

OBJECTIVE: To examine the relationship between mal-

nutrition and the severity of lung disease in human immu-

nodeficiency virus (HIV) positive and negative adults

with pulmonary tuberculosis (PTB).DESIGN: Cross-sectional study.

METHODS: Chest radiographs and anthropometric mea-

surements were obtained and bioelectrical impedance anal-

ysis was conducted in sputum-positive patients with pul-

monary tuberculosis. Lung disease in chest radiographs was

graded as normal, minimal, moderately advanced and far

advanced according to a conventional classification system.

RESULTS: Among 319 adults with PTB with or without

HIV co-infection, body mass index (BMI), fat mass and

phase angle were independently associated with increas-

ing severity of lung disease. Multiple logistic regression

analyses showed that BMI, fat mass and phase angle

were associated with increasing severity of lung diseaseamong 236 HIV-positive adults, when adjusted for sex,

age, and plasma HIV load.

CONCLUSION: The severity of lung disease in adults

with PTB is associated with the extent of malnutrition,

as reflected by BMI and body composition studies using

bioelectrical impedance analysis.

KEY WORDS: bioelectrical impedance analysis; HIV; lung

disease; malnutrition; tuberculosis

ACCORDING TO the World Health Organization(WHO), about one third of the worlds population isinfected with Mycobacterium tuberculosis, and themajority live in less developed countries where humanimmunodeficiency virus (HIV) infection is spreadingrapidly. In sub-Saharan Africa, the Indian subconti-nent, and South-east Asia, half or more of adults havelatent tuberculosis infection. The WHO estimatedthat the number of new cases of tuberculosis and theproportion with co-existing HIV infection will con-tinue to increase.1 The association between tuber-culosis and malnutrition has long been recognised, as

malnutrition predisposes to the development of clini-cal disease, and tuberculosis often exacerbates mal-nutrition.2,3 Individuals with immunosuppression havea greater risk of developing clinical tuberculosis,which explains the increased prevalence of tuberculo-sis in association with HIV infection. In some coun-tries in sub-Saharan Africa, including Malawi, theHIV seroprevalence rate among tuberculosis patientsis over 75%.47 Co-infection with HIV and tuberculo-

sis may result in an exacerbation of wasting seen intuberculosis or HIV infection alone.2,8 However,there is limited insight into the relationship betweenmalnutrition and the clinical features of tuberculosis.

Although nutritional status is known to be a riskfactor for pulmonary tuberculosis (PTB), the relation-ship between nutritional status and the severity of thedisease has not been well characterised. We hypothe-sised that more advanced lung disease, as assessed bychest radiographs, was associated with more severemalnutrition. To test this hypothesis, we conducted across-sectional study to examine the relationship be-

tween malnutrition and the extent of lung disease inadults with PTB with and without HIV infection. Inaddition to body mass index (BMI), body cell mass,fat mass and phase angle derived from bioelectricalimpedance analysis (BIA) were used to assess theextent of malnutrition in this study. BIA, a simple,non-invasive technique, has been recommended fornutritional studies in HIV-infected individuals andhas been shown to be sufficiently precise for body

Correspondence to: Dr Richard D Semba, Johns Hopkins University School of Medicine, Department of Ophthalmology,550 N. Broadway, Suite 700, Baltimore, MD 21205, USA. Tel: (1) 410-955-3572. Fax: (1) 410-955-0629. e-mail:[email protected]

Article submitted 25 January 2003. Final version accepted 6 August 2003.


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212 The International Journal of Tuberculosis and Lung Disease

composition analysis.810 BIA was shown to be agood predictor and superior to BMI as an estimatorof body fat.10 Body cell mass, the total mass of all thecellular elements in the body, represents the metabol-ically active component of the body. It comprises

those tissues that are most likely to be affected byphysical activity, nutrition or disease, and appears tobe an independent predictor of mortality among HIV-infected adults in the era prior to highly active anti-retroviral therapy.1114 Phase angle, the relationshipbetween resistance and reactance obtained from BIA,is considered to reflect water distribution betweenextra- and intracellular spaces and has been shown tobe an independent predictor of mortality during HIVinfection.13,15,16

MATERIALS AND METHODS

The study population consisted of adults who pre-sented with new sputum-positive PTB in Zomba Cen-tral Hospital between July 1999 and December 2000.Subjects were offered HIV testing and were screenedfor HIV antibodies after written informed consenthad been obtained. All subjects were given appropri-ate pre- and post-test HIV counselling. At enrolment,basic demographic information and a medical historywere collected and a standardised physical examina-tion was conducted. Subjects received standard short-course chemotherapy for tuberculosis as per theguidelines of the Malawi National Tuberculosis Pro-

gramme (NTP).17 Adults with a previous history oftreated PTB were excluded. Three sputum samplesfrom each subject were examined with Oramine-Odark-fluorescent staining method. Sputum-positivePTB was considered proven when at least one out ofthree sputum stains showed acid-fast bacilli. HIVinfection was diagnosed on the basis of a positive rapidtest (Determine 1/2 Rapid Test, Abbott, Johannesburg,South Africa) and confirmed by a positive enzyme-linked immunosorbent assay for HIV-1 antibodies(Wellcozyme; Wellcome Diagnostics, Dartford, Kent,UK). Plasma HIV load was measured using quantita-

tive HIV-1 RNA PCR (Roche Amplicor Monitor, ver-sion 1.5, Branchburg, NJ, USA) with a sensitivity limitof 400 HIV RNA copies/mL. The protocol wasapproved by the institutional review boards at the

Johns Hopkins School of Medicine (Baltimore, MD,USA) and the College of Medicine, University ofMalawi (Blantyre, Malawi), with final approval bythe Office for Protection from Research Risk of theNational Institutes of Health.

Nutritional assessment

Body weight was determined to the nearest 0.1 kgusing an adult balance (Seca 700 balance, Seca Cor-poration, Hanover, MD), and standing height wasdetermined to the nearest cm. Single-frequency BIAwas performed at 50 kHz and 800 A (RJL Systems,

Inc., Detroit, MI, USA) with standard tetrapolar leadplacement.18 BIA measurements were performed intriplicate for each subject. The reproducibility onrepeated BIA measurements was 99%. Impedance(Z) was calculated as (resistance2 reactance2)0.5.

Body cell mass was calculated as 0.76 [Ht1.60/Z(paral-lel)0.50 59.06] 18.52 Wt 386.66/120 for males,and as 0.96 [Ht2.07/Z(parallel)0.36 1.30] 5.79 Wt230.51/120 for females. Fat-free mass was calculatedas 0.50 (Ht1.48/Z0.55 1.0/1.22) 0.42 Wt 0.49 formales, and as 0.88 (Ht1.97/Z0.49 1.0/22.22) 0.081Wt 0.07 for females. Fat mass derived from BIAmeasures was calculated as body weight minus fat-free mass. Phase angle was calculated as arctan-gent (reactance/resistance).8,19 These equations werepreviously cross-validated in a sample of white, blackand Hispanic patients with and without HIV infec-

tion,8

and have been applied elsewhere in sub-Saharan Africa.20

Radiographic findings

A standard posterior-anterior chest radiograph wastaken of each subject. All radiographs were examinedby an experienced clinical officer in the Malawi NTP.Lung disease was graded according to an interna-tional classification of tuberculosis:21 1) minimal lungdisease was defined as infiltrates of slight to moderatedensity; disease present in a small portion of bothlungs; the total volume of infiltrate(s) being the vol-ume of one lung present above the second chon-

drosternal junction and the spine of the fourth junctionor the body of the fifth thoracic vertebra and no cavita-tions present; 2) moderately advanced disease wasdefined as: disease present in one or both lungs; thetotal extending not more than as follows: i) scatteredlesions of slight to moderate density do not involvemore than the total volume of one lung or the equiva-lent volume of both lungs, ii) dense, confluent lesionsdo not involve more than one third of the volume ofone lung, and iii) the total diameter of the cavities arenot greater than 4 cm; and 3) far advanced lung diseasewas defined as: lesions more extensive than moderately

advanced disease. All chest radiographs were inter-preted by a reader blinded to the HIV and clinical sta-tus of the subjects. To lessen inter- and intra-observerdifferences, the chest radiographs were also read by atuberculosis specialist (CCW); in cases of discordancein readings, films were reviewed and final classifica-tions were reached by consensus.

Data and statistical analysis

Data and statistical analysis were conducted usingSPSS 9.0 (SPSS, Inc., Chicago, IL, USA). Comparisonsbetween groups were made using t-tests and exacttests. Univariate analysis of variance was used to testfor linear trends across categories of lung disease.Nutritional status was assessed in adults with PTBwith and without HIV co-infection. Subjects were


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Malnutrition and severity of pulmonary TB 213

then separated into two groups according to theextent of malnutrition. BMI19 was considered con-sistent with malnutrition.22 The proportion of adultswith phase angle 5.3 was examined, as this cut-off was previously shown to be predictive of mortal-

ity among HIV-infected adults.23 Body cell mass andfat mass were divided into quartiles, with the lowestquartile considered the most consistent with wasting.Logistic regression models were fitted with BMI19.0, phase angle 5.3 and the lowest quartile offat mass and body cell mass as the outcome variable.Multiple logistic regression models were conductedto adjust for sex, age, HIV co-infection and plasmaHIV load. A test for trend across the categories ofextent of lung disease was performed by assigning thesubjects the mean value of their allocated categoryand then entering this as a continuous variable into

the logistic regression model. A significance level ofP 0.05 was used in this study.

RESULTS

Characteristics of patients with PTB

The study population consisted of 236 HIV-positiveand 83 HIV-negative adults with sputum-positivePTB. The overall HIV prevalence among the male andfemale participants was 67% and 80%, respectively.The mean age among all subjects was 33 years, rang-ing from 18 to 58 years. Education levels were signif-icantly lower among female participants (32.5% of

females vs. 8.7% of males never attended school, P0.01). Of female participants, 17.2% had continuededucation after primary school vs. 31.5% of maleparticipants (P 0.01). There were no significant dif-ferences in education levels by HIV status. HIV-positivemen with PTB had lower mean haemoglobin thanHIV-negative men (Table 1).

Nutritional status

The majority of subjects were malnourished, as over-all 61% of subjects had a BMI 19. There were nosignificant differences found in weight, mean BMI or

the proportion of individuals with BMI 19 betweenHIV-positive and -negative individuals (Table 1). Therewere no significant differences in resistance, imped-ance, fat-free mass, fat mass or between individualswith or without HIV infection. Reactance, body cell

mass and phase angle were significantly lower in HIV-positive than HIV-negative male participants. Theproportion of participants with phase angle5.3 wassignificantly higher in HIV-positive than in HIV-negative male participants. These differences werenot observed between the HIV-positive and HIV-negative female participants (Table 2).

Table 3 shows the linear trends across categories oflung disease associated with nutritional indicatorsin HIV-positive and -negative subjects. These datashow that among the HIV-positive individuals, moreadvanced lung disease was shown to be associated with

lower BMI, body cell mass, fat mass and phase angle.Among the HIV-negative individuals, more advancedlung disease was associated with lower BMI andlower phase angle.

Table 4 shows crude and adjusted odds ratios (OR)and 95% confidence intervals (CI) for associationsbetween extent of lung disease and lower BMI, bodycell mass, fat mass and phase angle in adults with PTBwith and without HIV co-infection. When comparedwith normal lung appearance, far advanced lung dis-ease was associated with lower BMI, fat mass andphase angle as shown by crude and adjusted OR. Thesame applied for minimal and moderately advanced

lung disease, which were associated with lower fatmass and BMI, respectively. There was no significantrelationship between body cell mass and extent oflung disease in adults with PTB with or without HIVco-infection in logistic regression analyses. Consider-ing the most marked comparison, for HIV-positiveindividuals with far advanced lung disease, the ORfor an independent association with lower BMI was6.88 (95%CI 2.3719.93), with lower fat mass 9.98(95%CI 2.0149.70), and with lower phase angle3.98 (95% CI 1.3711.55) when adjusted for sex, ageand plasma HIV load (Table 5).

Table 1 Characteristics of HIV-positive and HIV-negative adults presenting with pulmonary tuberculosis in Zomba, Malawi

Men Women

Characteristics*HIV-positive(n 100)

HIV-negative(n 49) P

HIV-positive(n 136)

HIV-negative(n 34) P

Age (years) 36 (8) 34 (12) 0.28 32 (9) 30 (11) 0.18Able to read (%) 93.0 87.8 0.29 70.9 55.9 0.09Primary education or higher (%) 30.0 34.7 0.56 17.5 20.5 0.67Haemoglobin (g/L) 96 (26) 111 (31) 0.01 92 (23) 99 (27) 0.13Anaemic (%) 91.0 67.3 0.01 86.0 85.3 0.91Plasma HIV load (copies 103/mL)

median (25th, 75th percentiles) 278 (134, 703) 228 (94, 630)

* Mean (SD) for continuous variables. Haemoglobin120 g/L for females and 130 g/L for males. HIV load not measured in 3 male and 10 female subjects.HIV human immunodeficiency virus.


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Table

4

ExtentoflungdiseaseandriskoflowBM

I,bodycellmassfatmassandphaseang

leinadultswithpulmonarytuberculosisinZomba,Malawi

BMI19

Bodycellmass,

lowestquartile

Fatmass,lowestquartile

Phaseangle5.3

Extentoflungdisease

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

Normal(n

4

2)

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

Minimal(n1

13)

2.02(0.974.16)

1.97(0.954.09)

0.85(0.381.93)

1.21(0.473.09)

3.17(1.049.66)

2.54(0.788.26)

1.43(0.702.93)

1.54(0.733.25)

Moderatelyadvanced(n8

6)

2.79(1.315.97)

2.86(1.336.19)

0.75(0.321.77)

0.84(0.322.28)

3.89(1.2611.06)

4.15(1.2413.82)

1.81(0.863.81)

2.11(0.954.65)

Faradvanced(n7

8)

8.12(3.4319.23)

8.83(3.6421.42)

1.25(0.542.90)

1.50(0.564.03)

3.73(1.1911.69)

4.94(1.4417.01)

3.11(1.406.88)

4.32(1.8110.32)

P

fortrend

0.0001

0.0001

0.19

0.51

0.02

0.007

0.003

0.0004

*Adjustedforage,sexandHIVinfection.

BMIbodymassindex;ORo

ddsratio;CIconfidencein

terval;HIVhumanimmunodeficiencyvirus.

Table

5

ExtentoflungdiseaseandriskoflowBM

I,bodycellmassfatmassandphaseang

leinHIV-positiveadultswithpulmonarytuberculosisinZomba,Malawi

BMI

19

Bodycellmass,lowestquartile

Fatmass,lowestquartile

Phaseangle5.3

Extentoflungdisease

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

CrudeOR

(95%CI)

AdjustedOR*

(95%CI)

Normal(n

3

6)

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

Minimal(n9

5)

1.76(0.813.83)

1.77(0.764.15)

0.69(0.301.63)

1.24(0.453.40)

3.06(0.989.50)

4.11(0.9817.26)

1.38(0.633.04)

2.08(0.865.06)

Moderatelyadvanced(n6

1)

2.12(0.924.89)

2.33(0.945.80)

0.62(0.241.57)

0.73(0.252.11)

3.09(0.9510.06)

6.22(1.3628.37)

1.50(0.643.51)

2.15(0.835.61)

Faradvanced(n4

4)

4.86(1.8213.0)

6.88(2.3719.93)

1.57(0.623.99)

1.47(0.504.27)

2.67(0.779.25)

9.98(2.0149.70)

2.43(0.926.40)

3.98(1.3711.55)

P

fortrend

0.0002

0.0003

0.09

0.30

0.05

0.02

0.08

0.02

*Adjustedforage,sexandplasmaHIVload.

BMIbodymassindex;ORo

ddsratio;CIconfidencein

terval;HIVhumanimmunodeficiencyvirus.


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216 The International Journal of Tuberculosis and Lung Disease

phase angle was 6.2 compared with a mean phaseangle of 4.2 in HIV-positive and 4.4 in HIV-negativeadults with far advanced pulmonary disease describedin the present study.

One limitation of the present study is that the

assessment of lung disease through chest radiographs,although done with a descriptive grading scheme, issubjective. The cross-sectional design of this studyrestricts our conclusions and does not provide infor-mation on whether poor nutritional status is a predic-tor of more severe PTB. In a recent study from ThyoloDistrict in southern Malawi, moderate to severe mal-nutrition, as assessed by BMI, was a risk factor forearly death, although the reasons are unknown.7

Wasting is a fundamental sign of tuberculosis in bothHIV-positive and HIV-negative patients, and the aeti-ology of the wasting has not been elucidated. Further

studies are needed to examine the role of oxidativestress and antioxidant micronutrients, the role ofinflammatory cytokines, and the relationship of severelung disease to mortality. It is unclear whether nutri-tional interventions will slow the progression of dis-ease or reduce morbidity and mortality if added totuberculosis chemotherapy. Controlled clinical trialscurrently in progress in developing countries shouldhelp provide insight into the role of micronutrientsupplementation for adults with pulmonary tuber-culosis, with and without HIV co-infection.

Acknowledgements

We thank Allan Menyere, Lesley Banda, Roseline Somanje, Agnes

Jusu, Grace Makocho, and Snehal Shah. We thank Karen Near and

Barbara Laughon, National Institute for Allergy and Infectious

Diseases, and Ken Bridbord, Fogarty International Center, for their

continued encouragement and support.

This study was supported in part by the National Institutes of

Health (AI41956, AI32414), the Fogarty International Center, and

the United States Agency for International Development (Cooper-

ative Agreement HRN A-0097-00015-00).

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R S U M

C O NTE XT E : Hpital Central de Zomba, Zomba, Malawi.

O B JEC T I F : Examiner les relations entre la malnutrition

et la gravit de la maladie pulmonaire chez des adultes

sropositifs et srongatifs pour le virus de limmuno-

dficience humaine (VIH) et atteints de tuberculose

pulmonaire.

S C HMA : Etude transversale.

M T HO DE S : On a obtenu les clichs thoraciques et les

donnes anthropomtriques et men une analyse dim-pdance biolectrique chez les patients bacilloscopie

positive atteints de tuberculose pulmonaire. Latteinte

pulmonaire apparaissant au clich thoracique a t code

comme normale, minimale, modrment avance ou trs

avance selon un systme conventionnel de classification.

R S UL T ATS : Parmi 319 adultes atteints de tuberculose

pulmonaire avec ou sans co-infection par le VIH, lindex

de masse corporelle, la masse graisseuse et langle de

phase se sont avr associs de manire indpendante

avec une svrit croissante de la maladie pulmonaire.

Les analyses de rgression logistique multiple ont mon-

tr que lindex de masse corporelle, la masse graisseuse

et langle de phase taient associs un accroissement de

la gravit de la maladie pulmonaire chez 236 adultes

sropositifs pour le VIH aprs ajustement pour le sexe,lge et la charge virale plasmatique du VIH.

C O NCL US IO N : La gravit de la maladie pulmonaire chez

les adultes atteints de tuberculose pulmonaire est asso-

cie ltendue de la malnutrition telle que reflte par

les tudes de composition corporelle utilisant une ana-

lyse dimpdance biolectrique.

R E S U M E N

C O NTE XT O : Hospital Central de Zomba, Zomba,

Malawi.

O B JET I VO : Examinar la relacin entre la malnutricin y

la gravedad de la enfermedad pulmonar, en adultos posi-tivos y negativos por el virus del inmunodeficiencia

humana (VIH) con tuberculosis pulmonar.

DI S EO : Estudio transversal.

M T ODO : Se obtuvieron radiografas de trax y medi-

ciones antropomtricas y se realizaron anlisis de impe-

dancia bioelctrica en pacientes con tuberculosis pulmo-

nar con baciloscopia positiva. En la radiografa de trax,

la enfermedad pulmonar fue graduada en inexistente,

mnima, moderadamente avanzada y avanzada, segn

un sistema convencional de clasificacin.

R E S UL T ADO S : En 319 adultos con tuberculosis pulmo-

nar con o sin coinfeccin VIH, el ndice de masa corpo-

ral, la masa grasosa y el ngulo de fase estaban indepen-

dientemente asociados con el aumento de gravedad de la

enfermedad pulmonar. Los anlisis de regresin logsticamltiple demostraron que el ndice de masa corporal, la

masa grasosa y el ngulo de fase estaban asociados con

el aumento de la gravedad de la enfermedad pulmonar

en 236 adultos VIH positivos, despus de un ajuste por

sexo, edad y carga viral plasmtica de VIH.

C O NCL US I N : La gravedad de la enfermedad pulmonar

en los adultos con tuberculosis pulmonar est asociada

al grado de malnutricin, tal como se refleja por los estu-

dios de composicin corporal, utilizando un anlisis de

impedancia biolctrica.

desnutrição e gravidade de pacientes com doenças hepáticasbom

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