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,3
*
SEAMEO-TROPMED Regional Center for Community Nutrition University of Indonesia, Indonesia;
**
Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH, Eschborn, Germany;
Department of General Internal Medicine, Faculty of Medicine, University of Indonesia, Indonesia;
Departments of General Internal Medicine and
Gastroenterology, University Medical Centre, Nijmegen, The Netherlands; and
Division of Human Nutrition and Epidemiology, Wageningen University, The Netherlands
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • malnutrition • tuberculosis • vitamin A • zinc • micronutrient • humans
|
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). In Indonesia, TB is one of the most
important public health problems with a prevalence of 0.29%, and 5.6%
of the world’s 7.5 million new cases of TB in 1990. TB ranks second
among the leading causes of death in Indonesia (Household Health Survey 1995
). Pulmonary TB, a chronic infectious disease caused
by Mycobacterium tuberculosis, is characterized by prolonged
cough, hemoptysis, chest pain and dyspnea. Systemic manifestations of
the disease include fever, malaise, anorexia, weight loss, weakness and
night sweats (Hopewell 1994
).
Although malnutrition has been described in TB patients previously
(Onwubalili 1988
, Saha and Rao 1989
,
Tsukaguchi et al. 1991
), contrary to what is commonly
believed, little is known about nutritional status with respect to the
micronutrients vitamin A, zinc and iron. Low concentrations of these
nutrients may affect host defense. Vitamin A deficiency was found to be
common among adults with TB and human immunodeficiency virus (HIV)
infection in Rwanda (Rwanganbwoba et al. 1998
). In the
prechemotherapeutic era, cod liver oil rich in vitamins A and D was
used regularly for the treatment of TB in an attempt to strengthen host
defenses (Goldberg 1946
). More recently, in vitro
studies have shown that retinoic acid can inhibit multiplication of
mycobacterium in macrophages (Crowle and Ross 1989
). In
addition, vitamin A has a vital role in lymphocyte proliferation and in
maintaining the function of epithelial tissues (Chandra 1991
). Zinc has been shown to be essential in vitamin A
metabolism because it is required to mobilize vitamin A from the liver
(Smith et al. 1973
). Zinc deficiency also affects host
defense in a variety of ways. It results in decreased phagocytosis and
leads to a reduced number of circulating T cells and reduced tuberculin
(purified protein derivative) reactivity, at least in animals
(McMurray et al. 1990
). Iron deficiency anemia has been
reported in patients with pulmonary TB, as indicated by low hemoglobin
concentrations, serum iron and total iron-binding capacity
(Saha and Rao 1989
), but how iron deficiency affects
host defense against M. tuberculosis is unclear.
Because of the limited data available on the relationship between nutritional status and TB, especially with respect to multiple micronutrient deficiencies, and because of the increasing incidence of TB, particularly in Southeast Asia, we decided to compare nutritional status of adult active pulmonary TB patients with that of matched healthy controls in Indonesia and investigate the concentrations of micronutrients in malnourished TB patients.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Cases were out-patients with untreated active pulmonary TB admitted
to the Rumah Sakit Umum Nasional Cipto Mangunkusumo, which is a major
general public hospital and the national referral hospital in Central
Jakarta, Indonesia. Controls were healthy subjects with no history of
pulmonary TB, matched with cases for sex and age, and selected randomly
from nonfamily neighbors of the patients in the smallest administrative
unit in Indonesia (rukun tetangga), usually comprising 
20 houses and
100 persons. Field workers asked the head of the administrative unit
(rukun tetangga) for a list of healthy subjects of the same sex and age
(within ± 2 y) as the patients. One person was selected at
random as a control from the list of 3–7 persons proposed. Selection
of cases was based on the following criteria: age 15–55 y; at least
two sputum specimens positive for acid-fast bacilli by microscopy;
and clinical and radiographic abnormalities consistent with pulmonary
TB. Exclusion criteria for cases and controls were as follows: previous
anti-TB treatment; pregnancy; lactation; use of corticosteroids or
supplements containing vitamin A, zinc or iron during the previous
month; moderate-to-severe injury or surgery during the last month; and
diseases such as abnormal liver function as measured by elevated serum
levels of aspartate amino transferase (ASAT) and alanine amino
transferase (ALAT), diabetes mellitus as measured by elevated fasting
blood glucose levels, neoplasm as determined by clinical examination,
chronic renal failure as determined by elevated serum levels of urea
and creatinine, and congestive heart failure.
Study design.
The study was designed as a case-control study. The sample size was
based on the ability to determine a difference with 
= 0.05 and
1-ß = 0.95 using a one-tailed test for concentrations of
serum retinol and zinc and of blood hemoglobin. Because serum zinc
concentration was the variable requiring the largest sample size, we
calculated that with a sample size of 35 in each group, a
between-group difference of 0.46 µmol/L in Zn
(Narang et al. 1995
) could be detected. We recruited 45
subjects for each group because we assumed that 25% of patients might
not meet the inclusion criteria.
Data collection.
Potential cases and controls were interviewed using a structured
questionnaire requesting information related to the inclusion and
exclusion criteria. Those apparently eligible were then screened
clinically including a chest X-ray by one of the coauthors (Z.A.),
a pulmonologist at the University Hospital Cipto Mangunkusumo, Medical
Faculty, University of Indonesia. All patients had evidence based on a
chest X-ray of lung infiltration indicating active TB at the time
of data collection. From those with evidence of TB, three specimens of
early morning sputum were examined by direct microscopy after
Kinyoun-Gabbett staining, which is a simplification of the
Ziehl-Nielsen method (Chadwick 1982
); specimens were
cultured in Kudoh medium (Chadwick 1982
).
Subjects were weighed without shoes using an electronic platform model
weighing scale (SECA 770 alpha; SECA, Hamburg, Germany) and weight
recorded to the nearest 0.1 kg; height was recorded to the nearest 0.1
cm using a microtoise. Body mass index (BMI) was calculated as body
weight divided by height squared (kg/m2). Subjects were
regarded as being malnourished if BMI < 18.5 kg/m2
(James et al. 1988
). Biceps, triceps, suprailiac and
subscapular skinfolds on the left side of the body were measured to the
nearest 0.2 mm three times at each site using a Holtain skinfold
caliper (Holtain, Crosswell, Crymych, Dyfed, UK) (Gibson 1990
). Calculations of proportion of total body fat and
fat-free mass were based on anthropometric data using the equations
of Durnin and Womersley (1974)
. Mid-upper arm
circumference was measured with a flexible steel tape (Gibson 1990
). Two field workers were trained and standardized by one
of the authors (E.K.) to take all of the anthropometric measurements.
At the end of the standardization period, the technical error of the
measurements was determined. The mean technical error, expressed as a
standard deviation (SD = d2/2n,
where d is the the difference between paired measurements and
n is the the number of subjects) was 0.13 cm for
mid-upper arm circumference, 0.35 mm for biceps skinfold, 0.22 mm
for triceps skinfold, 0.31 mm for subscapular skinfold and 0.26 mm for
suprailiac skinfold.
Blood samples (15 mL) were collected from fasting subjects via
venipuncture to determine total white blood cell count, hematocrit,
erythrocyte sedimentation rate (ESR), albumin and hemoglobin in blood,
zinc-protoporphyrin (ZPP) in erythrocytes, and to prepare plasma by
centrifugation at 750 x g for 10 min at room
temperature. All biochemical tests above were carried out on the same
day. Plasma was stored at -20°C until analysis of C-reactive
protein (CRP), retinol, -tocopherol and zinc. Hemoglobin
concentration, hematocrit, white blood cells, ASAT and ALAT were
measured directly using an automatic analyzer (Sysmex Microdilutor
F-800, Kobe, Japan). The intra- and interassay CV for hemoglobin were
<5%. ESR was determined directly using the Westergreen technique
(Kohli et al. 1975
). Albumin was determined by the
bromcresol green method (Dumas et al. 1997
). Hemoglobin,
hematocrit, white blood cells, ESR and albumin were analyzed in
Multilab Laboratory, Jakarta, which collaborates with the pulmonary
clinic. ZPP as a measure of free erythrocyte protoporphyrin was
measured in duplicate using the portable front-face
hematofluorometer (AVIV Biomedical, (Lakewood, NJ) at the
SEAMEO-TROPMED laboratory at the University of Indonesia
(Hastka et al. 1992
). Variability based on these
duplicate ZPP measurements was 1.6%. CRP was measured at the
University Medical Centre, Nijmegen, using an immunoturbidimetric
(Behringwerke, Marburg, West Germany) method (Metzmann 1985
). Variability based on analysis of 15 samples was 2.6%.
Plasma retinol and -tocopherol were measured using HPLC with a C-18
column (Bondapak, Waters, Milford, MA); a UV detector (model SPD-6AV,
Shimadzu, Tokyo); and methanol/water (95:5, v/v) as mobile phase at the
Nutrition Research and Development Center of the Department of Health
in Bogor, Indonesia (Arroyave et al. 1982
) using
standards from Sigma (St. Louis, MO). Plasma zinc was measured using
atomic absorption spectrometry (Prasad et al. 1965
) in
the laboratory of Clinical Chemistry and Hematology, University of
Bonn, Germany with values of a quality control analyzed with each set
of determinations within 3% of certified values.
Food intake was assessed on the basis of two consecutive 24-h recalls
(Bingham et al. 1988
) to estimate the intake of energy,
protein, fat, carbohydrate, vitamin A, zinc, iron and vitamin E. The
two recalls were conducted on two consecutive weekdays. The 24-h diet
recall was collected by two interviewers trained by one of the authors
(E.K.). Each 24-h recall was conducted using a standardized
four-stage protocol (Gibson 1993
). First, a complete
list of all food and beverages consumed during the previous day was
obtained. Second, detailed descriptions of all of the food and
beverages consumed, including the cooking methods and brand names were
recorded, together with the time and place of consumption. Third,
estimates of the amounts of all foods and beverages consumed were
recorded by referring to two- and three-dimensional models,
household measuring and serving utensils (e.g., spoons, plates or
cups), and food packages. Finally, the food recall was reviewed to
ensure that all items had been recorded correctly. Part of the training
session consisted of determining the differences between the amount
estimated by each trainee and the actual weight of the food. An
acceptable training level was considered to have been achieved when the
average difference between the trainee’s estimate and the actual food
weight was 
5 g. A pilot study was conducted by observing
five patients and five healthy subjects while they ate a meal; the next
day, a trained dietary interviewer had these subjects recall what and
how much they had eaten at that meal. In general, the subjects
accurately described what they had eaten. The calculation of nutrient
intake from dietary recalls was done using World Food (Version 2.0,
University of California, Berkeley CA), in which the Indonesian food
composition tables had been incorporated.
Ethical considerations.
The ethical guidelines of the Council for International Organizations of Medical Sciences (1991)
were followed and the
study was approved by the Committee on Health Research Ethics, Faculty
of Medicine, University of Indonesia, Jakarta. Informed consent was
obtained from each subject before the start of the study.
Statistical analysis.
A one-sample Kolmogorov-Smirnov test was used to check whether data
were normally distributed. Mean and standard deviation (SD)
are used for reporting normally distributed data, and median and
25th–75th percentiles are used for reporting nonnormally distributed
data. An independent sample t test was used to assess
the differences between patients and controls for normally distributed
parameters, whereas differences in nonnormally distributed parameters
were tested using the Mann-Whitney test. A multiple stepwise
regression analysis was performed to predict concentrations of plasma
retinol and zinc by using age, sex, BMI, body temperature, presence of
pulmonary cavity, white blood cell count, ESR and concentrations of
CRP, and albumin as independent variables. Differences in prevalence
were tested with a 
2 test. The SPSS software package
(Windows version 7.5.2, SPSS, Chicago, IL) was used for all statistical
analyses and a P-value < 0.05 was considered
significant.
|
RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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38°C) (54%), cough > 1 mo (93%), night
sweats (61%), hemoptysis (51%), dyspnea (68%), chest pain (63%) and
loss of appetite (76%). Of the cases, 26 (63%) had three positive
smears and a remaining 15 (37%) had two positive smears for
acid-fast bacilli, whereas 24 (59%) of cases had a positive sputum
culture. The radiographic signs of patients were as follows: all
patients had lung infiltration, 14 had pulmonary cavities, one had
miliary disease and one had pleural effusion. Because the prevalence of
HIV infection in this area was low (from the available data, possibly
<2%), no testing for HIV was carried out.
The mean BMI in all patients was 20% lower than in controls
(P < 0.001), and the mean proportion of fat in all
patients (17.7%) was lower than in controls (21.9%) (P
< 0.05). The number of patients with BMI < 18.5
kg/m2 (66%) was more than sixfold that of the
healthy controls (10%) (P < 0.001). The mean body
weight, BMI, skinfold thickness, mid-upper arm circumference,
proportion of fat, fat mass and fat free mass in male patients were
significantly lower than in male controls, whereas all of these
variables except biceps and suprailiac skinfold thickness were
significantly different between female patients and controls
(Table 1
). Serum albumin concentration was 10% lower in TB patients than in
controls (Fig. 1
). Serum albumin concentration was lower in malnourished TB patients
than in well-nourished healthy controls, malnourished healthy
controls and well-nourished TB patients (P < 0.05
for all comparisons) (Table 2
).
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and 11% lower median hematocrit (P
< 0.001). In malnourished TB patients, the mean concentrations of
hemoglobin were 16% lower than in well-nourished controls, and
11% lower than in malnourished controls (Table 2)
. The median CRP
concentration in TB patients was significantly higher than in controls
(Fig. 1)
. Of the TB patients, 24 had hemoglobin concentrations
indicating anemia, whereas only 9 controls had hemoglobin
concentrations below normal (Fig. 2
). The median concentrations of erythrocyte ZPP in TB patients were
significantly higher than in controls (P < 0.001) with
32 patients and 14 controls having concentrations above normal (>40
µmol/mol heme). The mean white blood cell count (8626
± 3207 vs. 6434 ± 1712 cells/mm3) and
the median ESR were significantly higher in patients (52, interquartile
range: 25–82 mm/h) than in controls (22, interquartile range: 12–31
mm/h) (P < 0.001 for both variables).
|
. If TB patients with
plasma CRP concentrations 10 mg/L are excluded, the proportion
with marginal vitamin A deficiency was 25%. No controls had elevated
plasma CRP levels. In malnourished TB patients, the mean plasma retinol
concentration was 32% lower than in well-nourished healthy
controls (P < 0.05), 27% lower than in
well-nourished TB patients and 18% lower than in malnourished
healthy controls (Table 2)
. Similarly plasma zinc concentrations in
patients were significantly lower than those in controls with eight
patients and two controls having plasma zinc concentrations < 10.7 µmol/L (Fig. 2)
. The mean plasma zinc concentration
in malnourished TB patients was 13% lower than in well-nourished
healthy controls (P < 0.05) and was 7% lower than in
well-nourished TB patients. Compared with malnourished healthy
controls, malnourished TB patients had 10% lower mean plasma zinc
concentration (Table 2)
. The mean plasma -tocopherol concentration
in patients was not significantly different from that in controls.
However, 16 patients and 10 controls had serum -tocopherol
concentrations below normal (<11.5 µmol/L) (Fig. 1)
. In a stepwise multiple regression analysis, plasma retinol concentration in patients was significantly associated with BMI (ß = 0.672, P = 0.008) and age (ß = -0.476, P = 0.032, R2 = 0.230 for both BMI and age). Sex, body temperature, presence of cavity, white blood cell count, ESR and concentrations of CRP and albumin were included in the model but did not contribute significantly to the prediction of plasma retinol concentration. Plasma zinc concentration was significantly associated with ESR (ß = -0.517, P = 0.005, R2 = 0.239), but not with CRP (ß = 0.015, P = 0.949) and the other factors mentioned above. ZPP concentration was not associated with CRP (ß = 0.090, P = 0.602) nor ESR (ß = 0.204, P = 0.249).
Intakes of energy, carbohydrate, fat, protein, vitamin A and iron tended to be lower (P = 0.20–0.93) in patients than in controls (data not shown).
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), India
(Saha and Rao 1989
) and Japan (Tsukaguchi et al. 1991
). As in our study, TB patients had significantly lower
BMI, skinfold thickness and serum albumin concentration than healthy
controls. Malnutrition per se had a more pronounced effect on serum
albumin concentration in TB patients. As a result, serum albumin
concentration in malnourished patients was lower than that in
well-nourished healthy controls, well-nourished patients and
malnourished healthy controls. Lower values of transthyretin
(previously referred to as prealbumin) and retinol-binding protein
were reported in the Indian and Japanese studies. The poorer
nutritional status of patients with pulmonary TB may be due to anorexia
(Hopewell 1994
), impaired absorption of nutrients or
increased catabolism. Energy and nutrient intake tended to be lower in
TB patients than in controls, but the differences were not significant.
Two 24-h recalls are not sufficient to determine whether patients have
a lower energy intake than controls (Bingham et al. 1988
). Because the number of subjects or number of days
required to obtain significant differences are much higher, it may be
preferable to use another method to determine food intake. On the other
hand, patients and controls may have similar food habits and food
intakes because their socioeconomic background and living conditions
are similar. Thus, infectious disease such as TB may led to impaired
absorption and increased rates of metabolism (Ginzburg and Dadamukhamedov 1990
, Ulijaszek 1997
). The
disease-induced production of cytokines such as interleukin-6 and
tumor necrosis factor- may induce fever, hepatic synthesis of acute
phase reactant proteins, inhibit production of serum albumin and cause
dramatic shifts in plasma concentration of certain essential
micronutrients (Beisel 1998
). TB is probably associated
with more severe malnutrition than other chronic illnesses; in the
Indian study referred to above (Saha and Rao 1989
), the
nutritional status of the patients with TB was worse than that of those
with leprosy.
Concentrations of selected micronutrients tested in our TB patients
were significantly lower than in controls. Low concentrations of
hemoglobin and of retinol and zinc in plasma in malnourished patients
were more pronounced than in healthy controls and well-nourished
patients. Furthermore, the prevalence of low concentrations of vitamin
A and zinc and of anemia was higher in patients than in controls. Low
concentrations of retinol in plasma can be due to a number of factors,
including reduced intake or reduced absorption of fat. In addition, the
infection itself can compromise vitamin A status in a number of ways.
It can increase urinary excretion of vitamin A as has been shown in
patients with fever, e.g., due to pneumonia and shigellosis
(Mitra et al. 1998b
, Stephensen et al. 1994
). During the acute phase response, leakage of
transthyretin (prealbumin) and albumin through the vascular endothelium
occurs, and production of retinol-binding protein and transthyretin
by the liver is reduced (Fleck and Myers 1985
). Finally,
low serum retinol levels can also result from increased utilization of
retinol by tissues (Fleck and Myers 1985
). It is likely
that a combination of mechanisms is operative in TB patients.
In our study, however, low plasma retinol concentration did not
correlate significantly with acute phase markers (CRP concentration and
ESR). By contrast, a study in children with shigellosis showed that the
serum concentration of CRP was negatively correlated with that of serum
retinol (Mitra et al. 1998a
). CRP is an acute
phase protein whose concentration changes rapidly as a result of
infection. Thus, CRP was probably not the best choice of protein to
control for the acute phase changes in plasma micronutrients during a
chronic illness such as TB. Therefore, it is not really surprising that
CRP did not correlate with micronutrient measures. In addition, this
finding may suggest that low plasma retinol is a result of a primary
deficiency.
Plasma zinc concentrations were significantly lower in TB patients than
in controls, in agreement with a study in India (Taneja 1990
). This was likely due to redistribution of zinc from
plasma to other tissues (Filteau and Tomkins 1994
) or
reduction of the hepatic production of the zinc-carrier protein
2-macroglobulin and to a rise in the
production of metallothionein, a protein that transports zinc to the
liver (Gabay and Kushner 1999
). This agrees with our
finding that ESR was negatively correlated with plasma zinc
concentration although not with CRP.
In TB patients in this study, concentrations of hemoglobin were
significantly lower and those of ZPP were significantly higher than in
controls. Elevated concentrations of ZPP, a measure of free erythrocyte
protoporphyrin, are indicative of iron-deficient erythropoiesis
(Hastka et al. 1992
). These results are not affected by
the acute phase response as shown here, i.e., ZPP did not significantly
correlate with CRP levels. Low iron status, as measured by low serum
iron concentrations and total iron-binding capacity, has also been
reported in pulmonary TB patients in England (Onwubalili 1988
). There are two explanations for the association of low
iron status with infection. One is that anemia results from chronic
infection. The other, which is more speculative, is that iron
deficiency would increase susceptibility to an infection such as TB. In
this context, it is relevant that cell-mediated immunity is
compromised in iron deficiency (Dallman 1987
) before
anemia becomes apparent.
In conclusion, this study shows that the nutritional status of patients with active pulmonary TB was poor compared with healthy controls. The prevalence of anemia and low concentrations of plasma retinol and zinc was significantly higher in patients than in controls. The low concentrations of hemoglobin, and of retinol and zinc in plasma were more pronounced in malnourished TB patients. Further studies are required to establish the role of these low concentrations in host defense against TB.
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FOOTNOTES |
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2 Current address: UNICEF Organization, 3 United
Nations Plaza, New York, NY.
4 Abbreviations used: ALAT, alanine amino
transferase; ASAT, aspartate amino transferase; BMI, body mass index;
CRP, C-reactive protein; ESR, erythrocyte sedimentation rate; HIV,
human immunodeficiency virus; TB, tuberculosis; ZPP,
zinc-protoporphyrin.
Manuscript received April 25, 2000. Initial review completed May 31, 2000. Revision accepted August 4, 2000.
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