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					Original Articles
VOLUME 16 NUMBER 2 MARCH/APRIL 2003


Role of pleural fluid cholesterol in differentiating transudative from exudative pleural
effusion:
R. Guleria, S. R. Agarwal, Sanjeev Sinha, J. N. Pande, Anoop Misra

ABSTRACT
Background. Pleural fluid cholesterol has been reported to be useful in distinguishing between
transudative and exudative pleural effusion. However, the difference in lipid profile between tubercular
and non-tubercular pleural effusion has not been studied.

Methods. The lipid profile of pleural fluid in 50 patients with exudative (25 tubercular and 25 non-
tubercular) and 25 with transudative effusion was studied. The diagnosis was based on clinical criteria
and/or a positive diagnosis from another site.

Results. The criteria that best identified an exudative pleural effusion were pleural fluid cholesterol ³60
mg/dl, pleural fluid to serum cholesterol ratio ³0.4, pleural fluid triglyceride ³40 mg/dl and pleural fluid
to serum triglyceride ratio ³0.3. Pleural fluid cholesterol had a sensitivity of 88% and a specificity of 100%
for exudates with an accuracy of 92%. Pleural fluid to serum cholesterol ratio had a sensitivity of 98% and
a specificity of 84%. These results were superior to the criteria proposed by Light et al. (sensitivity 98%
and specificity 80%).

Conclusion. Pleural fluid cholesterol estimation is an effective and cost-efficient method of
differentiating exudative from transudative pleural effusion. The lipid profile does not help in diagnosing
tubercular effusion.
Natl Med J India 2003;16:64–9

INTRODUCTION
Pleural effusion occurs in a number of pathological conditions and even exhaustive diagnostic tests fail to
reveal the aetiology in as many as 15%–20% of cases.1–3 The classification of pleural effusion as
transudative or exudative is the primary diagnostic step because, if the effusion is a transudate, no
further diagnostic procedures are necessary and therapy is directed towards the underlying disease
process. However, if the effusion is exudative a more extensive diagnostic work-up is required to
distinguish between the many possible causes of exudative effusion. In India, tubercular effusion is
common and may occur in a setting where the patient is predisposed to develop an effusion due to other
causes. The various criteria that have been employed include pleural fluid specific gravity, protein levels
and lactic dehydrogenase (LDH) levels.

In 1972, Light et al.4 compared various criteria for differentiating between transudative and exudative
pleural effusion and found none of them to be specific. They advocated the use of a combination of the
following criteria to differentiate between transudative and exudative pleural effusion with nearly 100%
sensitivity and specificity: pleural fluid protein to serum protein ratio >0.5; pleural fluid LDH >200 IU/L
and pleural fluid LDH to serum LDH ratio >0.6. However, several prospective studies5–8 were unable to
reproduce the results obtained by Light et al.4 In most of these studies, Light’s criteria had a >95%
sensitivity for exudates but the specificity was <78%.
Various causes may be responsible for the presence of cholesterol in the pleural effusion.9–11 However,
till recently, the cholesterol content of pleural fluid had been used along with the concentration of other
lipid fractions to distinguish between chylothorax and pseudochylothorax.12,13 No systematic study had
been done of the cholesterol level in pleural effusion due to various causes till recently. Few studies have
now shown that pleural fluid cholesterol levels differ significantly in transudative and exudative pleural
effusion.5,6,14–16 These studies have shown a high sensitivity and specificity for pleural fluid cholesterol
levels to differentiate between transudative and exudative effusion. We aimed to use the criteria of
pleural fluid cholesterol levels to distinguish between transudative and exudative pleural effusion and
also to assess possible diagnostic differences in the lipid profile of effusion due to tubercular and other
causes.

PATIENTS AND METHODS
Two gold standards were used for classifying a pleural effusion as transudative or exudative. One was
Light’s criteria, i.e. pleural fluid LDH >200 IU/L, pleural fluid to serum LDH ratio >0.6 and pleural fluid
protein to serum protein ratio >0.5.
The presence of any one of the three criteria established that the pleural fluid was exudative while the
diagnosis of transudative effusion was made in the absence of all three criteria.
The other gold standard was clinical criteria by which a patient was classified as having a transudative
effusion if he had a clinical condition that could give rise to a transudative effusion such as congestive
heart failure, cirrhosis of the liver or nephrotic syndrome, with a response to treatment of the underlying
condition and absence of any other condition which could give rise to a pleural effusion. Patients were
classified as having an exudative effusion if they fulfilled the criteria for diagnosis of tubercular,
malignant or parapneumonic effusion.

Patient selection
Fifty patients with exudative (25 tubercular and 25 due to malignancy and other causes) and 25 with
transudative pleural effusion were studied. All of them were outpatients or inpatients attending the
Department of Medicine at our institution. A detailed history, physical examination and chest X-ray were
done. The patients satisfying the following criteria were included in the study: age >15 years, clinically
and radiologically demonstrable moderate-to-large pleural effusion, and willingness to participate in the
study. The exclusion criteria were history of previous thoracocentesis and a bleeding diathesis. Patients
on diuretics for their underlying disease in the group of transudative effusion were not excluded from the
study.

Diagnostic criteria
Patients were divided into three groups: (i) tuberculous exudate, (ii) malignant exudate and exudate due
to other causes; and (iii) transudate as in congestive heart failure, nephrotic syndrome, cirrhosis of the
liver, etc. A tubercular effusion was diagnosed if all the following clinical criteria were present:

    1.   Fever, cough, pleuritic pain, malaise, anorexia, toxaemia, etc. compatible with a clinical
         diagnosis of tuberculous pleural effusion;
    2.   Exudative pleural effusion with predominantly lymphocytic pleocytosis and a few mesothelial
         cells;
    3.   Response to antitubercular therapy.

Patients who had granulomas on pleural biopsy or those in whom mycobacteria were isolated from the
pleural fluid, pleural biopsy or any other clinical specimen by smear and/or culture were diagnosed to
have tuberculous pleural effusion even if they did not fulfil any of the clinical criteria outlined above.

A malignant pleural effusion was diagnosed if one of the following criteria were fulfilled:

    1.   Demonstration of malignant cells on cytological examination of the pleural fluid;
    2.   Demonstration of malignant tissue in a pleural biopsy specimen;
    3.   Histologically proven primary malignancy with exclusion of any other cause known to be
         associated with pleural effusion.
         Congestive heart failure was diagnosed by an enlarged heart, pulmonary venous congestion on
         chest X-ray, peripheral oedema, response to treatment of heart failure and absence of
         malignancy or pulmonary infiltrate associated with an inflammatory process. Nephrotic syndrome
         was diagnosed when the patient had proteinuria >3.5 g/m2/day, hypoalbuminaemia and oedema.
         Cirrhosis of the liver was diagnosed if there was evidence of portal hypertension in the absence
         of heart failure, malignancy or pulmonary infiltrates, and response to diuretic treatment.

Investigations
A haemoglobin estimation, a total and differential leucocyte count, erythrocyte sedimentation rate (ESR)
and a Mantoux test with 1 TU PPD were done for all patients. The Mantoux test was considered positive if
the induration was >10 mm after 48–72 hours. Sputum was evaluated for mycobacteria by Ziehl–Neelsen
staining and culture on Lowenstein–Jensen medium for 8 weeks whenever an acceptable sample could be
obtained. In addition, a pleural biopsy was done wherever indicated and if consent was obtained.

Samples of venous blood and pleural fluid were obtained at almost the same time. Pleural fluid obtained
during thoracocentesis was sent for the following investigations: sugar, protein and LDH, red and white
blood cell counts including differential leucocyte count, lipid profile including total cholesterol, high
density lipoprotein (HDL) cholesterol, low density lipoprotein (LDL) cholesterol and triglyceride levels.
Pleural fluid was also investigated for mycobacteria by Ziehl–Neelsen staining and culture on Lowenstein–
Jensen medium and, cytopathological examination for cell type and any malignant cells. Closed pleural
biopsy was done by Cope’s needle.17 Patients with tubercular pleural effusion were treated with standard
chemotherapy and followed up regularly. Response to antitubercular treatment was defined as favourable
if the chest X-ray showed complete resolution of the pleural effusion or residual pleural thickening and
the patient felt better symptomatically. Patients with a pleural fluid cytology positive for malignancy
were subsequently treated at the oncology centre.

Statistical analysis
The cut-off points for tests being evaluated as well as cut-off points for traditional tests that would best
discriminate between transudative and exudative pleural effusion were chosen by drawing receiver
operator characteristics (ROC) curves wherein the sensitivity was plotted against 1–specificity.

The usefulness of each of the biochemical parameters for identifying exudates was evaluated using
Bayesian methods to measure the following: sensitivity, specificity and diagnostic accuracy. As
transudates and exudates are complementary for a given analytical parameter, the specificity for
exudates corresponds to the sensitivity for transudates. Therefore, we used specificity and sensitivity in
relation to the exudates in our study results. The statistical significance of differences between means
was estimated by Student’s t test and Wilcoxon rank-sum test. A p value <0.05 was considered significant.

RESULTS
The mean (SD) age of the patients with transudative effusion was 40 (15.9) years and of those with
exudative pleural effusion was 43.5 (17.5) years. The difference in age was significant between the non-
tubercular exudate and the 2 other groups, but not between those with transudative and exudative
effusion. There were 19 men and 6 women with transudative effusion.
Among the transudative effusions, 11 (44%) were bilateral, 11 (44%) right-sided and 3 (12%) left-sided. In
patients with tubercular effusion, the effusion was right-sided in 16 patients (64%) and left-sided in 9
(36%). In the group with non-tubercular exudate the effusions were left-sided in 13 (52%) and right-sided
in 12 patients (48%). Mantoux test was positive in 35% of patients with transudative effusion, 76% with
tubercular effusion and 44% with non-tubercular exudative effusion.

Pleural fluid cytology
Two patients (8%) with tubercular effusion had haemorrhagic fluid compared to 19 of 22 (86.4%) with
malignant pleural effusion. One patient with transudative effusion had haemorrhagic pleural fluid.
Cytological evaluation detected a malignant effusion in 8 of 22 patients (36.4%). The mean leucocyte
count in transudative effusion was 613 cells/cmm. The mean (SD) leucocyte count in patients with
tubercular effusion was 2256 (1946) cells/cmm compared to 1597 (2072) cells/cmm in non-tubercular
exudative effusion (p<0.001).

Pleural biopsy
A closed pleural biopsy was done in 13 of 25 patients with tubercular pleural effusion, and granulomas
were demonstrated in 9 of these (69.3%). Other patients had non-specific changes, not diagnostic or
suggestive of any particular disease state. A biopsy was also done in 12 of 25 patients with non-tubercular
effusion, and a diagnosis was established in 10 (83.3%). No acid-fast bacilli (AFB) were demonstrated by
Ziehl–Neelsen staining in the pleural fluid or biopsy specimens in any of the patients with tuberculous or
non-tuberculous pleural effusion. Mycobacteria were not cultured from the pleural fluid or pleural biopsy
specimen in any patient.

Pleural fluid analysis
Table I shows the results of the pleural fluid analysis and Table II shows the sensitivity, specificity and
accuracy of these.

Total leucocyte count of pleural fluid
Using a cut-off of 1000 cells/cmm, 24 of 25 transudates were correctly classified (specificity 96%) while
24 of 50 exudative effusions were misclassified (sensitivity 52%). At a cut-off of 2500 cells/cmm, the
specificity remained the same but sensitivity decreased to 28%.

Pleural fluid protein
Using a cut-off of 3 g/dl to separate transudates from exudates, 68 of 75 patients with pleural effusion
were correctly classified (accuracy 90.7%), 5 of 50 exudates were misclassified (sensitivity 90%) and 2 of
25 transudates were misclassified (specificity 92%). Among the misclassified exudates, 1 was tubercular
and 4 were malignant.
Ratio of pleural fluid protein to serum protein
Using 0.5 as the cut-off, 60 of 75 patients were correctly classified (accuracy 80%), 21 of 25 transudates
were correctly classified (specificity 84%) and 11 of 50 exudates were misclassified (sensitivity 78%).
Among the misclassified exudates, 6 were tubercular and 5 were malignant effusions.

Pleural fluid LDH
Using 200 IU as the cut-off, 64 of 75 patients were classified correctly (accuracy 85.3%). Only 1 of 25
transudates was misclassified (specificity 96%), while 10 of 50 exudates were misclassified (sensitivity
80%). Eight of the misclassified exudates were tubercular and 2 were malignant.


Table I. Mean (SD) and range of tests done in different types of effusions

Test                                        Transudates (n=25)                           Exudates (n=50)

                                         Mean (SD)              Range            Mean (SD)             Range

Total leucocyte count (per              287.8 (612.6)           0–3000         1926.4 (2016.9)         10–8000
cmm)

Pleural fluid protein (g/dl)             1.67 (1.25)          0.08–0.25           4.66 (1.2)           2.6–8.5

Pleural fluid to serum                   0.28 (0.18)           0.01–0.6          0.66 (0.18)          0.35–1.27
protein ratio

Pleural fluid LDH (IU/L)                 63.2 (39.5)            12–208         396.38 (419.2)         138–2460

Pleural fluid to serum LDH               0.36 (0.3)            0.05–1.4           1.68 (1.7)           0.51–9
ratio

Pleural fluid cholesterol                41.7 (13.2)             8–58           98.70 (31.8)           42–184
(mg/dl)

Pleural fluid to serum                   0.28 (0.1)            0.1–0.54           0.64 (0.2)          0.35–1.4
cholesterol ratio

Pleural fluid triglyceride               15.52 (7.5)             5–35           54.36 (23.4)           15–120
(mg/dl)

Pleural fluid to serum                   0.14 (0.06)          0.14–0.06          0.45 (0.17)          0.11–0.8
triglyceride ratio

LDH lactic dehydrogenase All the tests showed a statistically significant (p<0.001) difference between
transudates and exudates


Table II. Sensitivity, specificity, accuracy and area under the curve for tests studied, using clinical criteria
as the gold standard

Criteria                                  Sensitivity (%)   Specificity (%)   Accuracy (%)     Area under the
                                                                                               curve

Pleural fluid protein (g/dl)*                   90                92              90.7              0.8488

Pleural fluid to serum protein ratio*           78                84               80                09116

Pleural fluid LDH (IU/L)*                       80                96              85.3               09904

Pleural fluid to serum LDH ratio*               96                88              93.3              0.9744

Light’s criteria                                98                80               92                  –

Pleural fluid cholesterol (mg/dl)†              88               100               92               0.9752
Pleural fluid to serum cholesterol             98               84              93.3           0.9660
ratio†

Pleural fluid triglycerides (mg/dl)†           84               96               88            0.9620

Pleural fluid to serum triglycerides           86               96              89.3           0.9560
ratio†

LDH lactic dehydrogenase *classical cut-off †cut-off that gave the best discriminant value in this study


Table III. Sensitivity, specificity and accuracy of different criteria used in combination

Criteria                                                    Sensitivity       Specificity      Accuracy

Pleural fluid cholesterol

or pleural fluid protein                                        100               92             97.3

and pleural fluid protein                                        78               100            85.3

or pleural fluid to serum protein ratio                          98               96             97.3

and pleural fluid to serum protein ratio                         62               100            74.7

or pleural fluid LDH                                             88               96             97.3

and pleural fluid LDH                                            88               100            92.0

or pleural fluid to serum LDH ratio                             100               96             98.7

and pleural fluid to serum LDH ratio                             80               100            86.7

or pleural fluid to serum cholesterol ratio                      98               84             93.3

and pleural fluid to serum cholesterol ratio                     88               100            92.0

Pleural fluid to serum cholesterol ratio

or pleural fluid protein                                        100               80             93.3

and pleural fluid protein                                        88               96             90.7

or pleural fluid to serum protein ratio                         100               80             93.3

and pleural fluid to serum protein ratio                         70               100            80.0

or pleural fluid LDH                                            100               80             93.3

and pleural fluid LDH                                            98               100            98.7

or pleural fluid to serum LDH ratio                             100               80             93.3

and pleural fluid to serum LDH ratio                             90               100            93.3

Pleural fluid protein

or pleural fluid to serum protein ratio                          90               80             86.7

and pleural fluid to serum protein ratio                         72               96              80

or pleural fluid LDH                                            100               92             97.3

and pleural fluid LDH                                            90               100            93.3

or pleural fluid to serum LDH ratio                             100               88              96
and pleural fluid to serum LDH ratio                             82               100                88

Pleural fluid to serum protein ratio

or pleural fluid LDH                                            100               92                97.3

and pleural fluid LDH                                            72               100               81.3

or pleural fluid to serum LDH ratio                              98               92                 96

and pleural fluid to serum LDH ratio                             68               100               78.7

Pleural fluid LDH

or pleural fluid to serum LDH ratio                             100               96                98.7

and pleural fluid to serum LDH ratio                             92               96                93.3

LDH lactic dehydrogenase All values are percentages


Ratio of pleural fluid LDH to serum LDH
Using a cut-off of 0.6 for pleural fluid to serum LDH ratio, 70 of 75 patients were correctly classified
(accuracy 93.3%), 3 of 25 transudates were misclassified as exudates (specificity 88%) and 2 of 50
exudates were misclassified and both were tubercular.
The cut-off points which showed the best discriminant value in our study were:
Pleural fluid protein 3 g/dl
Pleural fluid to serum protein ratio 0.6
Pleural fluid LDH 135 IU/L
Pleural fluid to serum LDH ratio 0.7
Pleural fluid cholesterol 60 mg/dl
Pleural fluid to serum cholesterol ratio 0.4
Pleural fluid triglyceride 40 mg/dl
Pleural fluid to serum triglyceride ratio 0.3
Using these cut-offs, the sensitivity and specificity of each parameter for exudates was the same as the
sensitivity and specificity of different parameters using the cut-offs suggested by Light et al.4 Using a
combination of our criteria and those of Light et al., an exudate could be classified either if one of the
two criteria were met or if both criteria were fulfilled. The sensitivity and specificity for exudates, if the
above-mentioned combinations were applied, are shown in Table III. Using Light’s criteria as the gold
standard for classifying pleural effusions into transudative and exudative, our study had 54 exudates and
21 transudates. The sensitivity, specificity and accuracy of lipid parameters, using Light’s criteria as the
gold standard, are shown in Table IV.

DISCUSSION
The first step in determining the aetiology of a pleural effusion should be to find out whether it is a
transudate or an exudate. No single test or series of tests has yet proved to be completely reliable.
Several criteria have been proposed5–8 and one of these—pleural fluid cholesterol—seems to have a higher
diagnostic accuracy for identifying transudates. This study was designed to assess the utility of pleural
fluid concentrations of cholesterol in comparison to the traditional criteria of Light et a1.4 and its
individual parameters (pleural fluid LDH concentration, pleural fluid to serum LDH ratio, and pleural fluid
to serum protein ratio) to distinguish between exudates and transudates. We also looked for differences
in the lipid profile, if any, between tuberculous and non-tuberculous exudative effusions.


Table IV. Sensitivity, specificity and accuracy of lipid parameters using Light’s criteria as the gold
standard

Criteria                                                       Sensitivity       Specificity       Accuracy
                                                                  (%)               (%)               (%)

Pleural fluid cholesterol                                         80.0              95.2             84.0

Pleural fluid to serum cholesterol ratio                          92.6              80.9             89.3
Pleural fluid triglyceride                                        70.4              100              78.7

Pleural fluid to serum triglyceride                               81.5              100              86.7


Light et a1.4 used pleural fluid and serum levels of protein and LDH to establish criteria for
differentiating transudates from exudates with a sensitivity and specificity of near 100%. This high
diagnostic accuracy made the criteria of Light et a1.4 the ‘gold standard’ for initial categorization of
pleural effusion. However, Light’s criteria require 4 biochemical estimations which, in developing
countries such as India, may not be feasible in every patient due to economic constraints. Also, several
prospective studies5–8 were unable to reproduce the results obtained by Light et al. In our study, Light’s
criteria had a sensitivity of 98% but the specificity for exudates was only 80%.
For pleural fluid cholesterol, pleural fluid to serum cholesterol ratio, pleural fluid triglycerides, and
pleural fluid to serum trigly-ceride ratio, we determined the level which best discriminated transudative
from exudative pleural effusion.
All transudates had pleural cholesterol levels <60 mg/dl, a cut-off which misclassified 16% of tubercular
and 8% of non-tubercular exudates. Using this cut-off (60 mg/dl), pleural fluid cholesterol had a
sensitivity of 88% and specificity of 100% for exudates, with an accuracy of 92%. The results of our study
are comparable to the studies by Hamm et al.,5 Valdes et al.6 and Kalayci et al.18
We found that pleural fluid cholesterol, pleural fluid to serum cholesterol ratio, pleural fluid to serum
LDH ratio and the criteria of Light et al.4 had almost the same accuracy, but pleural fluid cholesterol had
the highest specificity. Pleural fluid LDH had the highest area under the curve followed by pleural fluid
cholesterol. Therefore, in clinical settings with a high prevalence of transudative effusion or where
patients clinically appear to have congestive heart failure (the criteria of Light et al.4 would classify
these as exudates), the measurement of pleural fluid cholesterol can be useful. The use of pleural fluid to
serum cholesterol ratio did not improve the accuracy of pleural fluid cholesterol estimation alone.
Romero et al.19 found pleural fluid LDH to have the highest specificity (95%), being significantly higher
than the Light criteria (p<0.05). They found the criteria of Light et al. and pleural fluid LDH-cholesterol to
be equally effective in differentiating exudates from transudates. A similar finding has been reported by
Costa et al.20 In previous studies, pleural fluid triglyceride has not been evaluated. The use of pleural
fluid triglyceride and pleural fluid to serum triglyceride ratio in our study had a high specificity (96%) with
an accuracy lower than that of pleural cholesterol.
Given the variability of results from one laboratory to another, defining the cut-off levels for a particular
laboratory may improve the specificity of the test without a loss in its sensitivity. This was the case in our
study.
It is evident from the comparative results of the classical and modified criteria depicted that the
accuracy of pleural fluid to serum protein ratio and pleural fluid to serum LDH ratio remains the same but
the specificity increased from 84% to 96%, and 88% to 96%, respectively. While the specificity remains the
same by modifying the criteria of pleural fluid LDH, the sensitivity and accuracy improves significantly.
Using Light’s criteria with modified cut-off points yielded an accuracy of 97.3% with a specificity of 92% in
comparison to an accuracy of 92% and specificity of 80% using the classical criteria.
We also evaluated a combination of Light’s criteria and our criteria in two ways:

    1.   Exudate is defined if any of the two criteria used in combination is fulfilled.
    2.   Exudate is defined if both criteria are fulfilled.
         The use of a combination of the two criteria gives a better sensitivity and specificity for
         exudates than either used alone.
         Using modified cut-off points, pleural fluid to serum cholesterol ratio and pleural fluid LDH used
         in combination, when both of them are required to define exudates, provide the best
         discrimination with an accuracy of 98.7% and specificity of 100% (Table III). Almost equivalent
         results with an accuracy of 98.7% and specificity of 96% are obtained on using either pleural fluid
         cholesterol and pleural fluid to serum LDH ratio in combination or pleural fluid LDH and pleural
         fluid to serum LDH ratio in combination when one of the two criteria is required to define an
         exudate. Therefore, in our study estimation of cholesterol and LDH in pleural fluid and serum
         gave an almost 100% sensitivity and specificity when used in various combinations, which is much
         higher than that obtained with the use of pleural fluid and serum protein and LDH as proposed by
         Light et al.4
         Using Light’s criteria4 as the gold standard, 54 patients were classified as having exudative
         effusion and 21 as having transudative effusion. Using a cut-off level of 60 mg/dl for pleural fluid
         cholesterol concentration, 84% of pleural effusions could be correctly classified with a specificity
         of 95.2% for exudates (Table IV). Use of pleural fluid to serum cholesterol ratio improved the
          accuracy to 89.3% but at the cost of lowering the specificity to 80.9%. Use of pleural fluid
          triglyceride and pleural fluid to serum triglyceride ratio yielded a specificity of 100% but
          accuracy of 78.7% and 86.7%, respectively. Therefore, among the lipid parameters, pleural fluid
          to serum triglyceride ratio appears to be the best with a specificity of 100% for exudates,
          misclassifying only 13% of pleural effusions. Using both pleural fluid cholesterol and pleural fluid
          to serum cholesterol ratio does not improve the discrimination significantly. Of the various
          combinations of lipid parameters, the use of pleural fluid cholesterol and pleural fluid to serum
          triglyceride ratio improves the accuracy to 90.7%, maintaining a specificity 95.2% for exudates
          (Table IV).

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All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India
R. Guleria, S. R. Agarwal, Sanjeev Sinha, J. N. Pande, Anoop Misra Department of Medicine
Correspondence to R. Guleria; randeepg@hotmail.com

				
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