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(Chest. 2002;122:1285-1291.)
© 2002 American College of Chest Physicians

Shifts of T4/T8 T Lymphocytes From BAL Fluid and Peripheral Blood by Clinical Grade in Patients With Pulmonary Tuberculosis*

Thomas C. Y. Tsao, MD, FCCP; Chi-Hong Chen, MD; Ji-hong Hong, MD, PhD; Meng-Jer Hsieh, MD; Kou-Ching Tsao, MSc and Cheng-Hei Lee, MD

* From the Division of Pulmonary and Critical Care Medicine (Drs. Tsao, Chen, Hong, Hsieh, and Lee), and Department of Clinical Pathology (Mr. Tsao), Chang Gung Memorial Hospital, Taipei, Taiwan.

Correspondence to: Thomas C. Y. Tsao, MD, FCCP, Division of Pulmonary and Critical Care Medicine, Chang Gung Memorial Hospital, 199 Tun-Hwa North Rd, Taipei, Taiwan; e-mail: drtsao{at}cgmh.org.tw


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objectives: We investigated the shifts of T4/T8 lymphocytes from BAL fluid (BALF) and peripheral blood by the clinical grade of pulmonary tuberculosis (TB), which is determined by factors such as extent of pulmonary involvement, fever, and loss of body weight.

Materials and methods: In order to explore these questions, BALF was collected from 45 patients presenting with active pulmonary TB and 14 healthy control subjects. The percentages for T-lymphocyte subpopulations, including CD4+, CD8+, and CD3+ T cells, were measured using two-color flow cytometry.

Results: A higher percentage of CD3+CD4+ T lymphocytes, with a relatively lower percentage of CD3+CD8+ T lymphocytes, was revealed for the patients with a higher grade of pulmonary TB, compared to patients with a lower grade of pulmonary TB, resulting in an increased BALF C4+/CD8+ ratio. By contrast, a higher percentage of CD3+CD8+ T lymphocytes with a relatively low percentage of CD3+CD4+ T lymphocytes was demonstrated for these patients with a higher grade of pulmonary TB, resulting in a decreased peripheral blood CD4+/CD8+ ratio.

Conclusions: Our findings suggest that compartmentalization of the CD4+ T lymphocytes in the infected lungs may occur for patients with higher grades of pulmonary TB.

Key Words: BAL fluid • pulmonary tuberculosis • T-lymphocyte subpopulation


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The clinical manifestations for pulmonary tuberculosis (TB) are determined by host immune factors in response to mycobacterial infection. T cell-mediated immunity, especially from CD4+ T-lymphocyte function, plays an important role in eliminating mycobacteria.1 2 3 In advanced or disseminated TB, numbers of circulating T lymphocytes (especially CD4+ cells) are reduced, while numbers of CD8+ cells are increased.4 5 6 We have previously reported increased lymphocyte and neutrophil percentages for BAL fluid (BALF) from patients with active pulmonary TB.7 There have been relatively few reports, however, investigating T-lymphocyte subpopulations for BALF from infected lungs, and the results were contradictory due to different patient populations.

For patients with active pulmonary TB, the TB bacilli infect and invade cells in the bronchiolar and alveolar lining. Therefore, bronchoalveolar T lymphocytes and their subpopulations may reflect the clinical course manifested as extent of pulmonary involvement, fever, and/or loss of body weight. Also, in patients with higher grades of pulmonary TB, more CD4+ T lymphocytes may be trapped in the infected lungs, reflecting a decreased circulating CD4+ T lymphocytes. In order to address these questions, BALF was collected from 45 patients with active pulmonary TB and 14 healthy subjects. T lymphocytes and their subpopulation percentages, including those for CD4+ and CD8+ T cells, were analyzed.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Selection
We studied 45 patients with active pulmonary TB and admitted to Chang Gung Memorial Hospital in Taipei, a university medical center. Thirty-one patients were men and 14 patients were women (mean ± SEM age, 51 ± 6 years; range, 21 to 77 years). Pulmonary TB was diagnosed by clinical presentations using chest radiographs, clinical manifestations, a minimum of one positive sputum smear result for acid-fast bacilli, and a positive sputum culture result for Mycobacterium tuberculosis. Accompanying miliary or extrapulmonary involvement was not found for any patients, nor was immunocompromised status as a result of infections such as HIV or immunosuppressant therapy. HIV infection was ruled out in all patients by lack of risk factors and negative serologic examination findings. Fourteen healthy volunteers, including 10 male and 4 female subjects, were included as control subjects (with normal chest radiographic findings, no disease symptoms, and not receiving medication).

Clinical Grading of Patients
To evaluate correlation for T-lymphocyte subpopulation percentages and clinical grading, TB patients were classified according to the extent of pulmonary involvement, presence of fever, and loss of body weight. Textbook grading for pulmonary involvement was adopted for disease assessment8 :

Grade 1, Minimal Lesions: Minimal lesions, including those of slight-to-moderate density not containing demonstrable cavitation. These may involve a small part of one or both lungs; however, the total extent, regardless of distribution, should not exceed the lung volume on one side above the second chondrosternal junction and the spine of the fourth or the fifth thoracic body.

Grade 2, Moderately Advanced Lesions: Moderately advanced lesions may be present in one or both lungs, but the total extent should not exceed the following limits: disseminated lesions of slight-to-moderate density that may extend throughout the total volume of one lung, or an equivalent in both lungs; dense and confluent lesions limited in extent to one third the volume of one lung; total diameter of cavitation, if present, must be < 4 cm.

Grade 3, Far-Advanced Lesions: Lesions are more extensive than lesions in grade 2.

All patients underwent plain posteroanterior and lateral chest radiography. Twenty-five patients of uncertain classification for pulmonary involvement underwent chest CT scans to obtain a clearer image. Fever was diagnosed where core body temperature was > 37.5°C, with loss of body weight confirmed by the patient. To avoid observer bias, radiographs and clinical course were assessed independently, in the first instance, by two pulmonary physicians prior to laboratory study to ensure objective and consistent evaluation.

Bronchoscopy and BAL
Bronchoscopy with BAL was performed as has been described in our previous studies.9 10 In brief, patients were pretreated with codeine phosphate, 5 mg IM, 30 min prior to the procedure, with midazolam, 2 to 3 mg IV, slowly, administered to some patients for anxiety. We used an Olympus 5.0-mm fiberoptic bronchoscope (Olympus; Tokyo, Japan), wedging it into the fourth or fifth subsegmental bronchus of patients anesthetized with a local spray of lidocaine. Lavage was performed using 50-mL aliquots of warmed normal saline solution introduced by syringe through the bronchoscopic aspiration port. Taking into account the dilution effect of the cytokines and their receptors in the BALF, a fixed volume of 300 mL of saline solution was infused sequentially. The return fluid was extracted through the same syringe. Individuals who could not tolerate the entire procedure or whose returned fluid was < 40% of the total infused volume were excluded. The BAL was performed for the involved bronchi (determined radiographically) within the first 3 days of antituberculous chemotherapy for 26 patients, within 5 days for 14 patients, and within 7 days for 5 patients. All returned fluid was filtered through four sterile layers of gauze, and then pooled and chilled immediately for cell counts and further isolation. The total cell count was evaluated on an aliquot of the pooled fluid using a hemocytometer. Differential cell counts were performed using a cytocentrifuge preparation with modified Wright-Giemsa staining. Cell viability was determined by trypan blue exclusion, and recovered cells were > 90% viable in all cases.

Cell Preparation
Cell pellets obtained from the BALF were resuspended in phosphate-buffered saline solution (PBS), and then spun in a density gradient Ficoll column after loading Histopaque (Sigma Chemical; St. Louis, MO) into the bottom of the tube. Interfaced cells were harvested and washed in PBS, then resuspended in RPM1–1640 medium containing 200 U/mL penicillin G, 200 µg/mL streptomycin, and 10% human AB serum (complete medium) at a concentration of 1 x 106 cells/mL. Alveolar macrophages were removed by adherence to Petri dishes after incubation for 30 min in a humidified incubator with 95% air and 5% CO2 at 37°C. The nonadherent cells were harvested by washing the dishes with warm medium three times followed by passage through nylon wool columns. The cells (> 95% CD3+ lymphocytes by cytofluorometry) were then ready for further immunofluorescent staining and flow cytometry. Peripheral blood mononuclear cells were isolated by layering the whole blood on Histopaque, and spinning at 400g for 30 min. Interfaced cells were harvested and then resuspended in PBS. The cells were then ready for immunofluorescent staining and flow cytometry.

Determination of T-Lymphocyte Surface Phenotype
To determine the T-lymphocyte phenotype, we employed immunofluorescent staining and flow cytometry. Cells prepared from BALF and peripheral blood were stained immediately using two-color direct fluorescence, as has been previously described.7 11 The following monoclonal antibodies, recognizing different cell surface receptors, were used: Leu-4 (anti-CD3), in the fluorescein isothiocyanate-conjugated form; Leu-3a (anti-CD4); Leu-2a (anti-CD8); and anti-IL2R (anti-CD25, recognizing very recently activated T-lymphocytes) in the phycoerythrin-conjugated form (Becton Dickinson; San Jose, CA). Immunofluorescence was analyzed using a fluorescence-activated cell sorter system (FACSort; Becton Dickinson). The CD3-, CD4-, CD8-, and CD25-positive T lymphocytes were identified in four quadrants by gating on lymphocytes using low forward angle and 90° light-scatter profiles in the flow cytometry analysis, as previously described. The proportion of positive cells was calculated by subtracting the background control value. The number of cells stained with control antibodies was < 1% for all cases.

Statistics
Values are expressed as median (range) or mean ± SEM. All data were compared using the nonparametric Mann-Whitney U Wilcoxon rank-sum W test, and the correlation analysis was performed using the nonparametric Spearman test. The null hypothesis was rejected at p < 0.05.12


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Clinical Grading of Patients
A total of 45 patients presented with active pulmonary TB, with pulmonary involvement assessed as minimal for 16 patients, moderately advanced for 15 patients, and far advanced for 14 patients. Of these patients, 25 patients presented with fever (7 patients with far-advanced pulmonary involvement, 10 patients with moderate pulmonary involvement, and 8 patients with minimal pulmonary involvement) and 14 patients reported loss of body weight (6 patients with far-advanced pulmonary involvement, 5 patients with moderate pulmonary involvement, and 3 patients with minimal pulmonary involvement).

Differential Cells Recovered From BALF
Tables 1 , 2 present the BALF differential cell count according to clinical grading. Increased lymphocyte and neutrophil percentages and decreased macrophage percentage were demonstrated for BALF from higher grade of pulmonary TB.


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  		Table 1.. BALF Differential Cell Counts From TB Patients by the Extent of Pulmonary Involvement*

 

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  		Table 2.. BALF Differential Cell Counts From Patients With Active Pulmonary TB by the Presence of Fever and Loss of Body Weight*

 
Correlation for Clinical Grade and Lymphocyte Subpopulations
Figure 1 presents CD4+ T-lymphocyte percentages for BALF and peripheral blood in healthy subjects and according to clinical grading. Significantly higher BALF CD3+CD4+ T-lymphocyte percentages were revealed for patients with far-advanced pulmonary involvement and presenting with fever or loss of body weight. By contrast, significantly lower percentages for peripheral blood CD3+CD4+ T lymphocytes were demonstrated for patients exhibiting far-advanced pulmonary involvement or loss of body weight. Figure 2 presents the CD8+ T-lymphocyte percentage in BALF and peripheral blood. Significantly lower percentages for BALF CD3+CD8+ T lymphocytes were revealed for patients with far-advanced pulmonary involvement compared to those with minimal pulmonary involvement. By contrast, significantly higher percentages for peripheral blood CD3+CD8+ T lymphocytes were revealed for patients with far-advanced pulmonary involvement or fever. Figure 3 presents the ratio of BALF CD4+/CD8+ T lymphocytes and peripheral blood. Significantly higher BALF CD4+/CD8+ ratios were revealed for patients exhibiting far-advanced pulmonary involvement, fever, or loss of body weight. By contrast, significantly lower peripheral blood CD4+/CD8+ ratios were found in those patients.



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  		Figure 1.. Percentage of CD3+CD4+ T lymphocytes recovered from BALF and peripheral blood for patients with active pulmonary TB. Values are presented as mean ± SEM. +p < 0.05, $p < 0.01, both compared to normal subjects and patients with minimal pulmonary involvement; #p < 0.05 compared to patients with moderately advanced pulmonary involvement; *p < 0.05, xp < 0.01 compared to normal subjects and patients without fever or loss of body weight. pul = pulmonary; HS = healthy subjects; G1 =minimal pulmonary involvement; G2 = moderately advanced pulmonary involvement; G3 = far-advanced pulmonary involvement; N = no; Y = yes.

 


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  		Figure 2.. Percentage of CD3+CD8+ T lymphocytes recovered from BALF and peripheral blood for patients with active pulmonary TB. Values are presented as mean ± SEM. +p < 0.05, $p < 0.01, both compared to patients with normal subjects and minimal pulmonary involvement; #p < 0.05 compared to patients with moderately advanced pulmonary involvement; xp < 0.01 compared to normal subjects and patients without fever. See Figure 1 legend for expansion of abbreviations.

 


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  		Figure 3.. Ratio of CD4+/CD8+ T lymphocytes recovered from BALF and peripheral blood for patients with active pulmonary TB. Values are presented as mean ± SEM. +p < 0.05, $p < 0.01, both compared to normal subjects and patients with minimal pulmonary involvement; #p < 0.05 compared to patients with moderately advanced pulmonary involvement; *p < 0.05 compared to normal subjects and patients without fever or loss of body weight. See Figure 1 legend for expansion of abbreviations.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We present a set of observations that reveal that patients with more advanced pulmonary involvement tended to reveal higher C3+CD4+ T-lymphocyte percentages and relatively lower C3+CD8+ percentages, resulting in increased CD4+/CD8+ ratios for the BALF. By contrast, a trend was noted, in cases of more advanced pulmonary involvement, for higher C3+CD8+ T-lymphocyte percentages and relatively lower C3+CD4+ percentages, resulting in decreased CD4+/CD8+ ratios in peripheral blood. Similar findings were demonstrated for patients presenting with fever or loss of body weight.

Resistance to TB is dependent on the function of CD4+ lymphocytes. Depletion of CD4+ T lymphocytes by injected antibody exacerbated infection in the lung, spleen, and liver in mice. By contrast, no effect was demonstrated for bacterial growth or lung cell activation as a result of CD8+ T-lymphocyte depletion for infected mice.13 The importance of interferon (IFN)-{gamma} for macrophage phagocytic function against mycobacterium has been proven by other workers.14 Secretion of IFN-{gamma} in response to mycobacterial infection may be due to the action of CD4+ T lymphocytes in the peripheral airways. Purified culture filtrate proteins obtained from mycobacterium stimulated IFN-{gamma} secretion by immune CD4+ but not by CD8+ T-lymphocytes in vitro.3 13 Ribera et al15 described higher IFN-{gamma} levels and an increased T4/T8 lymphocyte ratio for tuberculous pleural effusion compared to the malignant and nonspecific variant.

T-lymphocyte subpopulations for BALF from the infected lungs of pulmonary TB patients and normal subjects have been analyzed in some studies. An increased CD4+ T-lymphocyte percentage has been observed for TB patients compared with normal subjects by Law et al16 and Ozaki et al.17 By contrast, an increased CD8+ T-lymphocyte percentage, not CD4+ T-lymphocyte percentage, has been demonstrated by Taha et al.18 Similarly, the ratio determined by different investigators for BALF CD4+ and CD8+ lymphocytes has also varied, with an increased ratio determined by Law et al16 and Ozaki et al,17 no difference determined by Hoheisel et al,19 and a decreased ratio by Ainslie et al.20 Law et al16 noted similarities between BALF lymphocyte subpopulations and lymphocyte populations from tissue granuloma lung biopsies, suggesting that cells recovered from BAL reflect cell populations at the site of granuloma formation. Law et al16 described an increased CD4+/CD8+ ratio for HIV-negative TB patients; however, a decreased CD4+/CD8+ ratio was noted for HIV-positive TB patients. As there was no reference to HIV infection in the studies of Hoheisel et al19 and Ainslie et al,20 Law et al16 suggested that inclusion of HIV-positive patients with lower BALF CD4+/CD8+ ratios may have accounted for these differences. The fact that none of our patients were HIV positive provides support for this proposition. Moreover, disease grading may also contribute to CD4+ lymphocyte percentage and CD4+/CD8+ ratio. For our study, significantly higher BALF CD4+ lymphocyte percentage and CD4+/CD8+ ratio was demonstrated only in high-grade TB patients (ie, more advanced pulmonary involvement, with fever or loss of body weight) when compared with normal subjects.

TB patients with a higher grade of disease had a significantly higher percentage of CD8+ lymphocytes and lower CD4+/CD8+ ratio in peripheral blood than patients with a lower grade of disease. The above-mentioned findings are in accordance with results from previous studies suggesting a decreased CD4+ T-lymphocyte percentage and increased CD8+ T-lymphocyte percentage, causing a decreased CD4+/CD8+ ratio in peripheral blood for patients with advanced TB.4 5 6 These findings provide support for the concept of compartmentalization (ie, sequestration of CD4+ T lymphocytes in infected lungs for patients with advanced pulmonary TB).

Ozaki et al21 first described an increased number of neutrophils and lymphocytes with a decreased number of macrophages in the BALF from TB patients. One of our studies confirmed these findings.7 Furthermore, we demonstrated higher percentages of neutrophils and lymphocytes in the BALF from cavitary pulmonary TB lesions compared with those from noncavitary pulmonary TB lesions.10 In this study, we found that patients with a higher grade of TB had increased percentages of neutrophils and lymphocytes when compared with patients with lower grade of TB. Condos et al22 described that at presentation patients with less clinically and radiographically advanced TB (smear-negative, noncavitary disease) had a local immune response characterized by a predominance of lymphocytes. Furthermore, BAL cells from these patients secreted IFN-{gamma}, and not interleukin-4, suggesting a T-helper type 1 lymphocytic response. By contrast, in patients with smear-positive and/or cavitary disease, macrophages or polymorphonuclear leukocytes were the predominant BAL cell type. In this study, we did not study the difference of T-helper type 1 or T-helper type 2 lymphocytes by TB grade. However, an increased percentage of C3+CD4+ T lymphocytes in the BALF from patients with a higher grade of pulmonary TB might indicate that helper T lymphocytes are important in immune response against advanced active pulmonary TB.

In conclusion, patients with higher grades of pulmonary TB revealed higher percentages of C3+CD4+ T lymphocytes, with a lower relative percentage of C3+CD8+ T lymphocytes, resulting in increased C4+/CD8+ ratios in BALF. By contrast, these patients revealed a higher percentage of C3+CD8+ T lymphocytes and lower relative C3+CD4+ T-lymphocyte percentages, resulting in a decreased C4+/CD8+ ratio in peripheral blood. These findings provide evidence to support the proposition of compartmentalization (ie, sequestration of CD4+ T lymphocytes in infected lungs in cases of high-grade pulmonary TB).


   Footnotes
 
Abbreviations: BALF = BAL fluid; IFN = interferon; PBS = phosphate-buffered saline solution; TB = tuberculosis

Supported by Taiwan National Science Committee Research Grant NSC 89–2314-B-182A-026 and approved by ethics committee of Chang Gung Memorial Hospital.

Received for publication October 30, 2001. Accepted for publication April 22, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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