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APMC Vol. 14 No. 4 October – December 2020 302 www.apmcfmu.com
ORIGINAL ARTICLE Annals of Punjab Medical College
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary
Hypertension in Endemic Areas
Abdul Rasheed Qureshi1, Muhammad Irfan2, Zeeshan Ashraf3, Khalid Farooq Bhatti4
1
Assistant Professor, Department of Pulmonology, Gulab Devi Chest Hospital, Lahore Pakistan
Conception, Study design, Manuscript writing
Submitted for Publication: 13-07-2019
Accepted for Publication 30-09-2020
CORRESPONDING AUTHOR
Dr. Muhammad Irfan
Assistant Professor, Department of Pulmonology,
Gulab Devi Chest Hospital, Lahore Pakistan
Email: irfan16d2@gmail.com
2
Assistant Professor, Department of Pulmonology, Gulab Devi Chest Hospital, Lahore Pakistan
Data collection, Manuscript revision, Study supervision
3
Lecturer, Department of Statistics, Gulab Devi Educational Complex, Lahore Pakistan
Literature review, Data analysis, Manuscript revision
4
Senior Medical Officer, Department of Pulmonology, Gulab Devi Chest Hospital, Lahore Pakistan
Data collection, Manuscript revision, Study supervision
ABSTRACT
Background: Many patients with chronic lung disorders like infections, COPD, ILD, OSA & Thrombo-embolism, present
with dyspnea, not showing adequate improvement by conventional treatment. Most of these were diagnosed as pulmonary
hypertension by further multidisciplinary work-up. Such patients show reduced life expectancy due to late diagnosis and
insufficient treatment. Many TB patients often remain undiagnosed in this context. The understanding of etiology and risk
factors is essential for a high index of suspicion. Objective: To explore the etiology of Pulmonary Hypertension in chronic
respiratory patients. Study Design: A Retrospective Observational Study. Settings: Male pulmonology ward, Gulab Devi
Chest Hospital, Lahore Pakistan. Duration: 37 months from January 2014 to February 2017. Methodology: 231, consecutive
cases, having Age >14 years with clinical and radiological suspicion of pulmonary hypertension were included. Patients
having Age >90 years and <14years, not willing for further investigations were excluded. Detailed history, physical
examination, radiological, hematological, bacteriological biochemical and immunologic findings were recorded. PH was
diagnosed by ECG, Echocardiography, CT-Angiography. HRCT thorax & PFTs, were employed to recognize the underlying
lung disorders. Risk factors were identified. Data tabulated, analyzed statistically and conclusions were drawn. Results:
69/231 (29.87%) cases with active and 76/231(32.90%) with old-treated TB, 50(21.64%) COPD, 10(4.32%) pneumonia,
5(2.16%) CLD, six bronchiectasis and three cases of chest deformities were diagnosed PH. Cigarette smoking, DM and
obesity were major risk factors. Conclusion: Pulmonary Tuberculosis can be the dominant etiology of PH in high prevalence
populations.
Keywords: Pulmonary tuberculosis, Pulmonary hypertension, High prevalence population.
How to Cite: Qureshi AR, Irfan M, Ashraf Z, Bhatti KF. Pulmonary Tuberculosis is Often Over-Looked as An Etiology of Pulmonary Hypertension but A
High Index of Suspicion Unveils the Diagnosis. A Retrospective Study of 231-Cases. APMC 2020;14(4):302-7. DOI: 10.29054/APMC/2020.29
INTRODUCTION
Pulmonary hypertension (PH) is a devastating disease
associated with increasing debility and poor prognosis,
resulting from architectural lung damage and hypoxia. It
is characterized by persistent elevation of mean
pulmonary arterial systolic pressure > 25 mmHg at rest
and > 30 mmHg on exercise. It is considered as an
uncommon entity but shows high morbidity and
mortality.1 Previously it was recognized as a disease of
the young and middle-aged but currently it is considered
as disease of elderly with multiple co-morbidities.2-3
These patients usually present with debilitating
symptoms and show reduced life expectancy while late
diagnosis and inadequate treatment contributes to the
poor survival.4
It is classified into five main groups, (group-1) pulmonary
veno-occlusive disease and pulmonary capillary
hemangiomatosis, (group-2) due to left heart disease- left
ventricular systolic and diastolic dysfunction, valvular
disease, left heart inflow or outflow tract obstruction &
congenital cardiomyopathies, (group-3)lung disease like
COPD, ILD, mixed obstructive and restrictive disorders,
sleep disorders, alveolar hypoventilation, high altitude &
developmental lung disorders, (group-4), chronic
thrombo embolic phenomena, (group-5) PH with unclear
/multifactorial mechanisms like hematologic, systemic
disorders (sarcoidosis, Histiocytosis &
Lymphangiomyomatosis), metabolic and tumoric
obstructive diseases.5 PH can be caused by HIV infection,
chronic hepatitis B and C, hereditary
haemoglobinopathies and tuberculosis can also be the
possible etiology.6-7
These patients usually present with shortness of breath
disproportionate to radiological picture, not showing
adequate improvement, on conventional treatment but
multidimensional diagnostic work-up reveals the
diagnosis. PH remains associated with significant
morbidity and mortality, and a substantial reduction in
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary Hypertension Qureshi AR et al.
APMC Vol. 14 No. 4 October – December 2020 303 www.apmcfmu.com
quality of life. After failure of medical treatments, the
lung transplantation remains the only but difficult
option.8-9 Although identification of the etiology can be
challenging but is essential because it determines the
correct management options which can ameliorate the
severity of PH. We conducted this study to explore the
etiology of pulmonary hypertension in daily
pulmonology practice.
METHODOLOGY
Study Design: A Retrospective Observational Study.
Settings: Male ward of Pulmonary Medicine, Gulab Devi
Chest Hospital, Lahore Pakistan.
Duration: 37 months from January 2014 to February 2017.
Sample Technique: Non-probability consecutive
sampling.
Sample Size: 231 consecutive male patients.
Inclusion Criteria: Male patients, having Age >14 years,
dyspnea not responding to conventional treatment, and
clinical and radiological suspicion of pulmonary
hypertension were included in the study.
Exclusion Criteria: Patients having Age >90 years and
<14 years, not willing for further investigations were
excluded.
Data Collection Procedure: Pulmonary hypertension
was suspected by an unexplained dyspnea, desaturation
even at minimal activity like changing dress, visiting
toilet, saying prayer or walking a short distance and
sometimes an overt heart failure associated with raised
JVP, pedal edema, tender hepatomegaly and prominent
pulmonary artery & reticulations on x-ray chest. The
patients were re-evaluated with detailed history,
thorough physical examination and a multidisciplinary
diagnostic work-up. Basic hematological, biochemical
and immunological tests were performed. Sputum for
Acid Fast Bacilli and G-Xpert was done. ECG and
echocardiography were employed to evaluate the cardiac
status. Pulse oximetry and ABGs were used to evaluate
oxygen saturation. Multiple view radiography, HRCT
thorax & PFTs, were utilized to recognize the lung
disorders. Ultrasound abdomen & chest were used to
identify the risk factors. PH was diagnosed by Doppler
Echocardiography and CT- Angiography. The severity
was classified into mild (30----45 mmHg), moderate (46--
-60 mmHg) and severe (> 60 mmHg) groups. Six-Minute
Walk-Test was employed for objective assessment of
exercise capacity and to monitor the response of
treatment. TB-cases were treated according to the WHO
& COPD cases on the Global initiatives guide-lines and
all cases were followed up for six months, at least. Risk
factors and co-morbidities were identified. The files were
retrieved from the hospital registry, all multidisciplinary
findings were noted, tabulated, data analyzed and
conclusions were drawn by applying statistics.
Data Analysis: SPSS-16 was utilized for statistical
analysis. Quantitative results were expressed as mean
±SD, categorical data was presented as percentage. Fisher
exact test was utilized for the calculation of p-value.
A p-value < 0.05 was taken as significant.
RESULTS
231-male patients were enrolled. Age range was 14 – 90
years with median age 46 years, mean 48.68 with SD +
10.79, 95% CI for the mean 47.28-50.08 and Std. Error : + :
0.71. The clinical presentation of 231 patients is shown in
table 1.
Table 1: Frequency of clinical picture in 231 patients
Clinical Features
Total cases
Observed
cases
Percentage
Unexplained dyspnea
231
100.00 %
Cough
217
93.93 %
Expectoration
200
86.58 %
Fever
145
62.77%
Chest Pain
138
59.74%
Hemoptysis
32
13.85 %
Percentage is calculated for 231 patients
Table-1 shows that 100% patients presented with un-
explained dyspnea. Cough, expectoration & fever were
the main symptoms while chest pain and hemoptysis
were less common. The findings of physical examination
are shown by figure 1.
Figure 1: Frequency of Physical Signs in 231 Patients
Dyspnea was classified according to m-MRC scale as
grade 0 to grade 4. Its frequency is shown by the table 2,
in 231 patients.
86
37.22% 82
35.49%
48
20.77% 43
18.61%
16
6.92% 10
4.32%
0
10
20
30
40
50
60
70
80
90
100
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary Hypertension Qureshi AR et al.
APMC Vol. 14 No. 4 October – December 2020 304 www.apmcfmu.com
Table 2: Frequency of severity of dyspnea (m MRC
Scale) n=231
Dyspnea Severity
Observed cases
Percentage
Grade-0
0.00
0.00%
Grade-1 +
0.00
0.00%
Grade-2 ++
155
67.09%
Grade-3 +++
66
28.57%
Grade-4 ++++
10
4.32%
Percentage is calculated for 231 patients.
Majority of the patients showed m-MRC grade 2 & 3
dyspnea. The identified risk factors are shown in table 3.
Table 3: Frequency of risk-factors for pulmonary
hypertension (n = 231)
Risk Factors
Observed Cases
Percentage
Cigarette Smokers
174
75.32%
Diabetes Mellitus
24
10.38%
Obesity
09
3.89 %
Chronic Liver Disease
05
2.16 %
Pectus Excavatum
03
1.29 %
Percentage is calculated for 231 patients.
Cigarette smoking was the most common (75.32%) risk
factor. 174 smoker patients showed mean age 50.33 with
SD + 11.34, range 48 and variance 129.8. while 57 non-
smoker patients, displayed mean age 41.7, SD. + 7.67,
range 36 and variance 58.88. Fisher exact test statistic
value is 0.0005, which is highly significant at < 0.05. The
PASP value ranged from 35 to 105 mmHg, the mean value
was 53.69 with SD + 16.89 with 95% CI: 51.50-55.88, Std.
Error + 1.11, variance 285.37 and range 75. The mean
PASP value for TB-cases was 55.46 mmHg with SD
+16.06, 95% CI for the mean:52.82-58.09, variance 257.9
and range 75. COPD patients showed mean PAH value
of 51.52 mmHg with SD +15.58, 95% CI:47.09-55.94,
variance 242.9 and range 60. The p-value for PASP, by
Fisher exact test was 0.0001 with significance level at p <
0.05. The frequency of dyspnea severity is shown in figure
2.
Figure 2: Frequency of PH Severity in 231 patients
Only103 patients (44.58%) could perform lung function
test successfully. 20 patients showed mild obstruction, 28
moderate obstruction, 15 moderate restriction and 40
cases with severe restriction were noted. 12/231 cases
(5.19%) were with cardiac etiologies while 219 patients
(94.80%) were with non-cardiac causes. Among cardiac
group, one case (8.33%) was of ASD secundum,03 cases
(25.0%) of DCMP, 05 cases (41.66%) of severe LV systolic
dysfunction, and 03 cases (25.00%) of severe mitral
stenosis were found. The frequency of non-cardiac
etiologies is shown in figure 3.
Figure 3: Non-cardiac Etiologies in 219 pulmonary
hypertension patients
145/219 cases (66.21%) of Tuberculosis and 50/219 cases
(22.83%) of COPD were the main contributors.
The PASP values were higher for TB than COPD patients.
DISCUSSION
231 male patients with mean age 48.68 were diagnosed
pulmonary hypertension. The literature demonstrated
mean ages between 45 ± 17 and 65 ± 15 years at
diagnosis.6,7
Previously, pulmonary hypertension was considered as
the disease of the young and middle aged but changes in
the phenotype were observed in the past decades. Many
Western authors have reported it as a disease of elderly
with multiple co-morbidities.4-8 PH secondary to Left
Heart Disease is found in elderly patients which later on
develop right heart failure and PH also. The higher
prevalence of PH in the elderly may be related to
decreasing compliance of the pulmonary arteries with
aging.
Clinically, 100% patients presented with un-explained
dyspnea which is the most prominent finding of this
study. Even 128 patients (55.41%) could not perform lung
128
55.41%
71
30.73%
32
13.85%
0
50
100
150
Mild PH (30-
45mmHg)
Moderate PH
(46-60mmHg)
Severe PH
(>60mmHg)
PASP Grading n = 231
76
34.70% 69
31.50%
50
22.83%
10
4.56% 6
2.74%
5
2.28% 3
1.37%
0
10
20
30
40
50
60
70
80
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary Hypertension Qureshi AR et al.
APMC Vol. 14 No. 4 October – December 2020 305 www.apmcfmu.com
function test successfully because of poor control on
breathing.
Cough, expectoration & fever have also significant
contribution but these are non-specific symptoms, can be
found in any respiratory disorders. Hemoptysis signifies
tuberculosis, bronchiectasis or pneumonia. Oedema,
ascites and raised JVP, points towards cardiac
involvement, cyanosis can be found in advanced
respiratory and cardiac disorders while clubbing is a
feature of bronchiectasis, COPD, ILD, cyanotic heart
diseases & CLD. Pallor is a non-specific finding which can
be related to poor socio-economic status, malnutrition
and poor health education in addition to pathological
processes.
In this study, PASP was measured in the range of 30 to
105 mmHg by Doppler echocardiography. Which
indicated that echocardiography is an excellent modality
capable of diagnosing PH at an earlier stage, enabling
early diagnosis, prompt management and reducing
morbidity and mortality just by having a high index of
suspicion. Furthermore, it has eliminated the need of
diagnostic right heart catheterization for PH.9
174 cases (75.32%) with cigarette smoking is a big risk
factor. Cigarette smoking has direct effect on intra-
pulmonary vessels & is the major risk-factor for pre-
disposing a wide spectrum of chronic respiratory
disorders like COPD, recurrent respiratory infections,
respiratory failure and malignancies and is a big risk
factor for PH.10
We came across 09(3.89%) cases of obesity, which is an
independent risk factor for PH.11 Obesity directly
contributes to the development of PH because up to 5%
of otherwise healthy individuals with a BMI >30
kg·m−2 have been found with moderate or severe PH. The
possible explanation is that these patients are at increased
risk of left heart-disease, pulmonary thrombo-embolism
and sleep-disordered breathing. A recent meta-analysis
has demonstrated that bariatric surgery leads to clinical
improvements in PH, in obese patients.
24 cases (10.38%) of diabetes mellitus is a significant risk
factor displayed by this study. It has been demonstrated
that long-term survival appears worse in PH patients
with diabetes in comparison to PH patients without
diabetes.12
We encountered 05/219 cases (2.28%) of PH with chronic
liver disease having portal hypertension. Several
researchers have reported that 5% cases of portal
hypertension, irrespective of the cause, develop porto-
pulmonary hypertension.
Three cases (1.29%) with gross chest deformity (kypho-
scoliosis + Pectus Excavatum) were found in our series.
Such cases have reduced chest wall compliance, alveolar
hypoventilation, alveolar hypoxia and hypercapnia
causing pulmonary vasoconstriction and elevated PASP
levels.13
Out of 231, we came across 12 patients (5.19%) with
cardiac etiology. The cardiac cases included Mitral
Stenosis, DCMP, LV-systolic dysfunction and ASD
secundum. PH is a complication of Left Heart disease
including systolic and diastolic left ventricular
dysfunction and left-sided valvular heart disease.4-8
In non-cardiac group, 50/219 cases (22.83%) of PH
associated with COPD were found which can be due to
cigarette smoking active or passive or working at smoky
and polluted environment.11 Tuberculosis itself is
proposed to be etiologically responsible for the
development of COPD.14
06 cases (2.74%) of bronchiectasis and 10 patients (4.56%)
of slow resolving pneumonia were encountered in this
study. Although the level of PASP was lower in COPD as
compared to TB patients but it is an undisputed fact that
COPD with PH has the worst prognosis. In COPD,
hypoxia and emphysematous destruction of pulmonary
vascular bed is the main responsible factor. In this
condition PASP > 45 mmHg has five-year survival less
than 10%. Because pulmonary hypertension progresses
slowly in chronic obstructive pulmonary disease, these
cases remain unidentified several times and a poor out-
come is the result. A high index of suspicion is the only
tool to pick such cases. Andersen KH et al showed 36%
PH in COPD patients.15 A single study from Egypt,
reported a prevalence of 62.7% among those with chronic
obstructive pulmonary disease.
It is amazing that out of 219 non-cardiac cases, 145
patients (66.21%) had tubercular etiology. 69/145 cases
(47.58%) were with active disease while 76/145 cases
(52.41%) were, old-treated cases of tuberculosis, again
admitted for worsening chest symptoms. In chronic
tuberculosis when there is significant parenchymal
damage, there is destruction of vascular bed, vasculitis
and endarteritis, resulting into reduced cross-sectional
area of the pulmonary vasculature and PAH.16 This is the
reason that these patients present with dyspnea, out of
proportion to their radiological picture, desaturation with
minimal activity and some-times as overt heart failure
with pedal edema, raised JVP and tender hepatomegaly
that is why we had 60/219 patients (27.39%) of cor-
pulmonale in our study.17 Ahmed AE et al In their cross-
sectional study, described 14 patients of PH after
successful treatment of pulmonary tuberculosis, with
PASP values ≥ 40 mm Hg estimated by Doppler
echocardiography.18 Most of them had fibro-cavitary or
fibrotic changes in the chest X-ray. Another study by
Bhattacharya et al. has also reported PH in patients with
tuberculosis.19 Patel et al. have described 12% cases of PH
to develop from tuberculosis.20
Tuberculosis is the dominant etiology of PH in (66.21%)
this study. The high percentage of tuberculosis may be
due to the fact that we rank 5th among the high burden
countries with majority of the patients belonging to a
class, below the poverty line, and people are not well
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary Hypertension Qureshi AR et al.
APMC Vol. 14 No. 4 October – December 2020 306 www.apmcfmu.com
aware of the health education.21 Furthermore, the study
was conducted in a tertiary care hospital where TB
patients are referred from all corners of the country.
Anyhow it is clear from our results that tuberculosis
irrespective of active or inactive, is a dominant etiology of
PH in the community, which is often over-looked.
Refractory shortness of breath and poor clinical states are
usually not given due consideration and are attributed to
advanced TB-disease, MDR, malnutrition, poor socio-
economic status and various other factors without any
thought about PH. The old treated cases presenting with
worsening dyspnea are incorrectly interpreted as relapse
of TB and are put again on anti-TB treatment or
bronchodilators, for the treatment of dyspnea, without
precise diagnosis. Such mismanagement, resulting into
unhappy out-comes, needs to be avoided. Furthermore,
the development of PH and ultimately cor-pulmonale can
also be prevented by adequate and timely management
of pulmonary TB which otherwise, destroys lung
parenchyma & significantly reduces the span and quality
of life as well.
The prevalence of PH varies widely across different
populations with different etiologies and risk-factors. An
Egyptian study reported a prevalence of 62.7% among
COPD patients while the main class of PH in Africa is due
to left heart diseases. On the other hand, this study
revealed tuberculosis as the most common etiology.21,22
PH is no more a rare disease rather it is under-diagnosed.
Average time between the appearance of the symptoms
and confirmed diagnosis ranges from 1 to 4 years.23,24 This
is because pulmonary hypertension is present in the back-
ground of chronic lung disorders, for which patients
remain under treatment for longer periods & disease is
identified as diagnosis of exclusion. It is diagnosed
usually after a hectic multidisciplinary diagnostic work-
up. A high index of suspicion is the only tool, which can
take us to the early diagnosis.
This study has not only revealed the relevance of PH with
pulmonary tuberculosis, but also highlighted that
tuberculosis is the commonest culprit in high burden
populations, which is often over-looked for the etiology
of PH.
It is clear from this discussion that pulmonary
hypertension is associated with increasing morbidity,
mortality and poor quality of life. Early diagnosis &
prompt management is the golden rule to escape
unpleasant out-come. The findings of this study are
adequate to alert the physicians for diagnosing PH at an
early stage for the right treatment and favorable out-
come. One should make a positive search for PH in cases
of TB and other chronic lung disorders with shortness of
breath, mismatched with radiological picture and
refractory to conventional treatment.
In short, PH remains a fatal disease & tuberculosis is the
most common etiology, followed by COPD and Slow
Resolving Pneumonia. Cigarette smoking, DM, obesity,
CLD and chest deformities are the significant risk factors.
CONCLUSION
- Tuberculosis is the dominant etiology of pulmonary
hypertension in high burden populations.
- COPD is also a significant contributor followed by
Bronchiectasis and pneumonia.
- Cigarette smoking, DM, obesity, CLD and chest
deformities are significant risk factors.
- All the patients with shortness breath, refractory to
conventional treatment must be investigated in the
perspective of PH and treated on priority to reduce
the morbidity and mortality in the community.
LIMITATIONS
The main limitations of this study is that it is a single
centered, retrospective, observational study which
usually is considered, having lesser credibility as
compared to a prospective trial. Secondly the value of PH
has not been confirmed by right heart catheterization
which is the gold-standard, but is highly invasive,
expensive and unsuitable for screening. On the other
hand, echocardiography has emerged as a safe, sensitive
& specific modality for screening purpose. Calculation of
PASP in patients with severe tricuspid regurgitation can
be under or overestimated, so an experienced hand is
essential for the echocardiography of suspected cases.
Although current study successfully shows the
association of PH with TB but the questions about the
screening of TB patients for PH, like when to go for
screening, what tool should be opted and which
intervention can improve the out-come in TB-patients
with detected PH are still needing satisfactory answers.
Our setting is very much popular for the treatment of
tuberculosis and other chest disorders. Patients from
every corner of the country rush to our hospital for
unique facilities and high-class treatment, that is why,
more TB patients are found in our wards which can be a
source of bias but it does not affect the objectives of this
research.
SUGGESTIONS / RECOMMENDATIONS
Further nation-wide, multi-centered, prospective studies
with large sample size, preferably RCT should be
performed to additionally explore the subject and reduce
the bias, using protocols capable of answering the
questions regarding screening TB-patients & screening
tools for PH.
CONFLICT OF INTEREST / DISCLOSURE
No conflict of interest exists among the authors in this
article.
Pulmonary Tuberculosis; A Dominant Etiology of Pulmonary Hypertension Qureshi AR et al.
APMC Vol. 14 No. 4 October – December 2020 307 www.apmcfmu.com
ACKNOWLEDGEMENTS
Authors would like to thank Dr. Aqeel Ahmed, Nazia,
Sajida, Samina and Muhammad Tahir for their valuable
assistance.
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