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131]

Original Article

Spirometric Abnormalities Following Treatment for Pulmonary

Tuberculosis in Ilorin, Nigeria
Olutobi Babatope Ojuawo, Ademola Emmanuel Fawibe, Olufemi Olumuyiwa Desalu, Ayotade Boluwatife Ojuawo1, Adeniyi Olatunji Aladesanmi,
Christopher Muyiwa Opeyemi, Mosunmoluwa Obafemi Adio, Alakija Kazeem Salami
Departments of Medicine and 1Paediatrics, University of Ilorin Teaching Hospital, Ilorin, Kwara State, Nigeria

Abstract
Background: Pulmonary tuberculosis (PTB) contributes significantly to morbidity and mortality worldwide, and despite microbiological cure
for the disease, many patients still demonstrate residual respiratory symptoms and spirometric abnormalities. Aim and Objectives: The study
aimed at identifying the prevalence, pattern and factors associated with spirometric abnormalities in patients successfully treated for PTB in Ilorin,
Nigeria. Materials and Methods: This was a hospital‑based cross‑sectional study at the pulmonary outpatient clinics of the University of Ilorin
Teaching Hospital and Kwara State Specialist Hospital, Sobi, Ilorin. A total of 308 consenting patients who had been certified microbiologically
cured for bacteriologically confirmed PTB in the preceding 3 years had assessment of residual pulmonary symptoms, spirometry and plain chest
radiograph. Results: The prevalence of abnormal spirometry following treatment for PTB was 72.1% (confidence interval: 0.6682–0.7695),
with restrictive pattern being the predominant abnormality (42.2%). Over half of the patients (56.5%) had at least one residual respiratory
symptom. The significant predictors of abnormal spirometry were PTB retreatment (adjusted odds ratio [aOR] = 6.918; P = 0.012), increasing
modified Medical Research Council dyspnoea scores (aOR = 7.935; P = 0.008) and increasing radiologic scores (aOR = 4.679; P ≤ 0.001)
after treatment. Conclusion: There is significant residual lung function impairment in majority of the individuals successfully treated for PTB
in Ilorin. This highlights the need for spirometric assessment and follow‑up after treatment.

Keywords: Ilorin, post‑tuberculosis, spirometry, treatment

Introduction over 60 million people successfully treated in the past 20 years.

Tuberculosis (TB) remains a major public health concern,
contributing significantly to morbidity and mortality
worldwide. About 10 million people were estimated to have
TB globally in 2018, with about 1.5 million people succumbing
to the illness.[1] These figures have placed the condition as
a leading cause of death from infectious disease.[1] Nigeria
currently ranks first in Africa in terms of the burden of TB and
is among the thirty nations which collectively contribute to
87% of the estimated TB cases globally.[1] The incidence rate
locally in 2018 was pegged at about 219/100,000 population,
placing the nation as joint sixth with Bangladesh in terms of
the global burden of the condition.[2]
The treatment outcome of pulmonary TB (PTB) has generally
improved through numerous collaborative efforts with
Received: 01-02-2020, Revised: 17-04-2020,
Accepted: 19-04-2020, Published: 17-07-2020
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This figure, however, has been largely based on microbiological
cure as well as completion of prescribed medications.[3] There is
minimal consideration on the possible functional impairment of
the lungs which can result from the disease and its treatment.[3]
TB primarily affects the lung parenchyma causing structural
and functional compromise which results in acute and
chronic complications. [4] It also promotes long‑term
anatomic changes in the lungs leading to the development
of chronic complications. These complications include lung
fibrosis, fungal colonisation within residual TB cavities,
bronchiectasis, bronchial stenosis, emphysematous changes
Address for correspondence: Dr. Olutobi Babatope Ojuawo,
Department of Medicine, University of Ilorin Teaching Hospital, Ilorin,
Kwara State, Nigeria.
E‑mail: obk_ojuawo@yahoo.com
This is an open access journal, and articles are distributed under the terms of the Creative
Commons Attribution‑NonCommercial‑ShareAlike 4.0 License, which allows others to remix,
tweak, and build upon the work non‑commercially, as long as appropriate credit is given and
the new creations are licensed under the identical terms.
For reprints contact: reprints@medknow.com

How to cite this article: Ojuawo OB, Fawibe AE, Desalu OO, Ojuawo AB,
DOI: Aladesanmi AO, Opeyemi CM, et al. Spirometric abnormalities following
10.4103/npmj.npmj_18_20 treatment for pulmonary tuberculosis in Ilorin, Nigeria. Niger Postgrad
Med J 2020;27:163-70.

© 2020 Nigerian Postgraduate Medical Journal | Published by Wolters Kluwer - Medknow 163
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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin
and subsequent impaired lung function which contribute to
long‑term morbidity and mortality as well as a substantial
burden of medical cost.[5] Indeed, many patients develop
disabling chronic respiratory ailments after treatment
for PTB which poses a risk of reduced longevity despite
microbiological cure for the disease.[6]
Previous reports from India,[7] Tanzania,[8] Cameroon[9] and
Benin Republic[10] demonstrated that 76%, 74%, 45.4% and
45% of patients, respectively, who had completed treatment
for PTB had lung function abnormalities. Furthermore, the risk
factors for post‑PTB lung function impairment from previous
surveys include age >40 years,[8] recurrent TB episodes,[8]
duration of symptoms[9,10] and extensive fibrosis on chest
radiograph.[9] However, there is a dearth of information in
Nigeria regarding the pulmonary function abnormalities of
individuals following treatment for PTB despite the high
disease burden in the country and the continuous emerging
information on the residual effect of PTB on pulmonary
function.
This study aims to provide information on the prevalence,
pattern and factors associated with lung function abnormalities
in patients treated for PTB in Ilorin, North Central Nigeria.
Materials and Methods
Study locations
This hospital‑based cross‑sectional study was carried out
at the pulmonology outpatient clinic of the University of
Ilorin Teaching Hospital (UITH) as well as the Kwara State
Specialist Hospital (KSSH), Sobi, Ilorin, between February
and November 2018. These centres have the largest clinics
where patients with PTB are managed in Kwara State, Nigeria.
Ethical approval
Ethical approvals for the study were obtained from the
Ethical Review Committees of the UITH (Protocol number:
ERC/PIN/2017/03/0538 – approved 11 April 2017) and the
Kwara State Ministry of Health (Protocol number: MOH/KS/
EU/777/253 – approved 6 July 2018).
Written informed consent was obtained from all the patients
before enrolment into the study. Confidentiality was also
maintained, and all procedures were in line with the ethical
standards and Helsinki Declaration of 1975.
Study subjects
Adult patients (18 years and above) who had completed
at least 6 months of treatment for smear‑positive PTB and
or nucleic acid amplification‑based sputum GeneXpert
MTB/RIF confirmed PTB at the pulmonology outpatient
clinic of both hospitals within the 3 years before the study.
The patients recruited had evidence of microbiological cure at
the end of drug treatment (negative sputum smear) and were
consecutively invited to the clinic through telephone calls
after retrieving their phone numbers from the TB register of
both clinics.
164 Nigerian Postgraduate Medical Journal  ¦  Volume 27  ¦  Issue 3  ¦  July-September 2020
Exclusion criteria
• Individuals with contraindications to spirometry, for
example, recent myocardial infarction, recent thoracic,
abdominal or eye surgery
• Individuals with spine or chest deformities, for example,
kyphoscoliosis and pectus deformities
• Individuals who were current smokers or past smokers
• Individuals who were pregnant or those with pre‑existing
bronchial asthma, chronic obstructive pulmonary disease,
interstitial lung disease, congestive cardiac failure, stroke
or neuromuscular disease. Furthermore, individuals
on long‑term medications that could cause pulmonary
toxicity such as amiodarone, bleomycin and nitrofurantoin
were excluded
• Patients with TB/HIV co‑infection
• Individuals whose spirometry did not meet up with the
acceptability and repeatability criteria after repeated
attempts.
Sample size determination
The required sample size was obtained using Fisher’s statistical
formula for estimating minimum sample size in descriptive
health studies when population size is >10,000.[11]
Thus,
Z 2 pq
n=
d2
where n = the desired sample size when target population
is >10,000.
• Z = standard normal deviate, usually set at 1.96 which
corresponds to 95% confidence level
• p = proportion in the target population estimated to have a
particular characteristic. The prevalence of lung function
impairment in treated PTB individuals in Cameroon by
Mbatchou Ngahane et al.[9] is 45.4%. Therefore, P = 0.454
• q = 1 − p
• d = degree of accuracy desired, which is set at 0.05.
Therefore, the sample size calculated was:
(1.96 )
2
× ( 0.454 ) × ( 0.546 )
n= = 380.88 – approximately 381
( 0.05)
2
However, the total annual adult patients on treatment for
PTB in the pulmonology outpatient clinic of both hospitals
were <10,000.
The total number of adult patients treated for PTB in UITH
and KSSH, Ilorin, in 2017 was about 300 and 120 patients,
respectively, based on records of treatment in the TB register
of the hospitals. This gave an estimated number of 420 patients
annually from both facilities.
n
• The finite population correction factor of nf =
1+ n/ N
was applied to determine the final sample size.[11]
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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin
• Where nf  =  the desired sample size when population
is <10,000.
• Where n = calculated sample size when population
is >10,000.
• N = Total number of patients on treatment for PTB in
UITH and KSSH
381
Therefore, nf =
1 + 381/ 420
nf = 199.5 patients – approximately 200 patients.
The minimum sample size calculated was 200 patients.
However, 308 patients were eventually recruited over the
10‑month period (February–November 2018). This was done to
improve the quality of the statistical deductions made from the
study. Two hundred and twenty patients (220) were recruited
from UITH, Ilorin, whereas 88 were recruited from KSSH,
Ilorin, in line with the proportion of PTB cases managed in
both facilities (UITH: KSSH = 2.5:1).
Data collection and procedures
A structured questionnaire based on a modification of the
validated United Kingdom Medical Research Council (MRC)
respiratory symptoms questionnaire was administered to
obtain the patient’s demographics and clinical history.[12]
Spirometry was carried out by some of the authors who were
at least experienced senior resident doctors training in
respiratory medicine in the health facility using a desktop
spirometer (Schiller Spirovit SP‑1, Baar, Switzerland) in an
open area with adequate ventilation and sunlight. Calibration
was carried out daily before use with a 3‑l syringe. Face masks
were used to protect the researchers and their assistants. The
forced expiratory manoeuvres and evaluation for acceptability,
repeatability as well as test result selection were in accordance
with the American Thoracic Society and European Respiratory
Society (ATS/ERS) guidelines.[13]
Spirometry was performed in a comfortable upright sitting
position with both feet flat on the floor with legs uncrossed.
It was also ensured that the patient was off vigorous exercise
in the preceding hour. The forced expiratory manoeuvres
were explained to the participants before they underwent the
procedure. The patients were made to inhale maximally to total
lung capacity and asked to hold his/her breath, while a tight
seal was formed around a disposable mouthpiece. A nose clip
was also applied after which the patient was instructed to blow
out air as forcibly and as fast as possible until their lungs felt
empty. The patients were also given verbal encouragements
particularly towards the end of each manoeuvre. The
test was terminated when the curve obtained from three
measurements of pulmonary function was acceptable based
on the recommendation of the ATS/ERS guidelines as well as
if the test results met the repeatability criteria.[13] Repeatability
was determined if differences in forced vital capacity (FVC)
and forced expiratory volume in 1 s (FEV1) were <150 mL
between the greatest and second greatest values.[12] FVC, FEV1
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and FEV1/FVC were measured and the highest values were
documented for comparison and analysis. Each disposable
mouthpiece was discarded after individual use.
Airflow obstruction was defined as FEV1/FVC <70% with
FVC >80%, restrictive defects as an FEV1/FVC ratio of ≥70%
with FVC <80% predicted and mixed defects as FEV1/FVC
ratio of <70% with FVC of <80% predicted. Lung function
impairment was defined by the presence of at least one of
these three abnormalities based on the 2012 global lung
initiative (GLI) reference equations for ‘others’ category as
the equations for ‘blacks’ were largely derived from African
Americans. The severity for obstructive, restrictive and mixed
defects was graded according to the ATS/ERS task force
recommendations.[14]
All patients had a plain chest radiograph (posterior‑anterior view)
done at the time of recruitment to assess for residual cavities,
infiltrates or opacities. The cost of the plain chest radiographs
was borne by the researchers. Radiographic abnormalities were
scored using a validated scoring rubric derived from published
sources for evaluation of radiographic features of TB.[15] The
interpretation of the chest radiograph films was carried out
in conjunction with consultant radiologists in the hospitals.
The films were independently reviewed and reported by two
consultant radiologists, and the consistent reports derived from
both of them were applied to the scoring rubric. For X‑ray films
with significantly varying reports, a third opinion was sought
from a more senior consultant. Informed consent was gotten
from all patients before spirometry and radiologic evaluations.
Statistical analysis
Data were entered and analysed using the IBM SPSS Statistics
for Windows (Version 21.0; IBM Corporation, Armonk, New
York). Categorical variables were expressed in frequencies
and percentages. The Chi‑square test was used to determine
associations between categorical variables. Binary logistic
regression was carried out to determine the predictors of
abnormal lung function. Statistical significance was set at
P < 0.05.
Results
Sociodemographic characteristics of the recruited
subjects
A total of 386 patients were invited to participate in the study,
but 41 did not honour the invite, whereas 37 had at least one
exclusion criterion. Eventually, 308 patients were recruited,
with 172 (55.8%) being males demonstrating a male: female
ratio of 1.3:1 [Table 1]. Most of the patients were between the
ages of 21–30 years (88; 28.6%).
Clinical characteristics and laboratory parameters of the
recruited subjects
The predominant mode of PTB diagnosis was through sputum
GeneXpert  (242; 78.6%), and about a fifth of the recruited
patients (60; 19.5%) were cases of retreatment with many
of them (42; 70%) due to relapsed PTB. Regarding their
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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin

Table 1: Sociodemographic characteristics of the

recruited patients
Sociodemographic characteristics Frequency (%)
Age (years)
<20 26 (8.4)
21-30 88 (28.6)
31-40 80 (26.0)
41-50 44 (14.3)
51-60 28 (9.1)
61-70 30 (9.7)
>70 12 (3.9)
Mean age (years) 39.3±15.9
Sex
Male 172 (55.8) Figure 1: Bar chart illustrating the frequency and pattern of residual
Female 136 (44.2) respiratory symptoms of the patients
Level of education
No formal education 68 (22.1) abnormality detected. Seventy‑four (24.0%) patients had
Primary 42 (13.6) a mixed pattern, whereas 18 (5.8%) had the obstructive
Secondary 36 (11.7) pattern.
Tertiary 162 (52.6)
Marital status
Severity pattern of spirometric abnormalities in the
Single 96 (31.2) recruited subjects
Married 204 (66.2) Majority (68; 22.1%) of the patients with restrictive spirometric
Widowed 8 (2.6) pattern had moderate severity, followed by those with severe
Religion restriction (26; 8.4%) and very severe restriction (20; 6.5%), as
Islam 225 (73.1) shown in Table 2. The least frequency was observed in patients
Christianity 83 (26.9) with mild restrictive pattern (16; 5.2%).
Ethnic group
Yoruba 294 (95.5) Sociodemographic characteristics associated with
Hausa 3 (1.0) abnormal spirometry
Igbo 2 (0.6) As shown in Table 3, patients >40 years of age were slightly
Others 9 (2.9) more likely to develop lung function abnormalities when
compared to those who were 40 years and below (73.7% vs.
co‑morbid illnesses, 31 (10.1%) had systemic hypertension, 71.7%; P = 0.630). On the other hand, there was a statistically
10 (3.2%) had echocardiologically confirmed cor pulmonale, significant difference in favour of patients  ≤40  years of
whereas 7 (2.3%) had diabetes mellitus. The mean duration age among those with restrictive pattern when compared
from time of completion of PTB treatment to time of research to individuals >40 years (66.7% vs. 45.2%; P = 0.002).
was 10.3 ± 4.5 months, whereas the median duration from Abnormal spirometric pattern was also more prevalent in
onset of symptoms to diagnosis of PTB was 12 weeks with males than females although the difference was not statistically
an interquartile range of 8–16 weeks. significant (74.4% vs. 69.1%; P = 0.303).

Frequency and pattern of residual respiratory symptoms
in the subjects
The predominant residual respiratory symptom as demonstrated
in Figure 1 was exertional shortness of breath (130; 42.2%).
This was followed in a descending order by cough (84; 27.3%),
sputum production (52; 16.9%), chest pain (16; 5.2%) and
wheezing (14; 4.5%). Considering the overlap, 56.5% of the
patients had at least one residual respiratory symptom.
Prevalence of spirometric abnormalities among recruited
patients
Figure 2 illustrates that 222 (72.1%; confidence interval:
0.6682–0.7695) of the patients had abnormal spirometry.
One hundred and thirty patients (42.2%) had restrictive
pattern which was the most common spirometric
Clinical characteristics associated with abnormal
spirometry
Concerning the clinical characteristics shown in Table 4,
abnormal spirometric pattern was more prevalent in patients
who had residual symptoms when compared to those
without residual symptoms (91.9% vs. 46.3%; P ≤  0.001).
Likewise, individuals with significant lung parenchymal
destruction [Figure 3] depicted by radiographic scores >3
were also significantly associated with abnormal lung function
compared to those with scores of 3 and below (100% vs.
60.6%; P ≤  0.001). Increasing bacillary load on sputum
GeneXpert, cases of PTB retreatment and increasing modified
MRC (mMRC) dyspnoea scores also had a significant
relationship with abnormal spirometry (P ≤ 0.001; P = 0.001
and < 0.001, respectively). Individuals with respiratory

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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin

symptoms for >12 weeks before the diagnosis of PTB as well as and Banu Rekha et al.[16] in India who reported the prevalence
those with resting hypoxaemia also had significant associations of lung function abnormalities to be 76%, 74% and 65%,
with the presence of spirometric abnormalities (P = 0.045, respectively. It is, however, considerably higher than reports
respectively). from Cameroon [9] (45.4%), Benin Republic [10] (45%),
Egypt[17] (36%) and Indonesia[18] (24.6%). On the other hand,
Factors associated with abnormal spirometric pattern Akkara et  al.[19] in India stated a prevalence rate of 86.8%
after successful treatment for pulmonary tuberculosis following successful treatment for PTB which is higher
Previous PTB treatment (adjusted odds ratio [aOR] =6.918; than the figure obtained in this study. The variability in the
P = 0.012), increasing mMRC dyspnoea scores (aOR = 7.935; prevalence rates generally may be related to the duration from
P = 0.008) and increasing radiographic scores (aOR = 4.679; TB infection to commencement of treatment as well as the
P ≤ 0.001) were found to be significant independent predictors varying periods from completion of PTB treatment to time of
of spirometric abnormalities following treatment for PTB spirometric assessment. The high prevalence of spirometric
following multivariate logistic regression analysis [Table 5]. abnormalities in this study may also be related to the relatively
long mean duration between the onset of symptoms and the
time of diagnosis which was 12.6 weeks following which
Discussion significant lung parenchymal damage would have occurred
The prevalence of spirometric abnormalities was 72.1%, before antituberculous therapy. Furthermore, the relatively
with restrictive pattern (42.2%) being the most common high proportion of patients with PTB retreatment in this study
abnormality detected. This prevalence figure was close to may have contributed to this high prevalence.
findings by Gupte et al.[7] in India, Manji et al.[8] in Tanzania
The predominant restrictive pattern observed mirrors the
findings of Mbatchou Ngahane et  al.[9] in Cameroon, Banu
Table 2: Pattern and severity of spirometric abnormalities Rekha et al.[16] in India and Pasipanodya et al.[20] in the US.
in recruited patients However, some previous reports [8,17,21] found obstructive
Pattern and severity of spirometric abnormality Frequency (%) pattern to be the main form of spirometric abnormality. The
Restrictive pattern 130 (42.2)
restrictive pattern may have occurred following significant
Mild restrictive pattern 16 (5.2)
lung parenchyma destruction, fibrosis of the lung tissue,
Moderate restrictive pattern 68 (22.1) scarring and stiffening of the lungs as well as reduction in
Moderately severe restrictive pattern 0 lung compliance, all of which could be sequel to PTB based
Severe restrictive pattern 26 (8.4) on the various immune cytokines involved.[22] The fact that
Very severe restrictive pattern 20 (6.5)
Mixed/combined pattern 74 (24.0)
Mild mixed pattern 0
Moderate mixed pattern 0
Moderately severe mixed pattern 14 (4.5)
Severe mixed pattern 42 (13.6)
Very severe mixed pattern 18 (5.8)
Obstructive pattern 18 (5.8)
Mild obstructive pattern 6 (1.9)
Moderate obstructive pattern 12 (3.9)
Moderately severe obstructive pattern 0
Severe obstructive pattern 0
Figure 2: Pie chart showing the lung function pattern among the recruited
Very severe obstructive pattern 0 patients

Table 3: Sociodemographic characteristics associated with spirometric abnormalities

Characteristics Total Any abnormality (%) P* Obstructive P* Restrictive P* Mixed P*
Age group (years)
≤40 194 138 (71.1) 0.630 8 (5.8) 0.139 92 (66.7) 0.002 38 (27.5) 0.019
>40 114 84 (73.7) 10 (11.9) 38 (45.2) 36 (42.9)
Sex
Male 172 128 (74.4) 0.303 8 (6.3) 0.277 64 (50.0) 0.003 56 (43.8) <0.001
Female 136 94 (69.1) 10 (10.6) 66 (70.2) 18 (19.1)
Level of education
No formal education 68 52 (76.5) 0.360 2 (3.9) 0.209 40 (76.9) 0.002 10 (19.2) 0.014
Formal education 240 170 (70.8) 16 (9.4) 90 (52.9) 64 (37.6)
*Chi-square

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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin

Table 4: Clinical characteristics associated with spirometric abnormalities

Parameters Total Any abnormality (%) P* Obstructive P* Restrictive P* Mixed P*
Presence of residual symptoms
Yes 174 160 (91.9) <0.001 8 (5.0) 0.006 88 (55.0) 0.084 64 (40.0) 0.001
No 134 62 (46.3) 10 (16.1) 42 (67.7) 10 (16.1)
Radiographic score
≤3 218 132 (60.6) <0.001 16 (12.1) 0.008 88 (66.7) 0.003 28 (21.2) <0.001
>3 90 90 (100) 2 (2.2) 42 (46.7) 46 (51.1)
Bacillary load of smear (n=66)
Scanty 4 4 (100.0) 0.345 0 0.686 4 (100.0) 0.058 0 0.074
1+ 28 20 (71.4) 4 (20.0) 12 (60.0) 4 (20.0)
2+ 28 24 (85.7) 4 (16.7) 8 (33.3) 12 (50.0)
3+ 6 4 (66.7) 0 2 (50.0) 2 (50.0)
Bacillary load of GeneXpert
(n=242)
Very low 12 4 (33.3) <0.001 2 (50.0) 0.003 0 0.037 2 (50.0) 0.730
Low 96 54 (56.3) 0 38 (70.4) 16 (29.6)
Medium 96 78 (81.3) 4 (5.1) 46 (85.2) 28 (35.9)
High 38 34 (89.5) 4 (11.8) 20 (58.8) 10 (29.4)
Number of times previously
treated for PTB
Zero 248 168 (67.7) 0.001 16 (9.5) 0.173 104 (61.9) 0.074 48 (28.6) 0.008
One or more 60 54 (90.0) 2 (3.7) 26 (48.1) 26 (48.1)
mMRC score
Zero 10 0 <0.001 0 0.273 0 0.723 0 0.060
One 194 120 (61.9) 12 (10.0) 76 (63.3) 32 (26.7)
Two 78 76 (97.4) 6 (7.9) 40 (52.6) 30 (39.5)
Three 26 26 (100) 0 14 (53.8) 12 (46.2)
Duration of symptoms to initial
diagnosis (weeks)
≤12 210 144 (68.6) 0.045 14 (9.7) 0.231 82 (56.9) 0.507 48 (33.3) 1.000
>12 98 78 (79.6) 4 (5.1) 48 (61.5) 26 (33.3)
Resting oxygen saturation (%)
≤90 10 10 (100) 0.045 0 0.336 2 (20.0) 0.011 8 (80.0) 0.001
>90 298 212 (71.1) 18 (8.5) 128 (60.4) 66 (31.1)
*Chi-square. PTB: Pulmonary tuberculosis, mMRC: Modified Medical Research Council

Table 5: Regression analysis showing the predictors of

spirometric abnormalities after pulmonary tuberculosis
treatment
Parameters aOR 95% CI P
Duration of symptoms before 0.995 0.950-1.043 0.844
commencement of treatment (>12 weeks)
Previous treatment for PTB 6.918 1.523-31.425 0.012
Presence of residual symptoms 2.320 0.450-23.200 0.244
mMRC score 7.935 1.726-36.483 0.008
Radiologic score 4.679 2.921-7.496 <0.001
SpO2 <90% 1.552 0.837-2.467 0.076
Constant 0.000 0.261
Cox and Snell R: 0.452; Nagelkerke R2: 0.651. aOR: Adjusted odds ratio,
CI: Confidence interval, PTB: Pulmonary tuberculosis, mMRC: Modified
Medical Research Council
Figure 3: Chest radiographs depicting extensive lung parenchymal
patients with smoking history were excluded from this study damage following microbiological cure for pulmonary tuberculosis
may also have contributed to the relatively lower number of
individuals with obstructive pattern. Further evaluation of proportion (16/130; 12.4%) had mild severity, whereas the
the group with restrictive defect showed that only a small others had higher grades of severity. None of the patients

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Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin
with mixed pattern had mild severity. These findings signify
the extent to which PTB causes substantial lung function
impairment despite successful drug treatment.
Over half of the recruited patients (56.5%) had residual
respiratory symptoms, with the predominant residual
respiratory symptom being exertional shortness of breath.
The overall prevalence of residual symptoms in this study
was higher than previous reports from India[16] and Brazil,[23]
and the finding of exertional dyspnoea as the predominant
symptom after treatment for PTB was corroborated by Zakaria
and Moussa[17] in Egypt. Cough and chronic sputum production
was, however, the most common symptom in a similar study
in Indonesia.[24] The shortness of breath predominating in
this study may be explained by the preponderance of lung
restriction which can be linked to the reduced ability to inhale
fully as a result of extensive fibrosis and stiffening of the lung
parenchyma.[25]
Patients with previous PTB treatment had a higher likelihood
of developing lung function abnormality than those with the
first episode of PTB. This is consistent with the finding by Lee
et al.[26] in Korea who reported that cases of PTB retreatment
were associated with development of obstructive lung disease.
Furthermore, an incremental decline in lung function parameters
was observed by Hnizdo et al.[27] with increasing number of
PTB episodes. The repeated damage to the lung parenchyma
with each episode of the TB infection may contribute to lung
function impairment after treatment. Likewise, the increasing
mMRC dyspnoea scores identified as a predictor of abnormal
spirometry indicates that individuals with high scores would
require evaluation for lung function abnormalities. This may
be explained by the fact that the degree of effort intolerance is
likely to be linearly related to the underlying lung parenchymal
destruction culminating in lung function decline. The extent
of lung parenchymal destruction as a predictor of spirometric
abnormality depicted by increasing radiologic rubric scores
mirrors the findings by Chung et al.,[28] Willcox and Ferguson,[29]
Plit et al.[30] and Báez‑Saldaña et al.[31] Overall, these findings
could serve as a guide to clinicians in identifying patients with
PTB who will require further treatment and follow‑up care
beyond the use of antituberculous medications.
The limitations of this study include the fact that causality
could not be determined between lung function assessment
before diagnosis/commencement of PTB chemotherapy and
lung function impairment after treatment. Furthermore, further
confirmation of restrictive lung disease could not be done
due to non‑availability of facilities for measurement of lung
volumes through helium dilution, nitrogen washout and body
plethysmography. We also recognise the fact that the reference
equations derived for the multi‑ethnic GLI study[32] did not
significantly involve black sub‑Saharan African individuals.
However, this research work provides very germane information
regarding this very important aspect of PTB evaluation,
especially from a nation with a high burden of the disease, and
equally serves as a good template for future evaluations.
Nigerian Postgraduate Medical Journal  ¦  Volume 27  ¦  Issue 3  ¦  July-September 2020
Conclusion
Almost three‑quarters of the patients recruited had spirometric
abnormalities after successful treatment for PTB, with
restrictive pattern being the predominant spirometric
abnormality identified. The factors associated with abnormal
spirometry included previous TB treatment, increase in mMRC
dyspnoea scores and worsening lung parenchymal damage on
chest radiograph.
Recommendation
There is a need for greater public awareness regarding
the symptoms of PTB as well as the importance of early
presentation. This will help prevent significant lung
parenchymal destruction associated with delayed treatment
and ultimately avert lung function abnormalities following
treatment. Furthermore, it will be beneficial to include
post‑treatment spirometric assessment in the national PTB
treatment protocol, particularly in those with the recognised
risk factors in order to identify individuals who will require
extended respiratory clinic follow‑up and further management
of the non‑infectious sequelae of the disease.
Acknowledgement
We appreciate the efforts of Dr. Ronke Folaranmi,
Dr. Tolulope Olajuwon and Dr. Bisola Olasehinde in assisting
with the conduct of the spirometry. We also acknowledge
the efforts of the entire staff of the pulmonology outpatient
clinics of both hospitals and the staff of the Kwara State TB,
Leprosy and Buruli Control Unit for their logistic support and
contributions. The invaluable role of the radiology departments
of both health institutions is also highly appreciated.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
1. World Health Organisation. Global Tuberculosis Report 2019. Available
from: http://www.int/tb/publications/global_report/en. [Last accessed
on 2020 Jan 05].
2. World Health Organisation. Tuberculosis Country Profile; 2019.
Available from: http://www.who.int/tb/country/data/profiles/en.  [Last
accessed on 2020 Jan 05].
3. Long R, Maycher B, Dhar A, Manfreda J, Hershfield E, Anthonisen N.
Pulmonary tuberculosis treated with directly observed therapy: serial
changes in lung structure and function. Chest 1998;113:933‑43.
4. Shah M, Reed C. Complications of tuberculosis. Curr Opin Infect Dis
2014;27:403‑10.
5. Jordan TS, Spencer EM, Davies P. Tuberculosis, bronchiectasis and
chronic airflow obstruction. Respirology 2010;15:623‑8.
6. Hoger S, Lykens K, Beavers SF, Katz D, Miller TL. Longevity loss
among cured tuberculosis patients and the potential value of prevention.
Int J Tuberc Lung Dis 2014;18:1347‑52.
7. Gupte AN, Paradkar M, Selvaraju S, Thiruvengadam K, Shivakumar SV,
Sekar K, et al. Assessment of lung function in successfully treated
tuberculosis reveals high burden of ventilatory defects and COPD. PLoS
One 2019;14:e0217289.
8. Manji M, Shayo G, Mamuya S, Mpembeni R, Jusabani A, Mugusi F.
Lung functions among patients with pulmonary tuberculosis in Dar es
169
[Downloaded free from http://www.npmj.org on Tuesday, November 24, 2020, IP: 114.125.215.131]
Ojuawo, et al.: Post‑tuberculosis lung function impairment in Ilorin
Salaam – A cross‑sectional study. BMC Pulm Med 2016;16:58.
9. Mbatchou Ngahane BH, Nouyep J, Nganda Motto M,
Mapoure Njankouo Y, Wandji A, Endale M, et al. Post‑tuberculous lung
function impairment in a tuberculosis reference clinic in Cameroon.
Respir Med 2016;114:67‑71.
10. Fiogbe AA, Agodokpessi G, Tessier JF, Affolabi D, Zannou DM,
Adé G, et al. Prevalence of lung function impairment in cured
pulmonary tuberculosis patients in Cotonou, Benin. Int J Tuberc Lung
Dis 2019;23:195‑202.
11. Araoye MO. Research Methodology with Statistics for Health and
Social Sciences. Ilorin: Nathadex Press; 2003. p. 115‑21.
12. Cotes JE, Chinn DJ. MRC questionnaire (MRCQ) on respiratory
symptoms. Occup Med 2007;57:388.
13. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A,
et al. Standardisation of spirometry. Eur Respir J 2005;26:319‑38.
14. Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R,
et al. Interpretative strategies for lung function tests. Eur Respir J
2005;26:948‑68.
15. Simon G. Radiology in epidemiological studies and some therapeutic
trials. Br Med J 1966;2:491‑4.
16. Banu Rekha VV, Ramachandran R, Kuppu Rao KV, Rahman F,
Adhilakshmi AR, Kalaiselvi D, et al. Assessment of long term status of
sputum positive pulmonary TB patients successfully treated with short
course chemotherapy. Indian J Tuberc 2009;56:132‑40.
17. Zakaria MW, Moussa HA. Chronic obstructive pulmonary disease in
treated pulmonary tuberculosis patients. Egypt J Bronchol 2015;9:10‑5.
18. Maguire GP, Anstey NM, Ardian M, Waramori G, Tjitra E,
Kenangalem E, et al. Pulmonary tuberculosis, impaired lung function,
disability and quality of life in a high‑burden setting. Int J Tuberc Lung
Dis 2009;13:1500‑6.
19. Akkara SA, Shah AD, Adalja M, Akkara AG, Rathi A, Shah DN.
Pulmonary tuberculosis: The day after. Int J Tuberc Lung Dis
2013;17:810‑3.
20. Pasipanodya JG, Miller TL, Vecino M, Munguia G, Garmon R, Bae S,
et al. Pulmonary impairment after tuberculosis. Chest 2007;131:1817‑24.
21. Guliani A, Bhalotra B, Parakh U, Jain N. Even asymptomatic patients
may have serious lung function impairment after successful TB
treatment. Am J Resp Crit Care Med 2014;189:A3203.
170 Nigerian Postgraduate Medical Journal  ¦  Volume 27  ¦  Issue 3  ¦  July-September 2020
22. Di Naso FC, Pereira JS, Schuh SJ, Unis G. Functional evaluation in
patients with pulmonary tuberculosis sequelae. Rev Port Pneumol
2011;17:216‑21.
23. Nihues Sde S, Mancuzo EV, Sulmonetti N, Sacchi FP, Viana Vde S,
Netto EM, et al. Chronic symptoms and pulmonary dysfunction in
post‑tuberculosis Brazilian patients. Braz J Infect Dis 2015;19:492‑7.
24. Ralph AP, Kenangalem E, Waramori G, Pontororing GJ, Sandjaja,
Tjitra E, et al. High morbidity during treatment and residual pulmonary
disability in pulmonary tuberculosis: under‑recognised phenomena.
PLoS One 2013;8:e80302.
25. Ravimohan S, Kornfeld H, Weissman D, Bisson GP. Tuberculosis and
lung damage: from epidemiology to pathophysiology. Eur Respir Rev
2018;27. pii: 170077.
26. Lee SW, Kim YS, Kim DS, Oh YM, Lee SD. The risk of obstructive
lung disease by previous pulmonary tuberculosis in a country with
intermediate burden of tuberculosis. J Korean Med Sci 2011;26:268‑73.
27. Hnizdo E, Singh T, Churchyard G. Chronic pulmonary function
impairment caused by initial and recurrent pulmonary tuberculosis
following treatment. Thorax 2000;55:32‑8.
28. Chung KP, Chen JY, Lee CH, Wu HD, Wang JY, Lee LN, et al. Trends
and predictors of changes in pulmonary function after treatment for
pulmonary tuberculosis. Clinics (Sao Paulo) 2011;66:549‑56.
29. Willcox PA, Ferguson AD. Chronic obstructive airways
disease following treated pulmonary tuberculosis. Respir Med
1989;83:195‑8.
30. Plit ML, Anderson R, Van Rensburg CE, Page‑Shipp L, Blott JA,
Fresen JL, et al. Influence of antimicrobial chemotherapy on spirometric
parameters and pro‑inflammatory indices in severe pulmonary
tuberculosis. Eur Respir J 1998;12:351‑6.
31. Báez‑Saldaña R, López‑Arteaga Y, Bizarrón‑Muro A,
Ferreira‑Guerrero E, Ferreyra‑Reyes L, Delgado‑Sánchez G, et al.
A  novel scoring system to measure radiographic abnormalities and
related spirometric values in cured pulmonary tuberculosis. PLoS One
2013;8:e78926.
32. Quanjer PH, Stanojevic S, Cole TJ, Baur X, Hall GL, Culver BH,
et al. Multi‑ethnic reference values for spirometry for the 3‑95‑yr
age range: the global lung function 2012 equations. Eur Respir J
2012;40:1324‑43.