|Year : 2020 | Volume
| Issue : 3 | Page : 163-170
Spirometric abnormalities following treatment for pulmonary tuberculosis in Ilorin, Nigeria
Olutobi Babatope Ojuawo1, Ademola Emmanuel Fawibe1, Olufemi Olumuyiwa Desalu1, Ayotade Boluwatife Ojuawo2, Adeniyi Olatunji Aladesanmi1, Christopher Muyiwa Opeyemi1, Mosunmoluwa Obafemi Adio1, Alakija Kazeem Salami1
1 Department of Medicine, University of Ilorin Teaching Hospital, Ilorin, Kwara State, Nigeria
2 Department of Paediatrics, University of Ilorin Teaching Hospital, Ilorin, Kwara State, Nigeria
|Date of Submission||01-Feb-2020|
|Date of Decision||17-Apr-2020|
|Date of Acceptance||19-Apr-2020|
|Date of Web Publication||17-Jul-2020|
Dr. Olutobi Babatope Ojuawo
Department of Medicine, University of Ilorin Teaching Hospital, Ilorin, Kwara State
Source of Support: None, Conflict of Interest: None
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
|How to cite this article:|
Ojuawo OB, Fawibe AE, Desalu OO, Ojuawo AB, Aladesanmi AO, Opeyemi CM, Adio MO, Salami AK. Spirometric abnormalities following treatment for pulmonary tuberculosis in Ilorin, Nigeria. Niger Postgrad Med J 2020;27:163-70
|How to cite this URL:|
Ojuawo OB, Fawibe AE, Desalu OO, Ojuawo AB, Aladesanmi AO, Opeyemi CM, Adio MO, Salami AK. Spirometric abnormalities following treatment for pulmonary tuberculosis in Ilorin, Nigeria. Niger Postgrad Med J [serial online] 2020 [cited 2021 Jul 31];27:163-70. Available from: https://www.npmj.org/text.asp?2020/27/3/163/289907
| Introduction|| |
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. These figures have placed the condition as a leading cause of death from infectious disease. 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. 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.
The treatment outcome of pulmonary TB (PTB) has generally improved through numerous collaborative efforts with over 60 million people successfully treated in the past 20 years. This figure, however, has been largely based on microbiological cure as well as completion of prescribed medications. There is minimal consideration on the possible functional impairment of the lungs which can result from the disease and its treatment.
TB primarily affects the lung parenchyma causing structural and functional compromise which results in acute and chronic complications. 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 and subsequent impaired lung function which contribute to long-term morbidity and mortality as well as a substantial burden of medical cost. 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.
Previous reports from India, Tanzania, Cameroon and Benin Republic 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, recurrent TB episodes, duration of symptoms, and extensive fibrosis on chest radiograph. 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|| |
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 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.
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.
- 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.
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. 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:
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.
- The finite population correction factor of was applied to determine the final sample size.
- 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
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. 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.
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. 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. FVC, FEV1 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.
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. 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.
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 co-morbid illnesses, 31 (10.1%) had systemic hypertension, 10 (3.2%) had echocardiologically confirmed cor pulmonale, whereas 7 (2.3%) had diabetes mellitus. The mean duration from time of completion of PTB treatment to time of research was 10.3 ± 4.5 months, whereas the median duration from onset of symptoms to diagnosis of PTB was 12 weeks with an interquartile range of 8–16 weeks.
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.
|Figure 1: Bar chart illustrating the frequency and pattern of residual respiratory symptoms of the patients|
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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 abnormality detected. Seventy-four (24.0%) patients had a mixed pattern, whereas 18 (5.8%) had the obstructive pattern.
|Figure 2: Pie chart showing the lung function pattern among the recruited patients|
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Severity pattern of spirometric abnormalities in the recruited subjects
Majority (68; 22.1%) of the patients with restrictive spirometric pattern had moderate severity, followed by those with severe restriction (26; 8.4%) and very severe restriction (20; 6.5%), as shown in [Table 2]. The least frequency was observed in patients with mild restrictive pattern (16; 5.2%).
|Table 2: Pattern and severity of spirometric abnormalities in recruited patients|
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Sociodemographic characteristics associated with abnormal spirometry
As shown in [Table 3], patients >40 years of age were slightly more likely to develop lung function abnormalities when compared to those who were 40 years and below (73.7% vs. 71.7%; P = 0.630). On the other hand, there was a statistically significant difference in favour of patients ≤40 years of age among those with restrictive pattern when compared to individuals >40 years (66.7% vs. 45.2%; P = 0.002). Abnormal spirometric pattern was also more prevalent in males than females although the difference was not statistically significant (74.4% vs. 69.1%; P = 0.303).
|Table 3: Sociodemographic characteristics associated with spirometric abnormalities|
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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 symptoms for >12 weeks before the diagnosis of PTB as well as those with resting hypoxaemia also had significant associations with the presence of spirometric abnormalities (P = 0.045, respectively).
|Table 4: Clinical characteristics associated with spirometric abnormalities|
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|Figure 3: Chest radiographs depicting extensive lung parenchymal damage following microbiological cure for pulmonary tuberculosis|
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Factors associated with abnormal spirometric pattern after successful treatment for pulmonary tuberculosis
Previous PTB treatment (adjusted odds ratio [aOR] =6.918; P = 0.012), increasing mMRC dyspnoea scores (aOR = 7.935; P = 0.008) and increasing radiographic scores (aOR = 4.679; P ≤ 0.001) were found to be significant independent predictors of spirometric abnormalities following treatment for PTB following multivariate logistic regression analysis [Table 5].
|Table 5: Regression analysis showing the predictors of spirometric abnormalities after pulmonary tuberculosis treatment|
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| Discussion|| |
The prevalence of spirometric abnormalities was 72.1%, with restrictive pattern (42.2%) being the most common abnormality detected. This prevalence figure was close to findings by Gupte et al. in India, Manji et al. in Tanzania and Banu Rekha et al. in India who reported the prevalence of lung function abnormalities to be 76%, 74% and 65%, respectively. It is, however, considerably higher than reports from Cameroon (45.4%), Benin Republic (45%), Egypt (36%) and Indonesia (24.6%). On the other hand, Akkara et al. in India stated a prevalence rate of 86.8% following successful treatment for PTB which is higher than the figure obtained in this study. The variability in the prevalence rates generally may be related to the duration from TB infection to commencement of treatment as well as the varying periods from completion of PTB treatment to time of spirometric assessment. The high prevalence of spirometric 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 significant lung parenchymal damage would have occurred before antituberculous therapy. Furthermore, the relatively high proportion of patients with PTB retreatment in this study may have contributed to this high prevalence.
The predominant restrictive pattern observed mirrors the findings of Mbatchou Ngahane et al. in Cameroon, Banu Rekha et al. in India and Pasipanodya et al. in the US. However, some previous reports,, found obstructive pattern to be the main form of spirometric abnormality. The restrictive pattern may have occurred following significant lung parenchyma destruction, fibrosis of the lung tissue, scarring and stiffening of the lungs as well as reduction in lung compliance, all of which could be sequel to PTB based on the various immune cytokines involved. The fact that patients with smoking history were excluded from this study may also have contributed to the relatively lower number of individuals with obstructive pattern. Further evaluation of the group with restrictive defect showed that only a small proportion (16/130; 12.4%) had mild severity, whereas the others had higher grades of severity. None of the patients 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 and Brazil, and the finding of exertional dyspnoea as the predominant symptom after treatment for PTB was corroborated by Zakaria and Moussa in Egypt. Cough and chronic sputum production was, however, the most common symptom in a similar study in Indonesia. 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.
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. 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. 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., Willcox and Ferguson, Plit et al. and Báez-Saldaña et al. 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 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.
| 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.
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.
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
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]