Factors influencing the successful treatment of pulmonary infectious tuberculosis

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Factors influencing the successful treatment of infectious pulmonary tuberculosis

W-S. Chung,*^†Y-C. Chang,^† M-C. Yang^†

* Department of Internal Medicine, Hualien General Hospital, Hualien, ^†Institute of Health Care

S U M M A R Y Organisation Administration, College of Public Health, National Taiwan University, Taipei, Taiwan

S E T T I N G : Achieving successful treatment of infectious pulmonary tuberculosis (PTB) could reduce the spread of tuberculosis (TB) and the emergence of multidrug resistance.

O B J E C T I V E : To explore factors associated with success- ful treatment for sputum-positive PTB.

D E S I G N : This study used a population-based retrospec- tive cohort design. All PTB patients residing in southern Taiwan recorded in the tuberculosis registry from 1 Jan- uary to 30 June 2003 were identified. Each patient’s med- ical record was requested from treating hospitals and ret- rospectively reviewed for 15 months after the date PTB was confirmed.

R E S U L T S : There were 399 PTB patients included in the study. Factors significantly associated with successful treat-

ment included treatment by pulmonologists (OR 1.93), receiving directly observed therapy (DOT) (OR 1.76) and receiving treatment at the chest hospital (OR 5.41). Pa- tients of advanced age were less likely to achieve treatment success (OR 0.97). Among patients treated by pulmonolo- gists, those treated at the chest hospital had a significantly higher treatment success rate than those treated at other institutions (94.1% vs. 69.9%).

C O N C L U S I O N S : Patients treated with DOT and by pul- monologists, especially at the chest hospital, had a higher treatment success rate. DOT and training of care profes- sionals and institutions are therefore important factors that affect the successful treatment of TB.

K E Y W O R D S : infectious pulmonary tuberculosis; treatment success; health care institutions

TUBERCULOSIS (TB) is a serious public health, so- cial and economic problem. Infectious pulmonary tuberculosis (PTB) is a contagious disease that spreads through the air; when infectious people sneeze, cough and talk, they propel bacilli into the air. A person needs only a small number of bacilli to be infected. If stringent controls are not implemented, approximately 1 billion people will become infected, 150 million will become symptomatic and 36 million will die from TB between 2002 and 2020.¹

While the utilisation and accessibility of health care services have greatly improved since the National Health Insurance (NHI) programme was inaugurated in 1995, infectious PTB remains prevalent in Taiwan.

The NHI is a compulsory universal health programme that offers complete freedom of choice of health care providers, and all TB patients can seek free medical aid from any health care institution or any primary practitioner. More than 90% of the health care providers in Taiwan participate in the programme.^2,3

In the last 8 years, there has been an increasing trend in the number of TB patients treated by institutions other than TB sanatoria. The TB control system

in Taiwan, which has been operating for decades, was reformed with the implementation of the new public health system in 2001. Only around 10% of all patients with TB were reported and treated by TB sanatoria in 2001.⁴ However, despite convenient, readily available care for TB, there is an increasing trend in the number of TB patients in Taiwan. In 2002 there were 25 262 reported cases of TB, with a rate of 75 cases per 100 000 population. The treatment success rate for newly diagnosed PTB patients was 73%,⁵ lower than the 85% target set by the World Health Organi- zation (WHO).¹ TB is still the leading infectious cause of death in Taiwan, killing nearly 5.8/100 000 each year.⁶

The prevention of TB depends on the quality of the medical care available to patients. The organisation of the system through which this care is provided is essential to achieving successful prevention. Success- ful treatment of infectious PTB not only cures and saves lives, it also prevents the spread of infection and development of drug-resistant TB, which is far more difficult and costly to treat. As TB is a widespread disease, the need to establish effective treatment for cases

Correspondence to: Ming-Chin Yang, Room 637, 6F, No 17 Syujhou Rd, Jhongjheng District, Taipei 100, Taiwan. Tel:

(886) 7 3208159. Fax: (886) 7 316 1210. e-mail: mcy@ha.mc.ntu.edu.tw Article submitted 5 November 2005. Final version accepted 31 August 2006.

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with infectious PTB remains a major concern. We conducted a study to explore factors associated with successful treatment.

METHODS

We carried out a population-based medical record review in southern Taiwan, where the only chest specialty hospital geared towards specialised thoracic disease care, mainly for TB, is located. Hospitals and primary practitioners that provided TB care in the same region can be used as comparative care providers. Study areas include Chiayi County, Chiayi City, Tainan County and Tainan City. As mandated by law in Taiwan, all suspected and confirmed TB cases must be reported in a timely manner to the national computerised registry maintained by the Taiwan Center for Disease Control (CDC). Reporting of cases has been encouraged and reinforced through the implementation of a no-notification, no-reimbursement policy and a notification-for-fee policy since 1997.⁷ We requested data on all suspected and confirmed TB patients residing in the studied areas and recorded in the registry for the period 1 January to 30 June 2003.

The study team, including four registered nurses (each with a minimum of 6 years’ clinical experience), two head nurses (each with a minimum of 12 years’

clinical experience) and one pulmonologist, had un- dergone a series of training courses designed to ensure proper validation of data consistency. Site visits were arranged to review the medical record of each patient, and the 15-month follow-up of medical records after start of treatment was reviewed.

Health care institutions

Health care institutions that had ever reported cases in the study areas included the chest hospital, two ac- ademic medical centres, 11 regional hospitals and 15 district hospitals and primary practitioners (district hospitals and primary practitioners are regarded as being at the same level in terms of TB treatment). In Taiwan, institutions are classified by the government as follows: ‘medical centres’ are health care, training and research facilities that house over 500 acute-care beds; ‘regional hospitals’ have no fewer than 250 acute- care beds and are staffed by physicians of various specialties with the purpose of providing health care services to patients and training for specialists; and

‘district hospitals’ provide primary health care services similar to those offered by primary practitioners but with the added availability of in-patient care.

Infectious PTB

Infectious PTB is defined as sputum culture-confirmed disease caused by Mycobacterium tuberculosis, or two sputum smear examinations positive for acid-fast bacilli (AFB) or one positive sputum examination, radio- logical signs and a clinician’s decision to treat.⁸

Directly observed treatment

For directly observed treatment (DOT), a health worker or other trained person who is not a family member watches as the patient swallows anti-tuberculosis med- icines for at least the first 2 months of treatment.¹ DOT thus shifts the responsibility for cure from the patient to the health care system. In Taiwan, whether or not the patient is receiving DOT, TB is treated using WHO-recommended regimens; the initial phase consists of 2 months of isoniazid (H), ethambutol (E), rifampicin (R) and pyrazinamide (Z), followed by a 4-month continuation phase consisting of H, E and R (2HERZ/4HER).^9,10

Treatment success

Treatment success is defined as a patient who has been cured or has received a complete course of treatment.

A cured case is defined as a PTB patient who has finished treatment with a negative bacteriology result during and at the end of treatment. A case recorded as completed treatment is defined as a PTB patient who has finished treatment, but who has not met the crite- ria to be defined as a cure or a failure.^11,12

Ethical consideration

The study was approved by the Taiwan CDC. All staff members involved in the study signed a statement of agreement to maintain patient confidentiality.

Data analysis

Bivariate analyses with ² tests were used to compare differences in proportions of dichotomous and categorical variables, which extracted potential predictors of successful treatment. We then performed multi- variate logistic regression analyses on the potential predictors with P 0.10 obtained from bivariate analyses. We constructed a full model that included all the potential predictors identified through bivariate analyses and then applied the forward substitution model building procedure to construct a reduced model in which all the predictors were statistically significant.

Odds ratios (ORs) and 95% confidence intervals (CIs) of dichotomous and categorical risk variables on the binary outcome variables were calculated. All analyses were conducted using SPSS 10.0 software (SPSS Inc, Chicago, IL, USA), and all the tests were performed at the two-tailed significance level of 0.05.

RESULTS

From 1 January to 30 June 2003, 1072 TB cases were reported in the study areas. According to the data in the computerised register, 491 patients had at least a positive sputum smear or culture. We successfully reviewed the medical records of 482 (98%) patients.

After review, 83 patients were excluded, including one foreign labourer who was deported after diagnosis, 11 cases of extra-pulmonary TB, 38 cases of mis-

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diagnosis found during follow-up, 11 without any documented positive sputum smears or positive cultures, 19 cases with non-tuberculous mycobacteria, and three with multidrug-resistant TB (MDR-TB). The reason for excluding MDR-TB cases was because we only had a 15-month follow-up, which was not long enough for MDR-TB patients to have completed their treatment.^13,14

In Taiwan, new and retreatment cases receive basi- cally the same regimen. TB patients with a treatment history undergo drug susceptibility testing (DST). For the initial phase of treatment, 2HERZ is prescribed while awaiting the DST result, which helps in the decision as to whether or not to adjust treatment during the continuation phase. Of 22 (5.8%) patients who had received prior TB treatment, three patients with MDR-TB were excluded, and the remaining retreatment cases were included in the study. A final total of 399 patients, 293 men (73.4%) and 106 women (26.6%), were included in the analyses.

Descriptive analyses showed that 234 (59.1%) patients had positive AFB smears and 336 (90.8%) had positive mycobacterial cultures. Their ages at diagnosis ranged from 18 to 95 years (mean 6717), and the number of patients increased with age (12

25 years, 35 25–44 years, 101 45–64 years, and 251 64 years). The majority (64.1%) of the patients had comorbidities, the most common of which were diabetes (34.9%), chronic obstructive pulmonary disease (COPD) (21.9%), cancer (10.6%), bronchiectasis (9.5%), liver cirrhosis (3.8%) and uraemia (2.8%).

According to the chest X-rays (CXRs), 127 patients (31.9%) had cavitations. Among the 336 patients with positive mycobacterial cultures, 223 (66.4%) under- went species identification and were confirmed as hav- ing M. tuberculosis. Of the 399 patients, 250 (63.1%) received DOT at least during the initial treatment phase and 298 (74.7%) were treated by pulmonologists. Among these, 52 (13.0%) were treated at the chest hospital, 105 (26.3%) at medical centres, 144 (36.1%) at regional hospitals, and 98 (24.6%) at district hospitals or by primary practitioners. At the 15-month follow-up after initiation of treatment, the treatment success rate was 68.9% among those for whom follow-up was completed (Table 1).

Reduced models of multiple logistic regression analysis revealed that patients of advanced age were less likely to achieve treatment success (OR 0.97, 95%CI 0.96–0.99), and that compared with patients treated at a chest hospital, patients treated at medical centres, regional hospitals and district hospitals and by primary practitioners were also less likely to achieve treatment success (OR 0.18, 95%CI 0.05–0.63; 0.18, 95%CI 0.05–0.61; 0.21, 95%CI 0.06–0.75, respec- tively). Patients treated by pulmonologists were more likely to achieve treatment success (OR 1.94, 95%CI 1.18–3.20), as were patients who received DOT (OR 1.73, 95%CI 1.08–2.76) (Table 2).

After controlling for other factors, we found that patients treated at the chest hospital were still more likely to achieve treatment success (OR 5.41, 95%CI 1.61–18.18) compared with those at other health care institutions (including medical centres, regional hospitals, and district hospitals and primary practitioners).

Patients of advanced age were less likely to achieve treatment success (OR 0.97, 95%CI 0.96–0.99). Pa- tients who were treated by pulmonologists were more likely to achieve treatment success (OR 1.93, 95%CI 1.17–3.17), as were patients who received DOT (OR 1.76, 95%CI 1.10–2.8) (Table 3).

We also compared the outcome of care provided by pulmonologists at the chest hospital with that of other health care institutions and found that, amongst pulmonologists, those who offered services at the chest hospital achieved a higher treatment success rate (94.1% vs. 70.0%, P 0.001) and a lower mortal- ity rate (5.9% vs. 26.3%, P 0.001) than those who provided services at other health care institutions (Table 4).

Table 1 Characteristics of 399 patients with PTB and univariate analyses of potential predictors of

successful treatment

Characteristics

Patients n (%)

Successful treatment*

n (%) P value^†

Sex 0.392

Male 293 (73.4) 198 (67.6)

Female 106 (26.6) 77 (72.6)

Patients with comorbidities 0.018

No comorbidity 143 (35.9) 109 (76.2) With comorbidities 255 (64.1) 165 (64.7)

Unknown 1 1 (100)

CXR 0.015

Cavitations 127 (31.9) 98 (77.2) No cavitation 271 (68.1) 176 (64.9)

Unknown 1 1 (100)

Previous TB treatment 0.815

Yes 22 (5.8) 16 (72.7)

No 360 (94.2) 246 (68.3)

Unknown 17 12 (70.6)

DOT 0.002

Yes 250 (63.1) 186 (74.4)

No 146 (36.9) 86 (58.9)

Unknown 3 3 (100)

Diagnostic and treating

physicians 0.001

Pulmonologist 298 (74.7) 221 (74.2) Non-pulmonologist 102 (25.6) 55 (53.9)

Health-care institutions 0.001

Medical centre 105 (26.3) 68 (64.8) Regional hospital 144 (36.1) 92 (63.9) District hospital and

primary practitioners 98 (24.6) 66 (67.3) Chest specialty hospital 52 (13.0) 49 (94.2)

Total 399 (100) 275 (68.9)

* 15-month follow-up after start of treatment.

†² test.

PTB pulmonary tuberculosis; CXR chest X-ray; TB tuberculosis; DOT directly observed treatment.

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DISCUSSION

TB causes considerable morbidity and mortality world- wide. The persistence of TB and the emergence of MDR-TB as major public health problems result from the presence of individuals with active infection in whom the disease remains unsuccessfully treated.¹⁵ Treatment outcome results serve as a tool to control the quality of TB treatment provided by the health care institutions and the health system. However, completion of TB treatment is the most important priority of TB control programmes.¹⁶ Public health system reform, with decentralisation of TB prevention, has been implemented in Taiwan since 2001. However, although

Table 2 Multiple logistic regression for factors affecting the successful treatment of infectious PTB

Variables

Full model Reduced model*

Reference group OR (95%CI) OR (95%CI)

Age 0.03^† 0.97 (0.96–0.99) 0.03^† 0.97 (0.96–0.99)

Physician

Pulmonologist Non-pulmonologist 0.66^‡ 1.93 (1.17–3.18) 0.66^§ 1.94 (1.18–3.20)

DOT

Yes No 0.55^‡ 1.73 (1.07–2.79) 0.55^‡ 1.73 (1.08–2.76)

CXR

Cavitations No cavitation 0.02 1.02 (0.59–1.78)

Comorbidities

Yes No 0.23 0.8 (0.48–1.32)

Institutions

District hospital and primary practitioners

Chest hospital 1.52^‡ 0.22 (0.06–0.79) 1.57^‡ 0.21 (0.06–0.75)

Regional hospital 1.69^† 0.18 (0.05–0.64) 1.74^§ 0.18 (0.05–0.61)

Medical centre 1.68^§ 0.19 (0.05–0.67) 1.73^§ 0.18 (0.05–0.63)

Hosmer and Lemeshow ² 5.62 (P 0.689) ² 3.322 (P 0.91)

* Using forward substitution.

†P 0.001.

‡P 0.05.

§P 0.01.

PTB pulmonary tuberculosis; OR odds ratio; CI confidence interval; DOT direct observation of treatment; CXR chest X-ray.

Table 3 Multiple logistic regression for factors affecting the successful treatment of infectious PTB

Full model Reduced model*

Variables Reference group OR (95%CI) OR (95%CI)

Age 0.03^† 0.97 (0.96–0.99) 0.03^† 0.97 (0.96–0.1)

Physician

Pulmonologist Non-pulmonologist 0.65^‡ 1.92 (1.17–3.16) 0.66^§ 1.93 (1.17–3.17)

DOT

Yes No 0.57^‡ 1.76 (1.1–2.83) 0.56^‡ 1.76 (1.10–2.8)

CXR

Cavitations No cavitation 0.01 1.01 (0.58–1.73)

Comorbidities

Yes No 0.23 0.8 (0.48–1.32)

Institutions

Chest hospital Other health care institutions 1.65^§ 5.19 (1.52–17.66) 1.69^§ 5.41 (1.61–18.18)

Hosmer and Lemeshow ² 5.13 (P 0.74) ² 4.49 (P 0.81)

* Using forward substitution.

†P 0.001.

‡P 0.05.

§P 0.01.

PTB pulmonary tuberculosis; OR odds ratio; CI confidence interval; DOT direct observation of treatment; CXR chest X-ray.

Table 4 Comparison of outcome of care by pulmonologists at the chest hospital and at the other health care institutions

Chest hospital (n 51)*Yes

n (%)

(n 247)No n (%) P value Successful treatment (n 298)

Yes 48 (94.1) 173 (70.0) 0.001

No 3 (5.9) 74 (30.0)

Mortality (n 298)^†

Yes 3 (5.9) 65 (26.3) 0.001

No 48 (94.1) 182 (73.7)

* As one patient was not treated by a pulmonologist at the chest hospital, the number is different from Table 1.

†Patients who died during TB treatment.

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the NHI programme has improved the utilisation and accessibility of health care services for patients, TB cases continue to increase in Taiwan. This phenome- non prompted us to identify factors associated with successful treatment.

In our study, male predominance and elderly susceptibility to TB infection were observed, which are consistent with our national CDC report and other published data.^4,17–19 Although 5.8% of our study sub- jects had a history of previous TB treatment, their treatment success rate was not significantly different from that of new cases. This result may be associated with the small number of cases with a TB treatment history and the exclusion of MDR-TB patients from in our study.

Treatment at the chest hospital or by pulmonologists or receipt of DOT were found to be significant factors for successful treatment of TB. Patients treated with DOT had a significantly higher treatment success rate than those treated with self-administered therapy. Our study results were consistent with previous studies.^20–22 A recent study revealed that earlier DOT participation can lead to overall shorter treatment duration.²³ Increasing age was another indepen- dent factor for less successful PTB treatment; old age was significantly associated with treatment failure and death.^24,25 This seemed to be due not only to non- adherence to anti-tuberculosis treatment but also to more advanced disease, with greater mortality.²⁶

The higher treatment success rate observed at the chest hospital than in other institutions is likely due to the physicians’ expertise with TB, a more stringent out-patient follow-up procedure and more scrupulous patient education programmes. Patients treated by pulmonologists appeared to have a higher treatment success rate than those treated by non-pulmonologist physicians. A pivotal factor may be the unfamiliar- ity of non-pulmonologist physicians with the treatment of TB. Nonetheless, the fact that patients treated by pulmonologists at the chest hospital had a higher treatment success rate and a lower mortality rate than those treated by pulmonologists at other institutions indicated that both the training of care providers and the institution providing the care are important factors that affect the quality of care. The limitation of this study is that although we could record comorbidities from medical records, we could not ob- tain information about disease severity or possible causes of death, which may be a confounder of treatment success.

In conclusion, patients with TB treated by DOT and treated by pulmonologists, especially at the chest hospital, had a higher treatment success rate after ad- justing for age, comorbidities and CXR characteristics. Treating TB patients using DOT, and training care professionals and institutions in patient education and case holding are important factors that affect the outcome of TB care.

Acknowledgements

The authors are grateful to the Taiwan Department of Health for providing research grants.

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R É S U M É

C O N T E X T E : L’obtention d’un succès dans le traitement de la tuberculose pulmonaire (TBP) contagieuse pour- rait limiter la dispersion de la TB et l’apparition d’une multirésistance.

O B J E C T I F : Explorer les facteurs en association avec un traitement couronné de succès dans les cas de TBP à bacil- loscopie positive.

S C H É M A : Cette étude a utilisé un schéma de cohorte ré- trospective basé sur la population. Tous les patients TBP résidents au Sud de Taïwan inscrits dans les registres de la TB entre le 1^er janvier et le 30 juin 2003 ont été iden- tifiés. On a demandé dans les hôpitaux en charge les dos- siers médicaux de chaque patient et on les a examinés de manière rétrospective pendant 15 mois après confirma- tion de la TB.

R É S U L T A T S :On a inclus 399 patients TBP. Les facteurs

en association significative avec le succès du traitement comportent un traitement par des pneumologues (OR 1,928), le fait de bénéficier d’un traitement directement ob- servé (DOT) (OR 1,756) et le fait d’être traité à l’hôpital thoracique (OR 5,409). Les patients avec un âge avancé avaient moins tendance à avoir un traitement couronné de succès (OR 0,971). Parmi les patients traités par les pneumologues, le taux de traitement couronné de succès a été significativement plus élevé à l’hôpital que chez ceux traités dans d’autres institutions (94,1% vs. 69,9%).

C O N C L U S I O N :Les patients traités par DOT et par les pneumologues, particulièrement à l’hôpital thoracique, ont un taux plus élevé de succès de traitement. Pour cette raison, le DOT ainsi que la formation des professionnels de soins et des institutions sont d’importants facteurs affectant le succès du traitement de la TB.

R E S U M E N

M A R C O D E R E F E R E N C I A : El tratamiento exitoso de la tuberculosis pulmonar (TBP) contagiosa podría reducir la diseminación de la enfermedad y la aparición de farma- corresistencia múltiple.

O B J E T I V O : Explorar los factores asociados con el éxito del tratamiento de la TBP con baciloscopia positiva del esputo.

M É T O D O : Fue este un estudio de cohortes retrospectivo de base poblacional. Se incluyeron todos los pacientes con TBP residentes en el sur de Taiwán, consignados en el registro de TB entre el 1^o de enero y el 30 de junio de 2003. Se solicitó la historia clínica de cada paciente al hospital que había suministrado el tratamiento y se ana- lizaron los 15 meses posteriores a la confirmación del diagnóstico de TBP.

R E S U L T A D O S :El estudio comprendió 399 pacientes con TBP. Entre los factores asociados en forma significativa con el éxito del tratamiento se encontraron tratamiento

por un neumólogo (OR 1,928), suministro del tratami- ento breve directamente observado (DOT ; OR 1,756) y suministro del tratamiento en un hospital de enferme- dades respiratorias (OR 5,409). En los pacientes con edad avanzada había menos tendencia de éxito del tratami- ento (OR 0,971). De los pacientes tratados por neumó- logos, aquellos tratados en un hospital de enfermedades respiratorias presentaron una tasa de éxito significativa- mente superior a la tasa de los pacientes tratados en otros establecimientos (94,1% contra 69,9%).

C O N C L U S I Ó N :Los pacientes tratados con DOT por neu- mólogos, sobre todo en un hospital especializado, pre- sentaron una tasa más alta de tratamiento exitoso. Por esta razón, la capacitación de los proveedores de salud y del personal de los establecimientos sanitarios en la aplica- ción de DOT constituye un factor importante con reper- cusiones sobre el éxito del tratamiento antituberculoso.