INT J TUBERC LUNG DIS 13(5):620–625

© 2009 The Union

Risk factors for extra-pulmonary tuberculosis compared

to pulmonary tuberculosis

J. N. Lin,*† C. H. Lai,*† Y. H. Chen,†‡ S. S. J. Lee,§ S. S. Tsai,¶ C. K. Huang,* H. C. Chung,* S. H. Liang,*

H. H. Lin*
* Division of Infectious Diseases, Department of Internal Medicine, E-Da Hospital/I-Shou University, Kaohsiung,
† Graduate Institute of Medicine, ‡ Division of Infectious Diseases, Department of Internal Medicine, Kaohsiung Medical

University Hospital, Kaohsiung, § Division of Infectious Diseases, Department of Internal Medicine, Kaohsiung Veterans
General Hospital, Kaohsiung, ¶ Department of Healthcare Administration, E-Da Hospital/I-Shou University, Kaohsiung
County, Taiwan

SUMMARY

B A C K G R O U N D : Tuberculosis (TB) continues to be a ma- cases. Of the 766 patients, 3% of PTB patients had EPTB,
jor global health problem. Extra-pulmonary TB (EPTB) while 19.6% of EPTB patients also had PTB. The most
manifests with protean symptoms, and establishing a frequently involved EPTB site was the bone and joints
diagnosis is more difficult than pulmonary TB (PTB). (24.5%). The incidence of EPTB vs. PTB decreased sig-
S E T T I N G : A university-affiliated hospital in southern nificantly for each decade increase in patient age. Multi-
Taiwan. variate logistic regression analysis showed that being fe-
O B J E C T I V E : To analyse the risk factors for EPTB com- male, not being diabetic, having end-stage renal disease
pared with PTB. and not smoking were independent risk factors for EPTB.
D E S I G N : This retrospective study compared patients C O N C L U S I O N : This study defines the risk factors for
with EPTB and PTB in southern Taiwan by analysing EPTB compared with PTB. Awareness of these factors is
their demographic data and clinical underlying diseases. essential for physicians to have a high index of suspicion
Risk factors for EPTB were further analysed. for accurate and timely diagnosis.
R E S U LT S : A total of 766 TB patients were enrolled in K E Y W O R D S : Mycobacterium tuberculosis; tuberculo-
this study, with 102 (13.3%) EPTB and 664 (86.7%) PTB sis; extra-pulmonary tuberculosis; risk factors

TUBERCULOSIS (TB) continues to be a major global Although several retrospective studies have been
health problem, causing disability and death world- published to evaluate the risk factors for EPTB com-
wide. According to the World Health Organization’s pared with PTB, few have thoroughly analysed the as-
Tuberculosis Fact Sheet 2008, one third of the world’s sociated underlying diseases that could alter the pro-
population is estimated to be currently infected with portion of EPTB to PTB. The purpose of this study was
Mycobacterium tuberculosis.1 The incidence of TB has to compare the characteristics and underlying diseases
declined in most industrialised countries over the past of patients with EPTB and PTB, and to recognise pos-
decades where the number of cases has been stable or sible risk factors for EPTB.
declining since 1995.2,3 However, a striking increase
was noted in the early 1990s in the United States, METHODS
which has been attributed to the epidemic of human
immunodeficiency virus (HIV) infection, substantial Study population and design
levels of immigration from areas with a high TB prev- This retrospective study was approved by the institu-
alence and failure of TB control.4,5 tional review board (No. EMRP-097-018) at E-Da
The clinical manifestations of TB are diverse. The Hospital, a university-affiliated hospital in southern
most frequently involved organ is the lungs, although Taiwan. Patients notified as having TB disease to the
all organs can be affected by the bacilli.6,7 The propor- Centers for Disease Control and Prevention of Tai-
tion of patients with extra-pulmonary TB (EPTB) rela- wan from April 2004 to March 2008 were enrolled.
tive to pulmonary TB (PTB) varies and depends on Demographic information on age and sex, duration
associated diseases, ethnicity and countries.6–8 For ex- of symptoms, clinical underlying diseases—including
ample, EPTB has been detected more frequently among diabetes mellitus, end-stage renal disease (ESRD), liver
HIV-infected than non-HIV-infected individuals.9,10 cirrhosis, malignancies, immunosuppressive drug use,

Correspondence to: Hsi-Hsun Lin, 1 E-Da Road, Jiau-Shu Tsuen, Yan-Chau Shiang, Kaohsiung County, Taiwan 824. Tel:
(+886) 7615 0011 ext. 91469. Fax: (+886) 7615 0928. e-mail: erlongtw@yahoo.com.tw
Article submitted 10 June 2008. Final version accepted 14 November 2008.
 Risk factors for EPTB 621

alcoholism, smoking, HIV infection or AIDS, chronic t-test. The χ2 test was used to analyse the trend among
obstructive pulmonary disease (COPD), congestive different age groups. All P values were 2-tailed, and
heart failure, hypertension, intravenous drug use, P < 0.05 was considered statistically significant. To
history of TB infection and cerebrovascular accident identify the risk factors for EPTB and control for po-
—were collected from the medical records. ESRD tential confounders, all variables associated with a
was defined as renal failure requiring long-term di- level of significance of <0.20 in univariate analyses
alysis or kidney transplantation for survival. Liver were included in a logistic regression model for multi-
cirrhosis was defined on the basis of its typical sono- variate analysis (backward stepwise methods by likeli-
graphic appearance. Immunosuppressive drug use hood ratio). Odds ratios (OR), 95% confidence inter-
was defined as the use of cytotoxic agents or cortico- vals (95%CI) and P values were calculated for each
steroids (more than 30 mg prednisolone daily or its potential risk factor. Hosmer-Lemeshow goodness-
equivalent for ⩾1 week). Alcoholism was defined of-fit test was used to assess the fitness of the model.
as habitual alcohol consumption. COPD, congestive
heart failure and hypertension were defined as dis- RESULTS
eases diagnosed by the subspecialists and needing
long-term medication. The proportion of EPTB was Sites of extra-pulmonary TB
calculated for the trend for each decade increase in During the study period, 766 patients with TB were
patient’s age. To evaluate whether different age groups enrolled in this study, with 102 (13.3%) classified as
had a role in the clinical presentation of EPTB, age EPTB and 664 (86.7%) as PTB. All enrolled patients
groups (0–24, 25–39, 40–59, ⩾60 years) at diagnosis were Chinese living in Taiwan. Of the 766 patients,
were introduced as categorical variables, as described 3% of PTB patients had EPTB and 19.6% of EPTB
elsewhere.11 patients also had PTB. Among the EPTB cases, the
most frequently involved site was the bone and joints
Definition of pulmonary TB and extra-pulmonary TB (24.5%), followed by the genito-urinary system
The diagnosis of TB was based on: 1) sputum, pleural (20.6%), abdomen (18.6%), lymph nodes (17.6%),
effusion, pericardial effusion, ascites, urine, cerebral disseminated TB (10.8%), skin (2.9%), meninges
spinal fluid, synovial fluid and abscess or tissue cul- (2.0%), pericardium (1.0%) and others (laryngeal,
ture that yielded M. tuberculosis. Patients were ex- vocal chords 2.0%; Figure 1).
cluded from our study if acid-fast stain was positive on
the specimens but they were M. tuberculosis culture- Patient characteristics
negative; 2) histological findings of granulomatous Of these 766 patients, 561 (73.2%) were male and
inflammation (granulomas composed of epithelioid 205 (26.8%) were female. Females were significantly
cells and Langhans giant cells with or without case- predisposed to EPTB (P < 0.001). The mean age was
ous necrosis) combined with positive acid-fast stain in lower among EPTB than PTB patients (58.8 ± 18.8 vs.
the pathology specimens (i.e., lymph node, pleura, 63.9 ± 17.3 years, P < 0.01; Table 1). On the χ2 test
prostate, skin, gastro-intestinal tract, genito-urinary for trend, EPTB incidence decreased for each decade
tract, bone, tendon, synovial tissue) and favourable increase in patient’s age (OR 0.85, 95%CI 0.75–
clinical response to anti-tuberculosis chemotherapy. 0.95, P < 0.01; Figure 2). The median duration of
The definition of EPTB was based on the guidelines symptoms on presentation in patients with EPTB and
of the American Thoracic Society and the US Centers
for Disease Control and Prevention.12 As in previous
studies,6,13 EPTB was defined as extra-pulmonary in-
volvement with or without concomitant pulmonary
involvement. Patients with only pulmonary involve-
ment were categorised under the PTB group. Pleural
involvement in TB is a direct extension of disease from
the lung parenchyma, so patients with pleural involve-
ment were categorised under PTB for the purpose of
this analysis.

Statistical analysis
The results were analysed using the commercially
available SPSS software package (Statistical Package
for Social Sciences, version 14.0, SPSS Inc, Chicago,
IL, USA) to test the difference between case and con-
Figure 1 Proportional distribution of patients with EPTB and
trol patients. Categorical variables were analysed us- PTB by anatomic site. *Others includes TB of the vocal chords
ing the χ2 test or Fisher’s exact tests, as appropriate. and larynx. TB = tuberculosis; EPTB = extra-pulmonary TB; PTB =
Continuous variables were analysed using Student’s pulmonary TB.
622 The International Journal of Tuberculosis and Lung Disease

PTB were 30 days (mean ± standard deviation [SD], Risk factors for extra-pulmonary TB
61.2 ± 103.0 days) and 13 days (mean ± SD, 49.2 ± On univariate analysis, patients with diabetes melli-
119.2 days), respectively (P < 0.001; Table 1). tus were significantly predisposed to PTB relative to
EPTB (P < 0.01). In contrast, patients with ESRD
Table 1 Demographic characteristics and underlying diseases had a predisposition for EPTB (P = 0.001). Smokers
of patients with EPTB and PTB had a higher risk for PTB than non-smokers (P <
EPTB patients PTB patients
0.001; Table 1). There were no statistically significant
(n = 102) (n = 664) differences between patients with EPTB and PTB as
Characteristics n (%) n (%) P value regards the other underlying conditions, identified in
Age, years, mean ± SD 58.8 ± 18.8 63.9 ± 17.3 <0.01 Methods.
Age groups, years A multivariate logistic regression analysis model
⩽24 6 (5.9) 12 (1.8) Referent was used to further analyse the significant factors for
25–39 9 (8.8) 57 (8.6) 0.06
40–59 31 (30.4) 179 (27.0) 0.048
EPTB, and showed that being female (OR 1.69, 95%CI
⩾60 56 (54.9) 416 (62.7) 0.01 1.02–2.80, P = 0.04) and having ESRD (OR 3.74;
Male sex 58 (56.9) 503 (75.8) <0.001 95%CI 1.45–9.67, P < 0.01) were independent risk
Duration of symptoms, factors for EPTB. In contrast, diabetes mellitus (OR
days, median 30 13 <0.001 0.41, 95%CI 0.22–0.76, P < 0.01) and smoking (OR
Diabetes mellitus 15 (14.7) 191 (28.8) <0.01 0.57, 95%CI 0.34–0.95, P = 0.03) were negatively
ESRD 9 (8.8) 13 (2.0) 0.001 associated with EPTB (Table 2).
Liver cirrhosis 6 (5.9) 28 (4.2) 0.44
Malignancy 16 (15.7) 69 (10.4) 0.13 DISCUSSION
Immunosuppressive drug use 4 (3.9) 38 (5.7) 0.46
Alcoholism 2 (2.0) 28 (4.2) 0.41 TB can involve virtually any tissue or organ. Prompt
Smoking 31 (31.0)* 344 (52.8)† <0.001 and accurate diagnosis of EPTB is essential, but is
HIV infection 2 (2.0) 3 (0.5) 0.13
COPD 3 (2.9) 55 (8.3) 0.06 Table 2 Multivariate logistic regression mode of independent
CHF 3 (2.9) 20 (3.0) 1.00 risk factors for the development of EPTB compared to
Hypertension 27 (26.5) 137 (20.6) 0.18 PTB (n = 752)*
IDU 0 2 (0.3) 1.00 Risk factor OR 95%CI P value
History of TB 6 (5.9) 25 (3.8) 0.29
Age, years
History of CVA 4 (3.9) 33 (5.0) 0.81 ⩽24 1 Referent
* n = 100.
25–39 0.38 0.11–1.34 0.13
† n = 652. 40–59 0.60 0.20–1.82 0.37
EPTB = extra-pulmonary TB; PTB = pulmonary TB; SD = standard deviation; ⩾60 0.41 0.14–1.20 0.10
ESRD = end-stage renal disease; HIV = human immunodeficiency virus; COPD = Sex
chronic obstructive pulmonary disease; CHF = congestive heart failure; IDU = Female 1.69 1.02–2.80 0.04
intravenous drug user; TB = tuberculosis; CVA = cerebrovascular accident.
Male 1 Referent
Diabetes mellitus
Yes 0.41 0.22–0.76 <0.01
No 1 Referent
ESRD
Yes 3.74 1.45–9.67 <0.01
No 1 Referent
Malignancy
Yes 1.42 0.74–2.72 0.29
No 1 Referent
Smoking
Yes 0.57 0.34–0.95 0.03
No 1 Referent
HIV infection
Yes 5.78 0.83– 40.10 0.08
No 1 Referent
COPD
Yes 0.39 0.12–1.30 0.13
No 1 Referent
Hypertension
Yes 1.69 0.99–2.89 0.06
Figure 2 Case numbers of patients with EPTB and PTB (bars) No 1 Referent
and percentage of patients with EPTB in all TB patients in differ-
ent age groups (line). Significant difference by χ2 test for trend * Analysed by backward stepwise methods (likelihood ratio). Data were
in the ratio of EPTB with each decade increase in patient age (OR missing for 2 in the EPTB group (2/102, 1.97%) and 12 in the PTB group
(12/664, 1.81%).
0.85, 95%CI = 0.75–0.95, P < 0.01). EPTB = extra-pulmonary OR = odds ratio; CI = confidence interval; ESRD = end-stage renal disease;
tuberculosis; PTB = pulmonary tuberculosis; TB = tuberculosis; HIV = human immunodeficiency virus; COPD = chronic obstructive pulmo-
OR = odds ratio; CI = confidence interval. nary disease.
 Risk factors for EPTB 623

often delayed because symptoms vary depending on are known to have a disruption of their cell-mediated
the affected sites and patients may have few if any of immunity that is responsible for the killing of intra-
the classic signs and symptoms of cough, fever, night cellular organisms such as M. tuberculosis.25 There is
sweats, weight loss, anorexia or fatigue.7 As it is less a 6.9–52.5-fold increased risk of TB infection in pa-
common and less familiar to most physicians, espe- tients with chronic renal failure and on dialysis as
cially in relatively inaccessible sites, EPTB usually pres- compared to the general population.26 In the reports
ents a greater diagnostic challenge than PTB.14,15 To by Sen et al. and Abdelrahman et al.,27,28 EPTB was
establish a confirmation, therefore, invasive procedures more frequent among patients with ESRD. However,
are frequently needed, making a diagnosis even more to our knowledge, there is no similar study to compare
difficult. This was reflected in our study by the dura- the risk ratio of ESRD in patients with EPTB to PTB.
tion of symptoms in patients with EPTB being more One of the reasons may be that there are too few cases
than twice as long as in patients with PTB (median 30 involved in the studies to show the significance of
vs. 13 days). ESRD. However, ESRD is prevalent in Taiwan. Ac-
Taiwan is an endemic area for TB, with more than cording to data from the Taiwan Society of Nephrol-
16 000 newly reported cases and an incidence rate of ogy, the incidence and prevalence of ESRD in Taiwan
74.5 per 100 000 population per year.16 In our study, was 375 and 1760/100 000/year, which ranked first
the most common site of EPTB was the bone and joints, and second, respectively, worldwide.29 Our study re-
followed by the genito-urinary system, abdomen and vealed patients with ESRD had a 3.74-fold increased
lymph nodes. The distribution of EPTB is different risk of EPTB compared to PTB.
from previous studies. Yang et al. reported that the Smoking has been identified as a risk factor for
most common sites involved were the bone/joints and PTB as well as EPTB.30 Gonzalez et al.7 and Musellim
lymph nodes in the United States,6 while the genito- et al.31 found that smoking had a negative association
urinary system and skin were the most common sites for EPTB compared to PTB. In our studies, smoking
in a report from Hong Kong.17 The difference may was also identified as an independent risk factor for
be attributable to ethnicity or underlying associated PTB compared to EPTB. Chronic lung disease caused
diseases. by smoking may predispose patients to PTB infection.
In this study, we found on trend analysis that the As regards the other risk factors, including liver
incidence of EPTB decreased significantly by 15% for cirrhosis, malignancies, immunosuppressive drug use,
each decade increase in patient age. As previous pub- alcoholism, HIV infection, COPD, congestive heart
lished data show,6–8,13,17 extra-pulmonary sites tend failure, intravenous drug use, history of TB and cere-
to be more commonly involved in younger than older brovascular accident, there were no statistical differ-
patients. Our study was consistent with these studies ences between the EPTB and the PTB groups. In the
and further showed that there was a significant de- Hong Kong study,17 there was no association of EPTB
creasing trend of proportion of EPTB to PTB with in- with liver diseases, which was consistent with our
creasing age by decades. study. However, Gonzalez et al. reported liver cirrho-
PTB is more common in males than in females, sis to be a risk factor for EPTB in the United States.7
while the opposite is true for EPTB.6–8,13,17 Our study Regarding malignancies and immunosuppressive drug
corroborated this sex difference in the incidence rates use, our data and previously published data con-
of PTB and EPTB. The causes of sex differences in TB cluded consistently that there was no association with
occurrence are not well understood. Cellular immu- EPTB.13,17,31
nity, hormones, access to health care, socio-economic According to published reports,9,10 HIV infection
factors and cultural factors have been linked to these is well known to be associated with EPTB. However,
differences.18,19 Underdiagnosis or underreporting of there was no statistical significance of HIV infection in
TB in females have also been hypothesised.20,21 How- our study, which is undoubtedly explained by the very
ever, a study conducted in the United States suggested small number of HIV-infected cases in our series.
that differences in TB rates between the sexes may be Our study pointed out the important risk factors
due to a difference in transmission dynamics rather for EPTB. However, there are still some limitations to
than diagnosis or reporting biases.22 The real reasons our study. For example, surgeons infrequently suspect
for the sex difference in TB sites remain to be deter- EPTB infection before operations and few surgical
mined through further studies. specimens are sent for TB culture. This situation makes
Most studies have shown diabetes mellitus to be accurate diagnosis of EPTB lower than expected and
strongly associated with TB infection.23,24 When com- many patients with EPTB may have been excluded
pared to EPTB, patients with diabetes mellitus showed from our study. Further prospective studies are indi-
a predisposition for PTB.7,13,17 Our study was consis- cated to overcome this limitation.
tent with other studies indicating that non-diabetic pa-
tients had a higher risk for PTB compared to EPTB.
CONCLUSIONS
However, the exact mechanism is still unknown.
Another striking finding in this study is the rela- The protean and non-specific manifestations of EPTB
tionship between ESRD and EPTB. Patients with ESRD frequently make accurate diagnosis difficult. Our study
624 The International Journal of Tuberculosis and Lung Disease

suggests that younger age, female sex, non-diabetes —a hospital-based retrospective study. BMC Infect Dis 2008;
mellitus, ESRD and non-smoking were risk factors for 8: 8.
14 Alvarez S, McCabe W R. Extra-pulmonary tuberculosis revis-
EPTB relative to PTB. Although the exact mecha-
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EPTB may help physicians maintain a high index of J Med 1985; 79: 467– 478.
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RÉSUMÉ

C A D R E : La tuberculose (TB) reste un problème mondial OBJECTIF : Analyser les facteurs de risque de TBEP par
majeur de santé publique. Les symptômes de la TB extra- rapport à la TBP.
pulmonaire (TBEP) sont très variables et le diagnostic est S C H É M A : Cette étude rétrospective a comparé les pa-
plus difficile à établir que pour la TB pulmonaire (TBP). tients atteints d’une TBEP et TBP dans le Sud de Taiwan
 Risk factors for EPTB 625

en analysant leurs données démographiques et les mala- nies d’âge du patient. Une analyse multivariée de régres-
dies cliniques sous-jacentes. En outre, on a analysé les sion logistique a montré que les facteurs indépendants de
facteurs de risque de TBEP. risque de TBEP sont le sexe féminin, l’absence de diabète
R É S U LTAT S : Ont été enrôlés dans cette étude 766 pa- sucré, les maladies rénales au stade terminal et le fait de
tients TB dont 102 (13,3%) atteints de TBEP et 664 ne pas fumer.
(86,7%) de TBP. Parmi ces 766 patients, 3% de ceux at- C O N C L U S I O N : Cette étude signale les facteurs de risque
teints de TBP souffraient en outre d’une TBEP et 19,6% de TBEP par rapport à la TBP. Une bonne prise de con-
de ceux atteints de TBEP souffraient également d’une science de cette situation est essentielle pour que les méde-
TBP. Le site le plus fréquent de la TBEP est constitué cins gardent un index élevé de suspicion en vue d’un diag-
par les os et les articulations (24,5%). Le ratio de TBEP nostic précis et porté en temps utile.
décroît de manière significative dans chacune des décen-

RESUMEN

M A R C A D E R E F E R E N C I A : La tuberculosis (TB) continúa bién localización extrapulmonar y 19,6% de los pacien-

siendo un grave problema de salud. La TB extrapulmonar tes diagnosticados con TBEP presentaron también TBP.
(TBEP) se manifiesta con síntomas larvados y su diag- La localización extrapulmonar más frecuente fue osteo-
nóstico es más difícil de establecer que en la TB pulmo- articular (24,5%). El cociente de TBEP disminuyó sig-
nar (TBP). nificativamente con cada decenio de aumento en la edad
O B J E T I V O : Analizar los factores de riesgo de TBEP, en de los pacientes. Según el análisis de regresión logística
comparación con los factores de la TBP. multifactorial, el sexo femenino, la nefropatía terminal y
M É T O D O : En este estudio retrospectivo se compararon la ausencia de tabaquismo fueron factores independien-
los datos demográficos y las enfermedades clínicas subya- tes de riesgo de TBEP ; se observó una correlación nega-
centes de pacientes con TBP y TBEP en el sur de Taiwán. tiva de la diabetes sacarina con la TBEP.
Se profundizó el análisis de los factores de riesgo de C O N C L U S I Ó N : En el presente estudio se determinaron
TBEP. los factores de riesgo de TBEP con respecto a la locali-
R E S U LTA D O S : Se incluyeron en el estudio 766 pacientes zación pulmonar. Es importante el conocimiento de esta
tuberculosos, de los cuales 102 casos de TBEP (13,3%) enfermedad y que los médicos mantengan un alto índice
y 664 casos de TBP (86,7%). De los 766 pacientes, 3% de de presunción, con el fin de establecer el diagnóstico en
los pacientes con diagnóstico de TBP presentaron tam- forma precisa y oportuna.