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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
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.
BACKGROUND: Tuberculosis (TB) continues to be a ma-
jor global health problem. Extra-pulmonary TB (EPTB)
manifests with protean symptoms, and establishing a
diagnosis is more dif cult than pulmonary TB (PTB).
SETTING: A university-af liated hospital in southern
Taiwan.
OBJECTIVE: To analyse the risk factors for EPTB com-
pared with PTB.
DESIGN: This retrospective study compared patients
with EPTB and PTB in southern Taiwan by analysing
their demographic data and clinical underlying diseases.
Risk factors for EPTB were further analysed.
RESULTS: A total of 766 TB patients were enrolled in
this study, with 102 (13.3%) EPTB and 664 (86.7%) PTB
cases. Of the 766 patients, 3% of PTB patients had EPTB,
while 19.6% of EPTB patients also had PTB. The most
frequently involved EPTB site was the bone and joints
(24.5%). The incidence of EPTB vs. PTB decreased sig-
ni cantly for each decade increase in patient age. Multi-
variate logistic regression analysis showed that being fe-
male, not being diabetic, having end-stage renal disease
and not smoking were independent risk factors for EPTB.
CONCLUSION: This study de nes the risk factors for
EPTB compared with PTB. Awareness of these factors is
essential for physicians to have a high index of suspicion
for accurate and timely diagnosis.
KEY WORDS: Mycobacterium tuberculosis; tuberculo-
sis; extra-pulmonary tuberculosis; risk factors
TUBERCULOSIS (TB) continues to be a major global
health problem, causing disability and death world-
wide. According to the World Health Organization’s
Tuberculosis Fact Sheet 2008, one third of the world’s
population is estimated to be currently infected with
Mycobacterium tuberculosis.1 The incidence of TB has
declined in most industrialised countries over the past
decades where the number of cases has been stable or
declining since 1995.2,3 However, a striking increase
was noted in the early 1990s in the United States,
which has been attributed to the epidemic of human
immunode ciency virus (HIV) infection, substantial
levels of immigration from areas with a high TB prev-
alence and failure of TB control.4,5
The clinical manifestations of TB are diverse. The
most frequently involved organ is the lungs, although
all organs can be affected by the bacilli.6,7 The propor-
tion of patients with extra-pulmonary TB (EPTB) rela-
tive to pulmonary TB (PTB) varies and depends on
associated diseases, ethnicity and countries.6–8 For ex-
ample, EPTB has been detected more frequently among
HIV-infected than non-HIV-infected individuals.9,10
Although several retrospective studies have been
published to evaluate the risk factors for EPTB com-
pared with PTB, few have thoroughly analysed the as-
sociated underlying diseases that could alter the pro-
portion of EPTB to PTB. The purpose of this study was
to compare the characteristics and underlying diseases
of patients with EPTB and PTB, and to recognise pos-
sible risk factors for EPTB.
METHODS
Study population and design
This retrospective study was approved by the institu-
tional review board (No. EMRP-097-018) at E-Da
Hospital, a university-af liated hospital in southern
Taiwan. Patients noti ed as having TB disease to the
Centers for Disease Control and Prevention of Tai-
wan from April 2004 to March 2008 were enrolled.
Demographic information on age and sex, duration
of symptoms, clinical underlying diseases—including
dia betes mellitus, end-stage renal disease (ESRD), liver
cirrhosis, malignancies, immunosuppressive drug use,
SUMMARY
Risk factors for EPTB 621
alcoholism, smoking, HIV infection or AIDS, chronic
obstructive pulmonary disease (COPD), congestive
heart failure, hypertension, intravenous drug use,
history of TB infection and cerebrovascular accident
—were collected from the medical records. ESRD
was de ned as renal failure requiring long-term di-
alysis or kidney transplantation for survival. Liver
cirrhosis was de ned on the basis of its typical sono-
graphic appearance. Immunosuppressive drug use
was de ned as the use of cytotoxic agents or cortico-
steroids (more than 30 mg prednisolone daily or its
equivalent for ⩾1 week). Alcoholism was de ned
as habitual alcohol consumption. COPD, congestive
heart failure and hypertension were de ned as dis-
eases diagnosed by the subspecialists and needing
long-term medication. The proportion of EPTB was
calculated for the trend for each decade increase in
patient’s age. To evaluate whether different age groups
had a role in the clinical presentation of EPTB, age
groups (0–24, 25–39, 40–59, ⩾60 years) at diagnosis
were introduced as categorical variables, as described
elsewhere.11
Defi nition of pulmonary TB and extra-pulmonary TB
The diagnosis of TB was based on: 1) sputum, pleural
effusion, pericardial effusion, ascites, urine, cerebral
spinal uid, synovial uid and abscess or tissue cul-
ture that yielded M. tuberculosis. Patients were ex-
cluded from our study if acid-fast stain was positive on
the specimens but they were M. tuberculosis culture-
negative; 2) histological ndings of granulomatous
in ammation (granulomas composed of epithelioid
cells and Langhans giant cells with or without case-
ous necrosis) combined with positive acid-fast stain in
the pathology specimens (i.e., lymph node, pleura,
prostate, skin, gastro-intestinal tract, genito-urinary
tract, bone, tendon, synovial tissue) and favour able
clinical response to anti-t uberculosis chemotherapy.
The de nition of EPTB was based on the guidelines
of the American Thoracic Society and the US Centers
for Disease Control and Prevention.12 As in previous
studies,6,13 EPTB was de ned 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-
trol patients. Categorical variables were analysed us-
ing the χ2 test or Fisher’s exact tests, as appropriate.
Continuous variables were analysed using Student’s
t-test. The χ2 test was used to analyse the trend among
different age groups. All P values were 2-tailed, and
P < 0.05 was considered statistically signi cant. To
identify the risk factors for EPTB and control for po-
tential confounders, all variables associated with a
level of signi cance of <0.20 in univariate analyses
were included in a logistic regression model for multi-
variate analysis (backward stepwise methods by likeli-
hood ratio). Odds ratios (OR), 95% con dence inter-
vals (95%CI) and P values were calculated for each
potential risk factor. Hosmer-Lemeshow goodness-
of- t test was used to assess the tness of the model.
RESULTS
Sites of extra-pulmonary TB
During the study period, 766 patients with TB were
enrolled in this study, with 102 (13.3%) classi ed as
EPTB and 664 (86.7%) as PTB. All enrolled patients
were Chinese living in Taiwan. Of the 766 patients,
3% of PTB patients had EPTB and 19.6% of EPTB
patients also had PTB. Among the EPTB cases, the
most frequently involved site was the bone and joints
(24.5%), followed by the genito-urinary system
(20.6%), abdomen (18.6%), lymph nodes (17.6%),
disseminated TB (10.8%), skin (2.9%), meninges
(2.0%), pericardium (1.0%) and others (laryngeal,
vocal chords 2.0%; Figure 1).
Patient characteristics
Of these 766 patients, 561 (73.2%) were male and
205 (26.8%) were female. Females were signi cantly
predisposed to EPTB (P < 0.001). The mean age was
lower among EPTB than PTB patients (58.8 ± 18.8 vs.
63.9 ± 17.3 years, P < 0.01; Table 1). On the χ2 test
for trend, EPTB incidence decreased for each decade
increase in patient’s age (OR 0.85, 95%CI 0.75–
0.95, P < 0.01; Figure 2). The median duration of
symptoms on presentation in patients with EPTB and
Figure 1 Proportional distribution of patients with EPTB and
PTB by anatomic site. *Others includes TB of the vocal chords
and larynx. TB = tuberculosis; EPTB = extra-pulmonary TB; PTB =
pulmonary TB.
622 The International Journal of Tuberculosis and Lung Disease
Risk factors for extra-pulmonary TB
On univariate analysis, patients with diabetes melli-
tus were signi cantly predisposed to PTB relative to
EPTB (P < 0.01). In contrast, patients with ESRD
had a predisposition for EPTB (P = 0.001). Smokers
had a higher risk for PTB than non-smokers (P <
0.001; Table 1). There were no statistically signi cant
differences between patients with EPTB and PTB as
regards the other underlying conditions, identi ed in
Methods.
A multivariate logistic regression analysis model
was used to further analyse the signi cant factors for
EPTB, and showed that being female (OR 1.69, 95%CI
1.02–2.80, P = 0.04) and having ESRD (OR 3.74;
95%CI 1.45–9.67, P < 0.01) were independent risk
factors for EPTB. In contrast, diabetes mellitus (OR
0.41, 95%CI 0.22–0.76, P < 0.01) and smoking (OR
0.57, 95%CI 0.34–0.95, P = 0.03) were negatively
associated with EPTB (Table 2).
DISCUSSION
TB can involve virtually any tissue or organ. Prompt
and accurate diagnosis of EPTB is essential, but is
Table 1 Demographic characteristics and underlying diseases
of patients with EPTB and PTB
Characteristics
EPTB patients
(n = 102)
n (%)
PTB patients
(n = 664)
n (%) P value
Age, years, mean ± SD 58.8 ± 18.8 63.9 ± 17.3 <0.01
Age groups, years
⩽24 6 (5.9) 12 (1.8) Referent
25–39 9 (8.8) 57 (8.6) 0.06
40–59 31 (30.4) 179 (27.0) 0.048
⩾60 56 (54.9) 416 (62.7) 0.01
Male sex 58 (56.9) 503 (75.8) <0.001
Duration of symptoms,
days, median 30 13 <0.001
Diabetes mellitus 15 (14.7) 191 (28.8) <0.01
ESRD 9 (8.8) 13 (2.0) 0.001
Liver cirrhosis 6 (5.9) 28 (4.2) 0.44
Malignancy 16 (15.7) 69 (10.4) 0.13
Immunosuppressive drug use 4 (3.9) 38 (5.7) 0.46
Alcoholism 2 (2.0) 28 (4.2) 0.41
Smoking 31 (31.0)* 344 (52.8)†<0.001
HIV infection 2 (2.0) 3 (0.5) 0.13
COPD 3 (2.9) 55 (8.3) 0.06
CHF 3 (2.9) 20 (3.0) 1.00
Hypertension 27 (26.5) 137 (20.6) 0.18
IDU 0 2 (0.3) 1.00
History of TB 6 (5.9) 25 (3.8) 0.29
History of CVA 4 (3.9) 33 (5.0) 0.81
* n = 100.
† n = 652.
EPTB = extra-pulmonary TB; PTB = pulmonary TB; SD = standard deviation;
ESRD = end-stage renal disease; HIV = human immunodefi ciency virus; COPD =
chronic obstructive pulmonary disease; CHF = congestive heart failure; IDU =
intravenous drug user; TB = tuberculosis; CVA = cerebrovascular accident.
Figure 2 Case numbers of patients with EPTB and PTB (bars)
and percentage of patients with EPTB in all TB patients in differ-
ent age groups (line). Signifi cant difference by χ2 test for trend
in the ratio of EPTB with each decade increase in patient age (OR
0.85, 95%CI = 0.75–0.95, P < 0.01). EPTB = extra-pulmonary
tuberculosis; PTB = pulmonary tuberculosis; TB = tuberculosis;
OR = odds ratio; CI = confi dence interval.
Table 2 Multivariate logistic regression mode of independent
risk factors for the development of EPTB compared to
PTB (n = 752)*
Risk factor OR 95%CI P value
Age, years
⩽24 1 Referent
25–39 0.38 0.11–1.34 0.13
40–59 0.60 0.20–1.82 0.37
⩾60 0.41 0.14–1.20 0.10
Sex
Female 1.69 1.02–2.80 0.04
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
No 1 Referent
* Analysed by backward stepwise methods (likelihood ratio). Data were
missing for 2 in the EPTB group (2/102, 1.97%) and 12 in the PTB group
(12/664, 1.81%).
OR = odds ratio; CI = confi dence interval; ESRD = end-stage renal disease;
HIV = human immunodefi ciency virus; COPD = chronic obstructive pulmo-
nary disease.
PTB were 30 days (mean ± standard deviation [SD],
61.2 ± 103.0 days) and 13 days (mean ± SD, 49.2 ±
119.2 days), respectively (P < 0.001; Table 1).
Risk factors for EPTB 623
often delayed because symptoms vary depending on
the affected sites and patients may have few if any of
the classic signs and symptoms of cough, fever, night
sweats, weight loss, anorexia or fatigue.7 As it is less
common and less familiar to most physicians, espe-
cially in relatively inaccessible sites, EPTB usually pres-
ents a greater diagnostic challenge than PTB.14,15 To
establish a con rmation, therefore, invasive procedures
are frequently needed, making a diagnosis even more
dif cult. This was re ected in our study by the dura-
tion of symptoms in patients with EPTB being more
than twice as long as in patients with PTB (median 30
vs. 13 days).
Taiwan is an endemic area for TB, with more than
16 000 newly reported cases and an incidence rate of
74.5 per 100 000 population per year.16 In our study,
the most common site of EPTB was the bone and joints,
followed by the genito-urinary system, abdomen and
lymph nodes. The distribution of EPTB is different
from previous studies. Yang et al. reported that the
most common sites involved were the bone/joints and
lymph nodes in the United States,6 while the genito-
urinary system and skin were the most common sites
in a report from Hong Kong.17 The difference may
be attributable to ethnicity or underlying associated
diseases.
In this study, we found on trend analysis that the
incidence of EPTB decreased signi cantly by 15% for
each decade increase in patient age. As previous pub-
lished data show,6–8,13,17 extra-pulmonary sites tend
to be more commonly involved in younger than older
patients. Our study was consistent with these studies
and further showed that there was a signi cant de-
creasing trend of proportion of EPTB to PTB with in-
creasing age by decades.
PTB is more common in males than in females,
while the opposite is true for EPTB.6–8,13,17 Our study
corroborated this sex difference in the incidence rates
of PTB and EPTB. The causes of sex differences in TB
occurrence are not well understood. Cellular immu-
nity, hormones, access to health care, socio-economic
factors and cultural factors have been linked to these
differences.18,19 Underdiagnosis or underreporting of
TB in females have also been hypothesised.20,21 How-
ever, a study conducted in the United States suggested
that differences in TB rates between the sexes may be
due to a difference in transmission dynamics rather
than diagnosis or reporting biases.22 The real reasons
for the sex difference in TB sites remain to be deter-
mined through further studies.
Most studies have shown diabetes mellitus to be
strongly associated with TB infection.23,24 When com-
pared to EPTB, patients with diabetes mellitus showed
a predisposition for PTB.7,13,17 Our study was consis-
tent with other studies indicating that non-diabetic pa-
tients had a higher risk for PTB compared to EPTB.
However, the exact mechanism is still unknown.
Another striking nding in this study is the rela-
tionship between ESRD and EPTB. Patients with ESRD
are known to have a disruption of their cell-mediated
immunity that is responsible for the killing of intra-
cellular organisms such as M. tuberculosis.25 There is
a 6.9–52.5-fold increased risk of TB infection in pa-
tients with chronic renal failure and on dialysis as
compared to the general population.26 In the reports
by Sen et al. and Abdelrahman et al.,27,28 EPTB was
more frequent among patients with ESRD. However,
to our knowledge, there is no similar study to compare
the risk ratio of ESRD in patients with EPTB to PTB.
One of the reasons may be that there are too few cases
involved in the studies to show the signi cance of
ESRD. However, ESRD is prevalent in Taiwan. Ac-
cording to data from the Taiwan Society of Nephrol-
ogy, the incidence and prevalence of ESRD in Taiwan
was 375 and 1760/100 000/year, which ranked rst
and second, respectively, worldwide.29 Our study re-
vealed patients with ESRD had a 3.74-fold increased
risk of EPTB compared to PTB.
Smoking has been identi ed as a risk factor for
PTB as well as EPTB.30 Gonzalez et al.7 and Musellim
et al.31 found that smoking had a negative association
for EPTB compared to PTB. In our studies, smoking
was also identi ed as an independent risk factor for
PTB compared to EPTB. Chronic lung disease caused
by smoking may predispose patients to PTB infection.
As regards the other risk factors, including liver
cirrhosis, malignancies, immunosuppressive drug use,
alcoholism, HIV infection, COPD, congestive heart
failure, intravenous drug use, history of TB and cere-
brovascular accident, there were no statistical differ-
ences between the EPTB and the PTB groups. In the
Hong Kong study,17 there was no association of EPTB
with liver diseases, which was consistent with our
study. However, Gonzalez et al. reported liver cirrho-
sis to be a risk factor for EPTB in the United States.7
Regarding malignancies and immunosuppressive drug
use, our data and previously published data con-
cluded consistently that there was no association with
EPTB.13,17,31
According to published reports,9,10 HIV infection
is well known to be associated with EPTB. However,
there was no statistical signi cance of HIV infection in
our study, which is undoubtedly explained by the very
small number of HIV-infected cases in our series.
Our study pointed out the important risk factors
for EPTB. However, there are still some limitations to
our study. For example, surgeons infrequently suspect
EPTB infection before operations and few surgical
specimens are sent for TB culture. This situation makes
accurate diagnosis of EPTB lower than expected and
many patients with EPTB may have been excluded
from our study. Further prospective studies are indi-
cated to overcome this limitation.
CONCLUSIONS
The protean and non-speci c manifestations of EPTB
frequently make accurate diagnosis dif cult. Our study
624 The International Journal of Tuberculosis and Lung Disease
suggests that younger age, female sex, non-diabetes
mellitus, ESRD and non-smoking were risk factors for
EPTB relative to PTB. Although the exact mecha-
nisms that lead to such differences are still unknown,
our results provide a basis for further studies. More-
over, awareness of these predisposing factors for
EPTB may help physicians maintain a high index of
suspicion. Aggressive examinations, including acid-
fast staining, TB culture, invasive procedures or further
imaging studies, are required to achieve timely and
appropriate diagnosis and treatment of EPTB in sus-
picious cases.
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CADRE : La tuberculose (TB) reste un problème mondial
majeur de santé publique. Les symptômes de la TB extra-
pulmonaire (TBEP) sont très variables et le diagnostic est
plus dif cile à établir que pour la TB pulmonaire (TBP).
OBJECTIF : Analyser les facteurs de risque de TBEP par
rapport à la TBP.
SCHÉMA : Cette étude rétrospective a comparé les pa-
tients atteints d’une TBEP et TBP dans le Sud de Taiwan
RÉSUMÉ
Risk factors for EPTB 625
en analysant leurs données démographiques et les mala-
dies cliniques sous-jacentes. En outre, on a analysé les
facteurs de risque de TBEP.
RÉSULTATS : Ont été enrôlés dans cette étude 766 pa-
tients TB dont 102 (13,3%) atteints de TBEP et 664
(86,7%) de TBP. Parmi ces 766 patients, 3% de ceux at-
teints de TBP souffraient en outre d’une TBEP et 19,6%
de ceux atteints de TBEP souffraient également d’une
TBP. Le site le plus fréquent de la TBEP est constitué
par les os et les articulations (24,5%). Le ratio de TBEP
décroît de manière signi cative dans chacune des décen-
nies d’âge du patient. Une analyse multivariée de régres-
sion logistique a montré que les facteurs indépendants de
risque de TBEP sont le sexe féminin, l’absence de diabète
sucré, les maladies rénales au stade terminal et le fait de
ne pas fumer.
CONCLUSION : Cette étude signale les facteurs de risque
de TBEP par rapport à la TBP. Une bonne prise de con-
science de cette situation est essentielle pour que les méde-
cins gardent un index élevé de suspicion en vue d’un diag-
nostic précis et porté en temps utile.
MARCA DE REFERENCIA : La tuberculosis (TB) continúa
siendo un grave problema de salud. La TB extrapulmonar
(TBEP) se mani esta con síntomas larvados y su diag-
nóstico es más difícil de establecer que en la TB pulmo-
nar (TBP).
OBJETIVO : Analizar los factores de riesgo de TBEP, en
comparación con los factores de la TBP.
MÉTODO : En este estudio retrospectivo se compararon
los datos demográ cos y las enfermedades clínicas subya-
centes de pacientes con TBP y TBEP en el sur de Taiwán.
Se profundizó el análisis de los factores de riesgo de
TBEP.
RESULTADOS : Se incluyeron en el estudio 766 pacientes
tuberculosos, de los cuales 102 casos de TBEP (13,3%)
y 664 casos de TBP (86,7%). De los 766 pacientes, 3% de
los pacientes con diagnóstico de TBP presentaron tam-
bién localización extrapulmonar y 19,6% de los pacien-
tes diagnosticados con TBEP presentaron también TBP.
La localización extrapulmonar más frecuente fue osteo-
articular (24,5%). El cociente de TBEP disminuyó sig-
ni cativamente con cada decenio de aumento en la edad
de los pacientes. Según el análisis de regresión logística
multifactorial, el sexo femenino, la nefropatía terminal y
la ausencia de tabaquismo fueron factores independien-
tes de riesgo de TBEP ; se observó una correlación nega-
tiva de la diabetes sacarina con la TBEP.
CONCLUSIÓN : En el presente estudio se determinaron
los factores de riesgo de TBEP con respecto a la locali-
zación pulmonar. Es importante el conocimiento de esta
enfermedad y que los médicos mantengan un alto índice
de presunción, con el n de establecer el diagnóstico en
forma precisa y oportuna.
RESUMEN
