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INT J TUBERC LUNG DIS 12(4):436–440

© 2008 The Union

Incidence of tuberculosis among health care workers at


a private university hospital in South Korea

K-W. Jo,* J. H. Woo,† Y. Hong,* C-M. Choi,* Y-M. Oh,* S. D. Lee,* W. S. Kim,* D. S. Kim,* W. D. Kim,*
T. S. Shim*
* Division of Pulmonary and Critical Care Medicine, † Department of Infection Control and Division of Infectious Diseases,
University of Ulsan College of Medicine, Asan Medical Centre, Seoul, Korea

SUMMARY

SETTING: A private university hospital in South Korea. other departments were respectively 0.58 (95%CI
OBJECTIVE: To investigate the incidence of tuberculosis 0.30–1.01), 1.81 (95%CI 1.21–2.59) and 0.95 (95%
(TB) among health care workers (HCWs) employed at a CI 0.58–1.46). For nurses working in TB-related depart-
university hospital in South Korea. ments, the relative risk of developing TB was 3.4 times
D E S I G N : The occurrence of TB cases among HCWs over higher (95%CI 1.52–8.25) than for employees in other
a 6-year period (2001–2006) was reviewed. The preva- departments (P  0.005). The PR for nurses working in
lence of TB was compared with that of the general pop- TB-related department was 5.1 (95%CI 3.23–8.42).
ulation using a prevalence ratio (PR) adjusted by age C O N C L U S I O N : Among HCWs, nurses working in TB-
and sex. related departments were at increased risk of developing
R E S U L T S : The study involved 8433 people. TB devel- TB. This suggests that some TB develops via in-hospital
oped in 61 HCWs (0.72%). The prevalence ratio among infection.
all HCWs was 1.05 (95%CI 0.80–1.35). In occupational K E Y W O R D S : tuberculosis; health care workers; hospital-
subgroups, the PRs for doctors, nurses and employees in acquired infection

DESPITE RECENT PROGRESS in global control ef- sent the standardised reporting form for all TB cases
forts, tuberculosis (TB) remains a major public health to the KTBS via the internet. Based on the data col-
burden in many countries. TB is an established occu- lected following the implementation of the KTBS, it
pational disease of health care workers (HCWs),1–3 was presumed that TB incidence in South Korea was
and those infected may transmit the disease to suscep- in the intermediate range (92/100 000).
tible individuals.4,5 Recent reports suggest that HCWs There has been no study of the risk of TB among
in high-prevalence countries have an increased ten- HCWs in South Korea, with the exception of a single
dency to develop nosocomial TB infection.6–11 In con- study restricted to laboratory technicians.16 The ob-
trast, where the prevalence of TB is low, the risk of jective of the present study was thus to assess the oc-
HCWs acquiring TB is likely to be small.12 cupational risk of TB among HCWs employed at a
The TB burden in South Korea was assessed na- private university hospital in South Korea, an interme-
tionwide using TB prevalence surveys at 5-year inter- diate TB burden country.
vals from 1965 to 1995. These nationwide surveys re-
vealed that there has been a marked decrease in the STUDY POPULATION AND METHODS
prevalence of smear- and/or culture-positive TB, from
940 per 100 000 population in 1965 to 219/100 000 Subjects
in 1995.13 While these surveys provide reliable infor- The study involved a retrospective analysis of the
mation on the prevalence of TB and its trend over the medical records of all HCWs employed at the Asan
last 30 years, there were difficulties in surveying a Medical Centre, Seoul, South Korea, from January
random sample large enough to accurately measure 2001 to December 2006. All employees who worked
the declining prevalence of TB.14,15 As a result, an at the centre for least 6 months during the study pe-
internet-based routine reporting system for TB, the riod were investigated for the development of TB. A
Korean TB Surveillance System (KTBS), was developed list of HCWs with TB was obtained from data reported
and launched in June 2000. Physicians completed and to the Department of Infection Control at the Asan

Correspondence to: Tae Sun Shim, Division of Pulmonary and Critical Care Medicine, University of Ulsan College of Med-
icine, Asan Medical Centre, 388-1 Pungnap-Dong, Songpa-Ku, Seoul 138-736, South Korea. Tel: (82) 2 3010 3892. Fax:
(82) 2 3010 6968. e-mail: shimts@amc.seoul.kr
Article submitted 26 November 2007. Final version accepted 21 December 2007.
TB among Korean health care workers 437

Medical Centre and the KTBS. To obtain the list of included 5610 doctors and nurses (2389 and 3221,
HCWs with TB, the resident registration number was respectively) and 2823 persons employed in other de-
cross-matched between the lists of all HCWs and KTBS. partments, including paramedics, pharmacists, labo-
One of the several objectives of this study was to ratory technicians and office workers. The mean age
assess the incidence of active TB disease among HCWs. was 29.3  16.1 years and the male:female ratio was
In this study, TB therefore refers to active TB disease 0.52:1.
and not latent TB infection. As the tuberculin skin test TB developed in 61 HCWs (0.72%) during the
(TST) was not performed routinely at start of employ- study period. The overall incidence of TB among
ment in South Korea, we do not have previous records HCWs was therefore 723.3/100 000 and the PR was
of TST. TB was diagnosed by bacteriological culture, 1.05 (95% confidence interval [CI] 0.80–1.35). The
histological evidence of granuloma with caseation ne- mean age of the 61 tuberculous HCWs was 29.8 
crosis or clinical findings consistent with active TB. 5.9 years, females predominated (49/61, 80.3%), 41
This study was approved by the Institutional Re- were doctors or nurses (0.73%, 41/5610) and the
view Board of the Asan Medical Centre. other 20 were from other departments (0.71%, 20/
2823). The characteristics of TB occurrence among the
Bacteriological examinations HCWs are shown in the Table.
Mycobacterium tuberculosis was cultured on Ogawa TB developed in 8/5610 doctors, in 8/263 nurses
medium and identified by hybridisation methods using working in TB-related departments and in 25/2958
a commercial molecular probe (AccuProbe, Gen-Probe nurses working in other departments. There was no
Inc., San Diego, USA) or duplex PCR (Molecules and significant difference in TB prevalence between doctors
Diagnostics Inc., Wonju, South Korea). Drug suscep- (0.58, 95%CI 0.30–1.01) and nurses (1.81, 95%CI
tibility testing (DST) was carried out by the Korean 1.21–2.59). The combined prevalence ratio for doc-
Institute of Tuberculosis, a Supranational TB Refer- tors and nurses was 1.12 (95%CI 0.8–1.52), and for
ence Laboratory. personnel in other departments it was 0.95 (95%CI
0.58–1.46).
Statistical analysis Nurses comprised the only occupational subgroup
All analyses were performed using SPSS software (ver- with a high PR, with 29/3221 developing TB (0.9%,
sion 12.0, SPSS Inc., Chicago, IL, USA). Comparisons 900.3/100 000). The relative risk of developing TB
between the study and control groups were made
using Student’s t-test for continuous variables, and the
2 and Fisher’s exact tests for categorical variables. Table Clinical characteristics of health care workers with
All tests of significance were two sided; P  0.05 was tuberculosis
considered statistically significant. Occupational subgroups
The objective of this study was to assess the inci-
Doctors
dence of TB among HCWs. However, because there and nurses Others*
were more young people and females among HCWs (n  41) (n  20)
compared with the general population, it was difficult n (%) n (%) P value
to compare the results of the incidence of TB between Age, years, mean  SD 27.9  3.9 33.6  7.5 0.08
HCWs and the general population. We therefore used Sex 0.09
the prevalence ratio (PR) as a statistical technique. Male 6 (14.6) 7 (35.0)
Female 35 (85.4) 13 (65.0)
The PR was calculated as follows:
Height, cm, mean  SD 162.8  6.6 164.4  8.1 0.55
PR  (observed number of TB cases in HCWs)/ Weight, kg, mean  SD 54.5  9.2 55.2  9.3 0.27
(expected number of TB cases among South BMI, kg/m2, mean  SD 20.4  2.5 20.3  1.60 0.38
Koreans). Previous TB history 2 (4.9) 1 (5.0) 1
Smoking 4 (9.8) 4 (20.0) 0.42
As the PR was adjusted for age and sex, it was pos-
Site of TB 0.49
sible to estimate the TB incidence from the PR. (The Pulmonary TB 33 (80.5) 16 (80)
PR of the general population is always 1.) The expected TB lymphadenitis 4 (9.8) 2 (10)
number of TB cases among the South Korean popula- TB pleurisy 4 (9.8) 1 (5)
TB peritonitis 0 1 (5)
tion was derived from data from nationwide TB prev-
Comorbidity 0.95
alence surveys conducted in 1995.13 None 39 (95.1) 18 (90)
Present 2 (4.9) 2 (10)
Bronchial asthma 2 (4.9) 0
RESULTS Thyroid cancer 0 1 (5)
Gallbladder stone 0 1 (5)
Incidence of TB among HCWs
Previous TB history 2 (4.9) 1 (5) 1
Between January 2001 and December 2006, the work
force comprising those employed for 6 months at * Personnel in other departments (such as paramedics, pharmacists and
office workers).
the Asan Medical Centre was 8433 individuals. This SD  standard deviation; BMI  body mass index; TB  tuberculosis.
438 The International Journal of Tuberculosis and Lung Disease

departments, suggesting occupational acquisition of


TB rather than reactivation of latent TB. Because em-
ployees did not undergo TSTs to detect TB infection
when they were hired, we do not know whether HCWs
with TB disease are already infected before starting
work at this hospital or whether they were newly in-
fected with M. tuberculosis afterwards. However, the
finding that more TB patients were detected in TB-
related departments than in other departments sug-
gests that some of the HCWs developed the disease
via hospital infection.
There was no significant difference in the PR be-
tween HCWs and the general population. However,
among occupational subgroups, the PR for nurses was
higher than that of doctors and employees in other
Figure The PR of tuberculosis according to occupational sub- departments (including office workers), and was no-
groups. The PR of the general population is 1. TB  tuberculosis; tably higher among nurses working in TB-related de-
PR  prevalence ratio. partments (medical intensive care unit, respiratory
department ward and emergency room). This finding
is consistent with previous reports showing that TB
was 3.4 times higher (95%CI 1.52–8.15) for those risk among medical nurses employed in specialised
working in TB-related departments (medical intensive lung disease institutions is higher than among those in
care unit, respiratory department ward and emergency non-exposed institutions.6,7,17
room) compared with those working in other depart- The reported rates of TB in different groups of
ments (P  0.005). The PR for nurses working in HCWs in TB-endemic countries have varied widely,
TB-related departments was 5.1 (95%CI 3.23–8.42) with a higher risk of TB in HCWs reported by some
(Figure). studies and a lower risk by others. For example,
Kruuer et al. showed that the TB risk among HCWs
Clinical characteristics of HCWs who developed TB in Estonia was higher than in the general population.9
Of the 61 HCWs who developed TB, 49 (79%) had Similar results have been obtained in studies in Serbia8
pulmonary TB, six (9.8%) had TB lymphadenitis and and Japan,18 while opposite results were obtained in
five (8.2%) had TB pleurisy. Sputum acid-fast bacilli two other studies.19,20 There is a general trend for TB
(AFB) smear and bacteriological culture were per- risk among HCWs to be related to the TB incidence in
formed for 45 of the 49 HCWs with pulmonary TB; the country concerned. As South Korea is an interme-
positive sputum smears and cultures were obtained diate TB burden country, our result is consistent with
from respectively seven (15.6%) and 20 (44.4%) cases. previous studies.
Of 12 M. tuberculosis isolates for which DST was To stop the spread of TB in hospitals, several pre-
carried out, 11 (91.7%) were susceptible to all avail- ventive strategies should be implemented: administra-
able anti-tuberculosis drugs. The remaining isolate tive, engineering and personal respiratory protection.21
was multidrug-resistant (MDR, defined as resistance In the hospital used for this study, infectious TB pa-
to both isoniazid and rifampicin). However, this MDR- tients are placed in isolation rooms equipped with
TB individual was cured with first-line drugs only. ultraviolet germicidal irradiation (UVGI) and negative
The median period from employment at hospital pressure ventilation. HCWs or visitors who enter the
to development of TB was 894 days (range 35–6030). isolation room are required to wear N-95 respirators.
All patients were cured by first-line drugs and one All HCWs undergo an annual chest X-ray, but annual
(1.6%) patient had recurrence of the disease 4 years TSTs are performed only in nurses working in TB-
after treatment completion. related wards. The results of this study suggest that
stricter preventive strategies, such as contact investi-
gations of active TB disease, the installation of an iso-
DISCUSSION
lation room in the emergency room, and latent TB in-
In the present study, we determined the occupational fection screening by TST at the time of hiring should
risk of TB in the work force of a private university be implemented for all HCWs.
hospital in South Korea, a country with an intermedi- The present study had several limitations. The in-
ate TB burden. This is the first study to investigate the cidence of TB in HCWs in the hospital was determined
incidence of TB in HCWs in Korea. The most impor- from reports to the Department of Infection Control
tant finding was that TB developed much more fre- at the Asan Medical Centre and the KTBS. It is there-
quently in nurses working in TB-related departments fore possible that the incidence of TB was underesti-
compared to the general population or HCWs in other mated due to incomplete reporting. Second, when
TB among Korean health care workers 439

calculating the PR, the expected number of TB cases Memorial Hospital, 1988–2002. Int J Tuberc Lung Dis 2005;
in the general population was derived from data from 9: 1253–1258.
7 Kilinc O, Ucan E S, Cakan A, et al. Risk of tuberculosis among
the last nationwide TB prevalence survey, performed health care workers: can tuberculosis be considered as an oc-
in 1995. However, as the incidence of TB has been de- cupational disease? Res Med 2002; 96: 506–510.
creasing over the past 10 years in South Korea, it is 8 Skodric V, Savic B, Jovanovic M, et al. Occupational risk of
likely that there were fewer TB patients in the study tuberculosis among health care workers at the institute for pul-
period than in 1995, resulting in an underestimation monary diseases of Serbia. Int J Tuberc Lung Dis 2000; 4: 827–
831.
of PR for HCWs. Third, this study was carried out in
9 Kruuner A, Danilovitsh M, Pehme L, et al. Tuberculosis as an
only one hospital and may not represent the situation occupational hazard for health care workers in Estonia. Int J
in South Korean medical institutions in general. How- Tuberc Lung Dis 2001; 5: 170–176.
ever, the hospital in which this study was performed is 10 Kanyerere H S, Salaniponi F. Tuberculosis in health care
the biggest and one of the best equipped in Korea, workers in a central hospital in Malawi. Int J Tuberc Lung Dis
2003; 7: 489–492.
which suggests that the situation in Korean hospitals
11 Cubadaroglu C, Erelel M, Tabuk L. Increased risk of tubercu-
may be more serious than this study concludes. losis in health care workers: a retrospective survey at a teaching
In conclusion, among HCWs in a hospital in South hospital in Istanbul, Turkey. BMC Infect Dis 2002; 2: 14–17.
Korea, only nurses, particularly those working in TB- 12 Riley M, Loughrey C M, Wilkinson P, Patterson C C, Varghese
related departments, were more likely to develop TB G. Tuberculosis in health service employees in Northern Ire-
than individuals in the general population. Stricter pre- land. Respir Med 1997; 91: 546–550.
13 Hong Y P, Kim S J, Lew W J, Lee E K, Han Y C. The seventh
ventive strategies against the spread of TB in hospitals nationwide tuberculosis prevalence survey in Korea, 1995. Int J
need to be implemented. Tuberc Lung Dis 1998; 2: 27–36.
14 Lew W J, Lee E G, Bai J Y, et al. An Internet-based surveillance
Acknowledgement system for tuberculosis in Korea. Int J Tuberc Lung Dis 2006;
10: 1241–1247.
The authors acknowledge the support of the Department of Infec-
15 Seung K J, Bai G H, Kim S J, et al. The treatment of tuberculo-
tion Control at the Asan Medical Centre.
sis in South Korea. Int J Tuberc Lung Dis 2003; 7: 912–919.
16 Kim S J, Lee S H, Kim I S, et al. Risk of occupational tubercu-
losis in national tuberculosis programme laboratories in Korea.
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RÉSUMÉ

CONTEXTE : Un hôpital universitaire privé en Corée du les infirmières et les autres types d’HCW a été respective-
Sud. ment de 0,58 (IC95% 0,30–1,01), 1,81 (IC95% 1,21–
O B J E C T I F : Investiguer l’incidence de la tuberculose (TB) 2,59) et 0,95 (IC95% 0,58–1,46). Pour les infirmières
chez les travailleurs des soins de santé (HCW) employés travaillant dans des départements en relation avec la TB,
dans un hôpital universitaire de Corée du Sud. le risque relatif de développer une TB a été 3,4 fois
S C H É M A : On a révisé la survenue de cas de TB parmi les supérieur (IC95% 1,52–8,25) à celui des employés d’au-
HCW pendant une période de 6 années (2001–2006). tres départements (P  0,005). Le PR pour les in-
On a comparé la prévalence de la TB avec celle de la firmières travaillant dans un département en relation
population générale en utilisant un ratio de prévalence avec la TB a été de 5,1 (IC95% 3,23–8,42).
(PR) ajusté pour l’âge et le sexe. C O N C L U S I O N : Parmi les HCW, les infirmières travail-
R É S U L T A T S : L’étude a comporté 8433 personnes. La TB lant dans des départements en relation avec la TB en-
est survenue chez 61 HCW (0,72%). Le PR pour l’ensem- courent un risque accru de développer la TB. Ceci sug-
ble des HCW a été de 1,05 (IC95% 0,80–1,35). Dans les gère qu’un certain nombre de cas de TB apparaissent à
sous-groupes professionnels, le PR pour les médecins, la suite d’une infection hospitalière.
440 The International Journal of Tuberculosis and Lung Disease

RESUMEN

MARCO DE REFERENCIA : Un hospital universitario pri- el PR fue 0,58 (IC95% 0,30–1,01) para los médicos,
vado en Corea del Sur. 1,81 (IC95% 1,21–2,59) para el personal de enfermería
O B J E T I V O : Investigar la incidencia de tuberculosis (TB) y 0,95 (IC95% 0,58–1,46) para los empleados en otros
en los profesionales de la salud empleados en un hospital departamentos. El riesgo relativo de TB en el personal
universitario en Corea del Sur. de enfermería de departamentos relacionados con la TB
M É T O D O S : Se analizó la ocurrencia de casos de TB du- fue 3,4 veces mayor (IC95% 1,52–8,25) que el de los
rante un periodo de 6 años (2001–2006) en los profe- empleados en otros departamentos (P  0,005). El PR
sionales de la salud. La prevalencia de TB se comparó en el personal de enfermería de departamentos relacio-
con la prevalencia en la población general mediante el co- nados con la TB fue 5,1 (IC95% 3,23–8,42).
ciente de prevalencia (PR) ajustado según la edad y el sexo. C O N C L U S I Ó N : En los profesionales de la salud, el per-
R E S U L T A D O S : En el estudio se incluyeron 8433 perso- sonal de enfermería que trabaja en departamentos rela-
nas. Sesenta y un profesionales de la salud presentaron cionados con la TB presentó un riesgo más alto de TB.
TB (0,72%). El PR en todos los proveedores de salud fue Esto indica que parte de los casos de TB se adquiere por
1,05 (IC95% 0,80–1,35). En subgrupos por ocupaciones, infección intrahospitalaria.

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