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INT J TUBERC LUNG DIS 12(4):436440

2008 The Union

Incidence of tuberculosis among health care workers ata 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,

S U M M A R Y

University of Ulsan College of Medicine, Asan Medical Centre, Seoul, Korea

SETTING: A private university hospital in South Korea.

OBJECTIVE: To investigate the incidence of tuberculosis

(TB) among health care workers (HCWs) employed at a

university hospital in South Korea.

DESIGN: The occurrence of TB cases among HCWs over

a 6-year period (20012006) was reviewed. The preva-lence of TB was compared with that of the general pop-

ulation using a prevalence ratio (PR) adjusted by age

and sex.

RESULTS: The study involved 8433 people. TB devel-

oped in 61 HCWs (0.72%). The prevalence ratio among

all HCWs was 1.05 (95%CI 0.801.35). In occupational

subgroups, the PRs for doctors, nurses and employees in

other departments were respectively 0.58 (95%CI

0.301.01), 1.81 (95%CI 1.212.59) and 0.95 (95%

CI 0.581.46). For nurses working in TB-related depart-

ments, the relative risk of developing TB was 3.4 times

higher (95%CI 1.528.25) than for employees in other

departments (P 0.005). The PR for nurses working inTB-related department was 5.1 (95%CI 3.238.42).

CONCLUSION: Among HCWs, nurses working in TB-

related departments were at increased risk of developing

TB. This suggests that some TB develops via in-hospital

infection.

KEY WORDS: tuberculosis; health care workers; hospital-

acquired infection

DESPITE RECENT PROGRESS in global control ef-

forts, tuberculosis (TB) remains a major public healthburden in many countries. TB is an established occu-pational disease of health care workers (HCWs),13

and those infected may transmit the disease to suscep-tible individuals.4,5 Recent reports suggest that HCWsin high-prevalence countries have an increased ten-dency to develop nosocomial TB infection.611 In con-trast, where the prevalence of TB is low, the risk ofHCWs acquiring TB is likely to be small.12

The TB burden in South Korea was assessed na-tionwide using TB prevalence surveys at 5-year inter-vals from 1965 to 1995. These nationwide surveys re-vealed that there has been a marked decrease in the

prevalence of smear- and/or culture-positive TB, from940 per 100000 population in 1965 to 219/100000in 1995.13 While these surveys provide reliable infor-mation on the prevalence of TB and its trend over thelast 30 years, there were difficulties in surveying arandom sample large enough to accurately measurethe declining prevalence of TB.14,15 As a result, aninternet-based routine reporting system for TB, theKorean TB Surveillance System (KTBS), was developedand launched in June 2000. Physicians completed and

sent the standardised reporting form for all TB cases

to the KTBS via the internet. Based on the data col-lected following the implementation of the KTBS, itwas presumed that TB incidence in South Korea wasin the intermediate range (92/100000).

There has been no study of the risk of TB amongHCWs in South Korea, with the exception of a singlestudy restricted to laboratory technicians.16 The ob-jective of the present study was thus to assess the oc-cupational risk of TB among HCWs employed at aprivate university hospital in South Korea, an interme-diate TB burden country.

STUDY POPULATION AND METHODS

Subjects

The study involved a retrospective analysis of themedical records of all HCWs employed at the AsanMedical Centre, Seoul, South Korea, from January2001 to December 2006. All employees who workedat the centre for least 6 months during the study pe-riod were investigated for the development of TB. Alist of HCWs with TB was obtained from data reportedto 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.

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TB among Korean health care workers 437

Medical Centre and the KTBS. To obtain the list ofHCWs with TB, the resident registration number wascross-matched between the lists of all HCWs and KTBS.

One of the several objectives of this study was toassess the incidence of active TB disease among HCWs.

In this study, TB therefore refers to active TB diseaseand not latent TB infection. As the tuberculin skin test(TST) was not performed routinely at start of employ-ment in South Korea, we do not have previous recordsof TST. TB was diagnosed by bacteriological culture,histological evidence of granuloma with caseation ne-crosis or clinical findings consistent with active TB.

This study was approved by the Institutional Re-view Board of the Asan Medical Centre.

Bacteriological examinations

Mycobacterium tuberculosis was cultured on Ogawa

medium and identified by hybridisation methods usinga commercial molecular probe (AccuProbe, Gen-ProbeInc., San Diego, USA) or duplex PCR (Molecules andDiagnostics Inc., Wonju, South Korea). Drug suscep-tibility testing (DST) was carried out by the KoreanInstitute of Tuberculosis, a Supranational TB Refer-ence Laboratory.

Statistical analysis

All analyses were performed using SPSS software (ver-sion 12.0, SPSS Inc., Chicago, IL, USA). Comparisonsbetween the study and control groups were madeusing Students t-test for continuous variables, and the2 and Fishers exact tests for categorical variables.All tests of significance were two sided; P 0.05 wasconsidered statistically significant.

The objective of this study was to assess the inci-dence of TB among HCWs. However, because therewere more young people and females among HCWscompared with the general population, it was difficultto compare the results of the incidence of TB betweenHCWs and the general population. We therefore usedthe prevalence ratio (PR) as a statistical technique.

The PR was calculated as follows:

PR (observed number of TB cases in HCWs)/

(expected number of TB cases among SouthKoreans).

As the PR was adjusted for age and sex, it was pos-sible to estimate the TB incidence from the PR. (ThePR of the general population is always 1.) The expectednumber of TB cases among the South Korean popula-tion was derived from data from nationwide TB prev-alence surveys conducted in 1995.13

RESULTS

Incidence of TB among HCWs

Between January 2001 and December 2006, the workforce comprising those employed for 6 months atthe Asan Medical Centre was 8433 individuals. This

included 5610 doctors and nurses (2389 and 3221,respectively) and 2823 persons employed in other de-partments, including paramedics, pharmacists, labo-ratory technicians and office workers. The mean agewas 29.3 16.1 years and the male:female ratio was

0.52:1.TB developed in 61 HCWs (0.72%) during the

study period. The overall incidence of TB amongHCWs was therefore 723.3/100000 and the PR was1.05 (95% confidence interval [CI] 0.801.35). Themean age of the 61 tuberculous HCWs was 29.8 5.9 years, females predominated (49/61, 80.3%), 41were doctors or nurses (0.73%, 41/5610) and theother 20 were from other departments (0.71%, 20/2823). The characteristics of TB occurrence among theHCWs are shown in the Table.

TB developed in 8/5610 doctors, in 8/263 nurses

working in TB-related departments and in 25/2958nurses working in other departments. There was nosignificant difference in TB prevalence between doctors(0.58, 95%CI 0.301.01) and nurses (1.81, 95%CI1.212.59). The combined prevalence ratio for doc-tors and nurses was 1.12 (95%CI 0.81.52), and forpersonnel in other departments it was 0.95 (95%CI0.581.46).

Nurses comprised the only occupational subgroupwith a high PR, with 29/3221 developing TB (0.9%,900.3/100 000). The relative risk of developing TB

Table Clinical characteristics of health care workers withtuberculosis

Occupational subgroups

Doctorsand nurses(n 41)

n (%)

Others*(n 20)

n (%) Pvalue

Age, years, mean SD 27.9 3.9 33.6 7.5 0.08

Sex 0.09Male 6 (14.6) 7 (35.0)Female 35 (85.4) 13 (65.0)

Height, cm, mean SD 162.8 6.6 164.4 8.1 0.55

Weight, kg, mean SD 54.5 9.2 55.2 9.3 0.27

BMI, kg/m2, mean SD 20.4 2.5 20.3 1.60 0.38

Previous TB history 2 (4.9) 1 (5.0) 1

Smoking 4 (9.8) 4 (20.0) 0.42

Site of TB 0.49Pulmonary TB 33 (80.5) 16 (80)TB lymphadenitis 4 (9.8) 2 (10)TB pleurisy 4 (9.8) 1 (5)TB peritonitis 0 1 (5)

Comorbidity 0.95None 39 (95.1) 18 (90)Present 2 (4.9) 2 (10)

Bronchial asthma 2 (4.9) 0Thyroid cancer 0 1 (5)Gallbladder stone 0 1 (5)

Previous TB history 2 (4.9) 1 (5) 1* Personnel in other departments (such as paramedics, pharmacists andoffice workers).SD standard deviation; BMI body mass index; TB tuberculosis.

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438 The International Journal of Tuberculosis and Lung Disease

was 3.4 times higher (95%CI 1.528.15) for thoseworking in TB-related departments (medical intensivecare unit, respiratory department ward and emergencyroom) compared with those working in other depart-ments (P 0.005). The PR for nurses working inTB-related departments was 5.1 (95%CI 3.238.42)(Figure).

Clinical characteristics of HCWs who developed TB

Of the 61 HCWs who developed TB, 49 (79%) had

pulmonary TB, six (9.8%) had TB lymphadenitis andfive (8.2%) had TB pleurisy. Sputum acid-fast bacilli(AFB) smear and bacteriological culture were per-formed for 45 of the 49 HCWs with pulmonary TB;positive sputum smears and cultures were obtainedfrom respectively seven (15.6%) and 20 (44.4%) cases.

Of 12 M. tuberculosis isolates for which DST wascarried out, 11 (91.7%) were susceptible to all avail-able anti-tuberculosis drugs. The remaining isolatewas multidrug-resistant (MDR, defined as resistanceto both isoniazid and rifampicin). However, this MDR-TB individual was cured with first-line drugs only.

The median period from employment at hospitalto development of TB was 894 days (range 356030).All patients were cured by first-line drugs and one(1.6%) patient had recurrence of the disease 4 yearsafter treatment completion.

DISCUSSION

In the present study, we determined the occupationalrisk of TB in the work force of a private universityhospital in South Korea, a country with an intermedi-ate TB burden. This is the first study to investigate theincidence of TB in HCWs in Korea. The most impor-

tant finding was that TB developed much more fre-quently in nurses working in TB-related departmentscompared to the general population or HCWs in other

departments, suggesting occupational acquisition ofTB rather than reactivation of latent TB. Because em-ployees did not undergo TSTs to detect TB infectionwhen they were hired, we do not know whether HCWswith TB disease are already infected before starting

work at this hospital or whether they were newly in-fected with M. tuberculosis afterwards. However, thefinding that more TB patients were detected in TB-related departments than in other departments sug-gests that some of the HCWs developed the diseasevia 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 washigher than that of doctors and employees in otherdepartments (including office workers), and was no-tably higher among nurses working in TB-related de-

partments (medical intensive care unit, respiratorydepartment ward and emergency room). This findingis consistent with previous reports showing that TBrisk among medical nurses employed in specialisedlung disease institutions is higher than among those innon-exposed institutions.6,7,17

The reported rates of TB in different groups ofHCWs in TB-endemic countries have varied widely,with a higher risk of TB in HCWs reported by somestudies and a lower risk by others. For example,Kruuer et al. showed that the TB risk among HCWsin Estonia was higher than in the general population.9

Similar results have been obtained in studies in Serbia8

and Japan,18 while opposite results were obtained intwo other studies.19,20 There is a general trend for TBrisk among HCWs to be related to the TB incidence inthe country concerned. As South Korea is an interme-diate TB burden country, our result is consistent withprevious studies.

To stop the spread of TB in hospitals, several pre-ventive strategies should be implemented: administra-tive, engineering and personal respiratory protection.21

In the hospital used for this study, infectious TB pa-tients are placed in isolation rooms equipped withultraviolet germicidal irradiation (UVGI) and negative

pressure ventilation. HCWs or visitors who enter theisolation room are required to wear N-95 respirators.All HCWs undergo an annual chest X-ray, but annualTSTs are performed only in nurses working in TB-related wards. The results of this study suggest thatstricter preventive strategies, such as contact investi-gations of active TB disease, the installation of an iso-lation room in the emergency room, and latent TB in-fection screening by TST at the time of hiring shouldbe implemented for all HCWs.

The present study had several limitations. The in-cidence of TB in HCWs in the hospital was determinedfrom reports to the Department of Infection Controlat the Asan Medical Centre and the KTBS. It is there-fore possible that the incidence of TB was underesti-mated due to incomplete reporting. Second, when

Figure The PR of tuberculosis according to occupational sub-groups. The PR of the general population is 1. TB tuberculosis;PR prevalence ratio.

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TB among Korean health care workers 439

calculating the PR, the expected number of TB casesin the general population was derived from data fromthe last nationwide TB prevalence survey, performedin 1995. However, as the incidence of TB has been de-creasing over the past 10 years in South Korea, it is

likely that there were fewer TB patients in the studyperiod than in 1995, resulting in an underestimationof PR for HCWs. Third, this study was carried out inonly one hospital and may not represent the situationin South Korean medical institutions in general. How-ever, the hospital in which this study was performed isthe biggest and one of the best equipped in Korea,which suggests that the situation in Korean hospitalsmay be more serious than this study concludes.

In conclusion, among HCWs in a hospital in SouthKorea, only nurses, particularly those working in TB-related departments, were more likely to develop TB

than individuals in the general population. Stricter pre-ventive strategies against the spread of TB in hospitalsneed to be implemented.

Acknowledgement

The authors acknowledge the support of the Department of Infec-

tion Control at the Asan Medical Centre.

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R S U M

CONTEXTE : Un hpital universitaire priv en Core du

Sud.

OBJECTIF : Investiguer lincidence de la tuberculose (TB)

chez les travailleurs des soins de sant (HCW) employs

dans un hpital universitaire de Core du Sud.

SCHMA : On a rvis la survenue de cas de TB parmi les

HCW pendant une priode de 6 annes (20012006).

On a compar la prvalence de la TB avec celle de la

population gnrale en utilisant un ratio de prvalence

(PR) ajust pour lge et le sexe.

RSULTATS : Ltude a comport 8433 personnes. La TB

est survenue chez 61 HCW (0,72%). Le PR pour lensem-

ble des HCW a t de 1,05 (IC95% 0,801,35). Dans lessous-groupes professionnels, le PR pour les mdecins,

les infirmires et les autres types dHCW a t respective-

ment de 0,58 (IC95% 0,301,01), 1,81 (IC95% 1,21

2,59) et 0,95 (IC95% 0,581,46). Pour les infirmires

travaillant dans des dpartements en relation avec la TB,

le risque relatif de dvelopper une TB a t 3,4 fois

suprieur (IC95% 1,528,25) celui des employs dau-

tres dpartements (P 0,005). Le PR pour les in-

firmires travaillant dans un dpartement en relation

avec la TB a t de 5,1 (IC95% 3,238,42).

CONCLUSION : Parmi les HCW, les infirmires travail-

lant dans des dpartements en relation avec la TB en-

courent un risque accru de dvelopper la TB. Ceci sug-

gre quun certain nombre de cas de TB apparaissent la suite dune infection hospitalire.

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440 The International Journal of Tuberculosis and Lung Disease

R E S U M E N

MARCO DE REFERENCIA : Un hospital universitario pri-

vado en Corea del Sur.

OBJETIVO : Investigar la incidencia de tuberculosis (TB)

en los profesionales de la salud empleados en un hospitaluniversitario en Corea del Sur.

MTOD OS : Se analiz la ocurrencia de casos de TB du-

rante un periodo de 6 aos (20012006) en los profe-

sionales de la salud. La prevalencia de TB se compar

con la prevalencia en la poblacin general mediante el co-

ciente de prevalencia (PR) ajustado segn la edad y el sexo.

RESULTADOS : En el estudio se incluyeron 8433 perso-

nas. Sesenta y un profesionales de la salud presentaron

TB (0,72%). El PR en todos los proveedores de salud fue

1,05 (IC95% 0,801,35). En subgrupos por ocupaciones,

el PR fue 0,58 (IC95% 0,301,01) para los mdicos,

1,81 (IC95% 1,212,59) para el personal de enfermera

y 0,95 (IC95% 0,581,46) para los empleados en otros

departamentos. El riesgo relativo de TB en el personalde enfermera de departamentos relacionados con la TB

fue 3,4 veces mayor (IC95% 1,528,25) que el de los

empleados en otros departamentos (P 0,005). El PR

en el personal de enfermera de departamentos relacio-

nados con la TB fue 5,1 (IC95% 3,238,42).

CONCLUSIN : En los profesionales de la salud, el per-

sonal de enfermera que trabaja en departamentos rela-

cionados con la TB present un riesgo ms alto de TB.

Esto indica que parte de los casos de TB se adquiere por

infeccin intrahospitalaria.