Incidence of tuberculosis among health care workers at a private university hospital in South Korea

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1 INT J TUBERC LUNG DIS 12(4): 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. 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 ( ) was reviewed. The prevalence of TB was compared with that of the general population using a prevalence ratio (PR) adjusted by age and sex. RESULTS: The study involved 8433 people. TB developed in 61 HCWs (0.72%). The prevalence ratio among all HCWs was 1.05 (95%CI ). In occupational subgroups, the PRs for doctors, nurses and employees in other departments were respectively 0.58 (95%CI ), 1.81 (95%CI ) and 0.95 (95% CI ). For nurses working in TB-related departments, the relative risk of developing TB was 3.4 times higher (95%CI ) than for employees in other departments (P 0.005). The PR for nurses working in TB-related department was 5.1 (95%CI ). CONCLUSION: Among HCWs, nurses working in TBrelated departments were at increased risk of developing TB. This suggests that some TB develops via in-hospital infection. KEY WORDS: tuberculosis; health care workers; hospitalacquired infection DESPITE RECENT PROGRESS in global control efforts, tuberculosis (TB) remains a major public health burden in many countries. TB is an established occupational disease of health care workers (HCWs), 1 3 and those infected may transmit the disease to susceptible individuals. 4,5 Recent reports suggest that HCWs in high-prevalence countries have an increased tendency to develop nosocomial TB infection In contrast, where the prevalence of TB is low, the risk of HCWs acquiring TB is likely to be small. 12 The TB burden in South Korea was assessed nationwide using TB prevalence surveys at 5-year intervals from 1965 to These nationwide surveys revealed that there has been a marked decrease in the prevalence of smear- and/or culture-positive TB, from 940 per population in 1965 to 219/ in While these surveys provide reliable information on the prevalence of TB and its trend over the last 30 years, there were difficulties in surveying a random sample large enough to accurately measure the declining prevalence of TB. 14,15 As a result, an internet-based routine reporting system for TB, the Korean TB Surveillance System (KTBS), was developed and launched in June Physicians completed and sent the standardised reporting form for all TB cases to the KTBS via the internet. Based on the data collected following the implementation of the KTBS, it was presumed that TB incidence in South Korea was in the intermediate range (92/ ). There has been no study of the risk of TB among HCWs in South Korea, with the exception of a single study restricted to laboratory technicians. 16 The objective of the present study was thus to assess the occupational risk of TB among HCWs employed at a private university hospital in South Korea, an intermediate TB burden country. STUDY POPULATION AND METHODS Subjects The study involved a retrospective analysis of the medical records of all HCWs employed at the Asan Medical Centre, Seoul, South Korea, from January 2001 to December All employees who worked at the centre for least 6 months during the study period were investigated for the development of TB. A list of HCWs with TB was obtained from data reported 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 Medicine, Asan Medical Centre, Pungnap-Dong, Songpa-Ku, Seoul , South Korea. Tel: ( 82) Fax: ( 82) shimts@amc.seoul.kr Article submitted 26 November Final version accepted 21 December 2007.

2 TB among Korean health care workers 437 Medical Centre and the KTBS. To obtain the list of HCWs with TB, the resident registration number was cross-matched between the lists of all HCWs and KTBS. One of the several objectives of this study was to assess the incidence of active TB disease among HCWs. In this study, TB therefore refers to active TB disease and not latent TB infection. As the tuberculin skin test (TST) was not performed routinely at start of employment in South Korea, we do not have previous records of TST. TB was diagnosed by bacteriological culture, histological evidence of granuloma with caseation necrosis or clinical findings consistent with active TB. This study was approved by the Institutional Review Board of the Asan Medical Centre. Bacteriological examinations Mycobacterium tuberculosis was cultured on Ogawa medium and identified by hybridisation methods using a commercial molecular probe (AccuProbe, Gen-Probe Inc., San Diego, USA) or duplex PCR (Molecules and Diagnostics Inc., Wonju, South Korea). Drug susceptibility testing (DST) was carried out by the Korean Institute of Tuberculosis, a Supranational TB Reference Laboratory. Statistical analysis All analyses were performed using SPSS software (version 12.0, SPSS Inc., Chicago, IL, USA). Comparisons 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. All tests of significance were two sided; P 0.05 was considered statistically significant. The objective of this study was to assess the incidence of TB among HCWs. However, because there were more young people and females among HCWs compared with the general population, it was difficult to compare the results of the incidence of TB between HCWs and the general population. We therefore used the 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 South Koreans). As the PR was adjusted for age and sex, it was possible to estimate the TB incidence from the PR. (The PR of the general population is always 1.) The expected number of TB cases among the South Korean population was derived from data from nationwide TB prevalence surveys conducted in RESULTS Incidence of TB among HCWs Between January 2001 and December 2006, the work force comprising those employed for 6 months at the Asan Medical Centre was 8433 individuals. This included 5610 doctors and nurses (2389 and 3221, respectively) and 2823 persons employed in other departments, including paramedics, pharmacists, laboratory technicians and office workers. The mean age was 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 among HCWs was therefore 723.3/ and the PR was 1.05 (95% confidence interval [CI] ). The mean age of the 61 tuberculous HCWs was years, females predominated (49/61, 80.3%), 41 were doctors or nurses (0.73%, 41/5610) and the other 20 were from other departments (0.71%, 20/ 2823). The characteristics of TB occurrence among the HCWs are shown in the Table. TB developed in 8/5610 doctors, in 8/263 nurses working in TB-related departments and in 25/2958 nurses working in other departments. There was no significant difference in TB prevalence between doctors (0.58, 95%CI ) and nurses (1.81, 95%CI ). The combined prevalence ratio for doctors and nurses was 1.12 (95%CI ), and for personnel in other departments it was 0.95 (95%CI ). Nurses comprised the only occupational subgroup with a high PR, with 29/3221 developing TB (0.9%, 900.3/ ). The relative risk of developing TB Table Clinical characteristics of health care workers with tuberculosis Doctors and nurses (n 41) n (%) Occupational subgroups Others* (n 20) n (%) P value Age, years, mean SD Sex 0.09 Male 6 (14.6) 7 (35.0) Female 35 (85.4) 13 (65.0) Height, cm, mean SD Weight, kg, mean SD BMI, kg/m 2, mean SD Previous TB history 2 (4.9) 1 (5.0) 1 Smoking 4 (9.8) 4 (20.0) 0.42 Site of TB 0.49 Pulmonary 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 0.95 None 39 (95.1) 18 (90) Present 2 (4.9) 2 (10) Bronchial asthma 2 (4.9) 0 Thyroid 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 and office workers). SD standard deviation; BMI body mass index; TB tuberculosis.

3 438 The International Journal of Tuberculosis and Lung Disease Figure The PR of tuberculosis according to occupational subgroups. The PR of the general population is 1. TB tuberculosis; PR prevalence ratio. was 3.4 times higher (95%CI ) for those working in TB-related departments (medical intensive care unit, respiratory department ward and emergency room) compared with those working in other departments (P 0.005). The PR for nurses working in TB-related departments was 5.1 (95%CI ) (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 and five (8.2%) had TB pleurisy. Sputum acid-fast bacilli (AFB) smear and bacteriological culture were performed for 45 of the 49 HCWs with pulmonary TB; positive sputum smears and cultures were obtained from respectively seven (15.6%) and 20 (44.4%) cases. Of 12 M. tuberculosis isolates for which DST was carried out, 11 (91.7%) were susceptible to all available anti-tuberculosis drugs. The remaining isolate was multidrug-resistant (MDR, defined as resistance to both isoniazid and rifampicin). However, this MDR- TB individual was cured with first-line drugs only. The median period from employment at hospital to development of TB was 894 days (range ). All patients were cured by first-line drugs and one (1.6%) patient had recurrence of the disease 4 years after treatment completion. DISCUSSION In the present study, we determined the occupational risk of TB in the work force of a private university hospital in South Korea, a country with an intermediate TB burden. This is the first study to investigate the incidence of TB in HCWs in Korea. The most important finding was that TB developed much more frequently in nurses working in TB-related departments compared to the general population or HCWs in other departments, suggesting occupational acquisition of TB rather than reactivation of latent TB. Because employees 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 infected with M. tuberculosis afterwards. However, the finding that more TB patients were detected in TBrelated departments than in other departments suggests that some of the HCWs developed the disease via hospital infection. There was no significant difference in the PR between HCWs and the general population. However, among occupational subgroups, the PR for nurses was higher than that of doctors and employees in other departments (including office workers), and was notably higher among nurses working in TB-related departments (medical intensive care unit, respiratory department ward and emergency room). This finding is consistent with previous reports showing that TB risk among medical nurses employed in specialised lung disease institutions is higher than among those in non-exposed institutions. 6,7,17 The reported rates of TB in different groups of HCWs in TB-endemic countries have varied widely, with a higher risk of TB in HCWs reported by some studies and a lower risk by others. For example, Kruuer et al. showed that the TB risk among HCWs in Estonia was higher than in the general population. 9 Similar results have been obtained in studies in Serbia 8 and Japan, 18 while opposite results were obtained in two other studies. 19,20 There is a general trend for TB risk among HCWs to be related to the TB incidence in the country concerned. As South Korea is an intermediate TB burden country, our result is consistent with previous studies. To stop the spread of TB in hospitals, several preventive strategies should be implemented: administrative, engineering and personal respiratory protection. 21 In the hospital used for this study, infectious TB patients are placed in isolation rooms equipped with ultraviolet germicidal irradiation (UVGI) and negative pressure ventilation. HCWs or visitors who enter the isolation room are required to wear N-95 respirators. All HCWs undergo an annual chest X-ray, but annual TSTs are performed only in nurses working in TBrelated wards. The results of this study suggest that stricter preventive strategies, such as contact investigations of active TB disease, the installation of an isolation room in the emergency room, and latent TB infection screening by TST at the time of hiring should be implemented for all HCWs. The present study had several limitations. The incidence of TB in HCWs in the hospital was determined from reports to the Department of Infection Control at the Asan Medical Centre and the KTBS. It is therefore possible that the incidence of TB was underestimated due to incomplete reporting. Second, when

4 TB among Korean health care workers 439 calculating the PR, the expected number of TB cases in the general population was derived from data from the last nationwide TB prevalence survey, performed in However, as the incidence of TB has been decreasing over the past 10 years in South Korea, it is likely that there were fewer TB patients in the study period than in 1995, resulting in an underestimation of PR for HCWs. Third, this study was carried out in only one hospital and may not represent the situation in South Korean medical institutions in general. However, the hospital in which this study was performed is the biggest and one of the best equipped in Korea, which suggests that the situation in Korean hospitals may be more serious than this study concludes. In conclusion, among HCWs in a hospital in South Korea, only nurses, particularly those working in TBrelated departments, were more likely to develop TB than individuals in the general population. Stricter preventive strategies against the spread of TB in hospitals need to be implemented. Acknowledgement The authors acknowledge the support of the Department of Infection Control at the Asan Medical Centre. References 1 Menzies D, Fanning A, Yuan L, Fitzgerald M. Tuberculosis among health care workers. N Engl J Med 1995; 332: Sepkowitz K A. AIDS, tuberculosis and the health care worker. Clin Infect Dis 1995; 20: Schwartzman K, Loo V, Pasztor J, Menzies D. Tuberculosis infection among health care workers in Montreal. Am J Respir Crit Care Med 1996; 154: Markowitz S B. Epidemiology of tuberculosis among health care workers. Occup Med 1994; 9: Pearson M L, Jereb J A, Frieden T R, et al. Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis: a risk to patients and health care workers. Ann Intern Med 1992; 117: Jiamjarasrangsi W, Hirunsuthikul N, Kamolratanakul P. Tuberculosis among health care workers at King Chulalongkorn Memorial Hospital, Int J Tuberc Lung Dis 2005; 9: Kilinc O, Ucan E S, Cakan A, et al. Risk of tuberculosis among health care workers: can tuberculosis be considered as an occupational disease? Res Med 2002; 96: Skodric V, Savic B, Jovanovic M, et al. Occupational risk of tuberculosis among health care workers at the institute for pulmonary diseases of Serbia. Int J Tuberc Lung Dis 2000; 4: Kruuner A, Danilovitsh M, Pehme L, et al. Tuberculosis as an occupational hazard for health care workers in Estonia. Int J Tuberc Lung Dis 2001; 5: Kanyerere H S, Salaniponi F. Tuberculosis in health care workers in a central hospital in Malawi. Int J Tuberc Lung Dis 2003; 7: Cubadaroglu C, Erelel M, Tabuk L. Increased risk of tuberculosis in health care workers: a retrospective survey at a teaching hospital in Istanbul, Turkey. BMC Infect Dis 2002; 2: Riley M, Loughrey C M, Wilkinson P, Patterson C C, Varghese G. Tuberculosis in health service employees in Northern Ireland. Respir Med 1997; 91: Hong Y P, Kim S J, Lew W J, Lee E K, Han Y C. The seventh nationwide tuberculosis prevalence survey in Korea, Int J Tuberc Lung Dis 1998; 2: Lew W J, Lee E G, Bai J Y, et al. An Internet-based surveillance system for tuberculosis in Korea. Int J Tuberc Lung Dis 2006; 10: Seung K J, Bai G H, Kim S J, et al. The treatment of tuberculosis in South Korea. Int J Tuberc Lung Dis 2003; 7: Kim S J, Lee S H, Kim I S, et al. Risk of occupational tuberculosis in national tuberculosis programme laboratories in Korea. Int J Tuberc Lung Dis 2007; 11: Babus V. Tuberculosis morbidity risk in medical nurses in specialized institutions for the treatment of lung diseases in Zagreb. Int J Tuberc Lung Dis 1997; 1: Usui T, Yamanaka K, Nomura H, Tokudome S. Elevated risk of tuberculosis by occupation with special reference to health care workers. J Epidemiol 2000; 10: McKenna M T, Hutton M, Cauthen G, Onorato I M. The association between occupation and tuberculosis. A populationbased survey. Am J Respir Crit Care Med 1996; 154: Raitio M, Tala E. Tuberculosis among health care workers during three recent decades. Eur Respir J 2000; 15: Jensen P A, Lambert L A, Iademarco M F, Ridzon R. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care settings, MMWR Recomm Rep 2005; 54: RÉSUMÉ CONTEXTE : Un hôpital universitaire privé en Corée du Sud. OBJECTIF : Investiguer l incidence de la tuberculose (TB) chez les travailleurs des soins de santé (HCW) employés dans un hôpital universitaire de Corée du Sud. SCHÉMA : On a révisé la survenue de cas de TB parmi les HCW pendant une période de 6 années ( ). On a comparé la prévalence de la TB avec celle de la population générale en utilisant un ratio de prévalence (PR) ajusté pour l âge et le sexe. RÉSULTATS : L étude a comporté 8433 personnes. La TB est survenue chez 61 HCW (0,72%). Le PR pour l ensemble des HCW a été de 1,05 (IC95% 0,80 1,35). Dans les sous-groupes professionnels, le PR pour les médecins, les infirmières et les autres types d HCW a été respectivement de 0,58 (IC95% 0,30 1,01), 1,81 (IC95% 1,21 2,59) et 0,95 (IC95% 0,58 1,46). Pour les infirmières travaillant dans des départements en relation avec la TB, le risque relatif de développer une TB a été 3,4 fois supérieur (IC95% 1,52 8,25) à celui des employés d autres départements (P 0,005). Le PR pour les infirmières travaillant dans un département en relation avec la TB a été de 5,1 (IC95% 3,23 8,42). CONCLUSION : Parmi les HCW, les infirmières travaillant dans des départements en relation avec la TB encourent un risque accru de développer la TB. Ceci suggère qu un certain nombre de cas de TB apparaissent à la suite d une infection hospitalière.

5 440 The International Journal of Tuberculosis and Lung Disease RESUMEN MARCO DE REFERENCIA : Un hospital universitario privado en Corea del Sur. OBJETIVO : Investigar la incidencia de tuberculosis (TB) en los profesionales de la salud empleados en un hospital universitario en Corea del Sur. MÉTODOS : Se analizó la ocurrencia de casos de TB durante un periodo de 6 años ( ) en los profesionales de la salud. La prevalencia de TB se comparó con la prevalencia en la población general mediante el cociente de prevalencia (PR) ajustado según la edad y el sexo. RESULTADOS : En el estudio se incluyeron 8433 personas. Sesenta y un profesionales de la salud presentaron TB (0,72%). El PR en todos los proveedores de salud fue 1,05 (IC95% 0,80 1,35). En subgrupos por ocupaciones, el PR fue 0,58 (IC95% 0,30 1,01) para los médicos, 1,81 (IC95% 1,21 2,59) para el personal de enfermería y 0,95 (IC95% 0,58 1,46) para los empleados en otros departamentos. El riesgo relativo de TB en el personal de enfermería de departamentos relacionados con la TB fue 3,4 veces mayor (IC95% 1,52 8,25) que el de los empleados en otros departamentos (P 0,005). El PR en el personal de enfermería de departamentos relacionados con la TB fue 5,1 (IC95% 3,23 8,42). CONCLUSIÓN : En los profesionales de la salud, el personal de enfermería que trabaja en departamentos relacionados con la TB presentó un riesgo más alto de TB. Esto indica que parte de los casos de TB se adquiere por infección intrahospitalaria.