Increased risk of tuberculosis among health care workers in Samara Oblast, Russia: analysis of notification data

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1 INT J TUBERC LUNG DIS 9(1): IUATLD Increased risk of tuberculosis among health care workers in Samara Oblast, Russia: analysis of notification data B. Dimitrova,* A. Hutchings,* R. Atun, F. Drobniewski, G. Marchenko, S. Zakharova, I. Fedorin, R. J. Coker* * Department of Public Health and Policy, London School of Hygiene & Tropical Medicine, London, The Business School, Imperial College, London, Department of Infectious Diseases, Guy s, King s and St Thomas Medical School, London, United Kingdom; Samara Oblast Health Department, Samara, Russian Federation SUMMARY SETTING: Samara Oblast, Russia. OBJECTIVE: To compare the rates of tuberculosis (TB) in health care workers (HCWs) working in TB services, general health services (GHS) and the general population in a region of the Russian Federation. DESIGN: Analysis of notification rates of TB among HCWs, GHS workers and the general population during the 9-year period from 1994 to RESULTS: During , TB incidence among staff employed at the TB services in Samara Oblast was ten times higher than among the general population, reaching 741.6/ person years at risk. Staff working at in-patient TB facilities were found to be at highest risk, with an incidence rate ratio of 17.7 (95%CI ) compared to HCWs at the GHS. CONCLUSIONS: HCWs at TB services in the Russian Federation are at substantially increased risk for TB, suggesting significant risks from nosocomial transmission. Control of institutional spread of TB in the Russian Federation is an area that requires urgent attention, especially given the epidemic of human immunodeficiency virus that Russia is currently witnessing. KEY WORDS: tuberculosis; health care workers; Russia INCREASED RISKS of tuberculosis (TB) have been reported in health care workers (HCWs) and subgroups of HCWs (medical laboratory workers, hospital employees, pathologists and general health services [GHS] staff) compared to rates in the general population. 1 6 In regions where specialised TB hospitals remain, the risk for TB among staff can reach times that of the general population. 7,8 The Russian Federation has witnessed a marked increase in rates of TB during the last decade. 9 TB services in the Russian Federation are provided through an extensive network of specialised TB facilities, and treatment is associated with lengthy periods of hospitalisation. According to official statistics of the Russian Ministry of Health, rates of TB are six to eight times higher among HCWs employed in TB services than among the general population. 10 Samara Oblast is located about 750 km south-east of Moscow. It has a population of approximately 3.3 million people. About 1.3 million people live in Samara (the regional capital), with a further living in Togliatti, a nearby conurbation. Following a period of steady decline, the incidence of TB in Samara Oblast reached its lowest ever level of 30.7 per population in Over the last decade, the annual number of newly notified cases has been increasing, and in 2002 the TB incidence was 54.4/ among permanent residents and 74.9/ in all population groups (including prisoners, migrants, army recruits and other special groups). Individuals diagnosed with TB are routinely admitted to in-patient facilities, usually for a period of 3 months, and subsequently followed up in out-patient facilities. 11 The aim of this study was to estimate the incidence of TB in HCWs in Samara Oblast since 1994 and to compare incidence rates for different types of health care facility. STUDY POPULATION AND METHODS We conducted a review of data on the number of newly diagnosed TB cases per calendar year among health care staff from 1994 to We used as a source the electronic database at Samara Oblast TB Dispensary (OTBD), which contains individualised demographic, clinical and epidemiological data on all Correspondence to: Dr Richard Coker, Department of Public Health and Policy, London School of Hygiene & Tropical Medicine, Keppel Street, London, UK. Tel: ( 44) Fax: ( 44) richard.coker@ lshtm.ac.uk Article submitted 3 March Final version accepted 25 May 2004.

2 44 The International Journal of Tuberculosis and Lung Disease TB cases notified in Samara Oblast since Notification data are collected prospectively and, since 1994, have been entered into an electronic database. Diagnoses in all cases are based on clinical signs of active TB and radiological, clinical and bacteriological investigations. All TB cases are reviewed by the Central Physician Commission, a central collegial body that verifies the diagnosis of TB and registers all cases. Screening of staff by fluorography is performed every 6 months, with further follow-up if abnormalities are detected, as is routine throughout Russia. We obtained data on the total number of TB cases among HCWs in each calendar year for Samara Oblast and for each facility where TB patients were treated. Data on the annual TB incidence rates for the general population were obtained from official statistics of the Samara OTBD. For each TB facility we obtained data on the average number of persons employed in each calendar year from the OTBD. Health care staff studied included physicians, nurses, auxiliaries, laboratory technicians and other non-medical support staff. These data were derived from the Dispensary database. Each TB facility was categorised as providing inpatient or out-patient services. Where a facility provided both, and it was possible to separately identify the number of cases and staff between in-patient and out-patient services, the in-patient and out-patient services were categorised separately. A third category was created for facilities where it was not possible to separately identify cases and staff numbers between in-patient and out-patient services, or where individual staff worked across both types of service. Crude incidence rates per person years (py) at risk were calculated for staff working in TB facilities and staff working in the GHS. The average annual number of staff employed in each facility was used as an estimate of person years at risk. The rates for staff working in the GHS were calculated after subtracting staff working in TB facilities from the overall numbers for Samara Oblast. Differences in age, sex, occupation, TB site and detection by screening were assessed for cases from TB facilities and the GHS using t-tests for continuous variables and 2 tests for categorical variables. We used a Poisson regression model to estimate the incidence of TB and the incidence rate ratios for each category of TB facility compared with staff working in other health care facilities. Confidence intervals (CI) were calculated using robust standard errors to allow for over-dispersion in the data. 12 A test for trend was used to assess whether there was a trend in the incidence of TB associated with increasing in-patient provision in the three categories of TB facilities. We also tested for a trend in the annual incidence of TB among staff working in TB facilities by including year of notification in the model. RESULTS Forty-nine separate TB facilities provide diagnostic and curative services for adults with TB: four inpatient only facilities, 38 out-patient only facilities and seven facilities providing both in-patient and outpatient care (Table 1). The in-patient and out-patient facilities at Samara OTBD were categorised separately because they were on different sites. The annual average number of TB HCWs was 1999 during the study period, with most working in the TB dispensaries. The GHS had an average of HCWs during the same period. There were 80 cases of TB notified during the study period among HCWs working in TB facilities and 394 cases notified for workers in the GHS (Table 2). With a mean age of 39.5 years, cases among workers at TB facilities were, on average, older than cases in the GHS by 2.9 years (95%CI ). A higher proportion of cases in TB HCWs were female (88.8%) than among cases in the GHS (74%). Most cases in TB HCWs were in nurses (38.8%) and auxiliaries (27.5%), although the distribution was similar to cases in the GHS (P 0.76). There was no evidence of a difference in the proportion of pulmonary TB cases or the proportion of these with bacteriological verification. A higher proportion of cases (91.3%) was detected through screening in TB HCWs compared with 67.5% among the GHS (P 0.001). The crude incidence rate of TB in HCWs working in TB facilities was 741.6/ py (95%CI ) (Table 3). There was no evidence that the rate changed during the study period (incidence rate ratio 1.027/year, 95%CI ). In comparison, the crude incidence rate among HCWs in the GHS was 68.8/ py at risk (95%CI ), giving an incidence rate ratio of 10.8 (95%CI ) for HCWs in the TB services compared with those in the GHS. The rate in HCWs in the GHS was closer to the rates in the civil population Table 1 TB facilities in Samara Oblast, Average number of health care workers Facilities Cases Type of facility n n Hospitals (in-patients) Oblast TB Dispensary (in-patients) TB dispensaries in major towns (in-patients and out-patients) Samara City TB Dispensaries, Samara City TB physicians offices and Oblast TB Dispensary (out-patients) Rural TB physicians offices (out-patients) Total TB tuberculosis.

3 Tuberculosis control in health care workers 45 Table 2 TB cases among health care workers in Samara Oblast, TB facilities (n 80) Other health care facilities (n 394) P value Age, years: mean (SD) 39.5 (13.0) 36.6 (11.6) 0.04 Female sex, n (%) 71 (88.8) 292 (74.1) Occupation Doctor 13 (16.3) 77 (19.5) Nurse 31 (38.8) 164 (41.6) 0.76 Laboratory technician 5 (6.3) ] Auxiliary and other 31 (38.8) 153 (38.8) Site, n (%) Pulmonary 70 (87.5) 342 (86.8) Extra-pulmonary 10 (12.5) 52 (13.2) 0.87 Pulmonary cases with bacteriological verification,* n (%) 21 (30.0) 133 (38.9) 0.16 Detection by screening, n (%) 73 (91.3) 266 (67.5) * Culture-positive and/or smear-positive. TB tuberculosis; SD standard deviation. Figure TB incidence rates among staff of the TB services compared to the general health services and the general population, Samara Oblast, Russian Federation. GHS general health services; TB tuberculosis. (permanent residents only) of 56.3/ and the general population (including prisoners and other special groups reported separately) of 74.1/ during (Figure). After categorising TB facilities according to their in-patient and out-patient services, we found strong evidence of a trend of increasing incidence associated with greater provision of in-patient TB facilities (test for trend P 0.001). The rate was highest for staff working in in-patient facilities, with an incidence rate ratio of 17.7 (95%CI ) compared to workers in the GHS (Table 3). The two main TB facilities contributed the most cases among HCWs, with 18 at Samara City TB Hospital No. 1 and 13 at the OTBD. The crude TB incidence rate in HCWs at Samara City TB Hospital No. 1 was 1460/ py at risk. During , on average 137 persons were employed at TB Hospital No. 1 at any time, including 16 physicians, 49 medium-level health staff (nurses, laboratory technicians and pharmacists), 40 junior health staff (auxiliaries) and 32 other support personnel. The hospital is Table 3 Incidence of TB among HCWs by setting in Samara Oblast, Russian Federation Setting Incidence of TB per person years (95%CI) Incidence rate ratio (95%CI) HCWs in GHS 68.8 ( ) reference TB HCWs ( ) 10.8 ( ) By category of TB facility TB out-patient ( ) 4.6 ( ) TB out-patient and in-patient ( ) 12.0 ( ) TB in-patient ( ) 17.7 ( ) TB tuberculosis; HCWs health care workers; CI confidence interval; GHS general health services. a 300-bed facility situated on the outskirts of Samara city. During the study period it had an average of 1404 admissions for TB every year, the highest admission rate of all the region s TB facilities. The hospital provides care for the poorest and most disadvantaged TB patients. Although there is no consistent definition of a chronic case in the Russian literature, in practice TB cases are usually considered chronic when they have several years history of TB, radiological changes on X-ray showing cavitary and fibrotic lesions, and positive smear microscopy or culture results. The hospital also serves as a hospice for terminally ill prisoners with TB. In 2000, 35% of all patients admitted to the hospital were chronic infectious cases. 13 Many of these chronic cases probably had multidrug-resistant TB (MDR-TB, defined as resistance to at least isoniazid and rifampicin), with poor treatment outcomes. The second major site for cases in HCWs was the in-patient department of the OTBD, a tertiary referral facility for TB patients from Samara Oblast, providing consultative diagnostic services and conservative and surgical treatment. During the study period the average number of staff employed at the OTBD inpatient department annually was 119. Thirteen cases of TB were diagnosed among staff, corresponding to an incidence rate of 1210/ py at risk. Seven of these had worked for more than 12 years at that facility before being diagnosed with TB, and only three had worked there for fewer than 5 years. The dispensary has 180 beds and on average 886 admissions per year; approximately 500 surgical operations are performed annually in the treatment of TB. Other invasive treatment procedures are also widely used, including bronchoscopy for direct intrabronchial infusion of anti-tuberculosis drugs. 14 No TB cases among staff at the out-patient department were registered during the study period.

4 46 The International Journal of Tuberculosis and Lung Disease DISCUSSION The findings presented in this paper show that staff working in TB facilities in one region of the Russian Federation are at substantially increased risk of acquiring TB compared with their colleagues working in the GHS and the general population. It seems likely that these high rates are a consequence of occupational exposure, as higher rates were seen in in-patient than out-patient TB facilities; patients treated in out-patient facilities have traditionally completed several months of treatment and are likely to be less infectious, and therefore expose HCWs to less risk than in TB inpatient facilities. 11 The rates reported here in employees in TB services are higher than those reported previously from other regions of the Russian Federation. 15,16 Few young professionals seek employment at the TB services because of low salaries, occupational hazards and limited career development opportunities, which could explain the older mean age of cases and the higher proportion of female cases among workers at TB facilities. Other reports have shown that certain professional groups working within the TB services are at especially high risk including, in declining order of relative risk, those working within microbiology laboratories, specialised TB hospitals, out-patient TB facilities, and pathology departments. 17 Staff of internal disease wards in large general hospitals, emergency health services and those working in pharmacies seem to be at relatively low risk. 17 In Samara, 31 cases were notified from the pathology department of the forensic medicine services, services outside the TB services. Our research has a number of limitations. Notification bias may have resulted from HCWs with newly diagnosed TB being transferred from other health services to the TB services. Similarly, staff who acquire TB working in some disciplines, for example paediatrics, are prohibited from working in this discipline again and may seek employment in the TB service. These potential sources of bias would tend to increase the relative rates of TB in HCWs working in TB services if HCWs are incorrectly categorised as working in TB services for notification purposes. However, we consider that these potential sources of bias are unlikely to substantially alter our findings, for four reasons. First, formal procedures mean that TB cases are registered at their original place of work rather than in subsequent work settings. Second, we have attempted to avoid bias by reviewing the cases with dispensary chiefs. Third, over 90% of cases in TB facilities were detected by screening at those facilities. Fourth, data from Samara OTBD showed that only three of the 13 cases had been working at the Dispensary for fewer than 5 years before they were diagnosed with TB. A further potential source of bias may have occurred through better case detection among staff in TB facilities compared to the general population. This may result from the regular screening for TB and raised levels of awareness of the risks of disease amongst medical staff. Because of the retrospective nature of the study, data were not available on the demographic characteristics of HCWs across the different TB facilities or GHS, so we could not examine the extent to which differences in these characteristics may explain the observed age and sex differences. Moreover, the retrospective nature of the study also meant that sputum status and drug sensitivity patterns of isolates were unavailable, information on exposures to TB other than occupation was lacking, and follow-up data on identified cases were also lacking. The federal government, recognising the increased risk for staff working in some areas, supports control efforts through regulatory guidance administered through the network of sanitary epidemiological stations and TB dispensaries For example, under article 34 of the General Sanitary Epidemiological Law, certain professions are obliged to undergo screening for TB prior to entering employment and periodically thereafter. 18 Health care workers, those working in educational institutions, and workers in the food industries, public transport and other service branches, are obliged to be screened for TB once a year, while those working in health and educational facilities with young children and adolescents are screened every 6 months. 19 The occupational hazards experienced by health workers and other personnel working with TB services have recently been recognised in the Federal Law on TB Control, which ensures the provision of certain benefits including extended annual leave, reduced working hours, additional remuneration and early retirement. 21 It has been suggested that effective TB infection control programmes need to focus on the use of administrative measures to reduce the risk of exposure from those who have infectious TB, the use of engineering controls to prevent the spread and reduce the concentration of infectious droplets, and the use of personal protective respiratory equipment. 22 In the Russian Federation, resource limitations and a traditional emphasis on radiological diagnosis rather than microbiological determination means that diagnostic approaches have probably not effectively prioritised infectious patients, and the separation of infectious from non-infectious patients has not been institutionalised in practice. Moreover, limited resources and the maintenance of substantial hospital infrastructures have probably resulted in under-funding and inappropriate or inadequate engineering controls. Whilst the use of ultraviolet (UV) light is widespread, the effectiveness of old lamps and their positioning may, anecdotally, limit the benefits gained. Effective air filtration and airflow engineering in hospital settings are prohibitively expensive to install and main-

5 Tuberculosis control in health care workers 47 tain. Likewise, the cost of personal protective equipment is prohibitive in most Russian institutions and it is only very rarely available to staff. Institutional spread of TB is a phenomenon recognised worldwide. The recognition of the potential magnitude of this problem arose in part when disease from strains that were resistant to several first-line anti-tuberculosis drugs was observed in patients who had been cared for in the same hospital or institution. The epidemic of the human immunodeficiency virus (HIV) helped bring this spread to attention because of the rapidity with which co-infected cases developed TB. Russia is now witnessing an epidemic of HIV and has high rates of TB (and MDR-TB). The tradition of lengthy hospitalisation in the treatment of TB appears to put at risk HCWs working within those institutions and also, presumably, the patients residing there. Measures to reduce institutional spread have been introduced over the past 2 years, including safer sputum collection practices and measures to separate infectious from non-infectious patients. In addition, substantial investment since 2002 has improved microbiology laboratory capacity and quality. Institutional spread of TB in Russian hospitals represents a substantial public health threat and challenge, a challenge that is likely to grow in magnitude with an expanding HIV epidemic, and one that requires urgent attention. References 1 Menzies D, Fanning A, Yuan L, Fitzgerald M. Tuberculosis among health care workers. N Engl J Med 1995; 332: Sugita M, Tsutsumi Y, Suchi M, Kasuga H, Ishiko T. Pulmonary tuberculosis. An occupational hazard for pathologists and pathology technicians in Japan. Acta Pathol Jpn 1990; 40: Harrington J M, Shannon H S. Mortality study of pathologists and medical laboratory technicians. BMJ 1975; 4: Meredith S, Watson J M, Citron K M, Cockcroft A, Darbyshire J H. Are healthcare workers in England and Wales at increased risk of tuberculosis? BMJ 1996; 313: Cuhadaroglu C, Erelel M, Tabak L, Kilicaslan Z. Increased risk of tuberculosis in health care workers: a retrospective survey at a teaching hospital in Istanbul, Turkey. BMC Infect Dis 2002; 2: Kilinc O, Ucan E S, Cakan M D, et al. Risk of tuberculosis among healthcare workers: can tuberculosis be considered as an occupational disease? Respir Med 2002; 96: Kruuner A, Danilovitsh M, Pehme L, Laisaar T, Hoffner S E, Katila M L. Tuberculosis as an occupational hazard for health care workers in Estonia. Int J Tuberc Lung Dis 2001; 5: 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: World Health Organization. Global TB Control. Geneva, Switzerland: WHO, Ministry of Health. On the improvement of the provision of antituberculosis services to the population of the Russian Federation. Order No Moscow, Russian Federation: Ministry of Health, Coker R, Dimitrova B, Drobniewski F, et al. Tuberculosis control in Samara Oblast, Russia: institutional and regulatory environment. Int J Tuberc Lung Dis 2003; 10: Stata Corporation. Stata statistical software: release 7.0. College Station, TX: Stata Corporation, Annual Report of City Hospital 1. Samara City, Samara Oblast, Russia, Ministry of Health. On approval of standards (model protocols) for management of tuberculosis. Order No. 33 from 2 February 1998 of the Ministry of Health of the Russian Federation, Priimak A A, Plotnikova L M. Zabolevaemost tuberkulezom meditsinskikh rabotnikov i mery ikh sotsial noi zashchity. Probl Tuberk 1992; 11 12: Nechaeva O B, Shorikova L I, Vatolina V A, Mordovskoi G G, Kondrashin A G. Vliianie grupp riska na zabolevaemost tuberkulezom i profilakticheskai rabota s nimi. Probl Tuberk 1997; 5: Kosarev V. Occupational diseases of health care workers. Samara, Russian Federation: Samara State Medical University, Ministry of Health. About the sanitary-epidemiological wellbeing of the population. Federal Law No 52 of 12 March Moscow, Russian Federation: Ministry of Health, Ministry of Health. About conducting obligatory medical screening for TB and regulations for permission to work in certain professions for persons suffering from TB. Instruction of the MoH of the USSR from Moscow, Russian Federation: Ministry of Health, Ministry of Health. Sanitary rules by work in tuberculosis facilities in the system of the Ministry of Health of USSR, Moscow, Russian Federation: Ministry of Health, Ministry of Health. On prevention of the spread of tuberculosis. Federal Law N 77-FZ of Moscow, Russian Federation: Ministry of Health, Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities, MMWR 1994; 43(RR-13). RÉSUMÉ CONTEXTE : Oblast de Samara, Russie. OBJECTIF : Comparer les taux de tuberculose (TB) chez les travailleurs de soins de santé (HCW) travaillant dans les services TB, dans les services généraux de santé (GHS) et dans la population générale dans une région de la Fédération de Russie. SCHÉMA: Analyse des taux de déclaration de TB parmi les HCW, les travailleurs GHS et la population générale au cours d une période de 9 ans entre 1994 et RÉSULTATS : Pendant la période , l incidence de la TB parmi le personnel employé dans les services de TB dans l Oblast de Samara est 10 fois supérieure à l incidence de la TB dans la population générale et atteint 741,6/ personnes/année de risque. Le personnel travaillant dans les services d hospitalisation TB a le risque le plus élevé, avec un ratio d incidence de 17,7 (intervalle de confiance à 95% 11,6 27,1) par comparaison avec les HCW du GHS.

6 48 The International Journal of Tuberculosis and Lung Disease CONCLUSIONS : Les HCW dans les services TB de la Fédération de Russie encourent un risque substantiellement accru de TB, ce qui suggère des risques significatifs provenant de la transmission nosocomiale. La lutte contre la dispersion institutionnelle de la TB dans la Fédération de Russie constitue un secteur exigeant une attention urgente, particulièrement vu l épidémie du virus de l immunodéficience humaine (VIH) que connaît la Russie. RESUMEN MARCO DE REFERENCIA : Samara Oblast, Federación de Rusia. OBJETIVO : Comparar las tasas de tuberculosis en los trabajadores de atención en salud de los servicios de TB, en los servicios de medicina general y en la población general en una región de la Federación de Rusia. METODO : Análisis de las tasas de declaración de TB entre los trabajadores de la salud, los empleados de los servicios de medicina general y la población general durante un periodo de 9 años entre 1994 y RESULTADOS : Entre 1994 y 2002 la incidencia de TB entre el personal empleado en los servicios de TB de Samara Oblast fue 10 veces más alta que la incidencia de TB en la población general y alcanzó un riesgo de 741,6 por personas-año. El personal de los establecimientos hospitalarios para TB presentó el riesgo más alto con respecto a la de los trabajadores de los servicios de medicina general, con una razón de tasas de incidencia de 17,7 (intervalo de confianza 95% 11,6 27,0). CONCLUSIONES : Los trabajadores de atención en salud en los servicios de TB de la Federación de Rusia presentan un riesgo considerablemente aumentado de TB, lo cual indica un gran riesgo de transmisión nosocomial. La lucha contra la diseminación institucional de la tuberculosis en la Federación de Rusia es un asunto que requiere atención urgente, y aún más teniendo en cuenta la epidemia de infección por el virus de la inmunodeficiencia humana (VIH) que se presencia en este país.

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