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STATE OF THE ART

INT J TUBERC LUNG DIS 11(6):593–605 © 2007 The Union

STATE OF THE ART SERIES Occupational lung disease in high- and low-income countries Edited by M. Chan-Yeung NUMBER 5 IN THE SERIES

Risk of tuberculosis infection and disease associated with work in health care settings D. Menzies,* R. Joshi,† M. Pai* * Respiratory Epidemiology and Clinical Research Unit, Montreal Chest Institute, McGill University, Montreal, Canada; †Mahatma Gandhi Institute of Medical Sciences, Sevagram, India SUMMARY BACKGROUND:

Tuberculosis (TB) in health care workers (HCWs) was not considered a serious problem following the advent of effective antibiotic therapy. Interest was restimulated by the occurrence of several major nosocomial outbreaks. M E T H O D S : We have reviewed the available published literature regarding prevalence and incidence of TB infection and disease among HCWs in countries categorised by mean income. We included studies published in English since 1960 from low- and middle-income countries (LMICs) and since 1990 from high-income countries (HICs). We excluded outbreak reports and studies based only on questionnaires. R E S U L T S : The median prevalence of latent TB infection (LTBI) in HCWs was 63% (range 33–79%) in LMICs and 24% in HICs (4–46%). Among HCWs from LMICs, LTBI was consistently associated with markers of occu-

pational exposure, but in HICs it was more often associated with non-occupational factors. The median annual incidence of TB infection attributable to health care work was 5.8% (range 0–11%) in LMICs and 1.1% (0.2–12%) in HICs. Rates of active TB in HCWs were consistently higher than in the general population in all countries, although findings were variable in HICs. Administrative infection control measures had a modest impact in LMICs, yet seemed the most effective in HICs. C O N C L U S I O N S : TB remains a very important occupational risk for HCWs in LMICs and for workers in some institutions in HICs. Risk appears particularly high when there is increased exposure combined with inadequate infection control measures. K E Y W O R D S : tuberculosis; occupational TB; nosocomial transmission; health professionals; infection control

TUBERCULOSIS (TB) has long been recognised as an important occupational hazard for health care workers (HCWs). In the pre-antibiotic era, TB caused substantial morbidity and mortality among medical and nursing students.1 With the advent of effective antibiotic therapy and decreasing incidence in high-income countries (HICs), the risk declined, leading to complacency about

nosocomial transmission. In the late 1980s, dramatic nosocomial outbreaks of multidrug-resistant (MDR) TB occurred—largely in human immunodeficiency virus (HIV) infected populations. These caused as many as 200 secondary active cases, of whom 50–80% died.2 These outbreaks stimulated substantial investment in administrative, personal and engineering infection control measures in many hospitals in high-income countries. Implementation of a full hierarchy of these measures lead to successful reduction in transmission,3–6 but because multiple measures were implemented simultaneously, the impact of individual measures could not be established. Given their high cost, the efficacy and cost-effectiveness of these measures is of great interest. In low- and middle-income countries (LMICs), the risk of TB among HCWs has received less attention and remains less well defined. Fewer studies have documented prevalence or incidence of TB infection and/

Previous articles in this series Editorial: Chan-Yeung M, Becklake M. Occupational lung disease: under-recognised, underestimated and poorly managed, even today. Int J Tuberc Lung Dis 2007; 11 (2): 119. No. 1: Jeebhay M F, Quirce S. Occupational asthma in the developing and industrialized world: a review. Int J Tuberc Lung Dis 2007; 11 (2): 122–133. No. 2: Blanc P D, Torén K. Occupation in chronic obstructive pulmonary disease and chronic bronchitis: an update. Int J Tuberc Lung Dis 2007; 11 (3): 251–257. No. 3: Becklake M R, Bagatin E, Neder J A. Asbestos-related diseases of the lungs and pleura: uses, trends and management over the last century. Int J Tuberc Lung Dis 2007; 11 (4): 356–369. No. 4: Rees D, Murray J. Silica, silicosis and tuberculosis. Int J Tuberc Lung Dis 2007: 11(5): 474–484.

Correspondence to: Dr Dick Menzies, Respiratory Epidemiology and Clinical Research Unit, Montreal Chest Institute, 3650 St-Urbain, Room K1 24, Montreal, QC H2X 2P4, Canada. Tel: (1) 514 934 1934 ext: 32128. Fax: (1) 514 843 2083. e-mail: [email protected] [A version in French of this article is available from the Editorial Office in Paris and from the Union website www.iuatld.org]

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The International Journal of Tuberculosis and Lung Disease

or disease—all of these have been published since 1990. Although the International Union Against Tuberculosis and Lung Disease and the World Health Organization (WHO) issued recommendations for infection control within health facilities,7 the limited resources available preclude the implementation of more expensive controls, such as respirators or engineering controls. There is thus considerable interest in finding simple yet effective measures to prevent nosocomial transmission of TB in these settings. We have reviewed studies of occupational TB in HCWs. We sought to compare the prevalence and incidence of TB infection and disease plus associated risk factors in LMICs and HICs. We also wished to assess the impact of different TB infection control measures in these different settings.

METHODS Search strategy We searched PubMed from 1950 to December 2005. Our search strategy included the terms ‘tuberculosis’, ‘health personnel, health care workers’, ‘nosocomial infection control’, ‘disease transmission’, ‘occupation exposure’ and ‘nosocomial tuberculosis’. We handsearched the indices of the International Journal of Tuberculosis and Lung Disease, Tuberculosis and Tubercle & Lung Disease for relevant articles not captured by the electronic searches. We identified additional studies by searching reference lists of primary studies, review articles and text book chapters. Study selection Our search strategy aimed to identify all the available studies published in the English language that reported data on the incidence and prevalence of latent TB infection (LTBI) and TB disease among HCWs. This included cross-sectional tuberculin surveys, cohort studies that measured rates of tuberculin conversion, and studies measuring the incidence of TB disease among HCWs. We also examined those studies that documented the effect of infection control strategies on nosocomial transmission. We stratified the studies into two groups: those conducted in countries classified by the World Bank as low- or middle-income, and countries classified as high-income.8 For low- and middle-income countries, we selected all articles identified. For high-income countries, we only selected articles published after 1990, as this topic was carefully reviewed in 1994–95.1,2 We excluded case reports or descriptions of nosocomial outbreaks, as well as conference abstracts. We also excluded studies that utilised questionnaire responses to ascertain prevalence or incidence of latent or active TB. Data synthesis Data on the estimated incidence of all forms of TB disease in the general population, if not provided by the

authors of the individual studies, were obtained from the WHO Global TB database.9 These were compared with the corresponding estimates in HCWs to estimate attributable risk.

RESULTS Prevalence of LTBI As shown in Table 1, all studies relating to nosocomial transmission of TB to HCWs working in LMICs have been published since 1990.10–21 The median prevalence of LTBI was 63% (range 33–79% across studies). Of the 12 studies, seven reported prevalence estimates of 60%, and all but one study reported prevalence estimates in excess of 40%. Increasing age and more years of work in health care (i.e., longer cumulative exposure) were associated with higher prevalence of LTBI in most studies. Also, working in medical wards, participation in procedures such as sputum collection and autopsies and history of contact with TB patients were independent occupational risk factors for LTBI in several studies. In HICs (Table 2), relatively few LTBI prevalence surveys have been published since 1990. Findings were consistent with earlier surveys in that the median prevalence of positive tuberculin skin tests (TSTs) was 24%, with a highly variable range from 4% to 46%.22–29 Five of eight studies reported prevalence estimates of 20%. Positive TSTs were consistently associated with several non-occupational factors—notably older age, foreign birth and bacille Calmette-Guérin (BCG) vaccination. In two studies, non-occupational TB contact was significantly associated with prevalent TST reactions.22,26 Occupational risk factors included work in internal22,23 or respiratory medicine,28 more years of work in health care,26,27,29 and more direct indicators of TB exposure, including TB admissions26 or the percentage of patients with TB or HIV cared for.27 These surveys suggest that occupational risk remains above that of the general population. The median prevalence estimates in LMICs were nearly three times higher than those reported in HICs. A limitation of these cross-sectional tuberculin surveys is that recent TB infection cannot be distinguished from longstanding infection. Incidence of TB infection As seen in Table 3, only seven studies, all published after 2000, reported the annual risk of TB infection (ARTI) in LMICs.16,17,20,21,30–32 The median ARTI estimate was 5.3%, ranging from 0.5% to 14.3%. Incidence estimates were lower in studies that recruited young medical and nursing students. After accounting for the incidence of TB infection in the population (community ARTI), the risk attributable to occupational exposure ranged from 0% to 11.3%, with a median of 5.8%. Five of the seven studies reported attributable risks greater than 3%. In general, the

Table 1

Prevalence of LTBI in HCWs in low- and middle-income countries

Country, TB incidence/100 000

Author, year, reference

TST type

TST 10 mm/tested n/N (%)

HCWs with BCG %

Significant risk factors for positive TST after multivariate analysis Non-occupational

Molina-Gamboa, 199410 Do, 199911

Mexico, 50 Thailand, 142

5 TU PPDS* 5 TU PPDS

123/175 (70) 623/911 (68)

80 77

N/A Male sex BCG

Kassim, 200012

Cote d’Ivoire, 268

5 TU PPDS

405/512 (79)

83

Orrett, 200013 Alonso-Echanove, 200114

Trinidad, 11† Peru, 250

5 TU PPDS* 2 TU RT23

81/182 (44) 170/270 (63)

4 —

Higher educational level Older age N/A

Garcia, 200115

Mexico, 36‡

2 TU RT23*

280/823 (34)

84

Older age BCG

Bonifacio, 200216 Yanai, 200317

Peru, 211 Thailand, 142

5 TU 5 TU PPDS

58/97 (60) 764/1202 (63)

— 82

Keskiner, 200418 Kayanja, 200519

Turkey, 31 Uganda, 403

5 TU PPDS* 2 TU RT23

355/491 (72) 225/396 (57)

93 66

N/A Older age Male sex BCG scar BCG Older age

Pai, 200520 Roth, 200521

India, 168 Brazil, 62

1 TU RT23 5 TU PPDS

298/720 (41) 2181/4419 (49)

71 67

Older age Older age Male sex BCG

Occupational More years of work Physicians and nurses Maintenance personnel More years of work Work location More years of work More years of work Work in medical ward History of contact Collected sputum Use of common staff areas (laboratory) Autopsies Emergency/radiology Physicians and nurses More years of work

Occupation type Internal medicine Surgery/obstetrics More years of work More years of work Nursing Patient care

Data from these tables were adapted from: Joshi R, Reingold A L, Menzies D, Pai M. Tuberculosis among health-care workers in low- and middle-income countries: a systematic review. PLoS Med 2006; 3: 2376–2391. * Four studies measured TST at 72 h. † Incidence of all forms of TB in Trinidad, as reported in the study, is 270/100 000. ‡ Study conducted in Chihuahua, Mexico. The estimated incidence of all forms of TB in the city was 13.5/100 000 in the same year. LTBI latent TB infection; HCW health care worker; TB tuberculosis; TST tuberculin skin test; BCG bacille Calmette Guérin; TU tuberculin unit; PPDS purified protein derivative skin test; N/A not available or not stated in the paper.

Table 2

Prevalence of LTBI in HCWs in high-income countries

Author, year, reference Dooley,

199222

Fraser, 199423

Bailey, 199524

Country, TB incidence/ Workers, facilities 100 000

TST type

TST 10/tested N (%)

HCWs with BCG %

All HCWs, 1 hospital Physicians, 1 hospital

USA, 10

5 TU PPDS

218/880 (25)

5

USA, 11

5 TU PPDS

86/351 (25)

12

All HCWs, 1 hospital

USA, 11

5 TU PPDS

684/6070 (11)

N/A

5 TU PPDS

19/501 (4)

0

5 TU PPDS

1365/4651 (29)

31

Manusov, 199625 Medical students, USA, 10 1 university Menzies, 199826 All HCWs Canada, 8 17 hospitals

Zahnow, 199827

All HCWs, 17 HIV units

USA, 11

5 TU PPDS

248/1014 (24)

8

Plitt, 200128

Physicians, city-wide

Canada, 10

5 TU PPDS

257/560 (46)

44

Stuart, 200129

All HCW, 14 hospitals Non HCW

Australia, 6

10 TU PPDS

785/4070 (19)

89

589/4298 (14)

75

Significant risk factors for positive TST after multivariate analysis Non-occupational Older age Community TB contact Older age Foreign birth BCG Older age Ethnic origin Lower SES N/A Older age Foreign birth BCG Household TB contact Older age Foreign birth BCG vaccination

Older age Foreign birth BCG Older age Foreign birth BCG

Occupational Nurses—HIV ward Internal medicine Internal medicine Anesthesia NOT with patient contact N/A Clinical work More years of work More TB admissions More years of work Occupation type Years in HIV care % patients with HIV % patients with TB Cough-inducing procedures Respiratory medical specialty Foreign practice Health care work Years of hospital work Nursing

LTBI latent TB infection; HCW health care worker; TB tuberculosis; TST tuberculin skin test; BCG bacille Calmette Guérin; TU tuberculin unit; PPDS purified protein derivative skin test; HIV human immunodeficiency virus; N/A not available or not stated in the paper; SES socio-economic status.

Brazil, 62 Roth, 200521

Data from these tables were adapted from: Joshi R, Reingold A L, Menzies D, Pai M. Tuberculosis among health-care workers in low- and middle-income countries: a systematic review. PLoS Med 2006; 3: 2376–2391. * Per 100 000 per year. All figures represent WHO estimate for incidence of all forms of TB in the country. † Estimated ARTI in Peru from incidence of smear-positive TB using Styblo equation.33 ‡ National estimates for Brazil.34 § Estimated ARTI for Thailand in 1997.35 ¶ This Indian study reported a higher ARTI estimate of 5% when a whole-blood interferon-gamma assay was used to detect conversions. If that estimate is used, the risk attributable to nosocomial exposure would be 3.5%. # National estimates for India.36 ** Study conducted in four hospitals. LTBI latent TB infection; HCW health care worker; TB tuberculosis; TST tuberculin skin test; ARTI annual risk of TB infection; CI confidence interval; TU tuberculin unit; py person-year; NR not reported; WHO World Health Organization.

8.2 0.5‡ 8.7 (7.2–10.4) Two of four hospitals had administrative, personnel 105/1209 and engineering control 960**

Brazil, 62 India, 168 Maciel, 200532 Pai, 200520

5 TU, 2-step 10 mm

4.8 2.6 0.5‡ 1.5# 5.3 (1.4–13) 4.1 (1.5–8.7)¶ 8/76 6/147 Isolation N95 masks, surgical masks used None NR NR

270 356 NR 2 TU, 2-step 10 mm 5 TU, 2-step 10 mm 5 TU, 2-step 10 mm

Medical students, 12 months All HCWs, 331.6 py Medical, nursing students, 48 months Nursing students, 2 years Medical, nursing students, 18 months All HCWs, 6–12 months Brazil, 62 Thailand, 142 Brazil, 62

2 TU, 2-step 10 mm 1 TU, 1-step 10 mm

3.4 5.8 0 0.5‡ 1.4§ 0.5‡ 3.9 (1.1–12.1) 7.2 (1.9–12.5) 0.5 (0.4–0.8) 16/414 24/331.6 py 1/46

3† 14.3 (4.8–30.2) 5/35

Silva, 200230 Yanai, 200317 Levy, 200531

Infection control measures

Only 7.4% self-reported consistent use of N95 mask Respiratory isolation and respirator masks used Respiratory isolation facilities. 49% used N95 masks NR 1220 5 TU, 1-step 10 mm Residents interns, 12 months Peru, 211 Bonifacio,

200216

ARTI in HCWs % (95%CI) Converted/ re-tested n/N TST type TB testing protocol, admissions conversion definition per year Type of HCW, length of follow-up Country, TB incidence/ 100 000* Author, year, reference

Exposure to TB in hospital

Incidence of LTBI in HCWs in low- and middle-income countries Table 3

11.3


ARTI ARTI attributable in the to nosocomial population transmission % %

596

incidence of LTBI correlated well with indices of higher TB exposure in the hospital (e.g., more TB admissions per year, absence of TB infection control measures). Higher level of clinical training, BCG vaccination after baseline TST, nursing occupation and recent exposure to TB were independent risk factors for TST conversion in these studies. In HICs, all but two of the 15 studies were performed in the United States, and almost all were conducted between 1986 and 1996 (Table 4).24,27,37–49 In most studies, the ARTI as estimated from rates of tuberculin conversion was substantially higher than the estimated ARTI in the general population of 0.1%– 0.2%, estimated from incidence in the same country9 using the Styblo equation.33 However, despite the similarities of time and location, the estimated median ARTI was 1% (range 0.2%38 to 12%42). Some of this variation may have reflected higher rates in certain communities, particularly for single hospital studies, which were mostly located within large cities where TB rates are much higher than national TB rates.50,51 Some differences in findings reflect differences in testing protocols, particularly whether initial two-step TSTs were done, and some reflected different definitions of tuberculin conversion. However, these problems should have had relatively modest effects on estimates of tuberculin conversion. One important determinant of risk of infection is the likelihood of exposure. Rates were thus much lower in hospitals with very few TB admissions,26 or, in one study in a paediatric hospital,44 reflecting the low infectiousness of paediatric TB patients. The highest rates of tuberculin conversion were reported in three studies where there were substantial numbers of TB cases (annual admissions ranging from 56 to 269) and minimal infection control measures.40,41,49 In these hospitals, the estimated ARTI ranged from 2.1% to 7.2%. On the other hand, in hospitals with similar inadequate infection control measures but only 15– 22 TB admissions per year, the ARTI was less than 1%.24,37,47 In hospitals with moderate TB admissions but extensive infection control measures, ARTI rates were very low.38 In one hospital with a high number of admissions and excellent TB control measures, the ARTI among house staff was 1.6%,42 but was only 0.4% among all other HCWs during the same years.48 In summary, the risk of TB infection is highly variable (with higher ARTI estimates in LMICs), but is determined largely by the likelihood of TB exposure, as estimated by the annual number of TB admissions and the presence or absence of adequate TB infection control measures. Risk is highest when there is a high number of cases with poor infection control, intermediate when there are relatively few cases with inadequate controls or a high number of cases but good infection control, and low when there are few TB patients, or paediatric TB patients, or a moderate number of cases but adequate infection control measures.

All HCWs, 1 hospital 1990–1992





All HCWs, 17 HIV centres 1992–1995

All HCWs, 17 hospitals 1995–1996

Physicians, 1 hospital 1992–1998

USA 11

USA 10

Spain 33

USA 10

USA 10

USA 22‡

USA 9

USA 10

USA 9

USA 9

Canada 8

USA 8

USA 8

USA 8

Adal, 199438

Bailey, 199524

Rullán, 199639

Bourdreau, 199740

Louther, 199741

Behrman, 199842

Blumberg, 199843

Christie, 199844

Lobue, 199845

Zahnow, 199827

Menzies, 200046

Warren, 200147

Larsen, 200248

Miller, 200249

5 TU PPDS 1-step, annual T1 10, T2 10

5 TU PPDS 2-step, Q 6 months T1 10, T2 10

5 TU PPDS 1-step, annual T1 10, T2 10 and ↑ 10 mm



5 TU PPDS 1-step, annual T2 10 and ↑ 6 mm






2 TU RT23 1-step T2 10 and ↑ 6 mm




TST type, baseline, frequency, conversion definition*

200–260

200

21

1–37

N/A

25–30

5

200

19–22

56–118

269

35

22

11–13

15–20

TB admissions per year

Minimal

Full CDC hierarchy

N/A

Overall Poorly ventilated Well ventilated Low risk

Variable

Full CDC hierarchy

N/A

Full CDC hierarchy

Minimal

Minimal

Minimal

Minimal

N/A

Full administrative, and engineering

Minimal

Infection control measures used

Exposure to TB in hospital

Exposed 138/2362 Unexposed 18/886

69/5773

21/731

238/1289 153/471 76/651 9/73

22/766

59/9905

62/28 916 (over 9 years)

Total: 52/2144 US-born: 36/1928

ED: 6/50 General: 51/2514

65/898

Exposed: 36/249† Unexposed: 5/355

24/92

29/3106

23/11 188

43/6452

Converted/ re-tested n/N

2.1

0.38

1§

1.2 2.5 0.5 0.4

1.8

0.6

0.22

1.6 1.2

12 2

7.2

3.6

10.4

0.9

0.2

0.7

ARTI in HCWs %

0.7

0.1

0.1

0.2

0.1

0.2

0.1

0.1

0.2 0.2

0.1

0.35

0.3

0.1

0.1

0.1

ARTI in the population %

1.4

0.28¶

1.7

11.8 1.8

7.1

3.25

10.1

0.8

0.1

0.6

ARTI attributable to nosocomial transmission %

* T1 10; T2 10, ↑ 6 mm, Q 6 months conversion defined as first TST 100 mm with second TST 10 mm AND an increase of 6 mm. † Self-reading of negative tests. ‡ Incidence taken from city where hospital located (Philadelphia). § () TST associated with foreign birth, BCG. ¶ () TST associated with older age, BCG, poorer neighbourhood. LTBI latent TB infection; TB tuberculosis; HCW health care worker; TST tuberculin skin test; ARTI annual risk of tuberculosis infection; TU tuberculin unit; PPDS purified protein derivative skin test; N/A not available or not stated in the paper; ED emergency department; Q each; CDC Centers for Disease Control and Prevention; BCG bacille Calmette Guérin.




All HCWs, paediatric hospital 1986–1994

Residents, 1 hospital 1992–1997



USA 9

Ramirez, 199237

Type of HCW, institutions, years of study

Author, year, reference

Incidence of LTBI in health care workers in high-income countries

Country, TB incidence/ 100 000

Table 4

TB in health care workers

597

Serbia

Across 40 hospitals, retrospective cohort

Malawi

Tertiary care hospital, prospective and retrospective cohorts

Tertiary care facility, retrospective cohort

Tertiary care hospital, prospective cohort

India

Russia

Turkey

Thailand

South Africa Across 8 hospitals in province, retrospective cohort

Rao, 200466

Dimitrova, 200567

Hosoglu, 200568

Jiamrajarasangi, 200569

Naidoo, 200670

49 392/NR

3 959/NR

734/NR

64 855/2445

NR

7 312/NR

6 016/1174

571/3607

6 156/NR

2 979/NR

90/4862

3 359/NR

14 730/806

2 300/NR

267/600

3 042/14 532

725/760

—

310/1112

170/610

—

—

—

2652

—

—

512

16

—

—

2

—

1827

—

44

21

95

—

28

28

583/49 392

78/41 462

22/11 010

474/583 695

13/1032

205/73 120

125/60 163

33/571

59/80 028

96/2979

5/90‡‡

31/33 590

67/73 650

36/9200

9/3204

108/3042

22/4350

2/726

12/620

18/2560

HCWs HCWs exposed/ with TB TB patients HCWs/100 disease/py seeking care TB patients exposure

1180

188

199.9

81.2

1260.4

280.4

208

5780

69

3222

5556

96

91

391††

287

3550

506

275

1935

703

(1996)

718 ††† (2004)

142*** (2000)

40** (1995)

103## (2002)

168 (2002)

104¶¶ (2003)

168 (2000)

419§ (2001)

41§§ (1998)

389§ (1996)

277‡‡ (1998)

29** (2001)

66 (1998)

111†† (1998)

59** (1998)

389§

379# (1997)

379¶ (1997)

389§ (1996)

7‡ (1990)

TB disease TB disease incidence incidence among in the country† (year) HCWs*

1.6 (1.5–1.8)

1.32 (1.0–1.7)

5.0 (2.8–8.6)

0.7 (0.6–0.9)

7.5 (3.9–13.2)

2.69 (2.1–3.4)

1.2 (1.0–1.6)

13.8 (9.4–19.6)

1.8 (1.2–2.7)

8.3 (6.5–10.3)

20.0 (6.5–47.3)

3.2 (1.8–5.5)

1.4 (1.0–2.0)

3.5 (2.4–5.1)

4.8 (2.1–9.7)

9.1 (7.3–11.3)

1.33 (0.8–2.0)

0.7 (0.08–2.6)

4.9 (2.5–8.8)

9.5 (5.3–16.1)

462

46

160

32

1092

176.4

40

5361

28

2833

5279

67

25

280

228

3161

127

104

1546

629

Incidence Risk of TB disease rate ratio attributable to (relative risk) nosocomial (95%CI) transmission

Data from these tables were adapted from: Joshi R, Reingold A L, Menzies D, Pai M. Tuberculosis among health-care workers in low- and middle-income countries: a systematic review. PLoS Med 2006; 3: 2376–2391. * Per 100 000/year. † Per 100 000/year. All figures represent WHO estimate for incidence of all forms of TB in the country. ‡ Regional TB incidence rate: 48/100 000 (women aged 20–49 years). § The authors used case notification rates in the country for comparison in their study. ¶ Regional TB incidence rate: 286/100 000 in 1997. # Regional TB incidence rate: 1543/100 000 in 1997 in 15–43 year olds. ** The authors used average incidence rate over the entire study period for comparison. †† These figures represent sputum-positive pulmonary TB cases in both HCWs and the general population. ‡‡ HCW figures are for 1998 only. §§ Regional TB incidence rate: 36/100 000 in 1998. ¶¶ Regional TB incidence rate: 154/100 000 in 2003. ## Regional TB incidence rate: 74.9/100 000 in 2002. *** Regional TB incidence rate: 55.4/100 000 in 2000 (15–64 years). ††† Regional TB incidence rate: between 386 and 782 from 1999 to 2003. TB tuberculosis; HCW health care worker; py person-year; CI confidence interval; NR not reported; WHO World Health Organization.

All TB and general health facilities in Samara Oblast, retrospective cohort

All HCWs in the state, retrospective case control

Malaysia

Jelip, 200465

Tertiary care hospital, retrospective cohort

Central hospital, retrospective cohort

India

Gopinath,

Malawi

Kanyerere, 200363

2004 64

Turkey

Kilinc, 200262

Two secondary and two tertiary care hospitals each, retrospective cohort

TB referral centre, retrospective cohort

Ethiopia

Eyob, 200260

Harries,


Turkey

200261

All HCWs in the country, retrospective cohort

Estonia

Kruuner, 200158


Pulmonary facility, retrospective cohort

Across 40 hospitals, retrospective cohort

Cuhadaroglu, 200259

Alonso-Echanove, 200114 Peru

Malawi

Skodric, 200057

Harries,

South Africa Secondary care hospital, retrospective cohort

Wilkinson, 199855

199956

South Africa Four TB care hospitals, retrospective cohort

Balt, 199854

Central hospital, retrospective cohort

Malawi

Harries, 199753

Type of facility, study design

Nurses in two TB care and one tertiary care hospital, retrospective cohort

Croatia

Babus, 199752

Country

Incidence of TB disease (all forms) in HCWs in low- and middle-income countries

Author, year, Reference

Table 5

598 The International Journal of Tuberculosis and Lung Disease


Incidence of TB disease As seen in Table 5, 20 studies have reported on the incidence of TB disease among HCWs in LMICs.14,52–70 Two studies, one from Russia and another from South Africa, reported a lower TB disease incidence in HCWs than in the general population. In all the remaining studies, the annual risk of TB disease attributable to nosocomial exposure ranged from 25 to 5361 per 100 000 (median 228). Workers in facilities with fewer HCWs for every TB patient cared for had a higher incidence of TB disease. There was considerable variability in the risk of TB disease in different occupations. Radiology technicians, patient attendants, nurses, ward attendants, paramed-

Table 6

599

ics, clinical officers, laboratory personnel and physicians had a high incidence of TB disease, while the incidence was lowest in administrative staff. Workers in TB in-patient facilities, laboratories, general medicine wards and emergency rooms had a higher risk for TB disease compared to the general population. Workers in out-patient medical facilities had an intermediate risk, and workers in surgery, obstetrics and gynaecology, administration and operating theatres had lower risk of disease. Among HCWs in HICs, the variable estimates of risk of disease are more difficult to explain (Table 6).71–81 In contrast to the numerous studies of disease from LMICs, no study describing incidence of disease

Incidence of TB disease (all forms) in health care workers in high-income countries

Author, year, reference, country

Type of HCW, years of survey

Total occurrence of outcome

Method for measuring outcomes

CDC, 1995,71 USA

All HCWs, 1979–1990

15 TB deaths

Reported TB deaths

McKenna, 1996,72 USA

All HCWs, 1984–1985

321 TB cases

Reported TB cases, supplemental work history

Sepkowitz, 1995,73 USA

All HCWs, 1992–1994

20 TB cases

RFLP, all cases at 6 hospitals

Meredith, 1996,74 UK

All HCWs, 19881993

119 TB cases

Surveillance reported TB cases

Hill, 1997,75 UK

Hospital staff, 1992–1995

26 TB cases

Van Deutekom, 1997,76 The Netherlands Pleszewski, 1998,77 Canada

All HCWs, 1992–1995

8 TB cases

Reported TB cases, occupational health registry RFLP, TB registry

Nurses, GPs, residents, 1991–1996

6 TB cases 22 TB cases 1 TB case

Reported data

Raitio, 2003,78 Finland

All HCWs, 1970–2000

447 TB cases

Reported data

Bang, 2005,79 USA

All HCWs, 1990–1999

227 TB deaths

Driver, 2005,80 USA

All HCWs, 1994–1999

458 TB cases

Reported mortality data Reported data

Diel, 2005,81 Germany

All HCWs 1997–2002

10 TB cases

RFLP

Findings Proportional mortality ratio 3.5, white male service workers 3.5, nursing aides and orderlies Incidence rate ratio All HCWs to general population, 1.0 All HCWs to other workers, 0.85 Respiratory technicians to general population, 2.5 Nurses to general population, 1.2 Relative risk of clustered vs. non clustered cases for health care workers 2.7 Risk of TB in health care workers 2.7 times that of general population HCW risk relative to other professionals, 11.8/3.3 2.4 (aRR) Physicians risk relative to other professions 13.0 Incidence rate ratio Nurses to general population 2.4 Physicians to general population 1.4* Health care workers, aRR for clustering 0.11 (reduced occupational risk) Incidence rate ratio Nurses 0.4 GPs 0.8 Residents 3.4 Incidence rate ratio Younger HCWs (age 20–39) vs. general population 1.0 for nurses, physicians and nursing assistants 1.0 for all occupations aged 40–59 except for physicians in most recent years Proportional mortality ratio, hospital workers vs. general population 1.18 No rates given; TB in HCWs accounted for increasing proportion of all cases in New York state over period of study Relative risk for clustered cases compared to non-clustered cases in health care workers 7.0 Nosocomial TB risk seven times that of community risk

* In this study the rate ratio given for white nurses to white general population; for physicians all cases in foreign-born so rate ratio of physicians to foreign born general population. TB tuberculosis; HCW health care worker; RFLP restriction fragment length polymorphism; aRR adjusted rate ratio; GP general practitioner; WHO World Health Organization.

Data from these tables were adapted from: Joshi R, Reingold A L, Menzies D, Pai M. Tuberculosis among health-care workers in low- and middle-income countries: a systematic review. PLoS Med 2006; 3: 2376–2391. * Per 100 000 per year. † Average value computed. TB tuberculosis; OPD out-patient department; CXR chest X-ray; CO clinical officer; PA patient attendant; WA ward attendant; NS not significant; HCW health care worker; HEPA high efficiency particulate air; UV ultraviolet; LTBI latent tuberculosis infection; pm person-months.

Difference in LTBI rates, statistically significant Incidence of LTBI in hospitals with prevention measures in place (1998–1999) 8/1000 pm† Incidence of LTBI in hospitals without prevention measures (1998–1999) 16/1000 pm† 1 Negative pressure rooms (one hospital) 2 Class II biosafety cabinets in laboratory areas 1 Rapid diagnosis and treatment of TB patients 2 Isolation of TB patients in private rooms Roth 2005,21 Brazil, two hospitals with and two without preventive measures (1998)

1 N 95 mask use by HCWs 2 HEPA filter in laboratory areas

Increase in TB disease, statistically NS Decrease in LTBI rates, statistically significant Incidence of TB disease after prevention used* (1999) All HCWs 252.68 Incidence of LTBI per year after prevention (1999) 2.2% (0–5.1) Incidence of TB disease before prevention used* (1995–1997) All HCWs 179.21 Incidence of LTBI per year before prevention (1995–1997) 9.3% (3.3–15.3) 1 TB isolation room in wards 2 Maximising ventilation in wards 3 Class II safety cabinets in laboratory 4 UV germicidal irradiation system in laboratory 1 Early suspicion of TB 2 Early sputum collection and reporting 3 Early initiation of TB treatment 4 Isolation of patients with TB 5 One-stop OPD TB service Yanai 2003,17 Thailand, provincial referral hospital (1997–1998)

1 N 95 mask use by HCWs 2 HEPA filter in laboratory areas

Incidence of TB disease declined after preventive measures used, statistically NS Incidence of TB disease after prevention* (1999) CO 3603 PA 4348 WA 3954 TB officer 1785 Nurses 2060 Overall 3222 Incidence of TB disease before prevention* (1996) CO 7407 PA 5014 WA 3543 TB officer 3030 Nurses 2835 Overall 3707 1 Increased natural ventilated 2 Windows left open most of the time 1 Proper cough hygiene 2 Mask worn by TB patients when undergoing surgical procedures 1 Priority to patients with chronic cough in OPD 2 Rapid sputum collection, transport and reporting 3 Visitors kept to a minimum 4 CXR at quiet times in the day 5 TB patients spend more daytime outdoors when possible

Engineering Personal Administrative

Harries, Malawi, 40 TB care facilities (1998) 2002,61

Epidemiological measure in presence of preventive measure Epidemiological measure in absence of preventive measure Infection control strategies used

Author, year, reference, country, facilities (year of intervention)

Effectiveness of infection control measures As shown in Table 7, only three studies from LMICs evaluated the impact of infection control strategies on risk of TB infection or disease.17,21,61 It is therefore difficult to make any inferences regarding the effectiveness of control measures. One study determined that administrative measures had little impact on the development of TB disease, but after only one year— a relatively short interval to detect changes.61 Two studies detected significant reduction of TB infection within a year following introduction of multiple infection control measures.17,21 In one of these studies, the incidence of active disease in HCWs actually increased following the introduction of control measures, but this could have been due to concomitant increasing HIV prevalence in HCWs, which was not measured.17 The other study compared TB incidence rates in hospitals with different infection control policies, and other differences between the hospitals could have confounded the estimates.21 Overall, the limited

Impact of administrative, personal and engineering control measures on nosocomial transmission of TB in low- and middle-income countries

among workers in an institution or group of institutions in an HIC has been published since 1990. The majority of studies utilised reported TB case registries to describe mortality71 or morbidity.72,74,75,77,78,80 In two US studies, slight excess mortality was found among hospital workers79 or certain groups of less skilled HCWs.71 Risk among health care professionals was 2–3 times higher than other professionals in the United Kingdom,74,75 but was similar to overall rates in the general population in the US.72,77 Comparison with general population rates leads to an underestimate of the impact of occupational exposure. This is because TB should be much lower among health professionals than the general population, due to the healthy worker effect (actually demonstrated in one of the negative studies),72 higher socio-economic status (SES, as demonstrated in the UK studies) and younger age of HCWs. In one study, stratified by age group, the risk of TB among younger HCWs was significantly higher than in the general population of the same age.78 Three studies have utilised restriction fragment length polymorphism (RFLP) analysis to detect occupationally acquired TB. In two, HCWs were significantly more likely to belong to clusters of recently transmitted cases. Assuming that the non-clustered case rate represented the expected, or general population incidence, then these two studies could be interpreted to indicate significant risk from nosocomial transmission.73,81 On the other hand, in a study from the Netherlands, HCWs were significantly less likely to have clustered TB cases.76 In summary, the best designed studies indicate that HCWs have a 2–3 times higher risk of morbidity than expected when matched for employment and SES. There are too few TB deaths among HCWs to draw any conclusions about risk. Findings from DNA fingerprinting studies are contradictory.

Impact


Table 7

600

1-step T1 10, T2 10 mm 1-step T1 10, T2 10 mm

1-step T1 10, T2 10 mm

All HCWs, 3 hospitals, 1990–1992

Bourdreau, 1997,40 USA All HCWs, 1 hospital, 1989–1992

All HCWs, 1 hospital, 1992–1996

Jarvis, 1995,84 USA

Behrman, 1998,42 USA

Blumberg, 1998,43 USA Residents, 1 hospital, 1992–1997

TST Q 6 months Sub-micron masks None

↑ respiratory isolation

Isolation procedures TB infection control nurse ↑ isolation

↑ respiratory isolation ↑ patient adherence ↓ patient movement ↑ patients masks, pentamidine D/C ↑ respiratory isolation ↓ patient movement Worker education ↑ speed for AFB Better drug therapy ↑ respiratory isolation ↑ worker education Pentamidine changed None stated

Respiratory masks

↑ respiratory isolation

All HCWs, 1 hospital, 1991–1994

Sub-micron mask use

Better masks

Better masks TST of HCWs

None stated

Better masks

Minimal (some use of new masks)

Ventilation 4 criteria†

↑ ventilation

4 respiratory isolation rooms ↑ general ventilation Droplet shields Laminar airflow 50 respiratory isolation rooms

Sputum induction booth UV lights

None

None

Window exhaust fans Upper air UV lights Negative pressure rooms in EROPD Upper air UV lights Window exhaust fans

Window exhaust fans

Auto-door-closers Negative pressure isolation rooms

Engineering

Outcomes

11/90 (5.4%)

30/145 (21%)

26/840 (3.1%)

7/25 (28%)

Pre-interventions

ARI in HCWs

ARI in HCWs

ARI in HCWs

ARI in HCWs

ARI in HCWs

TST conversion

New MDR patients

No, 1.9% No, 0.94%

7.2%

6%

ED (n 50), 12% Rest (n 3000), 2%

6.9%

With changes, 14.6% No changes, 9%

26/90

Conv/tested (ARTI) 118/3579 (3.3%)

Conv/tested (ARTI)

Conv/tested (ARTI)

Conv/tested (ARTI)

Conv/tested (ARTI)

Outcome measure

Yes, 0.6% Yes, 0.98%

4.8%

1.1%

0% 1.2%

1.9%

2.9% 18%

0/44

185/17 618 (1.1%)

1/90 (0.7%)

51/1007 (5.1%)

22/727 (3.0%)

3/17 (18%)

Post-interventions

* T110; T2 10, ↑ 6 mm conversion defined as first TST 10 mm with second TST 10 mm AND an increase of 6 mm. † 1) patients in separate isolation rooms; 2) 6 ACPH; 3) negative pressure or inward airflow; 4) automatic door closing. TB tuberculosis; TST tuberculin skin test; HCW health care worker; AFB acid-fast bacilli; Q every; conv converted; ARTI annual risk of tuberculosis infection; UV ultraviolet; ER emergency room; OPD out-patient department; MDR multidrug-resistant; N/A not available or not stated in the paper.

Fridkin, 1995,85 USA

Louther, 1997,41 USA

Moro, 2000,83 Italy

Dust-mist masks

Moulded surgical masks

TST Q 4 months Sub-micron masks Dust-mist masks

Personal

Infection control strategies used Administrative ↑ respiratory isolation ↑ speed for AFB Sputum induction in respiratory isolation rooms ↑ respiratory isolation ↑ treatment ↑ speed for AFB ↑ respiratory isolation

1-step T1 10, T2 10 mm and ↑ 10 mm All HCWs, N/A T1 10, N/A 359 hospitals, 1992–1993 T2 10 mm

1-step T1 10, T2 10 mm

All HCWs, 1 hospital, 1991–1992 No HCWs, 1 hospital, 1994

Fella, 1995,5 USA

Blumberg, 1995,6 USA

1-step T1 10, T2 10 mm 1-step T1 10, T2 10 mm 1-step T1 10, T2 10 mm and ↑ 6 mm 1-step T1 10, T2 10 mm Not done

All HCWs, 1 hospital, 1991

Maloney, 1995,4 USA

1-step T1 10, T2 10 mm TST 10 mm and ↑ 6mm

TST: baseline, conversion definition*

All HCWs, 1 hospital, 1991–1993 Bangsberg, 1997,82 USA Residents, 1 hospital, 1992

All HCWs, 1 hospital, 1991

USA

Wenger,

1995,3

Workers, facilities, year of intervention

Impact of administrative, personal and engineering control measures on nosocomial transmission of TB in high-income countries

Author, year, reference, country

Table 8

602


available evidence suggests that reduction in the risk of TB infection is possible in low-income settings with simple administrative controls, but this needs to be evaluated in larger, better-controlled studies. In all studies conducted in HICs (Table 8),3–6,40–43,82–85 indicators of nosocomial transmission rapidly declined following the application of a full hierarchy of recommended infection control measures. Identification of the key interventions responsible for the decrease in transmission is difficult, because many measures were introduced simultaneously in most facilities. However, in one hospital, implementation only of administrative controls resulted in the complete elimination of MDR-TB transmission.83 In two studies, implementation of administrative controls resulted in reduced transmission and subsequent implementation of engineering controls led to further decreases.6,84 Two studies demonstrated significant reduction in transmission with improved ventilation.42,85 In one of these, the use of more efficient respirators did not reduce risk any further.85 In fact, there is no evidence that improved masks reduce transmission, making their use particularly controversial due to their high cost and need for fit testing. In summary, administrative controls appear to be most important in preventing nosocomial transmission. These controls are the cheapest and easiest to implement. However, in several studies, engineering controls also contributed to reductions in nosocomial transmission.

DISCUSSION The studies reviewed consistently indicate that HCWs in LMICs have a substantially increased risk of occupationally acquired TB infection and related disease. HCWs in HICs have more heterogeneous risk, reflecting more heterogeneous exposures. In facilities caring for significant numbers of TB cases each year, the risk is increased, particularly if infection control measures are inadequate. In HICs, implementation of all components of TB infection control programmes resulted in reduction of risk of TB infection and disease. Limited evidence based on uncontrolled observations suggests that administrative controls are the most important component of these programmes. Strengths of this review include the inclusion of all papers on this topic published in English since 1990 from HICs, and since 1960 from LMICs. Studies were included that measured objective outcomes, such as TSTs or active disease, and not those relying on questionnaires. Only non-outbreak reports were used, because outbreaks are inherently unusual situations in which estimates of risk and factors contributing to nosocomial transmission may be very aberrant. Findings in LMICs and HICs could be compared because the same methodologies were used in studies of prevalence and incidence of LTBI.

On the other hand, this review has a number of important limitations. The prevalence and incidence of LTBI was estimated from the TST, an imperfect test. Prevalent tuberculin reactions were thus associated with BCG vaccination, an important cause of falsepositive tests, or with older age and lower SES, markers of remote non-occupational TB exposure. The incidence of LTBI could have been over-estimated due to the boosting phenomenon, particularly if baseline testing only involved a single TST. In the studies that accounted for this problem in the analysis or design, findings were similar to studies that did not. Studies of disease occurrence among HCWs in LMICs were reported by single institutions. No single institution in HICs had enough TB cases among their workers to analyse this. Therefore, in HICs, studies analysed reported cases in TB registries or used DNA fingerprinting. These methodological differences reduce the comparability of the estimates of relative risk; all that can be concluded is that these studies consistently demonstrate increased risk. Assessment of efficacy of control measures was limited. In LMICs, only administrative measures have been assessed. Compliance with these measures is obviously an important modifier of their effectiveness, and is difficult to assess. For example, ventilation levels can be precisely controlled and measured, but diagnostic suspicion for TB is difficult to control and even more difficult to measure. In HICs, assessment of the effect of individual infection control measures has been hindered by the simultaneous implementation of multiple infection control procedures in most institutions. In some studies, the temporal sequence of infection control implementation allowed identification of measures that were more effective than others. The most important implication of this review is that risk of TB continues to be high for HCWs in all regions of the world. Exposure is approximately correlated with number of TB cases at the facility, and modified by TB control measures. Risk can be reduced, although never completely eliminated, by the implementation of administrative and engineering controls. Interestingly, no study has identified benefit of use of personal respirators, with or without a fit testing programme.

CONCLUSIONS TB infection and disease continue to be important occupational hazards for HCWs in all countries. In lowand middle-income countries, where infection control measures are limited by lack of resources and exposure is frequent, risk can be very substantial. In highincome countries, risk can be high for HCWs in facilities caring for a significant number of TB patients, particularly if the infection control measures are ineffective.


References 1 Sepkowitz K. Tuberculosis and the health care worker: a historical perspective. Ann Intern Med 1994; 120: 71–79. 2 Menzies R I, Fanning A, Yuan L. Tuberculosis among health care workers. N Engl J Med 1995; 332: 92–98. 3 Wenger P N, Otten J, Breeden A, Orfas D, Beck-Sague C M, Jarvis W R. Control of nosocomial transmission of multidrugresistant Mycobacterium tuberculosis among health care workers and HIV-infected patients. Lancet 1995; 345: 235–240. 4 Maloney S A, Pearson M L, Gordon M T, Del Castillo R, Boyle J F, Jarvis W R. Efficacy of control measures in preventing nosocomial transmission of multidrug-resistant tuberculosis to patients and health care workers. Ann Intern Med 1995; 122: 90–95. 5 Fella P, Rivera P, Hale M, Squires K, Sepkowitz K. Dramatic decrease in tuberculin skin test conversion rate among employees at a hospital in New York City. Am J Infect Control 1995; 23: 352–356. 6 Blumberg H M, Watkins D L, Jeffrey P A-C, et al. Preventing the nosocomial transmission of tuberculosis. Ann Intern Med 1995; 122: 658–663. 7 International Union Against Tuberculosis and Lung Disease, World Health Organization. Control of tuberculosis transmission in health care settings. Tubercle Lung Dis 1994; 75: 94–95. 8 World Bank. Country indicators. Washington, DC, USA: World Bank. www.worldbank.org/data/countrydata/countrydata.html Accessed April 2004. 9 World Health Organization. WHO report 2005. Global tuberculosis control: surveillance, planning, financing. WHO/HTM/ TB/2005.349. Geneva, Switzerland: WHO, 2005. 10 Molina-Gamboa J, Fivera-Morales I, Ponce-de-Leon-Rosales S. Prevalence of tuberculin reactivity among healthcare workers from a Mexican hospital. Infect Control Hosp Epidemiol 1994; 15: 319–320. 11 Do A N, Limpakarnjarat K, Uthaivoravit W, et al. Increased risk of Mycobacterium tuberculosis infection related to the occupational exposures of health care workers in Chiang Rai, Thailand. Int J Tuberc Lung Dis 1999; 3: 377–381. 12 Kassim S, Zuber P, Wiktor S Z, et al. Tuberculin skin testing to assess the occupational risk of Mycobacterium tuberculosis infection among health care workers in Abidjan, Cote d’Ivoire. Int J Tuberc Lung Dis 2000; 4: 321–326. 13 Orrett F A. Prevalence of tuberculin skin test reactivity among health care workers at a teaching hospital in Trinidad. Clin Microbiol Infect 2000; 6: 45–48. 14 Alonso-Echanove J, Granich R M, Laszlo A, et al. Occupational transmission of Mycobacterium tuberculosis to health care workers in a university hospital in Lima, Peru. Clin Infect Dis 2001; 33: 589–596. 15 Garcia-Garcia M L, Jimenez-Corona A, Jimenez-Corona M E, et al. Factors associated with tuberculin reactivity in two general hospitals in Mexico. Infect Control Hosp Epidemiol 2001; 22: 88–93. 16 Bonifacio N, Saito M, Gilman R H, et al. High risk for tuberculosis in hospital physicians, Peru. Emerg Infect Dis 2002; 8: 747–748. 17 Yanai H, Limpakarnjanarat K, Uthaivoravit W, et al. Risk of Mycobacterium tuberculosis infection and disease among health care workers, Chiang Rai, Thailand. Int J Tuberc Lung Dis 2003; 7: 36–45. 18 Keskiner R, Ergonul O, Demiroglu Z, Eren S, Baykam N, Dokuzoguz B. Risk of tuberculous infection among health care workers in a tertiary-care hospital in Ankara, Turkey. Infect Control Hosp Epidemiol 2004; 25: 1067–1071. 19 Kayanja H K, Debanne S, King C, Whalen C C. Tuberculosis infection among health care workers in Kampala, Uganda. Int J Tuberc Lung Dis 2005; 9: 686–688. 20 Pai M, Gokhale K, Joshi R, et al. Mycobacterium tuberculosis infection in health care workers in rural India—comparison of

21

22

23

24

25 26

27

28

29

30

31

32

33

34

35 36

37

38

39

603

a whole-blood interferon gamma assay with tuberculin skin testing. JAMA 2005; 293: 2746–2750. Roth V R, Garrett D O, Laserson K F, et al. A multicenter evaluation of tuberculin skin test positivity and conversion among health care workers in Brazilian hospitals. Int J Tuberc Lung Dis 2005; 9: 1335–1342. Dooley S W, Villarino M E, Lawrence M, et al. Nosocomial transmission of tuberculosis in a hospital unit for HIV-infected patients. JAMA 1992; 267: 2632–2634. Fraser V J, Kilo C M, Bailey T C, Medoff G, Dunagan W C. Screening of physicians for tuberculosis. Infect Control Hosp Epidemiol 1994; 15: 95–100. Bailey T C, Fraser V J, Spitznagel E L, Dunagan W C. Risk factors for a positive tuberculin skin test among employees of an urban, midwestern teaching hospital. Ann Intern Med 1995; 122: 580–585. Manusov E G, Bradshaw R D, Fogarty J P. Tuberculosis screening in medical students. Fam Med 1996; 28: 645–649. Menzies D, Fanning A, Yuan L, FitzGerald J M, the Canadian Collaborative Group in Nosocomial Transmission of Tuberculosis. Tuberculosis in health care workers: a multicentre Canadian prevalence survey: preliminary results. Int J Tuberc Lung Dis 1998; 2 (Suppl 1): S98–S102. Zahnow K, Matts J P, Hillman D, et al. Rates of tuberculosis infection in health care workers providing services to HIVinfected populations. Terry Beirn Community Programs for Clinical Research on AIDS. Infect Control Hosp Epidemiol 1998; 19: 829–835. Plitt S S, Soskolne C L, Fanning E A, Newman S C. Prevalence and determinants of tuberculin reactivity among physicians in Edmonton, Canada: 1996–1997. Int J Epidemiol 2001; 30: 1022–1028. Stuart R L, Bennett N J, Forbes A B, Grayson M L. Assessing the risk of tuberculosis infection among health care workers: the Melbourne Mantoux Study. Melbourne Mantoux Study Group. Med J Aust 2001; 174: 569–573. Silva V M, Cunha A J, Kritski A L. Tuberculin skin test conversion among medical students at a teaching hospital in Rio de Janeiro, Brazil. Infect Control Hosp Epidemiol 2002; 23: 591– 594. Levy M Z, Medeiros E A, Shang N, et al. TST reversion in a BCG-revaccinated population of nursing and medical students, Sao Paulo, Brazil, 1997–2000. Int J Tuberc Lung Dis 2005; 9: 771–776. Maciel E L N, Viana M C, Zeitoune R C G, Ferreira I, Fregona G, Dietze R. Prevalence and incidence of Mycobacterium tuberculosis infection in nursing students in Vitoria, Espirito Santo. Rev Soc Bras Med Trop 2005; 38: 469–472. Styblo K. Estimation of the annual risk of tuberculosis infection. Tuberculosis Surveillance Research Unit. Bull Int Union Tuberc 1978; 51 (Suppl): 1–101. Ministerio da Saude. Control da tuberculose: uma proposta de integracao ensino servicio. 4a ed. Brasilia, Brasil, Ministerio da Saude, 1994. Palwatwichai A. Tuberculosis in Thailand. Respirology 2001; 6: 65–70. Chadha V K, Kumar P, Jagannatha P S, Vaidyanathan P S, Unnikrishnan K P. Average annual risk of tuberculous infection in India. Int J Tuberc Lung Dis 2005; 9: 116–118. Ramirez J A, Anderson P, Herp S, Raff M J. Increased rate of tuberculin skin test conversion among workers at a university hospital. Infect Control Hosp Epidemiol 1992; 13: 579–581. Adal K A, Anglim A M, Palumbo C L, Titus M G, Coyner B J, Farr B M. Preventing nosocomial tuberculosis with HEPA respirators: a cost-effectiveness analysis. N Engl J Med 1994; 331: 169–173. Rullán J V, Herrera D, Cano R, et al. Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis in Spain. Emerg Infect Dis 1996; 2: 125–129.

604


40 Bourdreau A Y, Baron S L, Steenland N K, et al. Occupational risk of Mycobacterium tuberculosis infection in hospital workers. Am J Ind Med 1997; 32: 528–534. 41 Louther J, Riviera P, Feldman J, Villa N, DeHovitz J, Sepkowitz K A. Risk of tuberculin conversion according to occupation among health care workers at a New York City hospital. Am J Respir Crit Care Med 1997; 156: 201–205. 42 Behrman A J, Shofer F S. Tuberculosis exposure and control in an urban emergency department. Ann Emerg Med 1998; 31: 370–375. 43 Blumberg H M, Sotir M, Erwin M, Bachman R, Shulman J A. Risk of house staff tuberculin skin test conversion in an area with a high incidence of tuberculosis. Clin Infect Dis 1998; 27: 826–833. 44 Christie C D, Constantinou P, Marx M L, et al. Low risk for tuberculosis in a regional pediatric hospital: nine-year study of community rates and the mandatory employee tuberculin skintest program. Infect Control Hosp Epidemiol 1998; 19: 168– 174. 45 LoBue P A, Catanzaro A. Effectiveness of a nosocomial tuberculosis control program at an urban teaching hospital. Chest 1998; 113: 1184–1189. 46 Menzies R I, Fanning A, Yuan L, FitzGerald J M. Hospital ventilation and risk of tuberculous infection in Canadian health care workers. Ann Intern Med 2000; 133: 779–789. 47 Warren D K, Foley K M, Polish L B, Seiler S M, Fraser V J. Tuberculin skin testing of physicians at a midwestern teaching hospital: a 6-year prospective study. Clin Infect Dis 2001; 32: 1331–1337. 48 Larsen N M, Biddle C L, Sotir M J, White N, Parrott P, Blumberg H M. Risk of tuberculin skin test conversion among health care workers: occupational versus community exposure and infection. Clin Infect Dis 2002; 35: 796–801. 49 Miller A K, Tepper A, Sieber K. Historical risks of tuberculin skin test conversion among non-physician staff at a large urban hospital. Am J Ind Med 2002; 42: 228–235. 50 Ellis E, Sauvé L, Phypers M, Sheardown C, Allegakone M. Tuberculosis in Canada. Ontario, Canada: Public Health Agency of Canada, 2004. http://www.phac-aspc.gc.ca/publicat/tbcan04/ index.html Accessed November 2006. 51 US Department of Health and Human Services Public Health Service. Reported tuberculosis in the United States, 2001. Tuberculosis case rates: United States, 2003. Atlanta, GA, USA: Center for Disease Control and Prevention, 2003. 52 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: 254–258. 53 Harries A D, Kamenya A, Namarika D, et al. Delays in diagnosis and treatment of smear-positive tuberculosis and the incidence of tuberculosis in hospital nurses in Blantyre, Malawi. Trans R Soc Trop Med Hyg 1997; 91: 15–17. 54 Balt E, Durrheim D N, Weyer K. Nosocomial transmission of tuberculosis to health care workers in Mpumalanga. S Afr Med J 1998; 88: 1363–1366. 55 Wilkinson D, Gilks C F. Increasing frequency of tuberculosis among staff in a South African district hospital: impact of the HIV epidemic on the supply side of health care. Trans R Soc Trop Med Hyg 1998; 92: 500–502. 56 Harries A D, Nyirenda T E, Banerjee A, Boeree M J, Salaniponi F M. Tuberculosis in health care workers in Malawi. Trans R Soc Trop Med Hyg 1999; 93: 32–35. 57 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: 827–831. 58 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: 170–176. 59 Cuhadaroglu C, Erelel M, Tabak L, Kilicaslan Z. Increased

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65

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78

79

risk of tuberculosis in health care workers: a retrospective survey at a teaching hospital in Istanbul, Turkey. BMC Infect Dis 2002; 2: 14. Eyob G, Gebeyhu M, Goshu S, et al. Increase in tuberculosis incidence among the staff working at the Tuberculosis Demonstration and Training Centre in Addis Ababa, Ethiopia: a retrospective cohort study (1989–1998). Int J Tuberc Lung Dis 2002; 6: 85–88. Harries A D, Hargreaves N J, Gausi F, Kwanjana J H, Salaniponi F M. Preventing tuberculosis among health workers in Malawi. Bull World Health Organ 2002; 80: 526–531. Kilinc O, Ucan E S, Cakan M D, et al. Risk of tuberculosis among health care workers: can tuberculosis be considered as an occupational disease? Respir Med 2002; 96: 506–510. Kanyerere H S, Salaniponi F M. Tuberculosis in health care workers in a central hospital in Malawi. Int J Tuberc Lung Dis 2003; 7: 489–492. Gopinath K G, Siddique S, Kirubakaran H, Shanmugam A, Mathai E, Chandy G M. Tuberculosis among health care workers in a tertiary-care hospital in South India. J Hosp Infect 2004; 57: 339–342. Jelip J, Mathew G G, Yusin Y, et al. Risk factors of tuberculosis among health care workers in Sabah, Malaysia. Tuberculosis 2004; 84: 19–23. Rao K G, Aggarwal A M, Behera D. Tuberculosis among physicians in training. Int J Tuberc Lung Dis 2004; 8: 1392–1394. Dimitrova B, Hutchings A, Atun R, et al. Increased risk of tuberculosis among health care workers in Samara Oblast, Russia: analysis of notification data. Int J Tuberc Lung Dis 2005; 9: 43–48. Hosoglu S, Tanrikulu A C, Dagli C, Akalin S. Tuberculosis among health care workers in a short working period. Am J Infect Control 2005; 33: 23–26. Jiamjarasrangsi W, Hirunsuthikul N, Kamolratanakul P. Tuberculosis among health care workers at King Chulalongkorn Memorial Hospital, 1988–2002. Int J Tuberc Lung Dis 2005; 9: 1253–1258. Naidoo S, Mahommed A. Knowledge, attitudes, behaviour and prevalence of TB infection among dentists in the western Cape. SADJ 2002; 57: 476–478. Centers for Disease Control. Proportionate mortality from pulmonary tuberculosis associated with occupations—28 states, 1979–1990. MMWR 1995; 44: 14–19. 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: 587–593. Sepkowitz K A, Friedman C R, Hafner A, et al. Tuberculosis among urban health care workers: a study using restriction fragment length polymorphism typing. Clin Infect Dis 1995; 21: 1098–1102. Meredith S, Watson J M, Citron K M, Cockcroft A, Darbyshire J H. Are health care workers in England and Wales at increased risk of tuberculosis? BMJ 1996; 313: 522–525. Hill A, Burge A, Skinner C. Tuberculosis in national health service hospital staff in the west Midlands region of England, 1992–5. Thorax 1997; 52: 994–997. van Deutekom H, Gerritsen J J, van Soolingen D, van Ameijden E J, van Embden J D, Coutinho R A. A molecular epidemiological approach to studying the transmission of tuberculosis in Amsterdam. Clin Infect Dis 1997; 25: 1071–1077. Pleszewski B, FitzGerald J M. Tuberculosis among health care workers in British Columbia. Int J Tuberc Lung Dis 1998; 2: 898–903. Raitio M, Helenius H, Tala E. Is the risk of occupational tuberculosis higher for young health care workers? Int J Tuberc Lung Dis 2003; 7: 556–562. Bang K M, Weissman D N, Wood J M, Attfield M D. Tuberculosis mortality by industry in the United States, 1990–1999. Int J Tuberc Lung Dis 2005; 9: 437–442.


80 Driver C R, Stricof R L, Granville K, et al. Tuberculosis in health care workers during declining tuberculosis incidence in New York State. Am J Infect Control 2005; 33: 519–526. 81 Diel R, Seidler A, Nienhaus A, Rusch-Gerdes S, Niemann S. Occupational risk of tuberculosis transmission in a low incidence area. Respir Res 2005; 6: 35. 82 Bangsberg D R, Crowley K, Moss A, Dobkin J F, McGregor C, Neu H C. Reduction in tuberculin skin-test conversions among medical house staff associated with improved tuberculosis infection control practices. Infect Control Hosp Epidemiol 1997; 18: 566–570.

605

83 Moro M L, Errante I, Infuso A, et al. Effectiveness of infection control measures in controlling a nosocomial outbreak of multidrug-resistant tuberculosis among HIV patients in Italy. Int J Tuberc Lung Dis 2000; 4: 61–68. 84 Jarvis W R. Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis. Am J Infect Control 1995; 23: 146–151. 85 Fridkin S K, Managan L, Boyard R N. SHEA-CDC TB survey, Part II. Efficacy of TB infection control programs at member hospitals, 1992. Infect Control Hosp Epidemiol 1995; 16: 135– 140.

RÉSUMÉ C O N T E X T E : La tuberculose (TB) chez les travailleurs des soins de santé (HCW) n’a pas été considérée comme un problème grave après l’arrivée des traitements antibiotiques efficaces. L’intérêt a ce sujet a été stimulé à nouveau par le développement de plusieurs mini-épidémies nosocomiales sévères. M É T H O D E S : Nous avons fait la revue de la littérature publiée disponible concernant la prévalence et l’incidence de l’infection et de la maladie tuberculeuse chez les HCW dans les pays catégorisés selon leur revenu. Nous avons inclus les études publiées en anglais depuis 1960 provenant des pays à revenus faibles ou moyens (LMIC) et depuis 1990, celles en provenance de pays à revenus élevés (HIC). Nous avons exclu les rapports sur les miniépidémies et les études basées exclusivement sur les questionnaires. R É S U L T A T S : La prévalence médiane d’infection tuberculeuse latente (LTBI) chez les HCW est de 63% (extrêmes 33–79%) dans les LMIC et de 24% (4–46%)

dans les HIC. Parmi les HCW provenant des LMIC, la LTBI est associée de manière régulière avec des marqueurs d’exposition professionnelle, mais dans les HIC elle est davantage en association avec des facteurs autres que professionnels. L’incidence annuelle médiane de l’infection TB attribuable au travail dans les soins de santé est de 5,8% (extrêmes 0–11%) dans les LMIC et de 1,1% dans les HIC. Les taux de TB active chez les HCW sont régulièrement plus élevés que dans la population générale dans tous les pays, bien que les résultats aient été variables dans les HIC. Des mesures administratives de contrôle de l’infection n’ont que peu d’impact dans les LMIC, mais semblent les plus efficaces dans les HIC. C O N C L U S I O N S : La TB reste un risque professionnel très important pour les travailleurs des soins de santé dans les LMIC et pour les travailleurs dans certaines institutions des HIC. Le risque apparaît particulièrement élevé lorsqu’une exposition accrue est associée avec des mesures inadéquates de contrôle de l’infection. RESUMEN

Tras el advenimiento de un tratamiento antituberculoso eficaz, la tuberculosis (TB) en los profesionales de la salud (HCW) dejó de considerarse como un problema grave. Sin embargo, la constatación de importantes brotes epidémicos nosocomiales ha reavivado el interés. M É T O D O S : Se llevó a cabo un estudio de la literatura científica existente sobre prevalencia e incidencia de infección y enfermedad tuberculosa en los HCW en diferentes países, catalogados según el ingreso promedio. Se incluyeron estudios publicados en inglés desde 1960 provenientes de países con ingresos bajos e intermedios (LMIC) y desde 1990, provenientes de países con ingresos altos (HIC). Se excluyeron informes sobre brotes epidémicos y estudios basados exclusivamente en cuestionarios. R E S U L T A D O S : La mediana de la prevalencia de infección tuberculosa latente (LTBI) en profesionales sanitarios en LMIC fue del 63% (entre 33% y 79%) y del 24% en HIC (entre 4% y 46%). En los profesionales sanitaMARCO DE REFERENCIA :

rios de los primeros países, la LTBI se asoció constantemente con marcadores de exposición profesional, pero en los HIC se asoció con mayor frecuencia con factores no profesionales. La mediana de la incidencia anual de infección tuberculosa atribuible a la profesión sanitaria fue del 5,8% (entre 0 y 11%) en LMIC y del 1,1% (entre 0,2% y 12%) en HIC. Las tasas de TB activa fueron sistemáticamente más altas en los HCW que en la población general en todos los países, pero los hallazgos fueron variables en los HIC. Las medidas administrativas de control de las infecciones tuvieron una repercusión modesta en LMIC pero parecieron más eficaces en HIC. C O N C L U S I O N E S : La TB representa todavía un importante riesgo profesional para los proveedores de atención de salud en LMIC y para los profesionales de algunos establecimientos en los HIC. El riesgo parece particularmente alto cuando existe una mayor exposición, combinada con medidas deficientes de control de las infecciones.