Screening for tuberculosis among homeless shelter staff

Screening for tuberculosis among homeless shelter staff

American Journal of Infection Control 40 (2012) 459-61 Contents lists available at ScienceDirect American Journal of Infection Control American Jou...

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American Journal of Infection Control 40 (2012) 459-61

Contents lists available at ScienceDirect

American Journal of Infection Control

American Journal of Infection Control

journal homepage: www.ajicjournal.org

Brief report

Screening for tuberculosis among homeless shelter staff Simona Di Renzi MS a, Paola Tomao PhD a, *, Agnese Martini MD a, Silvia Capanna MS a, Luca Rubino MD b, Wanda D’Amico MS a, Fabio Tomei MD c, Paolo Visca PhD d, Nicoletta Vonesch MS a a

Italian Workers’ Compensation Authority (INAIL), Department of Occupational Medicine, Rome, Italy National Association for the Fight Against AIDS (ANLAIDS), Rome, Italy c National Coordination of Specialists in Occupational Medicine, Rome, Italy d Department of Biology, University “Roma Tre”, Rome, Italy b

Key Words: Health care worker Occupational infection Tuberculin skin test Interferon-g assay

The prevalence of tuberculosis (TB) among homeless shelter staff was assessed using the tuberculin skin test (TST) and the Quantiferon TB-Gold in tube interferon-g release assay (QFT-TB). Investigation of 51 participants for whom both QFT-TB and TST results were available showed 47.1% and 43.1% positivity, respectively, with excellent (92%) concordance between the 2 tests. The high risk for acquiring occupational TB necessitates the development of TB surveillance protocols for homeless shelter staff in Italy. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Tuberculosis (TB) is a major cause of disability and death worldwide. The HIV epidemic, the increasing immigration from countries with endemic TB, and the emergence of multidrugresistant Mycobacterium tuberculosis boost TB’s social impact. In 2009, the World Health Organization (WHO) reported 9.4 million incident cases of TB globally, most of them in Asia and Africa.1 The incidence of TB remains relatively low in Italy (7.6%).2 Health care workers (HCWs) can be exposed to patients with TB, and the risk of nosocomial TB has been recognized as a main occupational hazard for these workers.3,4 Because of the high incidence of TB among homeless people, as well as among immigrants and refugees from regions of high TB endemicity, homeless shelter staff should be considered at risk for acquiring occupational TB.4 Little pertinent information is available for this group of workers, however.5,6 Until recently, the tuberculin skin test (TST) was the main diagnostic tool for both active TB (A-TB) and latent TB (L-TB) screening. However, TST suffers from several methodological limitations, including the high rate of false-positive results in vaccinated populations, the subjectivity of the evaluation, and the booster effect.7 Recent in vitro tests have been developed to overcome these problems. The Quantiferon TB-Gold in tube (QFT-TB) assay (Cellestis, Darmstadt, Germany) is based on the quantification of interferon-g released by sensitized T cells in whole blood

* Address correspondence to Paola Tomao, PhD, INAIL, Department of Occupational Medicine, Via Fontana Candida 1, 00040 Monte Porzio Catone, Rome, Italy. E-mail address: [email protected] (P. Tomao). Conflict of interest: None to report.

incubated with M tuberculosis peptides ESAT-6, CFP-10, and TB7.7(p4).8 The QFT-TB assay is more specific than the TST because it uses antigens not shared by any of the bacille Calmette-Guérin (BCG) vaccinal strains or other mycobacterial species. The aims of this study were (1) to evaluate the prevalence of A-TB and L-TB in a group of homeless shelter staff, (2) to compare the applicability of the QFT-TB test with the TST, and (3) to identify potential risks related to specific work activities and sociodemographic characteristics. METHODS The study was conducted in September 2007 on 64 nuns at a missionary-run shelter for the homeless in central Italy. After providing written consent, each nun completed a questionnaire eliciting information on age, country of origin, previous workplace, work-related activities, duration of employment, history of contact with TB patient(s), clinical symptoms compatible with A-TB, previous TB diagnosis, BCG vaccination, and risk factors for HIV infection. After physical examination, all 64 participants were tested by the QFT-TB assay, but only 54 were tested with the TST. Discrimination between A-TB and L-TB was based on previously reported clinical, radiologic, and microbiological criteria.4 The QFT-TB assay was conducted in accordance with the manufacturer’s instructions and was interpreted as reported previously.8 The TST was administered by trained personnel following standard procedures with purified protein derivative (Tubersol; Sanofi Pasteur, Rome, Italy). The transverse diameter of the induration was read after 48-72 hours, and 10 mm was

0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.07.002

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considered a positive result. Participants who reported a positive TST on the enrollment questionnaire and had a diameter 10 mm on the TST were considered positives, whereas those who reported a previously negative TST but had a diameter 10 mm on the TST were considered converters (and positives). Negatives were those participants who reported a negative TST on the enrollment questionnaire and tested negative on both the TST and the QFT-TB assay. Statistical analyses were performed using SPSS 16.0 (SPSS Inc, Chicago, IL). Adjusted odds ratios for QFT-TB were calculated using logistic regression. According to the Italian law, no ethical approval was needed, because the study was conducted as part of a routine HCW surveillance program. RESULTS The mean age of the 64 nuns enrolled was 38.30  10.24 years (range, 25-71 years); 20.3% came from countries with a very low incidence of TB (<24 cases/100,000 inhabitants), 10.9% came from low-incidence countries (25-49 cases/100,000 inhabitants), and 68.8% came from high- or very high-incidence countries (>100 cases/100,000 inhabitants), according to WHO definitions.1 Moreover, 39.1% had previously worked in very low-incidence countries, 6.3% had worked in low-incidence countries, and 54.7% had worked in high- or very high-incidence countries. The mean time of residence in Italy was 12.7 years (range, 3-48 years), and 90.6% had work-related activities that pose a risk of TB both in their country of origin and in Italy. Only 6.5% reported receiving BCG vaccination in childhood or adolescence. A history of contact with TB- and HIVinfected patients was reported by 46.9% and 6.3% of the nuns, respectively (data not shown). Investigation of 51 nuns in whom both QFT-TB and TST results were available showed 47.1% and 43.1% positivity, respectively, with excellent (92%) concordance between the 2 tests (Table 1). Of the 22 nuns who tested positive on the TST, 17 were converters. In addition, 2 nuns who reported a negative TST on the enrollment questionnaire were QFT-TBepositive but TST-negative during this screening. All 5 nuns who were previously TST-positive also reported receiving a 6-month course of anti-TB therapy. None of the nuns exhibited clinical, radiologic, or microbiological evidence of A-TB during this study. Risk factors for a positive QFT-TB result were the origin and previous workplace in countries of high TB incidence (Table 2). No significant association was observed for work-related activities and age, although positivity was more frequent among nuns engaged in high-risk tasks and those aged >50 years.

Table 1 Comparison between TST and QFT-TB results in 51 participants TST, n (%)

QFT-TB Positive Negative Total

Positive

Negative

Total, n (%)

22 (43.1) 0 (0.0) 22 (43.1)

2 (3.9) 27 (52.9) 29 (56.9)

24 (47.1) 27 (52.9) 51 (100.0)

NOTE. Three of the 54 nuns who underwent the TST were excluded from the analysis because their results on the QFT-TB assay were indeterminate due to the low response of stimulated T cells to mitogen (<0.5 IU/mL). Concordance between the 2 tests was 92%.

Table 2 Covariates associated with positive QFT-TB results in 61 samples QFT-TB assay result, n (%) Characteristics

Negative

Age, years* 30 6 (50) 31e40 18 (60) 41e50 7 (87.5) >50 3 (27.3) Country of birth (WHO area) y Area A 9 (69.2) Area B 4 (66.7) Area C 0 Area D 11 (45.8) Area E 10 (55.6) Previous workplace (WHO area)y Area A 17 (73.9) Area B 2 (50) Area C 0 Area D 9 (42.9) Area E 6 (46.2) Work-related activities Low risk 2 (33) High risk 32 (58.2) Contacts with TB patient(s) No 19 (55.9) Yes 15 (55.6) BCG vaccination No 32 (56.1) Yes 2 (50) Risk factors for HIV infection No 33 (57.9) Yes 1 (25)

Adjusted odds ratio*

95% confidence interval

(50) (40) (12.5) (66.7)

1 0.812 0.035 43.845

0.14-4.55 0.00-1.27 0.99-1,923.45

4 (30.8) 2 (33.3) 0 13 (54.2) 8 (44.4)

1 32.214 151.149 128.469

0.77-1,335.28 3.79-6,031.76 2.80-5,898.94

6 (26.1) 2 (50) 0 12 (57.1) 7 (53.8)

1 15.308 16.408 4.447

4 (66.7) 23 (41.8)

1 0.062

0.00-2.20

15 (44.1) 12 (44.4)

1 1.105

0.19-6.30

25 (43.9) 2 (50)

0.134 1

24 (42.1) 3 (75)

1 0.941

Positive 6 12 1 8

0.69-335.60 2.02-133.40 0.68-28.96

0.00-4.09

0.02-35.16

NOTE. Multivariate analysis was performed on the 61 samples tested by QFT-TB that gave unambiguous results, that is, excluding the 3 indeterminate cases. *Mean age, 38.30  10.24 years; range, 25-71 years. yWHO areas are categorized based on number of TB cases per 100,000 population1: A, 0-24; B, 25-49; C, 50-99; D, 100-299; E, 300.

DISCUSSION In the health care setting, TB screening is an important part of policies and procedures in infection control programs, and new IFN-g release assays (IGRAs) represent an important upgrade of the TST. US guidelines recommend the use of IGRAs in all circumstances in which the TST is used, including surveillance of HCWs occupationally exposed to M tuberculosis.8 Conversely, in Italy guidelines suggest periodic administration of the TST, whereas IGRAs have been proposed as confirmatory tests only in TST-positive HCWs who had received the BCG vaccine.9 Formally, homeless shelter staff are not assimilated with HCWs, and thus they might elude routine surveillance for both L-TB and A-TB, even though they are exposed to individuals with a known high rate of TB infection. Indeed, 46% of A-TB cases reported in Italy in 2008 occurred in immigrants, representing a 16-fold higher incidence than that seen in native Italians.2 Although no data on TB incidence among homeless people in Italy are available, a very high prevalence of

both L-TB and A-TB has been reported for this group in other countries.10 Despite the low prevalence of TB in the general Italian population,2 w45% of our nuns working in homeless shelters tested positive for L-TB, with an estimated conversion rate of 37.2% (according to both the TST and QFT-TB results). The concordance between TST and QFT-TB results was excellent and can be explained by the low rate of vaccination among the nuns enrolled. The prevalence of L-TB found in the present study is nearly double that reported for HCWs in Italy11 and homeless caregivers in Japan,5 but is close to that reported in immigrants in Italy2 and HCWs from low/middle-income countries.12 Accordingly, multivariate analysis of our data showed that birth and previous workplace in endemic countries for TB were associated with QFT-TB positivity.

S. Di Renzi et al. / American Journal of Infection Control 40 (2012) 459-61

Our study has some limitations. Despite the high conversion rate observed among our participants, the possibility that some of them became infected before their transfer to Italy when performing a similar job in their country of origin cannot be ruled out. Moreover, the nonoccupational risk for TB exposure (eg, household) was not investigated, and this could have contributed to the overall high rate of L-TB positivity seen in our nuns. We conclude that L-TB is a significant health problem among homeless shelter staff in Italy. The high risk for acquiring occupational TB necessitates the development of surveillance protocols for this category of worker. References 1. World Health Organization. Global tuberculosis control 2008-2007-2005-2000. Available from: http://www.who.int/tb/publications/global_report/archive/en/ index.html. Accessed March 14, 2011. 2. Italian Ministry of Health. Report on tuberculosis in Italy, 2008. Available from: http://www.salute.gov.it/imgs/C_17_pubblicazioni_1222_allegato.pdf (in Italian). Accessed March 14, 2011. 3. Mirtskhulava V, Kempker R, Shields KL, Leonard MK, Tsertsvadze T, del Rio C, et al. Prevalence and risk factors for latent tuberculosis infection among health care workers in Georgia. Int J Tuberc Lung Dis 2008;12:513-9.

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4. Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health care settings, 2005. MMWR Morb Mortal Wkly Rep 2005;54:1-141. 5. Tabuchi T, Takatorige T, Hirayama Y, Nakata N, Harihara S, Shimouchi A, et al. Tuberculosis infection among homeless persons and caregivers in a hightuberculosis-prevalence area in Japan: a cross-sectional study. BMC Infect Dis 2011;11:22. 6. Dewan PK, Grinsdale J, Liska S, Wong E, Fallstad R, Kawamura LM. Feasibility, acceptability, and cost of tuberculosis testing by whole-blood interferon-g assay. BMC Infect Dis 2006;6:47. 7. Richeldi L. An update on the diagnosis of tuberculosis infection. Am J Respir Crit Care Med 2006;174:736-42. 8. Center for Disease Control and Prevention. Updated guidelines for using interferon gamma release assays to detect Mycobacterium tuberculosis infectiondUnited States, 2010. MMWR Morb Mortal Wkly Rep 2010;59:1-25. 9. Ministry of Welfare, Health, and Social Politics. An update of recommendations for tuberculosis control activities. “Management of contacts and healthcare associated tuberculosis.” Available from: http://www.salute.gov.it/imgs/C_17_ pubblicazioni_1221_allegato.pdf (in Italian). Accessed March 14, 2011. 10. Raoult D, Foucault C, Brouqui P. Infections in the homeless. Lancet Infect Dis 2001;1:77-84. 11. Girardi E, Angeletti C, Puro V, Sorrentino R, Magnavita N, Vincenti D, et al. Estimating diagnostic accuracy of tests for latent tuberculosis infection without a gold standard among healthcare workers. Euro Surveill 2009;14. pii¼19373. 12. Joshi R, Reingold AL, Menzies D, Pai M. Tuberculosis among health care workers in low- and middle-income countries: a systematic review. PLoS Med 2006; 3:e494.