- Email: [email protected]
Pandemic 2009 H1N1 influenza among health care workers
American Journal of Infection Control 41 (2013) 645-7
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Pandemic 2009 H1N1 influenza among health care workers Renata D. Lobo RN, MS a, *, Maura S. Oliveira MD, MS a, Cilmara P. Garcia MD a, Helio Hehl Caiaffa Filho MS b, Anna S. Levin MD, PhD a, c a
Infection Control Department, Hospital das Clínicas, University of São Paulo, Brazil LIM 03, Divisão de Laboratório Central, Hospital das Clínicas, University of São Paulo, Brazil c Department of Infectious Diseases and LIM-54, University of São Paulo, Brazil b
Key Words: Respiratory symptons RT-PCR Risk factor
To evaluate factors associated with pandemic influenza among health care workers (HCWs), a case-casecontrol study was conducted with 52 confirmed cases, 120 influenza-negative cases, and 102 controls. Comorbidities (odds ratio [OR], 19.05; 95% confidence interval [95% CI]: 4.75e76.41), male sex (OR, 5.11; 95% CI: 1.80e14.46), and being a physician (OR, 8.58; 95% CI: 2.52e29.27) were independent risk factors for pandemic influenza infection among HCWs. Contact with symptomatic coworker or social contact was protective (OR, 0.11; 95% CI: 0.04e0.29). To our knowledge, this is the first study of factors associated with acquiring influenza involving HCW in nonsevere cases. Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
During 2009 winter season (June-September), South America was affected by the 2009 H1N1 influenza pandemic. Hospital das Clínicas (HC), a tertiary care teaching hospital, has 2,200 beds divided in 7 institutes and 20,000 health care workers (HCWs). It was one of the reference hospitals for severe cases in the city1 and admitted 406 influenza patients.2 Specific influenza units were created: Main institute: a 7-bed adult intensive care unit (ICU), an 11-bed ward, and a 15-bed specific ward for pregnant patients; Children’s Institute: a 2-bed ICU, a 14-bed ward, and 2 pediatric emergency department rooms; and Heart Institute: 16 two-bed rooms. Contact and droplet precautions when caring for confirmed/ suspected cases were required of HCWs and N95 masks only for aerosol-generating procedures. This study aimed to evaluate factors associated with 2009 H1N1 influenza infection in HCWs. This was a case-case-control study. Three groups were defined: Confirmed pandemic influenza infection: HCW with respiratory symptoms with laboratory-confirmed 2009 H1N1 influenza (confirmed cases);
* Address correspondence to Renata D. Lobo, RN, Rua Cardeal Arcoverde, 201, ap 132, São Paulo-SP, 05407 000, Brazil. E-mail address: [email protected] (R.D. Lobo). Supported by Hospital das Clínicas, University of São Paulo, Brazil. Conflicts of interest: None to report.
symptomatic influenza-negative infection: HCW with respiratory symptoms tested and negative for 2009 H1N1 influenza (influenza-negative cases); and asymptomatic HCW: HCW without respiratory symptoms who worked at the same unit as a confirmed case during the same period (controls: 2 per confirmed case). Respiratory symptoms were defined as fever and at least 1 respiratory symptom. Reverse-transcription polymerase chain reaction (RT-PCR) for 2009 H1N1 influenza was performed from nasopharyngeal swabs according to the US Centers for Disease Control and Prevention protocol.3 It was available free of charge starting on August 24 for HCWs with respiratory symptoms and was required of all symptomatic HCW seeking leave from work. HCWs included were interviewed personally or by telephone from October 2009 to January 2010. Confirmed cases were compared with asymptomatic controls and were also compared with influenza-negative-cases. For dichotomous variables, odds ratios and 95% confidence intervals were determined. Continuous variables were compared using analysis of variance. Multivariate analysis using logistic regression compared confirmed cases with controls (variables with P .25 in the bivariate analysis). Variables in which 95% confidence intervals did not include 1.0 were maintained in the final model. Data were analyzed using EpiInfo 3.5.2 (Centers for Disease Control and Prevention, Atlanta, GA). One hundred eighty HCWs with respiratory symptoms were submitted to RT-PCR testing: 53 tested positive and 127 negative. Eight did not consent or were not located. Thus, 52 confirmed cases and 120 symptomatic influenza-negative cases were
0196-6553/$36.00 - Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2012.08.012
646
R.D. Lobo et al. / American Journal of Infection Control 41 (2013) 645-7
Table 1 Comparison of characteristics of health care workers with confirmed pandemic influenza infection, symptomatic influenza-negative infection, and asymptomatic HCWs in Hospital das Clínicas, São Paulo, Brazil
Variable Age, yr Mean (SD) Median (range) Male sex Presence of comorbidities Use of tobacco Obesity Chronic heart disease Pneumopathy Hypertension Diabetes Pregnancy Lung disease Others Professional category Physician Medical resident Nurse Nurse technician Student Administrative Other Workplace at HC Emergency room Intensive care unit Patient ward Other Activities at HC Direct patient care Work at another hospital Activities at another hospital Direct patient care Contact with suspected or confirmed pandemic influenza infection cases at HC Without respiratory protection Contact with suspected or confirmed pandemic influenza infection at another hospital Without respiratory protection Contact with suspected or confirmed pandemic influenza infection at home Contact with coworker or social contact with suspected or confirmed pandemic influenza infection Received influenza vaccine in 2009 Regular use of public transportation
HCWs with confirmed pandemic influenza Asymptomatic infection, n ¼ 52 HCWs, n ¼ 102 37.4 37 21 15 5 4 2
(10.1) (23e58) (40%) (29%) (33%) (27%) (13%) 2 (13%) 2 (13%) -
36.6 35 21 5 1 3
(9.6) (19-68) (21%) (5%) (20%) (60%) 1 (20%) -
OR (95% CI)
HCWs with symptomatic influenza-negative P value* infection, n ¼ 120 .58
2.61 7.86 2 0.24
(1.26e5.44) (2.67e23.18) (0.13e60.97) (0.02e2.91) -
36 33 31 42 5 5 3 11 3 2 4
.001 .0001 .57 .18 -
(9.5) (21-67) (26%) (35%) (12%) (12%) (7%) (26%) (7%) (5%) (9%)
ORy (95% CI)
P value .53
1.95 0.75 3.7 2.7 2 0.43 2
(0.98e3.87) (0.37e1.53) (0.73e19.24) (0.49e14.70) (0.20e17.42) (0.06e2.57) (0.20e17.42)
.06 .43 .06 .18 .47 .31 .47
10 (24%) .29
16 5 3 13 1 4 10
(31%) (10%) (6%) (25%) (2%) (8%) (19%)
7 5 26 35 4 9 16
(7%) (5%) (26%) (34%) (4%) (9%) (16%)
10 8 13 21
(19%) (15%) (25%) (40%)
13 15 36 38
(13%) (15%) (35%) (37%)
6.03 (2.11e17.82)z .00008
17 16 13 44 2 19 9
(14%) (13%) (11%) (37%) (2%) (16%) (8%)
32 25 23 40
(27%) (21%) (19%) (33%)
.53
.48
41 (79%) 18 (35%)
74 (73%) 15 (15%)
1.41 (0.60e3.38) 2.35 (1.29e4.28)
.40 .004
95 (79%) 36 (30%)
1.02 (0.42e2.42) 1.15 (0.73e1.83)
.96 .55
17 (94%) 33 (64)
13 (87%) 85 (83)
2.62 (0.16e82.33) 0.35 (0.16e0.75)
.44 .006
28 (77%) 88 (73%)
1.60 (0.73e3.47) 0.63 (0.32e1.26)
.20 .19
18 (35%) 11 (61%)
46 (45%) 9 (60%)
0.64 (0.32e1.28) 1.05 (0.21e5.34)
.21 .95
46 (38%) 20 (17%)
1.10 (0.46e2.64) 1.26 (0.34e4.66)
.82 .70
8 (73%) 18 (35%)
1 (11%) 26 (26%)
21.3 (1.38e724) 1.55 (0.75e3.19)
.006 .24
7 (35%) 21 (18%)
4.95 (0.79e34.90) 2.50 (1.19e5.23)
.04 .01
17 (33%)
76 (75%)
0.17 (0.08e0.35)
.0001
53 (44%)
0.61 (0.31e1.21)
.16
28 (54%) 30 (58%)
54 (53%) 81 (80%)
1.04 (0.53e2.02) 0.35 (0.16e0.78)
.91 .004
89 (74%) 81 (68%)
1.46 (0.65e3.26) 0.61 (0.30e125)
.35 .14
CI, confidence interval; HC, Hospital das Clínicas; OR, odds ratio. *Comparison of HCWs with confirmed pandemic influenza infection with asymptomatic HCWs. y Comparison of HCWs with confirmed pandemic influenza infection with HCWs with symptomatic influenza-negative infection. z Odds ratio calculated comparing the category “Physicians” with all other categories.
included. The control group included 102 HCW (1 confirmed case, a HCW who dispensed oseltamivir to outpatients, had no controls). Nine (17%) confirmed cases worked in specific influenza units; 4 worked in the emergency room. Table 1 compares confirmed cases with asymptomatic controls. Physician, male sex, comorbidities, work at another hospital, and contact with suspected/confirmed pandemic influenza infection at another hospital without respiratory protection were associated with confirmed cases. Contact with patients with suspected/ confirmed pandemic influenza infection at HC, contact with coworker or social contact with suspected/confirmed pandemic influenza infection, and use of public transport were more frequent among asymptomatic controls. Comparing confirmed cases with symptomatic influenzanegative cases, contact with suspected/confirmed pandemic influenza infection without respiratory protection at another hospital,
and contact with suspected/confirmed case at home were associated with acquiring 2009 H1N1 influenza (Table 1). Conjunctivitis was more frequent in confirmed cases, and sore throat and coryza were more frequent in influenza-negative cases. Forty-two (81%) confirmed cases and 89 (74%) influenza-negative cases received oseltamivir. Four confirmed cases were hospitalized, and 1 died. One symptomatic influenza-negative case was hospitalized, and no deaths occurred. None of the controls received oseltamivir, and none were hospitalized or died. Table 2 presents multivariate analysis. Comorbidities, male sex, being a physician, and contact with coworker or social contact with respiratory symptoms were significant. The pandemic caused widespread use of alcoholic solutions outside the hospital because of an unprecedented opportunity for education of the lay public, including government campaigns stimulating the use of alcohol hand rubs and cough etiquette. This
R.D. Lobo et al. / American Journal of Infection Control 41 (2013) 645-7 Table 2 Multivariate analysis of factors associated with acquiring confirmed pandemic influenza infection compared with asymptomatic controls among health care workers in Hospital das Clínicas, São Paulo, Brazil Variable Presence of comorbidities Male sex Being a physician Contact with coworker or social contact with respiratory symptoms
OR (95% CI) 19.05 5.11 8.58 0.11
(4.75e76.41) (1.80e14.46) (2.52e29.27) (0.04e0.29)
P value <.0001 .0021 .0006 <.0001
CI, confidence interval; OR, odds ratio.
may explain why, in our study, social contact and contact with coworker with respiratory symptoms was protective. However, contact with asymptomatic respiratory infection, including incubating influenza, could not be avoided unless HCWs took precautions during contact with all persons, which probably did not occur. It is possible that pandemic influenza was not acquired by the HCWs in the hospital but in the community from persons not clearly recognized as symptomatic. Perception of risk because of contact with symptomatic patients and a new virus, coupled with the administrative measures (rapid case identification/confirmation, influenza units, staff training), probably decreased HCW exposure to influenza patients. The high awareness level can be exemplified by increase in influenza vaccination coverage: 8,116 HCWs were vaccinated in 2009 compared with 22,333 HCWs in 2010 (A. M. Sartori, personal communication). Being a physician was a risk factor possibly because physicians frequently do not follow recommendations. A study on adherence to use of protective equipment against influenza included 292 HCWs and reported suboptimal adherence to personal protection equipment especially among physicians.4-7. Others examples not directly related to influenza, it has been observed that physicians present low compliance with guidelines on antibiotic prophylaxis and with the use of maximal barrier precautions and skin antisepsis of insertion site during CVC insertion. Another possibility is that physicians were exposed to more aerosol generating procedures. Unfortunately, adherence to infection control protocols was not monitored. Comorbidities have been described in patients with severe influenza.6,8,9 Our study involved mostly mild cases. In this outpatient population, comorbidities were significantly associated with acquiring symptomatic pandemic influenza. Most frequent conditions were smoking, obesity, chronic cardiopathy, pneumopathy, and hypertension. To our knowledge, this is the first study to determine factors associated with acquiring nonsevere influenza. It is difficult to explain why being male was a risk factor. We hypothesized there may have been a bias in control selection; however, among controls, 21% were male, and, based on our human resource department, the expected proportion was 24.5%,
647
suggesting no bias. In the community, during the influenza pandemic, men were less adherent to protective measures such as handwashing and cough etiquette.10 These sex differences may have occurred also among HCWs. Comparing both groups of symptomatic HCWs, there were minor differences in clinical presentation. It was difficult to distinguish between influenza and other respiratory infections. Unfortunately, the etiology of noninfluenza respiratory diseases was not investigated. Hospitalizations and death only occurred in pandemic influenza cases, suggesting that it was more severe. Evaluation for factors associated with confirmed cases was not conclusive. Acknowledgment The authors thank Núcleo de Informações em Saúde (NIS), Serviço médico dos funcionários (SAME), and Monique Perret Gentil. References 1. Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasil. (homepage on the Internet). Boletim eletrônico Epidemiológico (updated March 2010). Available from: http://portal.saude.gov.br/portal/arquivos/pdf/boletim_eletro nico_influenza_25_03.pdf. Accessed April 15, 2010. 2. Mota NV, Lobo RD, Toscano CM, Pedroso de Lima AC, Souza Dias MB, Komagata H, et al. Cost-effectiveness of sick leave policies for health care workers with influenza-like illness, Brazil. Emerg Infect Dis 2011 2009;17: 1421-9. 3. World Health Organization Collaborating Centre for influenza. CDC protocol of realtime RTPCR for influenza A(H1N1) revision 2 (6 October 2009). Available from: http://www.who.int/csr/resources/publications/swineflu/realtimeptpcr/ en/index.html. Accessed December 13, 2010. 4. Daugherty EL, Perl TM, Needham DM, Rubinson L, Bilderback A, Rand CS. The use of personal protective equipment for control of influenza among critical care clinicians: a survey study. Crit Care Med 2009;37:1210-6. 5. Bedouch P, Labarère J, Chirpaz E, Allenet B, Lepape A, Fourny M, et al. Compliance with guidelines on antibiotic prophylaxis in total hip replacement surgery: results of a retrospective study of 416 patients in a teaching hospital. Infect Control Hosp Epidemiol 2004;25:302-7. 6. Rubinson L, Wu AW, Haponik EE, Diette GB. Why is it that internists do not follow guidelines for preventing intravascular catheter infections? Infect Control Hosp Epidemiol 2005;26:525-33. 7. Lobo RD, Levin AS, Oliveira MS, Gomes LM, Gobara S, Park M, et al. Evaluation of interventions to reduce catheter-associated bloodstream infection: continuous tailored education versus one basic lecture. Am J Infect Control 2010;38:440-8. 8. Centro de Vigilância Epidemiológica Alexandre Vranjac. Secretaria Estadual da Saúde de São Paulo. (homepage on the Internet). Influenza pandêmica A (H1N1) 2009: (updated 2010; cited February 18, 2010). Available from: ftp://ftp.cve. saude.sp.gov.br/doc_tec/RESP/nt10_influ_atualfev.pdf. Accessed February 18, 2010. 9. Yu H, Feng Z, Uyeki TM, Liao Q, Zhou L, Feng L, et al. Risk factors for severe illness with 2009 pandemic influenza A (H1N1) virus infection in China. 2011;52:457e465. 10. Simonsen KA, Hunskaar S, Wensaas KA, Rørtveit S, Cox R, Njølstad G, et al. Influenza-like illness in Norway: clinical course, attitudes towards vaccination and preventive measures during the 2009 pandemic. Fam Pract 2012;29: 139-46.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Pandemic 2009 H1N1 influenza among health care workers Renata D. Lobo RN, MS a, *, Maura S. Oliveira MD, MS a, Cilmara P. Garcia MD a, Helio Hehl Caiaffa Filho MS b, Anna S. Levin MD, PhD a, c a
Infection Control Department, Hospital das Clínicas, University of São Paulo, Brazil LIM 03, Divisão de Laboratório Central, Hospital das Clínicas, University of São Paulo, Brazil c Department of Infectious Diseases and LIM-54, University of São Paulo, Brazil b
Key Words: Respiratory symptons RT-PCR Risk factor
To evaluate factors associated with pandemic influenza among health care workers (HCWs), a case-casecontrol study was conducted with 52 confirmed cases, 120 influenza-negative cases, and 102 controls. Comorbidities (odds ratio [OR], 19.05; 95% confidence interval [95% CI]: 4.75e76.41), male sex (OR, 5.11; 95% CI: 1.80e14.46), and being a physician (OR, 8.58; 95% CI: 2.52e29.27) were independent risk factors for pandemic influenza infection among HCWs. Contact with symptomatic coworker or social contact was protective (OR, 0.11; 95% CI: 0.04e0.29). To our knowledge, this is the first study of factors associated with acquiring influenza involving HCW in nonsevere cases. Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
During 2009 winter season (June-September), South America was affected by the 2009 H1N1 influenza pandemic. Hospital das Clínicas (HC), a tertiary care teaching hospital, has 2,200 beds divided in 7 institutes and 20,000 health care workers (HCWs). It was one of the reference hospitals for severe cases in the city1 and admitted 406 influenza patients.2 Specific influenza units were created: Main institute: a 7-bed adult intensive care unit (ICU), an 11-bed ward, and a 15-bed specific ward for pregnant patients; Children’s Institute: a 2-bed ICU, a 14-bed ward, and 2 pediatric emergency department rooms; and Heart Institute: 16 two-bed rooms. Contact and droplet precautions when caring for confirmed/ suspected cases were required of HCWs and N95 masks only for aerosol-generating procedures. This study aimed to evaluate factors associated with 2009 H1N1 influenza infection in HCWs. This was a case-case-control study. Three groups were defined: Confirmed pandemic influenza infection: HCW with respiratory symptoms with laboratory-confirmed 2009 H1N1 influenza (confirmed cases);
* Address correspondence to Renata D. Lobo, RN, Rua Cardeal Arcoverde, 201, ap 132, São Paulo-SP, 05407 000, Brazil. E-mail address: [email protected] (R.D. Lobo). Supported by Hospital das Clínicas, University of São Paulo, Brazil. Conflicts of interest: None to report.
symptomatic influenza-negative infection: HCW with respiratory symptoms tested and negative for 2009 H1N1 influenza (influenza-negative cases); and asymptomatic HCW: HCW without respiratory symptoms who worked at the same unit as a confirmed case during the same period (controls: 2 per confirmed case). Respiratory symptoms were defined as fever and at least 1 respiratory symptom. Reverse-transcription polymerase chain reaction (RT-PCR) for 2009 H1N1 influenza was performed from nasopharyngeal swabs according to the US Centers for Disease Control and Prevention protocol.3 It was available free of charge starting on August 24 for HCWs with respiratory symptoms and was required of all symptomatic HCW seeking leave from work. HCWs included were interviewed personally or by telephone from October 2009 to January 2010. Confirmed cases were compared with asymptomatic controls and were also compared with influenza-negative-cases. For dichotomous variables, odds ratios and 95% confidence intervals were determined. Continuous variables were compared using analysis of variance. Multivariate analysis using logistic regression compared confirmed cases with controls (variables with P .25 in the bivariate analysis). Variables in which 95% confidence intervals did not include 1.0 were maintained in the final model. Data were analyzed using EpiInfo 3.5.2 (Centers for Disease Control and Prevention, Atlanta, GA). One hundred eighty HCWs with respiratory symptoms were submitted to RT-PCR testing: 53 tested positive and 127 negative. Eight did not consent or were not located. Thus, 52 confirmed cases and 120 symptomatic influenza-negative cases were
0196-6553/$36.00 - Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2012.08.012
646
R.D. Lobo et al. / American Journal of Infection Control 41 (2013) 645-7
Table 1 Comparison of characteristics of health care workers with confirmed pandemic influenza infection, symptomatic influenza-negative infection, and asymptomatic HCWs in Hospital das Clínicas, São Paulo, Brazil
Variable Age, yr Mean (SD) Median (range) Male sex Presence of comorbidities Use of tobacco Obesity Chronic heart disease Pneumopathy Hypertension Diabetes Pregnancy Lung disease Others Professional category Physician Medical resident Nurse Nurse technician Student Administrative Other Workplace at HC Emergency room Intensive care unit Patient ward Other Activities at HC Direct patient care Work at another hospital Activities at another hospital Direct patient care Contact with suspected or confirmed pandemic influenza infection cases at HC Without respiratory protection Contact with suspected or confirmed pandemic influenza infection at another hospital Without respiratory protection Contact with suspected or confirmed pandemic influenza infection at home Contact with coworker or social contact with suspected or confirmed pandemic influenza infection Received influenza vaccine in 2009 Regular use of public transportation
HCWs with confirmed pandemic influenza Asymptomatic infection, n ¼ 52 HCWs, n ¼ 102 37.4 37 21 15 5 4 2
(10.1) (23e58) (40%) (29%) (33%) (27%) (13%) 2 (13%) 2 (13%) -
36.6 35 21 5 1 3
(9.6) (19-68) (21%) (5%) (20%) (60%) 1 (20%) -
OR (95% CI)
HCWs with symptomatic influenza-negative P value* infection, n ¼ 120 .58
2.61 7.86 2 0.24
(1.26e5.44) (2.67e23.18) (0.13e60.97) (0.02e2.91) -
36 33 31 42 5 5 3 11 3 2 4
.001 .0001 .57 .18 -
(9.5) (21-67) (26%) (35%) (12%) (12%) (7%) (26%) (7%) (5%) (9%)
ORy (95% CI)
P value .53
1.95 0.75 3.7 2.7 2 0.43 2
(0.98e3.87) (0.37e1.53) (0.73e19.24) (0.49e14.70) (0.20e17.42) (0.06e2.57) (0.20e17.42)
.06 .43 .06 .18 .47 .31 .47
10 (24%) .29
16 5 3 13 1 4 10
(31%) (10%) (6%) (25%) (2%) (8%) (19%)
7 5 26 35 4 9 16
(7%) (5%) (26%) (34%) (4%) (9%) (16%)
10 8 13 21
(19%) (15%) (25%) (40%)
13 15 36 38
(13%) (15%) (35%) (37%)
6.03 (2.11e17.82)z .00008
17 16 13 44 2 19 9
(14%) (13%) (11%) (37%) (2%) (16%) (8%)
32 25 23 40
(27%) (21%) (19%) (33%)
.53
.48
41 (79%) 18 (35%)
74 (73%) 15 (15%)
1.41 (0.60e3.38) 2.35 (1.29e4.28)
.40 .004
95 (79%) 36 (30%)
1.02 (0.42e2.42) 1.15 (0.73e1.83)
.96 .55
17 (94%) 33 (64)
13 (87%) 85 (83)
2.62 (0.16e82.33) 0.35 (0.16e0.75)
.44 .006
28 (77%) 88 (73%)
1.60 (0.73e3.47) 0.63 (0.32e1.26)
.20 .19
18 (35%) 11 (61%)
46 (45%) 9 (60%)
0.64 (0.32e1.28) 1.05 (0.21e5.34)
.21 .95
46 (38%) 20 (17%)
1.10 (0.46e2.64) 1.26 (0.34e4.66)
.82 .70
8 (73%) 18 (35%)
1 (11%) 26 (26%)
21.3 (1.38e724) 1.55 (0.75e3.19)
.006 .24
7 (35%) 21 (18%)
4.95 (0.79e34.90) 2.50 (1.19e5.23)
.04 .01
17 (33%)
76 (75%)
0.17 (0.08e0.35)
.0001
53 (44%)
0.61 (0.31e1.21)
.16
28 (54%) 30 (58%)
54 (53%) 81 (80%)
1.04 (0.53e2.02) 0.35 (0.16e0.78)
.91 .004
89 (74%) 81 (68%)
1.46 (0.65e3.26) 0.61 (0.30e125)
.35 .14
CI, confidence interval; HC, Hospital das Clínicas; OR, odds ratio. *Comparison of HCWs with confirmed pandemic influenza infection with asymptomatic HCWs. y Comparison of HCWs with confirmed pandemic influenza infection with HCWs with symptomatic influenza-negative infection. z Odds ratio calculated comparing the category “Physicians” with all other categories.
included. The control group included 102 HCW (1 confirmed case, a HCW who dispensed oseltamivir to outpatients, had no controls). Nine (17%) confirmed cases worked in specific influenza units; 4 worked in the emergency room. Table 1 compares confirmed cases with asymptomatic controls. Physician, male sex, comorbidities, work at another hospital, and contact with suspected/confirmed pandemic influenza infection at another hospital without respiratory protection were associated with confirmed cases. Contact with patients with suspected/ confirmed pandemic influenza infection at HC, contact with coworker or social contact with suspected/confirmed pandemic influenza infection, and use of public transport were more frequent among asymptomatic controls. Comparing confirmed cases with symptomatic influenzanegative cases, contact with suspected/confirmed pandemic influenza infection without respiratory protection at another hospital,
and contact with suspected/confirmed case at home were associated with acquiring 2009 H1N1 influenza (Table 1). Conjunctivitis was more frequent in confirmed cases, and sore throat and coryza were more frequent in influenza-negative cases. Forty-two (81%) confirmed cases and 89 (74%) influenza-negative cases received oseltamivir. Four confirmed cases were hospitalized, and 1 died. One symptomatic influenza-negative case was hospitalized, and no deaths occurred. None of the controls received oseltamivir, and none were hospitalized or died. Table 2 presents multivariate analysis. Comorbidities, male sex, being a physician, and contact with coworker or social contact with respiratory symptoms were significant. The pandemic caused widespread use of alcoholic solutions outside the hospital because of an unprecedented opportunity for education of the lay public, including government campaigns stimulating the use of alcohol hand rubs and cough etiquette. This
R.D. Lobo et al. / American Journal of Infection Control 41 (2013) 645-7 Table 2 Multivariate analysis of factors associated with acquiring confirmed pandemic influenza infection compared with asymptomatic controls among health care workers in Hospital das Clínicas, São Paulo, Brazil Variable Presence of comorbidities Male sex Being a physician Contact with coworker or social contact with respiratory symptoms
OR (95% CI) 19.05 5.11 8.58 0.11
(4.75e76.41) (1.80e14.46) (2.52e29.27) (0.04e0.29)
P value <.0001 .0021 .0006 <.0001
CI, confidence interval; OR, odds ratio.
may explain why, in our study, social contact and contact with coworker with respiratory symptoms was protective. However, contact with asymptomatic respiratory infection, including incubating influenza, could not be avoided unless HCWs took precautions during contact with all persons, which probably did not occur. It is possible that pandemic influenza was not acquired by the HCWs in the hospital but in the community from persons not clearly recognized as symptomatic. Perception of risk because of contact with symptomatic patients and a new virus, coupled with the administrative measures (rapid case identification/confirmation, influenza units, staff training), probably decreased HCW exposure to influenza patients. The high awareness level can be exemplified by increase in influenza vaccination coverage: 8,116 HCWs were vaccinated in 2009 compared with 22,333 HCWs in 2010 (A. M. Sartori, personal communication). Being a physician was a risk factor possibly because physicians frequently do not follow recommendations. A study on adherence to use of protective equipment against influenza included 292 HCWs and reported suboptimal adherence to personal protection equipment especially among physicians.4-7. Others examples not directly related to influenza, it has been observed that physicians present low compliance with guidelines on antibiotic prophylaxis and with the use of maximal barrier precautions and skin antisepsis of insertion site during CVC insertion. Another possibility is that physicians were exposed to more aerosol generating procedures. Unfortunately, adherence to infection control protocols was not monitored. Comorbidities have been described in patients with severe influenza.6,8,9 Our study involved mostly mild cases. In this outpatient population, comorbidities were significantly associated with acquiring symptomatic pandemic influenza. Most frequent conditions were smoking, obesity, chronic cardiopathy, pneumopathy, and hypertension. To our knowledge, this is the first study to determine factors associated with acquiring nonsevere influenza. It is difficult to explain why being male was a risk factor. We hypothesized there may have been a bias in control selection; however, among controls, 21% were male, and, based on our human resource department, the expected proportion was 24.5%,
647
suggesting no bias. In the community, during the influenza pandemic, men were less adherent to protective measures such as handwashing and cough etiquette.10 These sex differences may have occurred also among HCWs. Comparing both groups of symptomatic HCWs, there were minor differences in clinical presentation. It was difficult to distinguish between influenza and other respiratory infections. Unfortunately, the etiology of noninfluenza respiratory diseases was not investigated. Hospitalizations and death only occurred in pandemic influenza cases, suggesting that it was more severe. Evaluation for factors associated with confirmed cases was not conclusive. Acknowledgment The authors thank Núcleo de Informações em Saúde (NIS), Serviço médico dos funcionários (SAME), and Monique Perret Gentil. References 1. Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasil. (homepage on the Internet). Boletim eletrônico Epidemiológico (updated March 2010). Available from: http://portal.saude.gov.br/portal/arquivos/pdf/boletim_eletro nico_influenza_25_03.pdf. Accessed April 15, 2010. 2. Mota NV, Lobo RD, Toscano CM, Pedroso de Lima AC, Souza Dias MB, Komagata H, et al. Cost-effectiveness of sick leave policies for health care workers with influenza-like illness, Brazil. Emerg Infect Dis 2011 2009;17: 1421-9. 3. World Health Organization Collaborating Centre for influenza. CDC protocol of realtime RTPCR for influenza A(H1N1) revision 2 (6 October 2009). Available from: http://www.who.int/csr/resources/publications/swineflu/realtimeptpcr/ en/index.html. Accessed December 13, 2010. 4. Daugherty EL, Perl TM, Needham DM, Rubinson L, Bilderback A, Rand CS. The use of personal protective equipment for control of influenza among critical care clinicians: a survey study. Crit Care Med 2009;37:1210-6. 5. Bedouch P, Labarère J, Chirpaz E, Allenet B, Lepape A, Fourny M, et al. Compliance with guidelines on antibiotic prophylaxis in total hip replacement surgery: results of a retrospective study of 416 patients in a teaching hospital. Infect Control Hosp Epidemiol 2004;25:302-7. 6. Rubinson L, Wu AW, Haponik EE, Diette GB. Why is it that internists do not follow guidelines for preventing intravascular catheter infections? Infect Control Hosp Epidemiol 2005;26:525-33. 7. Lobo RD, Levin AS, Oliveira MS, Gomes LM, Gobara S, Park M, et al. Evaluation of interventions to reduce catheter-associated bloodstream infection: continuous tailored education versus one basic lecture. Am J Infect Control 2010;38:440-8. 8. Centro de Vigilância Epidemiológica Alexandre Vranjac. Secretaria Estadual da Saúde de São Paulo. (homepage on the Internet). Influenza pandêmica A (H1N1) 2009: (updated 2010; cited February 18, 2010). Available from: ftp://ftp.cve. saude.sp.gov.br/doc_tec/RESP/nt10_influ_atualfev.pdf. Accessed February 18, 2010. 9. Yu H, Feng Z, Uyeki TM, Liao Q, Zhou L, Feng L, et al. Risk factors for severe illness with 2009 pandemic influenza A (H1N1) virus infection in China. 2011;52:457e465. 10. Simonsen KA, Hunskaar S, Wensaas KA, Rørtveit S, Cox R, Njølstad G, et al. Influenza-like illness in Norway: clinical course, attitudes towards vaccination and preventive measures during the 2009 pandemic. Fam Pract 2012;29: 139-46.