Concise Communication

Outbreaks of Influenza A Among Nonvaccinated Healthcare Workers: Implications for Resource-Limited Settings

Anucha Apisarnthanarak, MD; Pilaipan Puthavathana, PhD; Rungrueng Kitphati, MD; Prasert Auewarakul, MD, PhD; Linda M. Mundy, MD  

From the Division of Infectious Diseases, Thammasart University Hospital, Pratumthani (A.A.), the Division of Microbiology, Siriraj Hospital, Bangkok (P.P., P.A.), and the Department of Science, Thai National Institute of Health, Nonthaburi (R.K.), Thailand; and the St. Louis University School of Public Health, St. Louis, Missouri (L.M.M.).

We identified 3 outbreaks of influenza A (attack rates, 18%–24%) among Thai healthcare workers in intensive care units. All outbreaks were epidemiologically linked to an index patient with pneumonia due to influenza A virus (subtype H3N2). The investigations of these outbreaks incurred costs that exceeded the estimated costs of healthcare worker influenza vaccination by more than 10-fold.

Received October 4, 2007; accepted February 16, 2008; electronically published July 14, 2008.

Influenza outbreaks have predominantly been reported among elderly patients who were in long-term care and among high-risk patients from spatially contained units, such as the transplantation, oncology, neonatology, and pediatric intensive care units.1-3 In these settings, dynamic viral transmission and location of vulnerable patients in close proximity led to recognized influenza outbreaks and allowed for effective intervention strategies. Additionally, prompt case identification and healthcare worker (HCW) vaccination programs are critical components of effective influenza prevention and control programs.4-5 In resource-limited settings, an infrastructure that allows for an annual HCW influenza vaccination program may not exist. We conducted a study to evaluate the costs and benefits of influenza prevention and control strategies among HCWs in 3 intensive care units (ICUs) at a Thai tertiary care hospital during 3 influenza seasons.

Methods

 

Study population, design, and definitions.

Thammasat University Hospital, located in central Thailand, annually employed 30 HCWs in the medical ICU, 25 HCWs in the surgical ICU, and 22 HCWs in the coronary care unit; each ICU was an 8-bed unit, and annual influenza vaccination was not routinely available for HCWs. Standard infection control practices for influenza included droplet and contact precautions for identified case patients, furlough for ill HCWs, limited transport of infected patients, discouragement of visitors for infected patients, and reinforcement of standard hand hygiene practices. Any case of influenza suspected in an HCW was confirmed by laboratory tests or by epidemiological linkage to an infected ICU patient. Healthcare-associated influenza in an HCW or an inpatient was considered present if there were 1 or more confirmatory laboratory test results after exposure to either an ICU patient or HCW who had influenza. An HCW who had an epidemiologically linked case of influenza infection was defined as one who did not undergo definitive laboratory testing for influenza, but who had signs or symptoms of influenza-like illness after contact with an index patient and/or other HCWs who had influenza. All ICU patients were investigated with regard to horizontal transmission by use of rapid tests and viral cultures on days 3, 5, and 7 after the index case identification.

Data collection and analysis.

Demographic, clinical, laboratory, and cost data were collected for influenza surveillance and for the outbreak investigations of patients and HCWs in the 3 ICUs from January 1, 2004, through December 31, 2006. Direct costs were estimated for influenza surveillance, infection control, the outbreak investigation, the antiviral prophylaxis and influenza vaccination of HCWs, and the occupational health program. Costs, rather than charges, were used as a representation of the costs for the institution that was undertaking the outbreak investigation. Hospital and occupational health program costs were estimated on the basis of the Thai insurance systems and the hospital's reimbursement system. For HCWs and ICU patients who had influenza A, costs that were calculated for rapid tests, molecular tests, and nasopharyngeal and tracheal aspirate cultures included all related materials, technician time, specimen transport to the reference viral laboratory center, and institutional overhead. All costs were converted from Thai baht currency to US dollars (40 baht = 1 US dollar). The costs of patient isolation, materials (ie, gloves, gowns, and surgical masks), and the time and effort used by HCWs to comply with these measures were calculated from prior cost estimates.5-6 The institutional review board at Thammarsart University Hospital approved this study prior to study initiation.

Diagnostic virologic testing.

On January 1, 2004, routine screening for influenza A began for all patients who were admitted to the 3 ICUs because of community-acquired or hospital-acquired pneumonia.4 Tracheal aspirate and nasopharyngeal swab specimens were obtained from patients and HCWs, respectively, for influenza rapid tests (SD Bioline Influenza Antigen A/B; MT Promedt Consulting), reverse-transcription polymerase chain reaction (PCR), and viral culture. All specimens were transported on frozen CO2 to the Thai National Institute of Health (Nonthaburi, Thailand). For direct typing and subtyping of influenza virus, RNA was extracted from clinical specimens with the QIAmp Viral RNA Minikit (Qiagen) and was analyzed with multiplex reverse-transcription PCR.7 Viral cultures were performed by incubation of samples in Madin-Darby canine kidney cell monolayers; antigenic typing and subtyping of influenza virus isolates were performed by hemagglutination inhibition.4

Results

 

During the 36-month study period, there were 3 distinct outbreaks of infection with influenza A virus subtype H3N2, 1 in each ICU. Outbreak 1, in April 2005, occurred in the medical ICU and involved 7 HCWs. Outbreak 2, in December 2005, occurred in the coronary care unit and involved 4 HCWs. Outbreak 3, in July 2006, occurred in the surgical ICU and involved 6 HCWs (Table). For each outbreak, the HCW attack rate ranged from 18% to 24%; each outbreak occurred after HCW exposure to the respective index patient infected with influenza A (H3N2) virus. There was a median of 3 days of exposure (range, 2–5 days) between the identification of the index patient and the identification of the infected HCWs, and all cultures of samples obtained from HCWs yielded influenza A (H3N2) virus. No HCW reported recent exposure (ie, within the past 2 weeks) to family members or friends with an influenza-like illness, and all HCWs who had influenza were furloughed from work.

Table 1. 
Table 1.  Nosocomial Influenza A Virus Infection and Outbreaks Among Healthcare Workers (HCWs) in 3 Intensive Care Units of a Thai Tertiary Care Hospital During the 2004–2006 Influenza Seasons

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All relevant hospital personnel (eg, hospital staff, bed and nursing management, clinical, and other supportive service personnel) were informed about the outbreak; the remaining HCWs in the ICU received an influenza vaccine (Fluarix; GlaxoSmithKline) and were observed for 2 weeks for fever and influenza-like illness. In each outbreak, the infection control team was notified within 1 day of the identification of the index patient. Each influenza outbreak was extinguished within 2 days (range, 1–2 days) after the notification of the infection control team (Figure).

Figure.  Epidemic curves for outbreaks of influenza A virus infection among healthcare workers and at-risk intensive care unit patients in a medical intensive care unit (A), a coronary care unit (B), and a surgical intensive care unit (C) in a Thai medical center. IC, infection control.

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Antiviral prophylaxis was administered to all remaining inpatients. The investigation of potential secondary horizontal influenza transmission led to the identification of 1 patient (1 [12.5%] of 8) with nosocomial influenza A during outbreak 1; 1 patient (1 [12.5%] of 8) during outbreak 2; and 1 patient (1 [12.5%] of 8) during outbreak 3. All 3 cases of hospital-acquired influenza occurred in patients who were located in close proximity (ie, in the next bed) to the ICU index patient, who had rapid test results and viral cultures negative for influenza A (H3N2) virus on admission, and who had subsequent rapid test results and viral cultures positive for the virus within a median of 2 days (range, 2–3 days) after the identification of the index patient. During the 36-month period when these 3 influenza outbreaks among HCWs occurred, there were 15 patients with influenza who were admitted to the ICUs, and an additional 30 HCWs from these ICUs acquired influenza A infection during the nonoutbreak periods (Table). Notably, there were no seasonal patterns associated with these influenza outbreaks.

The mean estimated costs were $2,710 (range, $2,245–$3,321) per outbreak investigation and $256 (range, $220–$330) for the annual influenza vaccination of all 77 ICU HCWs (Table). The benefits of influenza vaccination of these ICU HCWs include the reduced risk of influenza infection, the minimization of risk for influenza transmission to at-risk ICU patients, and the cost savings, in comparison with the costs of redirected infection control measures and HCW furloughs.

Discussion

 

Although occupational health programs in developing countries seem long overdue, understanding how to best prioritize HCW protection with resource-limited healthcare delivery systems remains a challenge. Although a panoply of interventions have been recommended to prevent and control the spread of influenza in healthcare settings,8-10 translating these recommendations into practice in resource-limited settings requires prioritizing the use of the existing infrastructure and available resources. Our findings revealed influenza A attack rates above 10% among unvaccinated HCWs, despite compliance with infection control measures.8 Although influenza outbreaks in spatially confined units have been reported worldwide, along with estimates for excess costs of care,11-13 our data provide additional evidence for the incorporation of annual influenza vaccination into ICU occupational health programs. Notably, all at-risk ICU HCWs in our study agreed to influenza vaccination. This level of compliance may not be generalizable to nonoutbreak situations or other geographic areas, but these findings suggest the potential benefits of focused education concerning the impact of vaccination on the safety of HCWs and the added protection for at-risk patients.

Influenza infection occurs year round in tropical countries.14 Given the potential threat for the emergence of pandemic influenza in southeast Asia, these 3 outbreaks of influenza A (H3N2) infection among unvaccinated HCWs highlight the relevance of vaccines in the promotion of global standards for occupational health. Additionally, the outbreak investigations incurred costs more than 10-fold higher than the estimated costs of HCW vaccination.5 Although indirect costs related to increased hospitalization among inpatients were not included, our estimates suggest that there is a fiscal benefit to annual influenza HCW vaccination, along with additional protection of at-risk ICU patients from influenza A infection.

Acknowledgments

 

Financial support. The study was supported by the National Center and Genetic Engineering and Biotechnology, the National Science and Technology Development Agency (grant BT-B-01-MG-13-5019 to A.A.), and the Thai Research Fund.

Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.

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  • Address reprint requests to Anucha Apisarnthanarak, MD, Division of Infectious Diseases, Thammasart University Hospital, Pratumthani, Thailand, 12120 ().

© 2008 by The Society for Healthcare Epidemiology of America. All rights reserved.