2
Understanding the Risk to Healthcare Personnel

Interest in the transmission of influenza viruses has increased in recent years due to the ongoing zoonotic infection of humans with avian H5N1 influenza viruses and the pandemic spread of a swine-like H1N1 strain in 2009. In particular, the recognition that person-to-person transmission is a major criterion that must be met for pandemic infection has stimulated research into the mechanisms by which influenza viruses are transmitted and what factors enhance or interfere with this transmission. In considering preventive efforts to avoid viral respiratory disease transmission, the committee emphasizes the importance of the use of a range of hazard controls, including vaccination, to protect healthcare personnel.

This chapter provides a synopsis of the discussion in the 2008 report regarding influenza transmission followed by an overview of recent (2007 to mid-2010) research on viral respiratory disease transmission. Studies on personal protective equipment (PPE) use to prevent viral respiratory disease transmission are also reviewed. The chapter concludes with the committee’s thoughts on immediate research needs and long-term research opportunities.

BACKGROUND AND CONTEXT FROM THE 2008 REPORT

The prior Institute of Medicine report examined research studies conducted through 2007 on the modes of influenza transmission and highlighted the paucity of data on the relative contributions of each to the risk of illness in the community or clinical setting. A major challenge in research on this issue has been the lack of consistency in the use of terms



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2 Understanding the Risk to Healthcare Personnel Interest in the transmission of influenza viruses has increased in re- cent years due to the ongoing zoonotic infection of humans with avian H5N1 influenza viruses and the pandemic spread of a swine-like H1N1 strain in 2009. In particular, the recognition that person-to-person trans- mission is a major criterion that must be met for pandemic infection has stimulated research into the mechanisms by which influenza viruses are transmitted and what factors enhance or interfere with this transmission. In considering preventive efforts to avoid viral respiratory disease trans- mission, the committee emphasizes the importance of the use of a range of hazard controls, including vaccination, to protect healthcare personnel. This chapter provides a synopsis of the discussion in the 2008 report regarding influenza transmission followed by an overview of recent (2007 to mid-2010) research on viral respiratory disease transmission. Studies on personal protective equipment (PPE) use to prevent viral res- piratory disease transmission are also reviewed. The chapter concludes with the committee’s thoughts on immediate research needs and long- term research opportunities. BACKGROUND AND CONTEXT FROM THE 2008 REPORT The prior Institute of Medicine report examined research studies con- ducted through 2007 on the modes of influenza transmission and high- lighted the paucity of data on the relative contributions of each to the risk of illness in the community or clinical setting. A major challenge in re- search on this issue has been the lack of consistency in the use of terms 29

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30 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL to describe particle size and to describe potential transmission routes (Box 2-1). As research efforts move forward, agreement is needed on terminology to be used so that studies can be compared. Box 2-1 provides the definitions used by the committee throughout the report, including in describing earlier studies. The terms and definitions of the transmission routes were developed at a recent Centers for Disease Control and Preven- tion (CDC) workshop (David Weissman, personal communication, CDC, November 2010) and are provided as a starting point. These are operational BOX 2-1 Terminology—Particle Size and Transmission Routes As noted above, the terms and definitions here are used to frame the dis- cussion, and efforts are needed to reach consensus agreement among the many relevant areas of research and clinical care. Particle Size: • Respirable particles—particles with da ≤ 10 μm that can be inhaled and penetrate to the alveolar region; although a substantial fraction deposit in the alveolar region, they deposit throughout the respiratory tract. These are the equivalent of “droplet nuclei.” • Inspirable particles—particles with 10 μm ≤ da ≤ 100 μm, which can be inhaled but cannot penetrate to the alveolar region; nearly all de- posit in the head airways region. Transmission Routes: • Contact transmission: o Direct contact transmission occurs when the virus is transferred by contact from an infected person to another person without a contaminated intermediate object. o Indirect contact transmission involves the transfer of viral agents by contact with a contaminated intermediate object. • Droplet spray transmission: Person-to-person transmission of the vi- rus through the air by droplet sprays. A key feature is deposition by impaction on exposed mucous membranes. • Aerosol transmission: Person-to-person transmission of influenza or other respiratory viruses through the air by aerosols in the inspirable (inhalable) size range or smaller. Particles are small enough to be inhaled into the oronasopharynx and distally into the trachea and lung. NOTE: da = aerodynamic diameter. Terminology regarding particles with da > 100 μm is needed. SOURCES: Nicas and Jones (2009); Personal communication, D. Weissman, November 2010.

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31 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL definitions and are not CDC policy. The definitions of particle size are adapted from a set of definitions described by Nicas and Jones (2009). Further work is needed on standardization of terminology. A common set of definitions accepted by the industrial hygiene, infectious disease, and healthcare communities would be most helpful in discussing future re- search and policy. Much of the discussion regarding influenza transmission has focused on the continuum between droplet spray and aerosol transmission, as well as on the role of contact transmission and the potential for transmis- sion through inoculation of the conjunctivae. Aerosol transmission, an issue in healthcare settings where patients have diseases such as tubercu- losis and measles, can occur at a short range between persons but can also involve infectious agents carried for longer distances by air currents. Fabian and colleagues (2008) collected exhaled breath of patients with active influenza. In 4 of 12 subjects, exhaled breath contained influenza, and more than 87 percent of exhaled particles were < 1 µm. One of the main reasons why there is no clear understanding of long- range transmission is because aerosol transmission of influenza and other respiratory viruses is difficult to study in human populations. To study long-range aerosol transmission properly, the background prevalence of the disease would need to be low in the community, and many other fac- tors would need to be controlled to rule out other transmission routes, such as droplet spray and contact (Tellier, 2009). Production of aerosols also varies by individual; some individuals produce large amounts of bioaerosols in coughs, sneezes, and even tidal breathing, while others do not. Therefore, some individuals may be more or less likely to transmit influenza infection or other viral respiratory diseases via aerosols. Context is likely to play an important role in shaping the importance of these transmission pathways in relation to illness occurrence. Re- searchers have shown that contextual factors may include environment, humidity, temperature, number and types of fomites, air flow, age of sus- ceptible and infected populations, and number of individuals and their interactions within space. Biological factors that may influence transmis- sion include virus strain characteristics, human physiology, immune sta- tus, and genetic susceptibility of the host. Modifications to the living environment have the potential to reduce the transmission of influenza virus or other respiratory viral agents. These modifications include increasing the rate of air exchange, using non-recirculated air, irradiating air prior to recirculation, and changing absolute humidity (Lowen et al., 2007; Shaman et al., 2010). Increased

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32 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL air exchange is expected to affect transmission by an aerosol route through a reduction in the concentration of infectious particles in the air. Because both temperature and humidity are known to impact the stability of influenza viruses in an aerosol (Harper, 1961, 1963; Hemmes et al., 1960; Schaffer et al., 1976), interventions to reduce transmission by al- tering these environmental conditions may be useful. Influenza A transmission has been studied in various animal species— including mice, guinea pigs, monkeys, and ferrets—with variable results. These studies show that animals develop influenza infection, and most demonstrate the possible role of aerosol transmission. Experiments per- formed in the 1930s demonstrated that influenza virus–naïve, asympto- matic ferrets that were caged with influenza virus–infected ferrets would subsequently develop disease and that, even in the absence of experimen- tal infection, ferrets occasionally displayed an influenza-like illness, after which they became immune to subsequent virus inoculation (Francis and Magill, 1935; Smith et al., 1933). Andrewes and Glover (1941) demon- strated transmission using an experimental design in which air flowed from infected to naïve ferrets through a tube containing S- and U-shaped bends, which would be expected to allow the transfer of only small (< 5 μm) respirable particles. In hamsters, by contrast, transmission of influenza viruses appeared to depend on contact between infected and ex- posed animals (Ali et al., 1982). A series of experiments with mice in the 1960s also provided some evidence suggesting aerosol transmission (Schulman, 1968; Schulman and Kilbourne, 1962). More recently, the gui- nea pig has been successfully used to study influenza transmission (Lowen et al., 2006). Transmission among humans has been studied less. Early volunteer studies found that infection via inhalation of respirable particles requires considerably less virus than infection via droplets placed on the nasal membranes (Alford et al., 1966; Couch et al., 1971, 1974; Douglas, 1975). Several observational studies of naturally occurring influenza provided insights into the challenges of studying transmission modes. One of the most well-known incidents of an influenza A outbreak hap- pened among passengers on a grounded airplane (Gregg, 1980; Moser et al., 1979). An observational study of 49 passengers delayed on a 737 jet for 3 hours and exposed to an index case with influenza suggested aero- sol transmission. Within 72 hours, 72 percent of the passengers became ill. Specimens from 31 of the 38 cases were cultured and found to have similar isolates. A second airline travel–associated outbreak also sug- gested aerosol transmission with a 37 percent attack rate and wide seat-

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33 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL ing distribution of secondary cases throughout the aircraft (Klontz et al., 1989). More recent studies of airline travel indicate close-proximity transmission (Baker et al., 2010; Han et al., 2009; Ooi et al., 2010), which could occur via one or more routes. Newer airplanes have more laminar air flow and improved filters over older planes, which may re- duce long-range aerosol transmission. Studies examining how air flow may help prevent transmission of viral respiratory diseases in closed and crowded settings, such as an airplane, are warranted. Wong and colleagues (2010) recently reported a nosocomial out- break of seasonal influenza in an acute-ward setting that appeared to be attributed to aerosol transmission. An aerosol-generating device was used on the influenza index case patient. At the same time, the authors identified an imbalance in the indoor airflow that likely created a direc- tional dispersion of air and potentially carried influenza aerosols to other areas of the ward. Other patients were infected following a temporal and spatial pattern of air flow originating from the index patient. Two of the staff also became ill even though they were required to adhere to strict hand hygiene and medical mask use. Additional observational studies of human influenza have provided further descriptions of influenza outbreaks, but the findings do not clarify potential mechanisms of transmission (discussed in IOM, 2008). For ex- ample, Drinka and colleagues (1996, 2004) compared influenza rates in several buildings of a long-term care facility during several seasons of influenza. Their initial study found that persons working in buildings with ventilation systems that provided outside air had much lower infec- tion rates than those working in buildings with partially recirculated air (Drinka et al., 1996). However, an update of this study found similar in- fection rates (Drinka et al., 2004). Reviews of other reported influenza outbreaks suggest droplet spray and contact transmission routes based on temporal and spatial patterns (Brankston et al., 2007; Cunney et al., 2000; Drinka et al., 1996; Morens and Rash, 1995). Studies of the clinical effectiveness of PPE have had mixed results in preventing severe acute respiratory syndrome (SARS) or respiratory syn- cytial virus (RSV) infections (see Appendix C). Challenges in studies of this type include difficulties in retrospectively separating the effects of PPE from the effects of other infection control measures. Specific issues regarding respiratory disease transmission to health- care personnel have focused on medical procedures that have a potential for creating aerosols, and data are primarily available for SARS, not in- fluenza. Fowler and colleagues (2004) observed a greater risk of devel-

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34 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL oping SARS for physicians and nurses performing endotracheal intuba- tion. Similarly, in a retrospective study of 43 nurses who worked in To- ronto with SARS patients, Loeb and colleagues (2004) found that assisting during intubation, suctioning before intubation, and manipulat- ing the oxygen mask were high-risk activities for acquiring SARS; wear- ing a face mask or N95 respirator was protective. As stated throughout the 2008 report, establishing how influenza is transmitted and understanding the contribution of each mode of trans- mission is critical to preventing its spread and reducing morbidity and mortality due to influenza infection, especially in healthcare settings. The 2008 report outlined a number of questions that remained to be addressed regarding influenza transmission (IOM, 2008): • Questions regarding transmission mode, including: What are the major modes of transmission? How much does each mode of transmission contribute individually or with other modes of transmission? What is the size distribution of particles expelled by infectious individuals, and how does that continuum of sizes affect transmission? Is the virus viable and infectious on fomites, and for how long? Are fomites a means of transmission, and are some more able to transmit than others? • Questions regarding infectivity, including: Can infection take place through mucous membranes or conjunctiva exposure? What is the time sequence of infectivity? • Questions specific to transmission in healthcare settings, includ- ing: What activities in the healthcare setting are associated with minimal or increased transmission? How distinct is transmission in different venues including health care, schools, and house- holds? • Questions specific to the role of PPE in preventing or reducing transmission, including: How effective is each type of PPE in reducing the risk of influenza transmission? How effective are face masks? What innovations regarding PPE are needed to en- hance effectiveness? What is the impact on transmission risk when patients wear face masks? • Questions specific to other potential forms of prevention, includ- ing: What is the role of ultraviolet (UV) light, humidity, temper- ature, pressure differentials, air flow and exchange, and ventilation in preventing transmission?

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35 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL The 2008 report concluded its discussion regarding research on in- fluenza transmission with a recommendation that a Global Influenza Re- search Network should be initiated and supported. This network would facilitate an understanding of the transmission and prevention of seasonal and pandemic influenza, with priority funding given to short-term clini- cal and laboratory studies. Furthermore, the recommendation stressed the need to develop rigorous, evidence-based research protocols and imple- mentation plans for clinical studies for use during an influenza pandemic (IOM, 2008). UPDATE ON RECENT RESEARCH In the 3 years since the writing of the prior report (IOM, 2008), re- search efforts continue to examine the various routes of transmission and explore approaches to preventing transmission. The following section provides an overview of recent research (2007 to mid-2010) and de- scribes animal studies, environmental monitoring and persistence studies, transmission modeling studies, and human studies. The literature searches on disease transmission conducted by the committee focused on influenza. Searches of bibliographic databases for studies on PPE use and transmission were broader and incorporated other viral respiratory diseases; only a few recent studies on other viral respiratory diseases were identified, however, and those are discussed and referenced in this report. Animal Studies Animal models complement epidemiological approaches by allowing the examination of influenza virus transmission from an infected to a susceptible host under well-controlled conditions. The ferret and guinea pig models are the current models of choice in influenza studies. Ferrets are naturally susceptible to infection with human influenza viruses, and these viruses transmit among them, making the ferret the current gold- standard animal model for the study of influenza. Prompted by the need for a more convenient animal model than the ferret in which to study transmission, the guinea pig was recently developed as such a model host (Lowen et al., 2006). Although signs of disease are generally not ob- served in influenza virus–infected guinea pigs, these animals are highly

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36 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL susceptible to infection with human strains, and human influenza viruses transmit efficiently from one guinea pig to another. Animal Models on Modes of Transmission The relative contributions of the various modes by which influenza viruses transmit is currently a subject of debate in the field. In the context of experimental studies using animals, transmission by the contact route is normally modeled by placing infected and naïve animals into the same cage together. It is important to note, however, that this set-up does not allow one to distinguish transmission by a contact route from short-range spread mediated by an aerosol. To study transmission specifically by in- spirable or respirable aerosols, animals are placed into separate cages so that air exchange can occur among them, but they cannot touch. Although this arrangement rules out contact-based transmission, when cages are placed in close proximity (as is usually the case), transmission may pro- ceed via the droplet spray or aerosol modes. Transmission of human seasonal and 2009 H1N1 pandemic strains among either ferrets or guinea pigs occurs efficiently using both experi- mental designs, indicating that transmission among ferrets and guinea pigs can proceed in the absence of direct or indirect contact among ani- mals (recent studies include Lowen et al., 2006, 2007, 2008; Maines et al., 2009; Munster et al., 2009; Steel et al., 2010; Tumpey et al., 2007). In addition, evidence for transmission of influenza viruses by the aerosol route has been obtained in the ferret and guinea pig models; early work in ferrets (Andrewes and Glover, 1941) and recent experiments per- formed in guinea pigs (Mubareka et al., 2009) demonstrate transmission over a distance of up to 3.5 feet. Recent attempts to model influenza virus transmission in BALB/c mice have been unsuccessful (Lowen et al., 2006); nevertheless, a mouse model was used by Schulman and Kilbourne to study transmission in the 1960s (Schulman, 1968; Schulman and Kilbourne, 1962). Because of the inefficiency of transmission and the low susceptibility of mice to human influenza viruses that have not been serially adapted in this host, current- ly the mouse model is not used widely for research on influenza virus transmission. Hamsters are also not in widespread use as a model for in- fluenza virus infection, but Ali and colleagues (1982) showed that certain human influenza isolates transmitted well when infected and naïve ham-

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37 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL sters were housed in the same cage; transmission in the absence of con- tact was not, however, observed. The potential for contact with contaminated surfaces to mediate in- fluenza virus transmission among guinea pigs was examined by Mubareka and colleagues (2009). Naïve guinea pigs were placed in cages that either had previously housed an acutely infected animal or had been contami- nated with high titers of influenza virus through direct application onto non-porous cage surfaces. In the former case, approximately 20 percent of exposed animals contracted infection, while with the latter design, no exposed animals became infected (Mubareka et al., 2009). When these results are compared to the high efficiency of transmission of the same virus by the aerosol route, they suggest that—at least in the guinea pig model—spread via fomites makes a minor contribution to the overall transmission of influenza viruses. Relationships Between Transmission and Symptoms, Timing Post-Infection, and Shedding Titers Because of their potential to produce infectious aerosols, coughing and sneezing are generally thought to promote transmission (Tumpey et al., 2007). Evidence against a critical role for sneezing and coughing arises from the guinea pig model: Although these animals do not sneeze or cough following influenza virus infection, viral spread is efficient among guinea pigs (Lowen et al., 2007). Influenza viruses have been isolated from the air surrounding infected guinea pigs (Mubareka et al., 2009) and even mice (Schulman, 1967); this virus is most likely expelled into the environment through normal breathing (Fabian et al., 2008). The timing of transmission events relative to initial infection of do- nor animals has not been examined closely (through the use of defined exposure periods) in the ferret or guinea pig models; the serial collection of nasal wash samples over the course of exposure does, however, allow an estimate of the time of transmission to be made. In the guinea pig model after exposure by contact and aerosol routes, virus was detected initially in the nasal washings of exposed animals at 1–3 days and 3–5 days, respectively (Lowen et al., 2006, 2007, 2008, 2009; Steel et al., 2009). The infection of exposed ferrets occurs with similar timing by contact and aerosol routes: Initial detection of virus in the nasal passages of exposed animals usually occurs between 1 and 3 days post-exposure (Itoh et al., 2009; Maines et al., 2006, 2009; Tumpey et al., 2007). Varia-

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38 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL tions in transmissibility among differing strains of influenza viruses do not show a strong correlation with differences in peak shedding titers (Maines et al., 2006, 2009; Mubareka et al., 2009; Steel et al., 2009; Tumpey et al., 2007), suggesting that, although efficient growth in the upper respiratory tract is most likely required for an influenza virus to transmit, additional criteria must be met for transmission to proceed. Relative Transmissibility of Influenza Viruses Derived from Different Host Species Viral strain and subtype specific differences in influenza virus transmission have been observed in recent studies of animal models. One strength of both the ferret and guinea pig models is that influenza viruses adapted to human hosts generally transmit more efficiently than avian-, swine-, or mouse-adapted strains. Thus, the low pathogenic avian strains A/duck/Alberta/35/1976 (H1N1) and A/duck/Ukraine/1963 (H3N8) did not transmit among guinea pigs, while certain highly pathogenic H5N1 influenza viruses have been observed to transmit among co-caged guinea pigs to a limited extent (Gao et al., 2009; Steel et al., 2009). Swine in- fluenza isolates of the H3 subtypes transmitted with 25 percent efficiency by the aerosol route among guinea pigs (Steel et al., 2010). By contrast, human H3N2 subtype viruses, as well as the H1N1 pandemic strain, gen- erally transmit to all exposed guinea pigs by either contact or aerosol routes (Lowen et al., 2006; Steel et al., 2010). Overall, seasonal H1N1 subtype viruses have been found to transmit less efficiently among gui- nea pigs than epidemic strains of the H3N2 subtype (Mubareka et al., 2009). A similar pattern of transmissibility is observed in the ferret mod- el: Avian influenza viruses do not transmit to exposed animals by an aerosol route (Tumpey et al., 2007; Van Hoeven et al., 2009), but some low and highly pathogenic strains do transmit by contact to a limited ex- tent (Belser et al., 2008; Maines et al., 2006; Sorrell et al., 2009; Van Hoeven et al., 2009; Wan et al., 2008). Human seasonal strains of both H3N2 and H1N1 subtypes transmit readily among ferrets (Itoh et al., 2009; Maines et al., 2006, 2009; Wan et al., 2008), and the pandemic H1N1 strain has been observed to transmit with similar efficiency (Itoh et al., 2009; Munster et al., 2009) or somewhat lower efficiency (Maines et al., 2009) by an aerosol route than seasonal influenza viruses.

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39 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL Interventions: Blocking Influenza Virus Transmission in Animal Models Interventions that offer the potential to limit transmission of influen- za viruses in healthcare settings include vaccination; the prophylactic and therapeutic use of antiviral drugs; non-pharmaceutical interventions, such as the use of good hand hygiene and PPE; use of source control; cohort- ing the patients; and modifications to the indoor environment. Changes in transmission achieved through vaccination were studied in the guinea pig model, and it was found that transmission could be abrogated through vaccination. This was the case whether the vaccinated animals were the donors or recipients in the transmission experiment. Vaccination was particularly effective in blocking spread if sterilizing immunity was achieved (as was seen using a live attenuated vaccine), but transmission was also reduced following suboptimal vaccination 1 (Lowen et al., 2009). Also in guinea pigs, twice-daily treatment with oseltamivir re- duced titers shed from the upper respiratory tract of treated donor guinea pigs and, in turn, prevented transmission to untreated aerosol contacts. This is similar to recent and past studies of prophylactic treatment of household contacts of infected persons that has been found to be very effective (Halloran et al., 2007; Hayden et al., 2000, 2004; Monto et al., 2002; Welliver et al., 2001). Research in the past several years has demonstrated in the guinea pig model that transmission between animals in separate cages occurs with lower frequency (or not at all) when the surrounding air is warm (30°C) or maintained at high (80 percent) or intermediate (50 percent) relative humidities (Lowen et al., 2007, 2008). Although field studies are re- quired to translate these findings to the human situation, they suggest that the modification of relative humidity in healthcare settings may be a means of controlling the spread of influenza virus infection. The impact of UV treatment of air on influenza viral spread has not been assessed in an animal model; if transmission proceeds at least in part by an aerosol route, however, such treatment is expected to be effective. 1 The authors describe suboptimal vaccines as those that may provide only partial pro- tection against the disease but are effective at limiting transmission (Lowen et al., 2009).

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60 PERSONAL PROTECTIVE EQUIPMENT FOR HEALTHCARE PERSONNEL needed. Studies should examine whether antiviral-coated PPE provides any additional protection and how maintenance and reuse are affected. RECOMMENDATIONS Recommendation: Develop Standardized Terms and Definitions CDC and the Occupational Safety and Health Administra- tion, in partnership with other relevant agencies and organi- zations, should work to develop standardized terms, def- initions, and appropriate classifications to describe transmis- sion routes and aerodynamic diameter of particles associated with viral respiratory disease transmission. This effort should involve a consensus from the industrial hygiene, infectious dis- ease, and healthcare communities. Recommendation: Develop and Implement a Comprehensive Research Strategy to Understand Viral Respiratory Disease Transmission The National Institutes of Health, in collaboration with other research agencies and organizations, should develop and fund a comprehensive research strategy to improve the un- derstanding of viral respiratory disease transmission, includ- ing, but not limited to, examining the characteristics of influenza transmission, animal models, human challenge stud- ies, and intervention trials. This strategy should include • an expedited mechanism for funding these types of studies and • clinical research centers of excellence for studying in- fluenza and other respiratory virus transmission. REFERENCES Aiello, A. E., R. M. Coulborn, V. Perez, and E. L. Larson. 2008. Effect of hand hygiene on infectious disease risk in the community setting: A meta- analysis. American Journal of Public Health 98(8):1372-1381. Aiello, A. E., G. F. Murray, V. Perez, R. M. Coulborn, B. M. Davis, M. Uddin, D. K. Shay, S. H. Waterman, and A. S. Monto. 2010. Mask use, hand hygiene, and seasonal influenza-like illness among young adults: A

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61 UNDERSTANDING THE RISK TO HEALTHCARE PERSONNEL randomized intervention trial. Journal of Infectious Diseases 201(4):491- 498. Al-Asmary, S., A. S. Al-Shehri, A. Abou-Zeid, M. Abdel-Fattah, T. Hifnawy, and T. El-Said. 2007. Acute respiratory tract infections among Hajj medical mission personnel, Saudi Arabia. International Journal of Infectious Diseases 11(3):268-272. Alford, R. H., J. A. Kasel, P. J. Gerone, and V. Knight. 1966. Human influenza resulting from aerosol inhalation. Proceedings of the Society for Experimental Biology and Medicine 122(3):800-804. Ali, M. J., C. Z. Teh, R. Jennings, and C. W. Potter. 1982. Transmissibility of influenza viruses in hamsters. Archives of Virology 72(3):187-197. Andrewes, C. H., and R. E. Glover. 1941. Spread of infection from the respiratory tract of the ferret. I. Transmission of influenza A virus. British Journal of Experimental Pathology 22:91-97. Ang, B., B. F. Poh, M. K. Win, and A. Chow. 2010. Surgical masks for protection of health care personnel against pandemic novel swine-origin influenza A (H1N1)-2009: Results from an observational study. Clinical Infectious Diseases 50(7):1011-1014. Atkinson, M. P., and L. M. Wein. 2008. Quantifying the routes of transmission for pandemic influenza. Bulletin of Mathematical Biology 70(3):820-867. Baker, M. G., C. N. Thornley, C. Mills, S. Roberts, S. Perera, J. Peters, A. Kelso, I. Barr, and N. Wilson. 2010. Transmission of pandemic A/H1N1 2009 influenza on passenger aircraft: Retrospective cohort study. British Medical Journal 340:c2424. Bellei, N., E. Carraro, A. H. S. Perosa, D. Benfica, and C. F. H. Granato. 2007. Influenza and rhinovirus infections among health-care workers. Respirology 12(1):100-103. Belser, J. A., O. Blixt, L. M. Chen, C. Pappas, T. R. Maines, N. Van Hoeven, R. Donis, J. Busch, R. McBride, J. C. Paulson, J. M. Katz, and T. M. Tumpey. 2008. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proceedings of the National Academy of Sciences (U.S.A.) 105(21):7558-7563. Blachere, F. M., W. G. Lindsley, T. A. Pearce, S. E. Anderson, M. Fisher, R. Khakoo, B. J. Meade, O. Lander, S. Davis, R. E. Thewlis, I. Celik, B. T. Chen, and D. H. Beezhold. 2009. Measurement of airborne influenza virus in a hospital emergency department. Clinical Infectious Diseases 48(4):438- 440. Boone, S. A., and C. P. Gerba. 2007. Significance of fomites in the spread of respiratory and enteric viral disease. Applied and Environmental Microbiology 73(6):1687-1696. Brankston, G., L. Gitterman, Z. Hirji, C. Lemieux, and M. Gardam. 2007. Transmission of influenza A in human beings. Lancet Infectious Diseases 7(4):257-265.

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