Science and Technology for the Built Environment Engineering control of respiratory infection and...

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Engineering control of respiratory infection and low-energy design of healthcare facilitiesYuguo Lia, Julian Tangbc, Catherine Noakesd & Michael J. Hodgsone

a Department of Mechanical Engineering, University of Hong Kong, Pokfulam, Hong Kongb Leicester Royal Infirmary, Leicester, United Kingdomc Alberta Provincial Laboratory for Public Health, Edmonton, Alberta, Canadad Pathogen Control Engineering Institute, School of Civil Engineering, Woodhouse Lane,University of Leeds, Leeds, LS2 9JT, United Kingdome Office of Occupational Medicine, Occupational Safety and Health Administration,Department of Labor, Washington, DC, USAAccepted author version posted online: 30 Oct 2014.Published online: 06 Jan 2015.

To cite this article: Yuguo Li, Julian Tang, Catherine Noakes & Michael J. Hodgson (2015) Engineering control of respiratoryinfection and low-energy design of healthcare facilities, Science and Technology for the Built Environment, 21:1, 25-34, DOI:10.1080/10789669.2014.965557

To link to this article: http://dx.doi.org/10.1080/10789669.2014.965557

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Engineering control of respiratory infection and low-energydesign of healthcare facilities

YUGUO LI1, JULIAN TANG2,3, CATHERINE NOAKES4,∗, and MICHAEL J. HODGSON5

1Department of Mechanical Engineering, University of Hong Kong, Pokfulam, Hong Kong2Leicester Royal Infirmary, Leicester, United Kingdom3Alberta Provincial Laboratory for Public Health, Edmonton, Alberta, Canada4Pathogen Control Engineering Institute, School of Civil Engineering, Woodhouse Lane, University of Leeds, Leeds LS2 9JT,United Kingdom5Office of Occupational Medicine, Occupational Safety and Health Administration, Department of Labor, Washington, DC, USA

Indoor microorganisms and infection have become an emerging direction in indoor air quality research science. Airborne dropletnuclei can serve as carriers of respiratory infectious diseases. The study of expiratory droplets and their exposure control has receivedparticular attention since the 2003 severe acute respiratory syndrome epidemics and the 2009 influenza pandemics. Little is knownabout how effective the commonly used indoor environment control strategies are for infection control. Significant questions alsoexist on the ventilation requirements for airborne infection control. There is a broad range of relevant important issues, includingthe exposure risk, and effective control methods in various indoor settings, such as hospitals, homes, schools, and offices. What isknown is that the minimum required ventilation rate for infection control in hospitals can be much higher than the general health andcomfort requirement in homes and offices. This has resulted in significant energy-efficiency issues in healthcare facilities. This reviewconsiders the current knowledge on airborne transmission of infection and the potential implications of a move to low-energy design,particularly in hospitals, on the risk of infection. The review outlines active research and development on reducing hospital energyuse while improving infection control and discusses the potential for conducting “clinical trials” to gain the necessary evidence tosupport changes in hospital ventilation design.

Current Practice and Guidelines in Infection Control

About 7% of total annual worldwide deaths, i.e., four millionpeople, are due to viral respiratory infections (World HealthOrganization [WHO] 2004). Among them, influenza is a se-rious threat; influenza epidemics occur worldwide each year,and the 2009 avian flu and H7N9 outbreaks have heightenedawareness of the risk posed by new strains of the virus. Withmany serious respiratory diseases associated with transmis-sion in high-occupancy indoor environments, the design ofthe environment, particularly the ventilation, is understand-ably a key feature of infection control in healthcare settingsworldwide. However with a global move to reduce the energyconsumption of all buildings through such measures as im-proving airtightness to reduce uncontrolled infiltration, ven-

Received April 27, 2014; accepted August 27, 2014Yuguo Li, PhD, CEng, Fellow ASHRAE, is a Professor. JulianTang, PhD, FRCPath, Member ASHRAE, is a Consultant Virol-ogist and Medical Virologist. Catherine Noakes, PhD, CEng, is aProfessor. Michael J. Hodgson, MD, is a Chief Medical Officerand Director.∗Corresponding author e-mail: C.J.Noakes@leeds.ac.ukColor versions of one or more of the figures in the article can befound online at www.tandfonline.com/uhvc.

tilation of healthcare buildings has come under scrutiny andquestions are being raised as to whether such high ventilationrates are indeed necessary. It is imperative to consider howa change in healthcare building design policies may impacton infection transmission. To discuss the implication of low-energy design in healthcare facilities on infection control, itis useful to review first the current knowledge, practice, andguidelines in infection control.

Microorganisms are believed to be transmitted from per-son to person or between animals and people through a num-ber of mechanisms, including physical contact, large droplets,or fine aerosols. Infection control guidelines worldwide forall approaches are typically based on a three-stage hierarchy(Centers for Disease Control [CDC] 2005): administra-tive control, environmental control, and personal protec-tive equipment. In the case of transmission by aerosolsand droplets, identification and separation of infectious pa-tients remains the first line of defense (CDC 2005); how-ever, environmental control approaches and application ofpersonal protective equipment have a particularly impor-tant role to play depending on the disease and its transmis-sion. The distinction between airborne and droplet trans-mission is based on the assumed behavior of differentlysized particles in air. The designation of fine particulates asthose with a diameter <5 µm and those with a diameter

26 Science and Technology for the Built Environment

>10 µm as large particles or droplets has long been the ba-sis of fundamental infection control strategies, as developedby the Association of Professionals for Infection Control(APIC 2013), the CDC (2005), and the WHO (2007).

Simplistically, droplet precautions recommend wearing sur-gical masks within 6 ft (2 m) of patients with an infection.The basis for this approach is the theory of settling timesby particle size; large droplets will rapidly deposit on sur-faces in the vicinity of the infectious source. Traditionally,patients at risk for transmitting disease through large particleshave not been placed in respiratory isolation. On the otherhand, patients with infections believed to be transmitted byfine aerosols through the airborne route have traditionally re-quired far more intense protection strategies, including earlyidentification, isolation into an airborne infection isolationroom with specialist ventilation, and the use of a fit testedrespirator by staff in such a room.

This distinction remains the mainstay of infection control,and ASHRAE has recently developed a position paper out-lining overall engineering concerns and summarizing implica-tions for engineers of many of the infectious diseases trans-mitted by airborne route and by large droplets (ASHRAE2013b). ASHRAE fundamentally relies on cognizant author-ities in the development of its formal positions, with the im-portance here being the implications for control strategies.Only in healthcare have control strategies explicitly consid-ered infections in ventilation requirements, with a hierarchyof measures recommended by guidance. Local exhaust ven-tilation can facilitate source control in high-risk procedures,pressurization minimizes transport of airborne microorgan-isms and other pollutants between spaces, a high ventilationrate dilutes and removes airborne microorganisms, and well-defined ventilation patterns can minimize transfer within aspace. Air cleaning through filtration or other means canprovide local control and enable recirculation of air. Guid-ance on these approaches is set out in a range of standardsand guidance, including ANSI/ASHRAE/American Societyfor Healthcare Engineering (ASHE) Standard170 (ASHRAE2013a), Facility Guidelines Institute (FGI) Guidelines for De-sign and Construction of Hospital and Outpatient Facilities(FGI 2014), and various CDC directions, including those onTB (CDC 2005) in the United States and Health TechnicalMemorandum 03–01 (Department of Health 2007) in theUnited Kingdom. For example, all of these standards stipulatethat patient and ward areas should have higher than averageventilation rates to minimize opportunist transmission fromundiagnosed sources, while high-risk areas, such as operatingrooms and isolation rooms, have ventilation rates in excessof 10 air changes per hour (ACH). Other buildings, such asschools, public access buildings, and offices, have mostly ig-nored any consideration of infectious hazards, although evenhere there is increasing awareness of the relationship betweenthe building and health, and filtration dedicated exhaust tothe outside and ultraviolet germicidal irradiation (UVGI) havebeen explored in some studies.

Nevertheless, in practice, this distinction between fine andlarge particles as separate modes of transmission is becom-ing ever harder to maintain. Ten years ago, a review of thetopic in a premier journal in medicine suggested that although

there were clearly agents that relied on only one or only theother mode of transmission, i.e., large or small particles, therewas a third group: organisms that were “facultative” users ofboth (Roy and Milton 2004). Shortly thereafter, a CDC reviewsuggested that a common agent, influenza A, might fit thatdescription and that the critical issue was then not whetherairborne, droplet, or both but in what proportion transmis-sion occurred (Tellier 2006). The issue has smoldered for manyyears in other common viral illnesses, including even the com-mon cold, where despite widespread beliefs to the contrary,experimental arrays show airborne transmission (Dick et al.1987). Recently, particle movement over short distances hasbeen modeled, and it was suggested that airborne transmissionof infectious diseases over short range might in fact follow thesame pattern as large droplet transmission (Liu et al. 2010; Li2011).

The problem has come to a head with the increase in in-ternational travel and the threat of pandemic migration, noless important because the degree and importance of airbornetransmission of influenza and the risks posed by new strainsremain unknown. There is also concern over other infections,particularly virulent or emerging diseases. It is long estab-lished that smallpox, a now eradicated disease, was trans-mitted through the airborne route (Milton 2012). In fact,careful review of older literature has raised questions abouteven hemorrhagic fever cases resulting from airborne trans-mission (Carey et al. 1972; Roels et al. 1999), a phenomenonreinforcing the current biosafety laboratory precaution rec-ommendations. The 2003 severe acute respiratory syndrome(SARS) outbreak demonstrated only too well the challenge ofdealing with a global outbreak of a new disease and the im-portance the environment can play in transmission (Li et al.2005). Preventing airborne transmission in pandemic settingsand ensuring infrastructure is sufficiently robust to deal withcurrent and new threats require far more intense approachesand represent a growing challenge for engineers.

Exposure to expiratory droplets and respiratory infection

Although the relative importance of large versus fine parti-cle transmission drives protection strategies in usual and pan-demic settings, little research has explored the content of thosedroplets and the implications for transmission.

The source represents the primary factor in transmission,although others modify the transmission process. These fac-tors may be grouped as follows:

• the infector and source (expiratory droplet number and size,respiratory activity, virus concentration, social contact),

• the environment (air/surface temperature, moisture, con-tamination, airflow pattern, ventilation rate, usage—ward,consulting room, waiting room, isolation room, operatingtheater, etc.),

• the virus (survival, site of infection), and• the susceptible (immunity, age, social contact, etc.).

While controlling the source is desirable, it is challenging, par-ticularly in healthcare facilities (Menzies et al. 2000). Such ap-proaches as masking infectious patients while they are moved

Volume 21, Number 1, January 2015 27

within a hospital building (CDC 2009) and applying localexhaust ventilation in certain respiratory procedures are ad-vocated. However in the wider hospital environment, control-ling transmission focuses on the transmission route, and theventilation and building design becomes a major factor. Withthe growing threat of pandemics, since the early 2000s, fromSARS, H5N1, and H1N1, engineering control strategies be-come not only relevant but of growing importance in definingthe environment factor in the transmission process.

Understanding the mechanism of exposure is important todevelop and understand an effective control strategy. For ex-ample, ventilation intervention decreases airborne transmis-sion by extracting, directing the flow of airborne infectiousagents away from susceptible persons, and/or diluting and re-moving airborne infectious agents from room air. If airbornetransmission represents more of a hazard than previously con-sidered, general dilution ventilation and approaches, such asair cleaning, represent more important aspects of ventilationfor public health than previously considered. It also followsthat a reduction in ventilation rates, as may be desired in low-energy healthcare buildings, potentially poses an increasinghazard. However, this is only part of the picture. Ventilationimpacts particles that remain airborne, but the influence ondroplet transmission or deposited particles and the subsequentexposure of susceptible persons to infectious agents throughcontact exposure is unclear. There is some evidence that aircleaning approaches reduce surface contamination, but theimpact on infection risk and the effectiveness of this as anintervention are largely unknown.

The uncertainty of the airborne route for many respiratorydiseases remains a crucial bottleneck of using ventilation as acommunity intervention measure. In the case of influenza, theUS$8 million project Evaluating Modes of Influenza Trans-mission (EMIT) is one of the most recent studies that may offerthe first evidential result soon (EMIT 2013). However, suchstudies are complex and challenging, and in most cases, evi-dence has to be derived from studies exploring specific aspectsof the transmission process. More than ten studies explore thesize distribution of expiratory droplets due to coughing, sneez-ing, speaking, and talking (e.g., Morawska et al. 2009; Chaoet al. 2009; Xie et al. 2009). The data by Duguid (1946) havebeen widely used in risk assessment models in the literature(e.g., Nicas et al. 2005; Yang and Marr 2011). Substantial un-certainty and differences exist in these measurements, possiblydue to individual inhomogeneity, instrumentation, and suchfactors as study control. Moreover, these studies generallycharacterize healthy volunteers, so while they yield valuableinformation on potential for human dispersion of particles,infection risks can only be inferred by extrapolation. Survivalof viruses and bacteria has been studied as a function of rel-ative humidity (RH) and temperature in air (Harper 1961;Yang and Marr 2011) and on surfaces (Nicas and Jones 2009;Weber and Stilianakis 2008), yet it can be hard to link thesedata to infection risk in humans.

More recently, researchers have explored the implicationsof specific viral content at various particle sizes. In a smallstudy of patients presenting with influenza-like illness, i.e.,influenza A or B virus confirmed by rapid test, Fabian et al.(2008) identified viral particles in the coughed secretions ofthree (60%) of the five patients infected with influenza A virus

and one (14%) of the seven infected with influenza B virus.Exhaled influenza virus RNA generation rates ranged from<3.2 to 20 influenza virus RNA particles per minute. Over87% of particles exhaled were under 1 micron in diameter,with unambiguous airborne potential.

Bishoff et al. (2013) recently studied patients with influenza-like illness to measure viral particles at ≤0.305, 0.914, and1.829 m (1, 3, and 6 ft) from a patient’s head. Twenty-six patients (43%) released influenza virus into room air,with 5 (19%) emitting up to 32 times more virus than oth-ers. Emitters surpassed the airborne 50% human infectiousdose of influenza virus at all sample locations. The primar-ily small influenza virus particles (diameter <4.7 µm) showeddecreasing concentrations with increasing distance from thepatient’s head (P < 0.05). The authors questioned the cur-rent paradigm of localized droplet transmission during non-aerosol-generating procedures

National Institute for Occupational Safety and Health(NIOSH) researchers (Noti et al. 2012) studied influenzageneration in a simulated patient room and recovered par-ticles in all aerosol fractions (5.0% in >4 µm aerodynamicdiameter, 75.5% in 1–4 µm, and 19.5% in <1 µm; n =5). They demonstrated that tightly sealed masks (glue, notso practical in living workers) to the face blocked en-try of 94.5% of total virus and 94.8% of infectious virus(n = 3). A tightly sealed respirator blocked 99.8% of totalvirus and 99.6% of infectious virus (n = 3). A poorly fittedrespirator blocked 64.5% of total virus and 66.5% of infec-tious virus (n = 3). A mask documented to be loosely fittingby a PortaCount fit tester, to simulate how masks are worn byhealthcare workers, blocked entry of 68.5% of total virus and56.6% of infectious virus (n = 2).

Milton et al. (2013) studied the effect of placing surgicalmasks on patients to capture influenza virus in large dropletspray. Fine particles contained 8.8-fold (95% confidence inter-val [CI] 4.1 to 19) more viral copies than did coarse particles,supporting Bischoff et al. (2013). Surgical masks reduced vi-ral copy numbers in the fine fraction by 2.8-fold (95% CI 1.5to 5.2) and in the coarse fraction by 25-fold (95% CI 3.5 to180). Overall, masks produced a 3.4-fold (95% CI 1.8 to 6.3)reduction in viral aerosol shedding.

Finally, Lindsley et al. (2010) showed that such airborneparticles of influenza A, influenza B, and RSV migrated froman urgent-care clinic throughout a healthcare facility. Theseresults supported the possibility that influenza and respiratorysyncytial virus (RSV) can be transmitted by the airborne routeand suggest that further investigation of the potential of theseparticles to transmit infection is important.

The bottom line from these recent particle size and contentstudies is that fine particles contribute substantially to the air-borne particle load, especially in the “facultative” airborneviruses; however, the contribution to the burden of diseaseremains unclear. No arrays of studies are underway to de-velop predictive tests on which aspect is more important and,therefore, which transmission prevention strategy should beprimary.

To assess the impact and magnitude of such risks, engineerswill need to engage and work with a multi-disciplinary teamof physicians and hospital infection control teams (HICTs) tomake such an assessment.

Reducing healthcare building energy use whilemaintaining or improving effective airborneinfection control

Given the current climate, it is clear that low-energy consider-ations will eventually need to be applied to hospitals. So, onwhat basis should there be concern about the risks of increasesin airborne hospital-acquired infections (HAIs) if designs arechanged and new technology introduced to save energy? Isthere any risk at all? Although not systematically investigatedin a controlled manner, there are a large number of reviewsand case reports that demonstrate that an effective ventilationsystem working at a minimum number of ACH is requiredfor both thermal comfort and good airborne hygiene levelsin hospitals (Li et al. 2007; Eames et al. 2009; Aliabadi et al.2011).

However, in a hospital environment, it is not simply the ven-tilation alone that adds to the energy cost. As well as higherventilation rates, infection control generally leads to a higherusage of related environmental control strategies, such as theuse of HEPA filters that add pressure losses and higher fanpower, greater water quality control (for legionella), more con-trol of moisture level due to the impact of moisture contenton survival of pathogens, etc. (ASHRAE 2013a; 2013b). Thequestion is, “Is it possible to develop low-energy design with-out compromising infection control?”

To answer this question, different low-energy design strate-gies must be examined. It may be useful to categorize low-energy design strategies into three categories.

• Category A—those with direct impact on infection control(such as reducing ventilation rate, air disinfection, and useof natural ventilation; see WHO [2009]).

• Category B—those with indirect impact on infection con-trol (such as use of displacement ventilation, use of separatedehumidification control system, use of liquid desiccant de-humidification systems, etc.).

• Category C—those with no impact on infection control(e.g., good housekeeping measures, such as turning offlights when not in use, using renewable or Combined Heatand Power (CHP) energy sources, or installing energy effi-cient control systems, such as variable-speed drives).

Within these categories, good design and maintenance of anytechnology is the first step in ensuring energy efficiency. For ex-ample, a well-constructed isolation room with a good level ofairtightness, well-designed airflow pattern and pressurization,and properly commissioned ventilation and control systemsis likely to require less energy to operate than one with poorflows that requires post-construction modifications to createan acceptable environment for comfort and infection control.Similarly, where filters are required, conducting lifecycle costanalysis as part of the design process benefits both the effec-tive operation of the system and the protection provided topatients.

For Category A low-energy technologies, changes to theirapplication in hospitals need special attention. There is a grow-ing body of experimental and laboratory evidence to informsome of these approaches, yet there remain many unknowns.

Quantitative data on ventilation rates in particular is lim-ited; however, Menzies et al. (2000) showed increased riskof tuberculosis infection at ventilation rates below 2 ACH.Some researchers advocate reducing ventilation rates on en-ergy grounds, but in the absence of good evidence, care shouldbe taken when dealing with strategies that result in reducingthe number of ACH; if this results in a higher concentrationof ambient, airborne infectious agents, then this might pose ahazard, particularly in environments housing more vulnerableinpatients (e.g., transplant patients, HIV/AIDS patients, pre-mature neonates). A small number of studies have explorednatural ventilation in full-scale settings and have shown thatsome naturally ventilated hospitals can be thermally comfort-able (Lomas and Giridharan 2012) and that very high ventila-tion rates, and hence dilution, can be achieved under certainweather conditions (Qian et al. 2010; Gilkeson et al. 2013).However, studies also show that the system can perform badlyunder different weather and operational conditions (Gilkesonet al. 2013). Similarly there is a growing body of experimental(Xu et al. 2003; NIOSH 2009) and computational (Noakeset al. 2006; Sung and Kato 2011; Gilkeson and Noakes 2013)studies with a small amount of field data (Escombe et al.2009; Menzies et al. 2003) that suggests ultraviolet air disin-fection (UVGI) is a viable and possibly energy-efficient (Koet al. 2001) approach to controlling airborne infection. Per-sonalized ventilation is another approach where there couldbe some potential benefits in both energy and infection con-trol. In the case of the short-range airborne route, traditionalmethods, such as ventilation dilution, are not effective, butthere may be a role for alternatives, such as personalized ven-tilation, to provide near-occupant protection (Sekhar et al.2005; Melikov 2004).

For Category B technologies, it can be even more difficultto judge if a particular technology is suitable for infectioncontrol. The use of displacement ventilation can be a goodexample (Li et al. 2011). Displacement ventilation is known toprovide better ventilation efficiency when certain conditionsare met. Hence displacement ventilation has also beenconsidered as a possible energy-efficiency solution in hospitalwards. Guity et al. (2009) suggested that displacementventilation at 4 ACH performed equal to or better thanoverhead ventilation (mixing ventilation) at 6 ACH forthermal comfort, ventilation effectiveness, and contaminantconcentration in a single-patient ward. However, displace-ment ventilation has not been widely applied in hospitals,and it is difficult for a practical engineer to decide if sucha system can be non-harmful to infection control. Basedon the simple engineering principle, Li et al. (2011) arguedthat “further field data on the locking-up phenomenon,weak plume trapping, particle deposition in the thermallystratified layers, the effect of occupant height variation, plumestrength, droplet size and human movement, total exposureand risk analysis are needed” (p. 88); “[i]f a study focuses onlyon the preferable conditions, it is likely that displacementventilation will be found to perform superior to traditionalmixing ventilation and other designs” (p. 88); and “[b]ased onthe available data and as our understanding at present, andfor protecting both the healthcare workers and/or other pa-tients/visitors, we do not recommend the use of displacement

ventilation in hospitals in either single-patient ormultiple-patient wards for control of exhaled substances orany harmful infectious aerosols” (p. 88). Other technologieswhere there is uncertainty over risk include those focused onthermal control. Ventilation systems that separate sensibleand latent loads are known to have lower energy require-ments, requiring smaller centralized air handling units andless ductwork. Provision of ceiling-mounted radiant panelsfor local heating have become increasingly popular as theydo not have the burn risk or tendency to trap dust thatconventional wall-mounted radiators do. Chilled beams offera low-energy approach to local cooling and are permitted byANSI/ASHRAE/ASHE Standard 170 (ASHRAE 2013a).Concerns have been expressed over possible infection riskslinked with cleaning and the potential for condensation topromote microbial growth, although the limited researchevidence does not support these fears (Devlin 2011).

Understanding of all these low-energy technologies interms of infection control presents a challenge, particularlygiven the uncertainties over transmission routes. Researchershave focused on building an understanding based on engi-neering principles; using proxy methods, such as tracer exper-iments and computer simulation (Tang et al. 2010); and com-paring technologies through risk analysis approaches, such asthe so-called Wells–Riley equation (Riley et al. 1978) and itsvarious modifications (e.g., Beggs and Sleigh 2003; Fennellyand Nardell 1998). Engineers and building operators also needto understand the basic principles of non-engineering controlstrategies, such as administrative measures, and personal pro-tection methods, such as use of masks and respirators.

A specific example—relationships betweenrespiratory-assist devices and the built environment

Oxygen masks are a frequently used and essential respiratorysupport device in hospital wards worldwide. They are alsoa potential source and disseminator of airborne respiratorypathogens (Figure 1), principally because many of the pa-tients that need to use them are likely to be infected with suchpathogens.

After the SARS outbreaks of 2003, a series of airflow visu-alization studies on respiratory-assist devices clearly demon-strated the potential for human exhalation flows to generateand disseminate airborne pathogens (Somogyi et al. 2004; Huiet al. 2006a, 2006b, Ip et al. 2007). Indeed, one of the largesthospital ward outbreaks of SARS described in Hong Kongwas likely to have been caused by the use of a nebulizer by anundiagnosed patient with SARS (Wong et al. 2004; Li et al.2005). Particle sampling studies conducted on a respiratoryward (Hathway et al. 2013) also indicated that the use of pa-tient ventilators and nebulizers changed the particle size distri-bution; respiratory-assist devices were correlated with highernumbers of smaller particles, indicating greater potential forairborne transmission.

The fate of particles released by such patients is de-termined by the built environment. For those in a single-bedded negative-pressure isolation room, continuously exhal-

ing aerosols of pathogen-laden air, dilution and removal by theventilation system combined with personal protective equip-ment protect healthcare workers who enter the room, and thedilution combined with designed pressure relationships min-imize the risks to those outside. If this ventilation system isinadequate, risks to those within the room may be excessiveand leakage out of the room upon opening the door (result-ing in a transient flow reversal, despite the negative pressure)may pose a real threat to other healthcare workers and visitorsoutside the room (Tang et al 2005, 2013). While the risks of air-borne pathogens being present on a general ward environmentis lower, outbreaks are reported, and it is only the diluting andremoval functions of an adequate ventilation system that cankeep the concentrations of such airborne pathogens within theroom to a safe level.

Such factors must be considered in low-energy hospitaldesign. With respiratory-assist devices likely to enhance anyairborne pathogen release at potentially smaller particle sizes,the ventilation in both ward and isolation facilities will stillbe required to be maintained at an adequate rate to preventthe build-up of airborne pathogens to a level that poses adanger—and this concentration may vary according to differ-ent pathogens (Franz et al. 1997). The reverse situation is alsoof concern, where isolation facilities are maintained at positivepressure using filtered air to protect vulnerable patients (e.g.,bone marrow transplant patients) from potentially contami-nated air entering the room from outside, particularly whenhealthcare workers and visitors are entering and leaving theroom. Thus, before a reduction in ventilation rates or changesto ventilation design are considered as a means to reduce theenergy cost of such healthcare facilities, a careful assessment ofthe patient group and clinical needs is required to ensure thatpatients and healthcare workers are not put at any increasedrisk as a result.

Future needs

Is current knowledge sufficient for future managers and de-signers to be concerned about the consequences of reducingthe ventilation rate across a hospital facility? One might hopeso, and new hospital designs certainly seem to have takenthe risks of contact transmission of infectious agents, suchas methicillin-resistant Staphylococcus aureus (MRSA), seri-ously, at least to some extent. Yet, even such design and costconcessions for the sake of infection control require constantattendance and vigilance on the part of the microbiologistsinvolved (Wilson and Ridgway 2006).

In comparison to airborne transmission, the evidence forcontact transmission as a route of HAIs is stronger but re-lies mostly on “bundled” interventions (Gurieva et al. 2012).Nevertheless, hand hygiene campaigns have taken the worldby storm (Boyce and Pittet 2002; Syed et al. 2013; Allegranziand Pittet 2009; Monistrol et al. 2012; Allegranzi et al. 2013),appropriately becoming an international effort sponsored bythe WHO. Must the evidence for the clinical significanceand impact of airborne transmission risks need to reach thesame level of awareness in the professional and popular cul-ture and media to be able to significantly influence hospital

Fig. 1. Jet-like exhalation flows generated by the use of oxygen masks on a simulated patient. a. Close-up view showing the emanationof exhaled airflows from the mask vents that can potentially carry airborne pathogens. b. More distant “room” view demonstratingthe capability of the oxygen mask to disseminate airborne pathogens beyond the immediate vicinity of the patient to other occupantsof the room. Images courtesy of Dr. David Hui (Department of Medicine, The Chinese University of Hong Kong). ©David Hui.Reproduced by permission of Dr. David Hui. Permission to reuse must be obtained from the rightsholder. Experimental setupdescribed in Hui et al. (2006a, 2006b).

design? Does this require more than one or two multi-unit butnot multi-hospital experimental studies? Given the plethoraof recent studies suggesting a significant contribution of theairborne route for influenza (Tang et al. 2006; Tellier 2006,2009), SARS associated coronavirus (SARS-CoV; Tang et al.2006; Li et al. 2007), and other more ancient pathogens, suchas tuberculosis (Tang et al. 2006; Menzies et al. 2000; Li et al.2007), one might argue that it already has. The very visibleuse of face masks in some affected countries (well publicizedby national and international media) certainly contributed tothe awareness of the airborne route of transmission for thesepathogens.

Yet, there is still data lacking from a more direct inter-ventional study at a hospital level. In the majority of cases,the benefits of technology have to be inferred rather than di-rectly measured, and even those studies that are conductedin the field generally rely on an existing building rather thana designed intervention. There has therefore been discussionamong experts if there is a need for “clinical trials” of energycontrol strategies, such as reducing or increasing the ventila-tion rate. Does this really matter? On one hand, given the cur-rent uncertainties of the proportion and clinical significanceof the airborne route in causing HAIs, managers and design-ers could just ignore any potential implications of reducedventilation rate or introduction of new technology—and seewhat happens. Yet in many instances this will be contrary tohealthcare design guidance, and in this increasingly litigiousclimate, this same evidence may be interpreted as indicatingthe potential for such infections to occur more frequently ina reduced ACH environment. If there is evidence available insupport of a technology, any design team has the challenge ofinterpreting that evidence, determining the quality of the find-ings, and establishing whether the approach can be applied totheir scenario. These difficulties with evidence-based designhave been acknowledged by ASHE (2008).

However, clinical-type trials are feasible in some cases and,for example, have been conducted to investigate the poten-tial benefits of air cleaning technology. Escombe et al. (2009)showed that both UVGI and negative air ionizers reduced the

transmission of TB from humans to guinea pigs in a clinicalsetting, while Kerr et al. (2006) showed that the installationof ionizers in an ICU reduced the incidence of acinetobactorinfections. Both trials had their challenges. Escombe et al.’sstudy (2009) relied on a proxy measure (guinea pigs), althoughit had a very comprehensive set of data, including ventilationmeasurements and molecular typing of guinea pig infectionsand patient samples. Kerr et al.’s study (2006) demonstrateda reduction in infection rates but was unable to conclude themechanism for transmission and, hence, show that the inter-vention acted on an airborne route. In both cases, the trial wasconducted in a single clinical environment, measured sufficientinfections for statistical significance, and relied on switchingan intervention on or off with a comparable patient cohort.

So how would one go about designing a more direct inter-ventional study to test the hypothesis? Does a reduced ventila-tion rate increase the risk of acquiring HAIs via the airborneroute? And secondarily, if yes, how much can the ventilationrate be reduced to save energy and not increase the level ofHAIs? On paper, it might seem very simple: compare infec-tion rates over the course of a year between comparable patientcohorts with different ventilation rates. However, there are agreat number of factors that would need to be considered:Which patients? Which infections? How should ventilation bemeasured and/or adjusted?

Conducting a study in a single hospital ward, comparingstandard with reduced or increased ventilation rate, and fo-cusing on a small number of target HAIs would enable gooddata collection in terms of patient details and environmen-tal characterization. However, this approach may not have thenumbers of infections needed to give reliable data and may notbe translatable to other climates, infections, patient groups, orventilation designs.

Perhaps an alternative approach is to identify a number ofhospitals from different countries with different climates andpatient case mixes that could participate. Ask the HICTs todocument all suspected HAIs for 1 year to capture all seasonalvariations. Next, ask the hospital engineers to adjust overallACH across the hospitals by a certain amount (say 10%–20%)

and ask the same HICTs to document the rate of HAIs for asecond year. Finally, return the ventilation rates their originallevel in the third year and ask the HICTs to document allsuspected HAIs to see if this rate has returned to a similarlevel as in the first year of the study. This approach, whichtreats the entire hospital environment as a “black box,” has anumber of advantages and disadvantages.

Advantages include not having to detail every type of clini-cal activity taking place in the hospital but just assuming thatthe patient case mix and the healthcare staff involved will re-main more or less the same during the 3 years of the study.Such a study would also have the advantage that it is ableto track multiple different infections across multiple climatesand can therefore give a greater insight into which effects arecontext specific and which are generalizable. Disadvantageswith this approach include that it may not be clear exactlywhere the greatest impact of the reduced ACH intervention isbeing seen and that a broad study may well reduce the abil-ity to collect detailed information on the environments andpatients.

Planning such a study is a large and complex task. Con-ducting a study to assess the impact and magnitude of suchrisks would require an international multi-disciplinary team.In each participating hospital, an infection control risk as-sessment (ICRA) team with expertise in infectious disease,infection prevention, patient care, engineering, epidemiology,facility design, construction, and safety (FGI 2014) wouldbe involved. These local teams would need to work with aninternational research team with engineers, epidemiologists,statisticians, physicians, microbiologists, and infection controlspecialists. Participating hospitals would have to be selectedcarefully, i.e., avoiding those with planned major renovationsor relocations of key services and personnel during the studyperiod. Unforeseeable events, such as major climate events(earthquakes, volcanic eruptions, tsunamis, major forest fires,etc.) or unpredictable political or economic changes, could im-pact the results, so participating hospitals in countries that arepolitically and economically stable should be selected. Whenidentifying spaces to adjust ventilation, clinical risks wouldhave to be considered. In the case of such areas as circulationzones, waiting rooms, outpatients, and wards, the particularpatient group, design of the building, and minimum ventila-tion rates specified in the guidance for the particular settingneed to be considered. In high-risk environments, such as iso-lation rooms, operating theaters, and those wards with themost vulnerable patients (i.e., immune compromised, trans-plant etc.), airflow characteristics as well as ventilation ratesare important, and it is likely that these spaces would all beexcluded from any study. Feasibility and control would also bea factor; the study would only be able to compare spaces whereventilation can reliably be adjusted and maintained at a par-ticular flow rate. Flow rate measurements would be requiredto adjust for variation between different hospitals, and a studywould have to control for any other infection control interven-tions that may be implemented in the hospital over the studyperiod. Another potential confounder is which infections thevarious HICTs would agree are a result of HAIs and, in par-ticular, a result of an airborne HAI. Differences between thesedefinitions may confound any conclusion from the study, but

this problem is not insurmountable, and a consensus couldbe reached between the participating HICTs involved in thestudy.

While there are considerable challenges, such a study couldbe definitive if enough of the participating hospitals’ conclu-sions agree, and it should provide evidence, either way, forthe impact of reduced ventilation rate on HAIs. This datawould then hopefully support (or not) the concerns about thisenergy-saving option on patient and staff welfare in these typesof healthcare facilities.

However, to conclude that such a study is impossible to con-duct with feasible resources and within the constraints, then,as a community, the evidence must be taken seriously frompast and ongoing studies investigating transmission mecha-nisms and control using proxy methods. In the absence offull trial data, this must be accepted as the best evidence tosupport infection control in healthcare building design, work-ing to implement the outcomes from such studies rather thaninsisting on clinical data or nothing. Achieving this will re-quire a multi-disciplinary effort to identify the key researchand development needs, to ensure that studies address—as faras possible—both engineering and clinical aspects, and to es-tablish collaborative approaches to tackle the practical impli-cations of turning research findings into new innovation. Forexample, a lot of energy-efficient design is presently done us-ing computer modeling. Designers need to be careful in howsuch modeling results are interpreted. Input from engineerswill be required to assist with this, especially in defining theappropriate starting condition parameters. Clinical and infec-tion control experts also need to be involved to ensure thatmodels and interpretations properly capture how the buildingwill be used. As a collaborative team, this enables considera-tion of parameters that may have not been identified by anyparty working in isolation.

Summary

Infection control is an important design factor in hospitals,elderly care homes, and other healthcare facilities. Low-energydesign has a useful potential in healthcare facilities but needsto take into account any potential risks in terms of infectioncontrol.

In many situations, the uncertainty of the transmissionroute for a respiratory pathogen remains a crucial bottleneckin choosing the most effective engineering control strategies.The effect of environmental conditions, such as air tempera-ture and humidity, is also incompletely understood for mostpathogens.

There is a complete lack of integrated studies on low-energyhealthcare building design for infection control. Some stud-ies of individual energy efficient technologies and their po-tential impact on infection control issues are available. Bal-ancing the infection risk and low-energy design requires amulti-disciplinary effort, knowledge sharing between differ-ent experts, and developing approaches to better translate re-search into practice. For new technologies, ultimately, well-designed and controlled field studies should be able to provide

robust evidence for their applicability to infection control,particularly for their use at the community level.

Disclaimer

This manuscript creates no new standards or requirements.It represents the views of the author and not those of theDepartment of Labor.

Funding

Li thanks the financial support of the Research Grants Coun-cil (RGC) of the Hong Kong SAR Government (projectHKU7142/12) and National Science Foundation of China(NSFC) of the State Council of Chinese Government (project51278440) for his research on hospital ventilation and short-range airborne exposure; the findings are useful to therelevant part in this article. Tang acknowledges fundingfrom the Singapore National Medical Research Council(NMRC/1208/2009) for the work related to oxygen masks asa potential disseminator of airborne infectious agents. Noakesacknowledges the support of the U.K. Engineering and Phys-ical Sciences Research Council (EPSRC).

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