S38 Vol. 35 No. 10 Supplement 1 Bloomfield et alsoil<strong>in</strong>g under <strong>the</strong> flush<strong>in</strong>g rim and scale material <strong>in</strong><strong>the</strong> toilet bowl for up to 3 weeks after notification <strong>of</strong><strong>in</strong>fection. 58 Flush<strong>in</strong>g toilets seeded with Salmonellaenteritidis resulted <strong>in</strong> contam<strong>in</strong>ation <strong>of</strong> <strong>hand</strong> contactsurfaces such as toilet seats and toilet seat lids.<strong>The</strong>se represent recent examples <strong>of</strong> studies thathave been reported. <strong>The</strong>se and o<strong>the</strong>r studies are alsoreviewed elsewhere. 82,92-94In develop<strong>in</strong>g <strong>hygiene</strong> policies for prevent<strong>in</strong>g GI <strong>in</strong>fections,one <strong>of</strong> <strong>the</strong> difficulties is assess<strong>in</strong>g <strong>risks</strong> associatedwith <strong>hand</strong> transmission relative to o<strong>the</strong>r <strong>risks</strong>such as <strong>in</strong>adequate cook<strong>in</strong>g or storage <strong>of</strong> food or <strong>in</strong>halation<strong>of</strong> <strong>in</strong>fected vomit particles. Gillespie et al 15 reportedan evaluation <strong>of</strong> reported outbreaks l<strong>in</strong>ked to UK householdsfor 1992 to 1999 that suggested, <strong>of</strong> <strong>the</strong> 85% <strong>of</strong> outbreaksdesignated as foodborne, cross contam<strong>in</strong>ationwas implicated <strong>in</strong> 20% <strong>of</strong> outbreaks compared with30% and 31% <strong>of</strong> outbreaks for which <strong>in</strong>adequate storageand cook<strong>in</strong>g, respectively, were thought to be <strong>the</strong>cause. <strong>The</strong>re were no data to suggest what percentage<strong>of</strong> cross contam<strong>in</strong>ation events <strong>in</strong>volved <strong>the</strong> <strong>hand</strong>s, andGillespie et al 15 expressed concern that most <strong>of</strong> <strong>the</strong> reportedoutbreaks were l<strong>in</strong>ked to home cater<strong>in</strong>g, thusnot necessarily representative <strong>of</strong> normal daily rout<strong>in</strong>e.Aerosol transmission can result from settl<strong>in</strong>g on <strong>hand</strong>and food contact surfaces, but, for norovirus, <strong>in</strong>fectioncan sometimes result from direct <strong>in</strong>halation <strong>of</strong> <strong>in</strong>fectedparticles <strong>of</strong> vomit by people immediately adjacent to<strong>the</strong> person who vomits. <strong>The</strong> potential for airborne transmission<strong>of</strong> norovirus was demonstrated <strong>in</strong> studies <strong>in</strong>a restaurant and a primary school, <strong>in</strong> which close proximityto <strong>in</strong>fected persons <strong>in</strong> <strong>the</strong> immediate aftermath <strong>of</strong>a vomit<strong>in</strong>g attack was identified as a risk factor. 95,96Transmission <strong>of</strong> RT <strong>in</strong>fections. <strong>The</strong> last 2 years haveseen an unprecedented global focus on develop<strong>in</strong>gstrategies for prevent<strong>in</strong>g transmission <strong>of</strong> <strong>in</strong>fluenza.<strong>The</strong> WHO 97 is tak<strong>in</strong>g a lead on pharmaceutical <strong>in</strong>terventionssuch as vacc<strong>in</strong>es and antivirals but has alsomade recommendations for o<strong>the</strong>r <strong>in</strong>terventions, 98which <strong>in</strong>clude highlight<strong>in</strong>g <strong>the</strong> importance <strong>of</strong> <strong>hygiene</strong>,and <strong>in</strong> particular <strong>hand</strong> <strong>hygiene</strong>, <strong>in</strong> m<strong>in</strong>imiz<strong>in</strong>g spread<strong>in</strong> <strong>the</strong> home and community.Risks from exposure to respiratory pathogens via <strong>the</strong><strong>hand</strong>s. As shown <strong>in</strong> Fig 3, exposure to RT viruses canoccur ei<strong>the</strong>r by <strong>in</strong>halation <strong>of</strong> <strong>in</strong>fected mucous or<strong>in</strong>oculation <strong>of</strong> <strong>the</strong> nasal mucosa or eyes with viruscontam<strong>in</strong>ated<strong>hand</strong>s, which <strong>the</strong>n cause <strong>in</strong>fection via<strong>the</strong> mucous membranes and upper RT. Rh<strong>in</strong>ovirusand RSV are deposited <strong>in</strong>to <strong>the</strong> front <strong>of</strong> <strong>the</strong> nose or<strong>in</strong>to <strong>the</strong> eye (where <strong>the</strong>y pass down <strong>the</strong> lacrymalduct), ei<strong>the</strong>r on <strong>the</strong> end <strong>of</strong> <strong>the</strong> f<strong>in</strong>ger or possibly sometimes<strong>in</strong> aerosolized droplets. 99 Rubb<strong>in</strong>g <strong>the</strong> eyes andnose with <strong>the</strong> f<strong>in</strong>gertips is a common occurrence;Hendley et al found that 1 <strong>in</strong> 2.7 attendees <strong>of</strong> hospitalTable 6. Infectious doses for viruses that causerespiratory diseases*VirusM<strong>in</strong>imal <strong>in</strong>fectious dose associatedwith <strong>in</strong>tranasal <strong>in</strong>oculationRespiratory syncytial virus 100-640 TCID 50Rh<strong>in</strong>ovirus 0.032-0.4 TCID 50 ; also cited as 1-10 TCID 50Influenza 2-790 TCID 50Para<strong>in</strong>fluenza 1.5-80 TCID 50*From Boone and Gerba. 94rounds rubbed <strong>the</strong>ir eyes, and 33% picked <strong>the</strong>ir nose,with<strong>in</strong> a 1-hour observation period. 100A review <strong>of</strong> <strong>the</strong> data 94 (Table 6) suggests that <strong>the</strong> <strong>in</strong>fectiousdose for respiratory viruses is relatively small.Alford et al suggest that aerosolized doses <strong>of</strong> as little as1 TCID 50 (tissue culture <strong>in</strong>fective dose) <strong>of</strong> <strong>in</strong>fluenzavirus could <strong>in</strong>fect volunteers. 101Evidence for transmission <strong>of</strong> rh<strong>in</strong>ovirus and RSV <strong>in</strong>fectionsvia contam<strong>in</strong>ated <strong>hand</strong>s comes from a number<strong>of</strong> studies:d A number <strong>of</strong> studies have demonstrated that self<strong>in</strong>oculationby rubb<strong>in</strong>g <strong>the</strong> nasal mucosa or conjunctivaewith rh<strong>in</strong>ovirus-contam<strong>in</strong>ated f<strong>in</strong>gers canlead to <strong>in</strong>fection. 100,102 Over a period <strong>of</strong> 10 years,Gwaltny and Hayden performed <strong>in</strong>tranasal challengeson 343 healthy young adults who had no antibodyto <strong>the</strong> challenge, and <strong>in</strong>fected 321 (95%). 103After <strong>hand</strong>l<strong>in</strong>g contam<strong>in</strong>ated c<strong>of</strong>fee cups and o<strong>the</strong>robjects, more than 50% <strong>of</strong> subjects developed <strong>in</strong>fection.104 Hall et al showed that volunteers touch<strong>in</strong>gcontam<strong>in</strong>ated objects and/or <strong>the</strong> f<strong>in</strong>gers <strong>of</strong> symptomatic<strong>in</strong>dividuals had a higher attack rate <strong>of</strong> coldsif <strong>the</strong>y touched <strong>the</strong>ir eyes or nose. 105d In a 4-year family trial, Hendley and Gwaltney 104found that prophylactic treatment <strong>of</strong> mo<strong>the</strong>rs’ f<strong>in</strong>gerswith iod<strong>in</strong>e reduced <strong>the</strong> <strong>in</strong>cidence <strong>of</strong> RT <strong>in</strong>fections.When illness occurred <strong>in</strong> <strong>the</strong> family, mo<strong>the</strong>rswere <strong>in</strong>structed to dip <strong>the</strong>ir f<strong>in</strong>gers <strong>in</strong> iod<strong>in</strong>e uponawaken<strong>in</strong>g <strong>in</strong> <strong>the</strong> morn<strong>in</strong>g, <strong>the</strong>n every 3 or 4 hoursor after activities that washed <strong>the</strong> iod<strong>in</strong>e from <strong>the</strong>sk<strong>in</strong>. <strong>The</strong> secondary attack rate <strong>in</strong> mo<strong>the</strong>rs was 7%<strong>in</strong> <strong>the</strong> iod<strong>in</strong>e group and 20% <strong>in</strong> placebo families.No <strong>in</strong>fections occurred <strong>in</strong> mo<strong>the</strong>rs after 11 exposuresto an <strong>in</strong>fected <strong>in</strong>dex case <strong>in</strong> <strong>the</strong> iod<strong>in</strong>e group, comparedwith 5 <strong>in</strong>fections after 16 exposures <strong>in</strong> <strong>the</strong>placebo group.d Hall et al showed that <strong>in</strong>fected <strong>in</strong>fants excrete prodigiousamounts <strong>of</strong> RSV <strong>in</strong> <strong>the</strong>ir nasal secretions forseveral days 105 and that RSV could be recoveredfrom <strong>hand</strong>s that had touched surfaces contam<strong>in</strong>atedwith secretions from <strong>in</strong>fected <strong>in</strong>fants. 99 Hall andDouglas found that close contact with symptomatic<strong>in</strong>fants who were produc<strong>in</strong>g abundant secretions,
Bloomfield et al December 2007 S39or <strong>the</strong>ir immediate environment, was necessary for<strong>in</strong>fection. 106Sources and spread <strong>of</strong> RT pathogens to <strong>the</strong> <strong>hand</strong>s. Figure3 illustrates that <strong>the</strong> risk <strong>of</strong> exposure to RT pathogensvia <strong>hand</strong>s depends on <strong>the</strong> extent to which <strong>the</strong>sepathogens are spread from an <strong>in</strong>fected person dur<strong>in</strong>gnormal daily activities. Relevant data come from varioussources and are summarized below. Taken toge<strong>the</strong>r,<strong>the</strong> data suggest that, when a household member is<strong>in</strong>fected, exposure <strong>of</strong> o<strong>the</strong>r household members via<strong>hand</strong>s is likely to occur dur<strong>in</strong>g normal daily activitiesand that <strong>the</strong> numbers <strong>of</strong> organisms <strong>in</strong>volved are with<strong>in</strong>those required to <strong>in</strong>itiate <strong>in</strong>fection if transferred to <strong>the</strong>eyes or nose.People <strong>in</strong>fected with cold viruses shed large quantities<strong>of</strong> virus-laden mucus. Droplets <strong>of</strong> nasal secretionsgenerated by cough<strong>in</strong>g, sneez<strong>in</strong>g and talk<strong>in</strong>g can travelover a distance .3 m to contam<strong>in</strong>ate surround<strong>in</strong>gsurfaces. 37,98,107-109 Up to 10 7 <strong>in</strong>fectious <strong>in</strong>fluenza particlesper milliliter has been detected <strong>in</strong> nasal secretions.110 <strong>The</strong> mean duration <strong>of</strong> a cold is 7.5 days.Viral shedd<strong>in</strong>g may occur 24 to 48 hours before illnessonset but generally at lower titers than dur<strong>in</strong>g <strong>the</strong>symptomatic period. Titers generally peak dur<strong>in</strong>g <strong>the</strong>first 24 to 72 hours <strong>of</strong> illness and decl<strong>in</strong>e with<strong>in</strong> severaldays, with titers low or undetectable by day 5. Childrencan shed virus for up to 3 weeks, whereas immunocompromisedpeople may cont<strong>in</strong>ue to shed virus forweeks to months. 98Infectious material can also be deposited directly on<strong>hand</strong>s and tissues dur<strong>in</strong>g sneez<strong>in</strong>g and blow<strong>in</strong>g <strong>the</strong>nose. Contam<strong>in</strong>ation <strong>of</strong> <strong>hand</strong>s can occur by <strong>hand</strong>shak<strong>in</strong>gor touch<strong>in</strong>g contam<strong>in</strong>ated surfaces. Pathogens shed<strong>in</strong>to <strong>the</strong> environment from <strong>the</strong>se sources can survivefor significant periods and are readily spread around<strong>the</strong> home to and from <strong>the</strong> <strong>hand</strong>s and via <strong>hand</strong>kerchiefsand tissues, tap and door <strong>hand</strong>les, telephones, or o<strong>the</strong>r<strong>hand</strong> contact surfaces:ddGwaltney and Hendley demonstrated that most subjectswith experimental colds had rh<strong>in</strong>ovirus on <strong>the</strong>ir<strong>hand</strong>s and that virus could be recovered from 43% <strong>of</strong>plastic tiles <strong>the</strong>y touched. 104 For people with rh<strong>in</strong>oviruscolds, virus was found on 39% <strong>of</strong> <strong>hand</strong>s and 6%<strong>of</strong> objects <strong>in</strong> <strong>the</strong>ir immediate environment. 100 Reeddemonstrated recovery <strong>of</strong> virus from naturally contam<strong>in</strong>atedobjects <strong>in</strong> <strong>the</strong> surround<strong>in</strong>gs <strong>of</strong> personswith rh<strong>in</strong>ovirus colds. 102In a recent study, W<strong>in</strong><strong>the</strong>r et al 111 recruited volunteerssuffer<strong>in</strong>g from colds to stay overnight <strong>in</strong> hotelrooms. After checkout, but before room clean<strong>in</strong>g,10 objects identified as frequently touched weresampled for rh<strong>in</strong>ovirus. Virus was found on 35%<strong>of</strong> objects, <strong>in</strong>clud<strong>in</strong>g door <strong>hand</strong>les, light switches,pens, faucet and toilet <strong>hand</strong>les, and televisionremote controls. Some people contam<strong>in</strong>ated noneor few sites, most contam<strong>in</strong>ated several, and somecontam<strong>in</strong>ated almost all (up to 8) sites. In a secondstudy <strong>in</strong> which <strong>the</strong> same subjects stayed overnight<strong>in</strong> a hotel room <strong>in</strong> which <strong>hand</strong> contact surfaces (lightswitch phone button and <strong>hand</strong>set) had been contam<strong>in</strong>atedwith rh<strong>in</strong>ovirus-contam<strong>in</strong>ated mucus, 60% <strong>of</strong>subjects became contam<strong>in</strong>ated with rh<strong>in</strong>ovirus.d Ansari et al showed that <strong>hand</strong>s readily pick up rh<strong>in</strong>ovirusand PIV by touch<strong>in</strong>g contam<strong>in</strong>ated objects. 112As much as 70% <strong>of</strong> <strong>in</strong>fectious rh<strong>in</strong>ovirus has beenshown to transfer to a recipient’s f<strong>in</strong>gers after contactfor 10 seconds. 113 In a study with volunteers who<strong>hand</strong>led contam<strong>in</strong>ated doorknobs or faucets, recoveryrates from 3 to 1800 plaque-form<strong>in</strong>g units <strong>of</strong> rh<strong>in</strong>oviruswere obta<strong>in</strong>ed from f<strong>in</strong>gertips. 114d In a study <strong>of</strong> US day care centers and domestichomes, <strong>in</strong>fluenza A virus was detected on 23% <strong>of</strong>day care center surfaces sampled dur<strong>in</strong>g <strong>the</strong> fall <strong>of</strong>2003 and 53% <strong>of</strong> surfaces sampled dur<strong>in</strong>g <strong>the</strong> spr<strong>in</strong>g.Although no <strong>in</strong>fluenza was detected on home surfacesdur<strong>in</strong>g <strong>the</strong> summer, <strong>in</strong>fluenza was detected on59% <strong>of</strong> surfaces sampled dur<strong>in</strong>g March <strong>in</strong> 5 homes<strong>in</strong> which <strong>the</strong>re was an <strong>in</strong>fluenza-<strong>in</strong>fected child. No viruswas recovered from 3 o<strong>the</strong>r homes <strong>in</strong> which allhousehold members were healthy. Influenza viruswas recovered most frequently from telephone receivers(80%) and least frequently from computerkeyboards (40%). O<strong>the</strong>r surfaces found to be contam<strong>in</strong>ated<strong>in</strong>cluded refrigerators; kitchen faucets; lightswitches; microwaves; TV remote controls; doorknobs;and bath, faucet, and toilet <strong>hand</strong>les. Influenzavirus was recovered from 69% <strong>of</strong> <strong>the</strong> day care centerdiaper chang<strong>in</strong>g areas, <strong>in</strong>dicat<strong>in</strong>g presence <strong>of</strong> virus <strong>in</strong><strong>in</strong>fant feces. 94Transfer <strong>of</strong> RT <strong>in</strong>fections via contam<strong>in</strong>ated <strong>hand</strong>s dependson <strong>the</strong> ability <strong>of</strong> <strong>the</strong> virus to survive and reta<strong>in</strong>its <strong>in</strong>fectivity outside <strong>the</strong> human host. <strong>The</strong> potentialfor survival varies significantly between nonenvelopedrh<strong>in</strong>ovirus and RSV, compared with <strong>the</strong> enveloped <strong>in</strong>fluenzavirus and PIV:d Kramer et al 81 and Hendley et al 100 review data show<strong>in</strong>gthat rh<strong>in</strong>ovirus and RSV can survive for significantperiods (2 hours to 7 days for rh<strong>in</strong>ovirus, up to6 hours for RSV) on dry surfaces and for at least 2hours on human sk<strong>in</strong>.d Ansari et al 115 and Brady et al 116 showed that, althoughPIV can survive on nonabsorbent surfacesfor up to 10 hours, survival on <strong>hand</strong>s was relativelypoor (1-2 hours).d Bean et al 117 showed that <strong>in</strong>fluenza virus could surviveup to 24 to 48 hours on nonporous surfaces and up to8 to 12 hours on cloth, paper, and tissues. By contrast,virus could be recovered from <strong>hand</strong>s for only 5 m<strong>in</strong>utesand <strong>the</strong>n only if <strong>hand</strong>s were contam<strong>in</strong>ated with