Pediatr Infect Dis J, 2000;19:S97–102 Vol. 19, No.
10
Copyright © 2000 by Lippincott Williams & Wilkins, Inc.
Transmission of viral respiratory infections in
the home
DONALD A. GOLDMANN, MD
For centuries it was assumed that infectious dis-
eases were spread primarily by airborne miasms. Con-
temporary concepts of disease transmission include
Downloaded from http://journals.lww.com/pidj by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8K2+Ya6H515kE= on 05/09/2021
direct contact spread, indirect contact spread (primar-
ily via hands or fomites), endogenous infection, droplet
contact spread, airborne spread (droplet nuclei, skin
squames and fungal spores), common vehicle spread
and vector spread. Prevention of transmission of viral
infection in day care and the home requires a firm
understanding of how pathogens are transmitted.
Three viral pathogens provide insight into current
understanding of the transmission of infectious dis-
eases, as well as remaining knowledge gaps. Respira-
tory syncytial virus appears to be spread primarily by
hands contaminated by contact with contaminated
respiratory secretions. There is still considerably con-
troversy regarding the principal mode of transmission
for rhinovirus. Some investigators believe that contam-
ination of the hands followed by inoculation of the eyes
or nose is of paramount importance, whereas others
favor transmission by droplets and droplet nuclei. The
controversy regarding transmission of influenza cen-
ters on whether or not this virus can be spread by
airborne droplet nuclei. Experiments in animals and
natural experiments in humans provide considerable
support for airborne spread.
HISTORICAL PERSPECTIVE
Rational infection control measures require a clear
understanding of how pathogens are transmitted. Re-
search performed during this century has radically
transformed our knowledge of the epidemiology and
transmission of microorganisms. We now recognize
that transmission often is complex and multifactorial,
whereas scientists and laymen in earlier centuries
were fixated on the dangers of airborne spread. They
were convinced that disease was transmitted by mi-
asms, clouds of noxious vapors emanating from sewage
From the Division of Infectious Diseases, Department of Med-
icine Children’s Hospital, and Department of Pediatrics, Harvard
Medical School, Boston, MA.
Key words: Virus, home, cross-infection, respiratory syncytial
virus, rhinovirus, influenza.
Address for reprints: Donald A. Goldmann, M.D., Division of
Infectious Diseases, Children’s Hospital, 300 Longwood Ave.,
Boston, MA 02115. E-mail Don.Goldmann@TCH.harvard.edu.
S97
Printed in U.S.A.
and rotting organic matter. Accordingly those brave
souls who cared for victims of the plague wore hoods
with long beaks into which they placed herbs to mask
the odors of putrefying flesh and, ostensibly, to protect
them from contagion. The massive cholera epidemic in
London in 1849 provided a particularly good test of the
role of miasms in spreading disease. William Farr, a
noted epidemiologist who campaigned side by side with
Florence Nightingale for improved hygiene in hospi-
tals, believed that miasms from the polluted Thames
River were responsible for the outbreak. He demon-
strated a remarkably close inverse correlation between
elevation of habitation above the Thames and risk of
disease. However compelling these data may have
seemed at the time, John Snow proved that cholera was
spread by contaminated water, not putrid air, when he
halted the epidemic by removing the handle from the
Broad Street water pump. Belief in the importance of
miasms in transmitting infection succumbed slowly to
advances in science and epidemiology. Even at the turn
of the century, yellow fever and malaria (literally, from
the Italian for “bad air”) among workers digging the
Panama Canal was attributed to miasms rising from
the muck in the canal bed.
Just as air polluted with miasms was felt to be
important in contagion, so was clean air believed to be
critical in preventing and curing infectious diseases.
Fresh air and rest were the mainstays of tuberculosis
therapy in the preantimicrobial era. In the early part of
this century, hospital construction featured pavilions
with ready access to the outdoors. At Children’s Hos-
pital in Boston, for example, children routinely were
wheeled out onto sun porches in their individual carts
even on the coldest days so that they would have the
benefit of fresh air (Fig. 1). In summer children were
placed on a ship (the original Boston Floating Hospital,
from which the New England Medical Center origi-
nated) and sent out to Boston harbor so that they
would not be exposed to the foul air that enveloped the
city. This boat plied the waters of Boston Harbor until
it burned in 1927. A similar hospital ship operated out
of Southport in Manhattan.
The work of Wells and his protégé Riley at Johns
Hopkins Hospital in Baltimore radically transformed
our understanding of airborne transmission of infec-
tion.1 They demonstrated that tiny droplet nuclei pro-
S98 THE PEDIATRIC INFECTIOUS DISEASE JOURNAL
FIG. 1. Pediatric patients on a sun porch at Children’s Hospi-
tal, Boston. Children’s Hospital Archives.
duced by talking, coughing or sneezing could carry
microorganisms over considerable distances. These
droplet nuclei were just a few micrometers in size and
could easily waft on air currents and evade upper
respiratory tract host defenses. Their classic studies
demonstrated clearly that tuberculosis is transmitted
primarily via airborne droplet nuclei. Meanwhile un-
derstanding of other mechanisms of transmission was
expanding quickly. Building on the work of Semmel-
weiss, epidemiologists explored the role of transmis-
sion of microorganisms via the hands. The role of
contaminated food, water and fomites played was clar-
ified. It was recognized the large respiratory droplets
were important in the spread of some pathogens, such
as meningococci.
CURRENT UNDERSTANDING OF
TRANSMISSION OF MICROORGANISMS
Widely recognized mechanisms of transmission can
be classified as follows: direct contact spread (including
bloodborne transmission); contact spread (including
fecal-oral transmission); endogenous infection (autoin-
fection); droplet contact spread; airborne spread (drop-
let nuclei, skin squames or “rafts,” fungal spores);
common vehicle (common source) spread; vector
spread.
Direct contact spread results from direct contact
with an infected individual, as might occur when one
sibling spreads streptococcal impetigo to another dur-
ing play. Indirect contact involves contamination of an
intermediate object. Most often this “object” is the
hands. For example a mother who puts a dressing on
her child’s staphylococcal boil and does not wash her
hands might transmit staphylococci to another child
during diapering. Or a father who changes the diaper
of a child with Shigella gastroenteritis might transmit
this pathogen to the rest of the family if he prepares
lunch without washing his hands. Environmental ob-
jects, or fomites, may also be involved in indirect
Vol. 19, No. 10, Oct., 2000
contact spread of infection. For example cytomegalovi-
rus can be spread in day care if a child drools on a toy
and another child snatches it away and puts it in his
mouth. Campylobacter may be transmitted if a chop-
ping block used to cut up contaminated raw chicken is
subsequently used to prepare salad. Droplet contact
spread occurs over distances of no more than 3 or 4 feet
because these relatively large droplets quickly settle
out of the air. Large respiratory droplets can harbor
pathogens such as Bordetella pertussis, group A Strep-
tococcus and Neisseria meningitidis. Endogenous infec-
tion is caused by an individual’s own microbial flora.
For example if a father chokes on a piece of purloined
Halloween candy and aspirates oral secretions into his
lungs, he may develop pneumonia from his own oral
flora. Airborne spread via droplet nuclei already has
been explained. Airborne transmission can also occur
rarely via skin squames, or flakes, shed from the skin
of individuals heavily colonized with pathogens such as
staphylococci. British investigators use the more pic-
turesque term, “rafts,” which provides a vivid picture of
how skin squames ferry microorganisms through the
air. Fungal pathogens, such as coccidioidomycosis, can
be transmitted over amazingly long distances via fun-
gal spores stirred up by the wind. Fungal spores of
pathogens such as Aspergillus pose an airborne threat
to immunocompromised patients. Common vehicle
transmission occurs when many people are exposed to
a contaminated item. For example common vehicle
transmission might occur among children who con-
sume improperly processed apple cider contaminated
with Escherichia coli O157. Finally vector spread re-
fers to transmission via insects. This is rarely a prob-
lem in the home, but it is worth noting that the feet of
flies, ants and other insects can become contaminated
with pathogens in the environment and very rarely can
spread infection to humans. Of course mosquitoes can
transmit malaria, yellow fever, dengue and West Nile
encephalitis, and ticks carry Lyme disease and Rocky
Mountain spotted fever, to name just a few of the legion
of vector-borne infections.
Three viral respiratory pathogens, respiratory syn-
cytial virus, rhinovirus and influenza virus, that are
commonly encountered in the home provide excellent
illustrations of the basic principles of transmission of
microorganisms. They also demonstrate that signifi-
cant gaps persist in our understanding of the epidemi-
ology of common viral pathogens.
RESPIRATORY SYNCYTIAL VIRUS (RSV)
RSV is the major cause of viral respiratory infection
in young children worldwide. Attendance in day care
virtually guarantees that an infant will be infected
with RSV within the first year or two of life. Bronchi-
olitis is the major clinical manifestation, resulting in
hospitalization of 0.5 to 1.0% of infected infants.
Vol. 19, No. 10, Oct., 2000 THE PEDIATRIC INFECTIOUS DISEASE JOURNAL
Although it would seem logical that a respiratory
virus would be spread primarily by droplets or droplet
nuclei, this does not appear to be the case with RSV. In
a classic study Hall et al.2 in Rochester demonstrated
that direct and indirect contact transmission were far
more important. Highly symptomatic infants who were
producing abundant secretions were placed in cribs.
Three categories of nurse volunteers were brought into
the room. “Cuddlers” played with the infant, changed
his or her diaper and performed other routine care.
“Touchers” did not touch the baby but had extensive
contact with the child’s environment, which had been
heavily contaminated with secretions. “Sitters” sat
next to the crib reading a book for 3 h but did not touch
anything in the immediate environment. Five of the 7
cuddlers, 4 of 10 touchers and none of 14 sitters
developed RSV infection. In retrospect the reasons for
these striking findings are clear. Infants with RSV
excrete prodigious concentrations of virus in their na-
sal secretions for a number of days.3 RSV survives
quite well on inanimate objects, more than 5 h on
impervious surfaces such as a countertop, providing
caregivers with abundant opportunities to contaminate
their hands (Fig. 2).4 Once the hands are contami-
nated, virus can be spread by indirect contact to other
children. In addition if caregivers touch their eyes or
nose before washing their hands, they can infect them-
selves, with attack rates during the annual fall/winter
RSV season approaching 50%.5 RSV in adults often is
manifested as a severe cold, and sick caregivers subse-
quently can infect others by direct contact.
Studies of nosocomial RSV infection conducted at
Children’s Hospital provide additional support for the
importance of indirect contact spread.6 Surreptitious
surveillance of nurses’ compliance with gown and glove
precautions demonstrated complete adherence in only
FIG. 2. Survival of respiratory syncytial virus on surfaces.
TCID50, 50% tissue culture-infectious doses.4
S99
38.5% of encounters with symptomatic infants. After
open surveillance was initiated, compliance reached
95% and remained at that level even after open sur-
veillance was discontinued. Improved compliance re-
sulted in a dramatic decline in the rate of nosocomial
RSV infection, from 6.4 to 3.1 cases per 1000 patient
days. Although the attack rate increased as the num-
ber of patients with community-acquired RSV infection
on the ward increased, the slope of this relationship
decreased dramatically (Fig. 3). The impact of strict
compliance with gown and glove precautions was most
impressive during the height of the seasonal epidemic
in the community. Thus barrier precautions are an
extremely effective deterrent to the transmission of
RSV, provided that they are observed on contact with
both the infected infant and its contaminated environ-
ment. Presumably gloving was more important than
gowning because it is difficult to imagine extensive
indirect contact transmission via clothing.
It is entirely reasonable to assume that careful
handwashing after contact with infected babies and
their environment would have been equally effective in
reducing the risk of nosocomial RSV infection. Hand-
washing agents containing detergents or alcohol are
quite effective at killing RSV, although chlorhexidine
without alcohol is not.7
Some investigators have advocated performing rapid
tests for RSV on all symptomatic infants during the
annual RSV season and cohorting RSV-positive patients
with contact precautions. This approach was more effec-
tive than gowns and gloves or cohorting alone in one
study,8 although compliance was not measured. In an-
other study the rate of nosocomial infection in a newborn
nursery declined when rapid testing was combined with
cohorting, visitation restrictions and gowns, gloves and
masks.9 However, it may not be cost effective to test
routinely all symptomatic infants for RSV, because a
child presenting with bronchiolitis during the annual
RSV season is very likely to have RSV infection.
FIG. 3. Correlation between incidence density of nosocomial
respiratory syncytial virus infection and exposure to patients
excreting virus.6
S100 THE PEDIATRIC INFECTIOUS DISEASE JOURNAL
RHINOVIRUS
The common cold is an extraordinarily noisome im-
pediment to everyday quality of life. Children can
expect to suffer approximately four to eight episodes
per year, and adults might have three to five episodes
annually. Although many viruses can produce the
symptoms of a cold (e.g. parainfluenza viruses, RSV,
coronaviruses), rhinovirus is the most frequent cause of
the common cold and the best studied from an epide-
miologic point of view. Unfortunately there are more
than 100 distinct serologic types of rhinovirus, and
exposure to one rhinovirus does not confer significant
immunity against other serotypes.
Work at the Common Cold Research Unit in Salis-
bury, England, after World War II definitively estab-
lished that colds could be produced by inoculating
secretions from infected patients into the nose or eyes
of volunteers, who were happy to have a vacation in a
facility with central heating and a fine view.10 When
rhinovirus was established as an etiologic agent for the
common cold, these findings were replicated by inocu-
lating volunteers with live virus.11 Interestingly sub-
sequent work demonstrated that it was exceedingly
difficult to transmit the virus orally or by kissing.12
The question remained as to whether rhinovirus is
transmitted primarily by direct contact, indirect con-
tact, droplet contact or droplet nuclei. This seemingly
innocuous issue has produced intense controversy, pri-
marily between investigators from the University of
Virginia (who believe that contact with secretions is
the principal mode of spread) and researchers at the
University of Wisconsin (who have found evidence for
airborne spread). The Virginia group (Hendley and
Gwaltney) demonstrated that most subjects with ex-
perimental colds had rhinovirus on their hands and
that rhinovirus could be recovered from 43% of plastic
tiles they touched.13 When the Virginia group studied
natural rhinovirus colds, virus was found on 39% of
hands of symptomatic individuals and on 6% of objects
in their immediate environment.14 Virus could survive
for hours or even days on environmental surfaces and
for at least 2 h on human skin. Volunteers who had
contact with contaminated objects or with fingers of
individuals with rhinovirus colds had a high rate of
infection if they inoculated their own nose or eyes. Any
doubt about the tendency of individuals to put their
potentially contaminated fingers in their nose or eye
was dispelled by Hendley et al.,14 who found that
one-third of grand rounds attendees picked their nose
and one in 2.7 rubbed their eyes during the 1-h lecture.
Perpetrators tended to repeat these maneuvers. Trans-
mission could be interrupted by treating surfaces with
disinfectant or applying iodine to the fingers.15
In a randomized trial of families with children,
Hendley and Gwaltney15 found that prophylactic treat-
ment of mothers’ fingers with iodine reduced the inci-
Vol. 19, No. 10, Oct., 2000
dence of secondary respiratory infections in these
mothers. Specifically when illness occurred in the fam-
ily, mothers were instructed to dip their fingers in
iodine or a colored placebo upon awakening in the
morning, then every 3 or 4 h or after activities that
washed the iodine from the skin. Because iodine has
residual activity on the hands, it was hypothesized that
if virus-laden secretions contaminated fingertips, it
would be killed on contact. In 4 years of evaluation the
secondary attack rate in mothers was 7% in the iodine
group and 20% in placebo families. No confirmed rhi-
novirus infections occurred in susceptible mothers af-
ter 11 exposures to an index case with proven rhinovi-
rus infection in the iodine group, vs. 5 infections after
16 exposures in the placebo group (P ⫽ 0.1).
In contrast to these studies, which emphasized the
importance of indirect contact spread of rhinovirus via
contaminated fomites and fingers, the Virginia group
found little evidence for transmission via droplets or
droplet nuclei. Exposure of volunteers to infected indi-
viduals across a small table (providing an opportunity
for both droplet and droplet nucleus transmission)
resulted in only an 8% infection rate, far less than the
rate with self-inoculation via contaminated hands.16
Moreover no infection was seen when infected and
uninfected volunteers faced each other through a wire
mesh.
Meanwhile the Wisconsin group was performing
very intriguing studies in various “natural” models of
exposure to rhinovirus colds. In one model sick volun-
teers were housed with susceptible volunteers in a
room 11.9 by 5.8 by 2.7 m17 (Fig. 4). The volunteers
played board, card and video games during the study.
The pool of virus “donors” was constantly replenished
with highly symptomatic volunteers when nasal secre-
tions began to diminish. A somewhat surprising result
of these studies was the length of exposure required for
infection in the recipients; 200 h of exposure was
FIG. 4. Experimental conditions for studying the transmission
of rhinovirus colds.17
Vol. 19, No. 10, Oct., 2000 THE PEDIATRIC INFECTIOUS DISEASE JOURNAL
FIG. 5. Correlation of hours of exposure to individuals with
rhinovirus colds and the risk of infection.17
required to achieve a 50% attack rate (Fig. 5). Dick and
his colleagues contended that the exposure times in the
Virginia studies were inadequate to rule out droplet
and airborne transmission.
The Wisconsin group extended these studies in an
ingenious experimental model in which donors and
recipients played poker for 12 h sitting at round ta-
bles18 (Fig. 6). Three trials were performed, which
included 24 donors and 36 recipients. One-half of the
recipients were fitted with diabolical restraints, either
arm braces that allowed them to play cards but not
touch their face or a shield that left the hands free but
kept them away from the face. The attack rates for
rhinovirus infection in the restrained and unrestrained
recipient volunteers were 56 and 67%, respectively,
strongly supporting transmission via the air, not the
hands. Furthermore when 12 susceptible volunteers
were removed to a separate room and compelled to play
stud poker with chips and cards heavily contaminated
with secretions from ill volunteers, none became ill.
Surprisingly, relatively low titers of virus were found
even on chips and cards that were sticky with secre-
tions. The Wisconsin group argued that the high rate of
FIG. 6. Experimental conditions for studying the transmission
of rhinovirus colds during a poker game. D, donor; R, recipient.18
S101
transmission via the hands in the Virginia experiments
might be attributable to intensive contact with fresh
wet secretions produced by volunteers who essentially
blew their nose into their hand.
INFLUENZA
The explosive spread of influenza after the annual
introduction of virus into a community suggests air-
borne transmission. However, there are surprisingly
few studies that shed light on this issue.
The ferret model of influenza provides a convenient
system in which to study the transmission of influen-
za.19 Efficient transmission of infection from ill to
susceptible ferrets was documented regardless of
whether the ferrets were separated by a long straight
air duct or by ducts in the shape of a “s” or “u.”
Presumably, large respiratory droplets could not nego-
tiate the bends in the ducts, whereas aerosols of droplet
nuclei could. Studies in a mouse model of influenza also
supported transmission by droplet nuclei.20 These ex-
periments were replicated in a natural human experi-
ment in the Veterans Administration Hospital in Liv-
ermore, CA.21 Patients with tuberculosis were housed
either in a building with ceiling ultraviolet radiation or
in a nonirradiated building, depending on the stage of
their tuberculosis management. The attack during the
1957 to 1958 influenza season was only 2% in the
irradiated group, compared with 19% in the nonirradi-
ated patients and 18% in hospital personnel.
Perhaps the most dramatic evidence for airborne
spread of influenza occurred during a flight from An-
chorage to Kodiak, with an intermediate stop in
Homer, AK.22 The plane experienced mechanical diffi-
culty in Homer and had to remain on the ground, its
ventilation system inoperative, for a number of hours.
Within 72 h 72% of the 54 people on the plane became
ill with typical symptoms of influenza. The attack rate
was highest in those who remained on the crippled
plane the longest; the 6 passengers who immediately
deplaned remained well. This point-source outbreak
was initiated by a 21-year-old woman who boarded the
flight in Homer and developed fever, chills and cough
within 15 min. During her stay on board, people on the
plane moved about frequently, but few had close con-
tact with her. It appeared that airborne spread was
responsible for this outbreak, perhaps aided by the
relatively low humidity, which prolongs survival of
influenza virus.
SUMMARY
Respiratory viruses in the home exploit multiple
modes of transmission. RSV is transmitted primarily
by contact with ill children and contaminated objects in
the environment. Influenza appears to be spread
mainly by airborne droplet nuclei. Despite many years
of study, from the plains of Salisbury, to the hills of
S102 THE PEDIATRIC INFECTIOUS DISEASE JOURNAL
Virginia, to the collegiate environment of Madison, WI,
the precise routes rhinovirus takes to inflict the misery
of the common cold on a susceptible population remain
controversial.
REFERENCES
1. Wells WF. Airborne contagion and air hygiene. Boston: Har-
vard University Press, 1955.
2. Hall CB, Douglas RG. Modes of transmission of respiratory
syncytial virus. J Pediatr 1981;99:100 –3.
3. Hall CB, Douglas RG Jr, Geiman JM. Respiratory syncytial
virus infections in infants: quantitation and duration of
shedding. J Pediatr 1976;89:11–15.
4. Hall CB, Douglas RG Jr, Geiman JM. Possible transmission
by fomites of respiratory syncytial virus. J Infect Dis 1978;
88:203–5.
5. Hall CB. Nosocomial viral respiratory infections: perennial
weeds on pediatric wards. Am J Med 1981;70:670 – 6.
6. Leclair JM, Freeman J, Sullivan BF, Crowley CM, Goldmann
DA. Prevention of nosocomial respiratory virus infections
through compliance with glove and gown isolation precau-
tions. N Engl J Med 1987;317:329 –34.
7. Platt J, Bucknall RA. The disinfection of respiratory syncytial
virus by isopropanol and a chlorhexidine-detergent hand-
wash. J Hosp Infect 1985;6:89 –94.
8. Madge P, Paton JY, McColl JH, Mackie PLK. Prospective
controlled study of four infection control procedures to pre-
vent nosocomial infection with respiratory syncytial virus.
Lancet 1992;340:1079 – 83.
9. Snydman DR, Greer C, Meissner HC, McIntosh K. Prevention of
nosocomial transmission of respiratory syncytial virus in a
newborn nursery. Infect Control Hosp Epidemiol 1988;9:105– 8.
Vol. 19, No. 10, Oct., 2000
10. Tyrell DAJ. Common colds and related diseases. Baltimore:
Williams & Wilkins, 1965.
11. D’Alession DJ, Peterson JA, Dick CR, et al. Transmission of
experimental rhinovirus colds in volunteer married couples.
J Infect Dis 1976;133:28 –36.
12. Hendley JO, Wenzel RP, Gwaltney JM Jr. Transmission of
rhinovirus colds by self-inoculation. N Engl J Med 1973;288:
1361– 4.
13. Gwaltney JM Jr, Hendley JO. Transmission of experimental
rhinovirus infection by contaminated surfaces. Am J Epide-
miol 1982;116:828 –33.
14. Hendley JO, Wenzel RP, Gwaltney JM Jr. Transmission of
rhinovirus colds by self-inoculation. N Engl J Med 1973;288:
1361– 4.
15. Hendley JO, Gwaltney JM Jr. Mechanisms of transmission of
rhinovirus infections. Epidemiol Rev 1988;10:242–58.
16. Gwaltney JM Jr, Moskalski PB, Hendley JO. Hand-to-hand
transmission of rhinovirus colds. Ann Intern Med 1978;88:
463–7.
17. Jennings LC, Dick EC. Transmission and control of rhinovi-
rus colds. Eur J Epidemiol 1987;3:327–35.
18. Dick EC, Jennings LC, Mink KA, et al. Aerosol transmission
of rhinovirus colds. J Infect Dis 1987;156:442– 8.
19. Andrewes CH, Glover RE. Spread of infection from the
respiratory tract of the ferret: I. Transmission of influenza A
virus. Br J Exp Pathol 1941;22:91–7.
20. Schulman JL, Kilbourne ED. Airborne transmission of influ-
enza virus infection in mice. Nature 1962;195:1129 –30.
21. McLean RL. General discussion. Am Rev Respir Dis 1961;83:
36 – 8.
22. Moser MR, Bender TR, Margolis HS, Noble GR, Kendal AP,
Ritter DG. An outbreak of influenza aboard a commercial
airliner. Am J Epidemiol 1979;110:1– 6.