MAJOR ARTICLE
Risk of Vaccinia Transfer to the Hands of Vaccinated
Persons after Smallpox Immunization
Thomas R. Talbot,1 Ellis Ziel,2 Jennifer K. Doersam,2 Bonnie LaFleur,3 Sharon Tollefson,2 and Kathryn M. Edwards2
Departments of 1Medicine, 2Pediatrics, and 3Preventive Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee
Transmission of vaccinia virus after smallpox vaccination is a concern. We conducted a prospective examination
of the protection afforded by vaccination-site bandages in recently vaccinated individuals. After smallpox
vaccination, inoculation sites were covered with 2 occlusive dressings. Site assessment and bandage changes
occurred every 3–5 days until the site was healed. At each visit, specimens from the vaccination site, outer
dressing surface, and contralateral hand were obtained for vaccinia culture. For 148 vaccinated subjects, vaccinia
was detected from vaccination lesions of every subject on several occasions. Only 6 (0.65%) of 918 dressing
(95% CI, 0.24%–1.4%) and 2 (0.22%) of 926 hand (95% CI, 0.03%–0.78%) specimens tested positive for
vaccinia. The mean number of bandage changes was 9.6 (95% CI, 9.17–10.0). Vaccinia autoinoculation did
not occur. The rate of vaccinia recovery outside occlusive bandages covering smallpox vaccination sites was
remarkably low, suggesting excellent protection against inadvertent transmission.
Routine smallpox vaccination ended in 1972 because
of a decreasing incidence of disease and increasing concern about vaccine safety [1]. With the recent bioterrorism attacks involving anthrax and the heightened
concern for intentional release of other biologic agents,
the United States reinstituted smallpox vaccination in
January 2003. In a 3-phase plan for vaccination, military and first-responder teams of selected health care
workers were initially vaccinated. The first phase encountered resistance because many health care facilities
and providers declined to participate as a result of con-
Received 5 September 2003; accepted 16 October 2003; electronically published
28 January 2004.
Presented in part: 13th Annual Meeting of the Society of Healthcare
Epidemiology of America, Arlington, Virginia, 7 April 2003 (abstract 264).
Financial support: National Institute of Allergy and Infectious Diseases Division
of Microbiology and Infectious Diseases (study 02-054, contract N01-AI-25462)
and Emerging Infections Diseases Cooperative Agreement (salary support for T.R.T.).
J.K.D. receives 2% salary support from Aventis Pasteur for work on another study.
Reprints or correspondence: Dr. Thomas R. Talbot, A-4103C Medical Center N.,
1161-21st Ave. S., Vanderbilt University Medical Center, Nashville, TN 37232
(tom.talbot@vanderbilt.edu).
Clinical Infectious Diseases 2004; 38:536–41
2004 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2004/3804-0011$15.00
536 • CID 2004:38 (15 February) • Talbot et al.
cerns of possible transmission of vaccinia virus to atrisk patients [2].
Smallpox vaccination entails the induction of a localized skin infection from live vaccinia virus, a related
poxvirus, to confer immunity to smallpox (variola).
Spread of vaccinia virus occurs predominantly through
contact. Individuals may transmit virus from their vaccination sites, potentially leading to substantial morbidity and even mortality in immunocompromised patients or those with eczema [3]. The risk of nosocomial
transmission of vaccinia from a vaccinated health care
worker has been thought by some to pose a greater risk
than the possibility of smallpox release [4].
Precautions to reduce the potential spread of vaccinia
from vaccinated individuals include application of an
occlusive bioadhesive dressing over the lesion site and
careful attention to dressing care and hand hygiene.
The recent civilian and military vaccination campaigns
reassuringly illustrated the efficacy of this approach:
there were rare cases of secondary vaccinia transmission
[5, 6]. In a clinical investigation that complements the
practical experience seen in these vaccination campaigns, we conducted a prospective surveillance study
by using viral culture data to investigate the recovery
of vaccinia from vaccination sites covered by occlusive
bandages.
PATIENTS, MATERIALS, AND METHODS
Study subjects. Subjects for this study were recruited from
individuals enrolled at a study site (Vanderbilt University; Nashville, TN) participating in a multicenter, double-blind, randomized clinical trial investigating the safety and efficacy of 3
different dilutions of the Aventis Pasteur smallpox vaccine
(APSV), a liquid formulation of calf lymph origin smallpox
vaccine derived from the New York Board of Health vaccinia
strain and maintained frozen at ⫺20C. In this trial, healthy
vaccinia-naive subjects aged 18–32 years were recruited; those
who met appropriate screening qualifications and who did not
meet any of the exclusion criteria for vaccination (table 1) were
enrolled. All vaccinated subjects were eligible for participation
in the prospective culture surveillance study, which was conducted under a separate consent process. Both the randomized
trial and the surveillance study were approved by the Vanderbilt
University Institutional Review Board; all subjects consented
to both studies. Human experimentation guidelines of the US
Department of Health and Human Services and Vanderbilt
University were followed in the conduct of this research.
Vaccination methods and follow-up. As a part of the safety
and efficacy trial, eligible subjects were randomized to receive
1 of 3 strengths of APSV (undiluted or dilutions of 1:5 or 1:
10). Frozen vaccine was reconstituted with diluent containing
glycerin, phenol, and sterile water and was administered in the
deltoid area via scarification by 15 punctures with a bifurcated
Table 1.
needle, as described elsewhere [1]. Vaccination sites were covered with 2 occlusive bandages, an initial waterproof gauzeimpregnated transparent bandage (Opsite Post-Op; Smith &
Nephew) and an outer waterproof semipermeable bandage (Tegaderm; 3M HealthCare). Subjects were seen in clinic every 3–
5 days for scheduled dressing changes, assessment of vaccine
response, and adverse event evaluation. These dressing changes
were performed by the study staff until the vaccination site was
well scabbed, which usually occurred several weeks after vaccination. Subjects were taught how to remove old dressings and
apply new ones in case an unscheduled dressing change was
needed before the next clinic visit. Sterile gloves and clean
bandages were provided to each volunteer. Subjects were instructed to place soiled bandages in biohazard bags provided
by study staff and to dispose of the bags at the next scheduled
clinic visit. Subjects were also repeatedly counseled at each visit
to avoid manipulation of the vaccination site and dressing and
to use gloves and thoroughly wash hands after any dressing
manipulation. There were no restrictions on work activities
after vaccination, in accordance with the US Centers for Disease
Control and Prevention guidelines [7]. At all follow-up visits,
each subject was assessed by history, symptom report, and physical examination for evidence of autoinoculation. Because of
study constraints, close contacts of subjects were not actively
examined for evidence of secondary transmission.
Culture methods. Samples for viral culture were obtained
from each subject at each scheduled follow-up visit, beginning
with the first visit 3–5 days after vaccination. We used cottontipped swabs to obtain specimens from the palmar surface of
the index finger on the hand contralateral to the dressing site
Exclusion criteria for vaccinia vaccination.
History of autoimmune disease
Use of immunosuppressive medications
History of HIV infection
History of solid-organ or bone marrow transplantation
History of malignancy
History of or current illegal injection drug use
Eczema (active or quiescent)
Current exfoliative skin disorders
Prior vaccination with any vaccinia-vectored or other pox-vectored experimental vaccine
Presence of medical or psychiatric conditions or occupational responsibilities which precluded subject
compliance with the protocol
Acute febrile illness (temperature, ⭓38.1C) on the day of vaccination
Allergies to components of the vaccine
Presence of a typical vaccinia scar or history of smallpox vaccination
Pregnancy or lactation for women
Household or sexual contacts with any of the following conditions or factors: history of or concurrent
eczema, history of exfoliative skin disorders, history of the immunosuppressive conditions noted
above, ongoing pregnancy, or children aged !12 months
Risk of Vaccinia Transfer • CID 2004:38 (15 February) • 537
(hand sample), from the outer surface of the outer dressing
before bandage removal (dressing sample), and from the vaccination site lesion (lesion sample) at each visit. Before the
hand and dressing samples were obtained, the swabs were moistened with sterile saline. However, a dry swab was used to obtain
the lesion sample to avoid disruption of the healing process.
Samples were obtained at each clinic visit until the lesion was
well scabbed without drainage and no longer required dressing.
Study staff changed gloves between the removal of the old
bandage and the placement of the new bandage. Samples of
the vaccination lesions were obtained at day 28 after vaccination
for all subjects, regardless of the lesion status. In those subjects
whose sites had not yet healed, dressing and hand samples were
also obtained for culture.
By means of methods described elsewhere [8], specimens
were directly inoculated into 1 mL of standard Hank viral transport media and frozen at ⫺70C for batch processing. It was
expected that vaccinia would be recovered from a majority of
the lesion specimens, because these cultures were obtained from
direct contact with the vaccinia pustule. All lesion specimens
were inoculated undiluted and at dilutions of 1:10, 1:100, and
1:1000 in triplicate directly onto plates coated with BSC-40
cells (African green monkey kidney) and washed with sterile
PBS. After incubation, cells were fixed with formalin and
stained with crystal violet to visualize the presence of characteristic vaccinia plaques. Plates without plaque formation at 2
days were considered to be negative for vaccinia. Quantitative
titers for positive specimens were expressed as the average of
the triplicate counts in log10 plaque-forming units (pfu) per
milliliter. Specimens with titers that were too high to quantify
at initial dilution underwent further dilutions up to 1:100,000.
Because vaccinia recovery was expected to be low from the
hand and bandage specimens, undiluted specimens were
screened for the presence of vaccinia before performing triplicate dilutions. Specifically, 0.2 mL of each hand and dressing
specimen was inoculated undiluted into tubes coated with BSC40 cells. The presence of distinctive cytopathic effect (CPE) [9]
was assessed every 48–72 h. Tubes without CPE at 10 days were
considered to be negative for vaccinia. Positive hand and bandage specimens were then titrated for the lesion specimens, as
described above. As the study progressed, it became apparent
that all vaccinia-positive hand and bandage specimens that exhibited CPE within 10 days after inoculation also developed
viral plaques within 48 h when inoculated on the titration
plates. Therefore, to reduce the screening time from 10 to 2
days, midway through the study, undiluted hand and dressing
specimens were inoculated directly onto the tissue plates and
screened for pfu. Specimens with plaque formation at 48 h
were then titrated as described above for the lesion specimens.
Clinical data collection. Demographic information (age
and sex) was obtained at the start of the study. At each follow538 • CID 2004:38 (15 February) • Talbot et al.
up visit, data on the number of dressing changes performed
by the subject since the previous clinic visit (unscheduled
changes) and on concurrent illnesses were collected. Data were
abstracted from charts at study completion for information on
adverse local and systemic findings after vaccination, including
the development of fever (temperature, ⭓38.4C), local axillary
lymphadenopathy, and focal satellite lesions of vaccinia around
the initial site.
Analysis. Rates of vaccinia retrieval were expressed as the
number of positive cultures for each specimen type per total
cultures obtained. Clinical characteristics were compared
among subjects with ⭓1 positive dressing specimen to those
without any positive dressing culture results. Categorical variables were compared by Fisher’s exact test, and continuous
variables were compared by Student’s t test for normally distributed data and the Wilcoxon rank sum test for nonparametric data. A similar comparison between those subjects with
and without positive hand specimen results was planned as
well.
RESULTS
All 148 volunteers enrolled in the primary clinical trial at Vanderbilt University participated in the surveillance study. The
mean age (SD) of the cohort was 23.6 3.65 years; 56%
of the subjects were female. The cohort consisted of health care
workers, students enrolled in area colleges and universities, and
other community members. All subjects completed follow-up.
The specific dilution of vaccine received was evenly distributed
among the 3 potencies (undiluted vaccine, 51 subjects; 1:5
dilution, 48; 1:10 dilution, 49). Subjects completed an average
of 6.9 follow-up visits (95% CI, 6.79–7.10) for a mean duration
of follow-up of 27.9 days (95% CI, 27.5–28.2). Bandages were
changed an average of 9.6 times (95% CI, 9.17–10.0; mean
number of scheduled changes, 6.9 [95% CI, 6.75–7.05]; mean
number of unscheduled changes, 2.7 [95% CI, 2.30–3.08]).
There was no evidence of autoinoculation of vaccinia in any
subject.
Table 2. Summary of data for 2843 specimens collected for viral
culture and titer results from positive specimens obtained from
patients who received smallpox vaccination.
No. (%) of
a
Total no. of specimens Peak titer, Titer range,
log10
specimens
positive
mean log10
Specimen site obtained for vaccinia
pfu/mL
pfu/mL
Lesion
999
5.25
2.7–7.3
Dressing
918
6 (0.65)
1.77
0.5–2.7
Hand
926
2 (0.22)
1.40
1.0–1.8
NOTE.
a
773 (77)
pfu, Plaque-forming units.
For specimens positive for vaccinia.
vaccination. Each sample had a titer of 1.0 log10 pfu/mL; the
results of the culture of the dressing sample at this visit were
negative. Because of the small number of positive hand culture
results, we were unable to perform an analysis of risk factors
for retrieval of vaccinia from the hands, such as hand hygiene
or number of bandage changes.
DISCUSSION
Figure 1. Course of vaccinia shedding from the vaccination site of a
representative subject. Numbers on the curve correspond to specific virus
titers.
A total of 2843 specimens (999 lesion samples, 918 dressing
samples, and 926 hand samples) were obtained (table 2). Vaccinia was isolated from the vaccination lesions of every subject
on multiple occasions (mean total number of positive lesion
cultures, 5.22; 95% CI, 5.06–5.39). Peak lesion titers occurred
an average 12.8 days after vaccination (95% CI, 12.3–13.3 days),
with a mean peak lesion titer of 5.25 log10 pfu/mL (95% CI,
5.13–5.38 log10 pfu/mL; range, 2.7–7.3 log10 pfu/mL). A typical
time course of vaccinia shedding is shown in figure 1.
Only 6 (0.65%) of 918 dressing samples (95% CI, 0.24%–
1.4%) were positive for vaccinia. The range for dressing specimen titers was 0.5–2.7 log10 pfu/mL, with a mean peak titer
of 1.77 log10 pfu/mL (95% CI, 0.82–2.71 log10 pfu/mL). The
mean time to a positive dressing culture was 10.2 days (95%
CI, 6.47–15.2 days), with 5 of the 6 positive specimens obtained
7–10 days after vaccination (figure 2). Although 6 (4.1%) of
148 subjects (95% CI, 1.5%–8.6%) had 1 positive dressing specimen result, vaccinia was not recovered on a second occasion
from any subject. There was no significant difference between
individuals with and without a positive dressing specimen result
with regard to age, sex, dilution of vaccine received, number
of dressing changes (scheduled, unscheduled, and total), time
to site healing, occurrence of fever or lymphadenopathy, occurrence of satellite lesions, peak lesion culture titer, mean lesion culture titer, total duration of follow-up, or total number
of follow-up visits (table 3). Rarely, subjects presented at followup without a dressing covering the site, and a dressing culture
could not be obtained.
Vaccinia was recovered from only 2 (0.22%) of 926 hand
specimens (95% CI, 0.03%–0.78%), each of which had been
obtained from a different subject (figure 2). For one subject,
vaccinia was recovered from the hand, dressing, and lesion
specimens 10 days after vaccination. Virus titers at this time
were 4.6 log10 pfu/mL at the vaccination site, 2.7 log10 pfu/mL
on the outer dressing, and 1.8 log10 pfu/mL on the hand. The
other subject with a positive hand culture result had vaccinia
recovered from both the hand and the lesion at 15 days after
Our investigation provides contemporary viral culture surveillance confirming that the risk of inadvertent vaccinia transmission from vaccination sites covered by occlusive bandages
to areas outside of the bandage is quite low. Although a direct
correlation between the recovery of vaccinia on a vaccinated
person’s hands and cases of secondary contact spread has not
been established, the extremely low rate of vaccinia recovery
outside of the occlusive bandage provides great reassurance that
contact transmission is unlikely.
The inadvertent transmission of vaccinia to unvaccinated
individuals (“contact vaccinia”) has been a particular concern
for health care workers as a result of potential transmission to
immunosuppressed patients [3]. Precautions to prevent spread
of vaccinia include the use of occlusive bandages over the site,
careful attention to dressing care, and meticulous hand hygiene.
The low incidence of contact vaccinia in the recent civilian and
military vaccination campaigns in the United States has provided reassurance regarding the very low risk of vaccinia transmission when proper bandaging and hand hygiene practices
are used [5, 6]. There have been no reported cases of contact
spread to date in the civilian campaign [5]. In the military
experience, only 21 cases of contact vaccinia occurred over
306,673 person-months of contact [6]. Our data, which use
viral culture information, provide additional support for these
findings.
Figure 2. Time line of retrieval of dressing (solid bars) and hand
(hatched bars) culture specimens positive for vaccinia in relation to the
day of smallpox vaccination. One subject had positive results of both a
hand and a dressing culture on day 10 after vaccination; the second
subject with a positive hand specimen result did not have vaccinia recovered from any dressing specimen.
Risk of Vaccinia Transfer • CID 2004:38 (15 February) • 539
Table 3. Comparison between subjects who had vaccinia recovered from dressing
specimens with those who had negative dressing specimen results among subjects
who received smallpox vaccination.
Characteristic
Age, mean years SE
No. (%) of male subjects
Subjects with a
positive dressing
culture result
(n p 6)
Subjects with a
negative dressing
culture result
(n p 142)
21.8 0.72
23.7 0.31
3 (50)
62 (43.7)
Undiluted
2 (33)
47 (33.1)
1:5
2 (33)
46 (32.4)
1:10
2 (33)
49 (34.5)
Dilution of vaccine, no. (%) of patients
No. of dressing changes, mean SE
Scheduled
6.83 0.40
6.90 0.08
3.5 0.76
2.65 0.20
10.33 0.92
9.56 0.22
Time to lesion healing, mean days SE
24.0 1.95
24.2 0.37
Lesion titer, mean log10 pfu/mL SE
2.46 0.13
2.56 0.05
Peak lesion titer, log10 pfu/mL, mean SE
5.37 0.42
5.25 0.06
Unscheduled
Total
Development of fever
1 (16.7)
18 (12.7)
Development of lymphadenopathy
3 (50)
87 (61.3)
Presence of satellite lesions
1 (16.7)
18 (12.7)
Total duration of follow-up, mean days SE
Total no. of follow-up visits, mean SE
NOTE.
27.3 0.33
27.9 0.19
7.0 0.37
6.94 0.08
There were no significant differences between the 2 groups for any noted variable.
Before the recent campaign and our investigation, studies
conducted on recombinant HIV-vaccinia virus vaccines had
evaluated the infectivity of the vaccination lesions and the protection provided by standard dressings. In one trial, the vaccination site was covered by gauze and 2 occlusive bandages,
and outer bandage surfaces were negative for vaccinia and no
household or sexual contacts developed clinical or serologic
evidence of vaccinia exposure [10]. In a similar trial, Graham
et al. [8], who used a single occlusive transparent polyurethane
dressing over the site, recovered vaccinia from 12 (18.2%) of
66 cultures of samples from the dressing surface. The addition
of a second occlusive dressing and a sterile gauze pad reduced
the rate of positive dressing cultures to 3% (3 of 103 cultures).
Despite the supporting evidence from these studies, there
has been continued skepticism about the protection conferred
by occlusive bandages and meticulous infection-control practices. In a recent review article citing historical reports, Sepkowitz [4] commented that nosocomial vaccinia required “relatively minor contact with a source case” (p. 443). Many of
the highlighted cases, however, resulted from contact with individuals who had disseminated complications from vaccination, such as eczema vaccinatum and generalized vaccinia—
situations with a greater degree of viral shedding and, thus, a
higher likelihood of secondary transmission, a distinction not
540 • CID 2004:38 (15 February) • Talbot et al.
made in the review. Reflecting these concerns, some conclusions
reached in this review have subsequently been questioned by
Neff et al. [11].
In our study, vaccinia was recovered from the external surface
of the outer bandages in 5 of the 6 subjects during days 7–10
after inoculation. This is the usual time when local symptoms,
such as pain and pruritus, reach their peak, and inadvertent
touching of the site might be expected to occur. Vaccinated
individuals should therefore use particular care to avoid manipulation of the inoculation site during the first weeks after
vaccination. We did not see a statistically significant association
between vaccinia recovery and the number of unscheduled
bandage changes performed by the subjects, measures of high
viral shedding, such as peak and mean lesion titers, and surrogate markers of a severe host immune response that may
serve as a measure of vaccinia burden (e.g., fever and lymphadenopathy). However, the number of subjects with a positive
dressing culture was only 6, limiting the statistical power to
detect subtle differences between those with and without positive cultures.
There are a few limitations to our study. Subjects received a
different smallpox vaccine (APSV) from the currently administered lyophilized vaccine (Dryvax; Wyeth Laboratories) used
in the military and civilian campaigns. The degree of vaccinia
shedding from vaccination pustules induced from these 2 vaccines has not been directly compared; however, both are derived
from the same vaccinia strain. In this study, a systematic evaluation for secondary transmission was not performed, thus
potentially limiting any conclusions regarding the risk of vaccinia transmission. However, autoinoculation of vaccinia,
which occurred more than twice as often as secondary transmission in the recent military campaign (48 cases vs. 21 cases
of secondary spread [6]), also serves as a measure of transmission. In our investigation, surveillance for episodes of autoinoculation of vaccinia was performed, and autoinoculation
of vaccinia did not occur. This suggests that there is a low risk
of transmission from covered vaccination sites, but definitive
conclusions on the risk of all types of vaccinia transmission
cannot be made. There was also no comparison group to determine the rate of vaccinia transmission to the hands of individuals without bandages covering the vaccination site. Although this would allow direct comparison of the recovery of
vaccinia from sites covered by occlusive bandages to the recovery from unbandaged sites, we were unable to perform such
an investigation, because current US Centers for Disease Control and Prevention guidelines do not recommend leaving vaccination sites uncovered [7].
The generalizability of our results to a broader population
could be questioned, because subjects in our trial were monitored intensively, and meticulous dressing care and hand hygiene were emphasized on many occasions. Present plans for
vaccinated civilians involve monitoring and education of vaccinees [12], but not to the extent seen in this trial. Whether
such differences lead to higher rates of recovery of vaccinia
from site bandages requires additional study. Finally, this investigation only examined 1 type of vaccination site dressing.
Other bandages, such as the gauze bandage currently used for
vaccinated non–health care workers, may not be as protective
as the occlusive bandages used in our study. A trial comparing
vaccinia retrieval from sites covered by several bandage types
is currently under way at our institution. With hope, this will
provide additional contemporary data regarding the protection
provided by vaccination-site bandages.
The reinstitution of smallpox vaccination has evoked many
new questions about an old, nearly forgotten vaccine. Although
experience is quite extensive, current vaccinia administration
is being introduced into a very different environment, which
has led many to question the vaccine’s safety [4]. Although no
infection-control measure can be absolutely effective, our study
reinforces the recent civilian and military vaccination experi-
ence that intensive education and proper infection-control procedures limit the potential for secondary transmission of vaccinia from sites covered with 2 occlusive bandages. This will,
we hope, allay many of the concerns regarding the risk of
contact vaccinia and allow a wider acceptance of the vaccine.
Acknowledgments
We thank the members of the Vanderbilt Pediatric Clinical
Research Office (particularly Jennifer Hicks, Jennifer Kissner,
Diane Anders, Karen Adkins, and Frankie Motley), William
Schaffner, Peter F. Wright, the Vanderbilt General Clinical Research Center, Aventis Pasteur, and colleagues at the National
Institute of Allergy and Infectious Diseases Division of Microbiology and Infectious Diseases (particularly Stephen Heyse,
Mamodikoe Makhene, Walla Dempsey, and Holli Hamilton),
for their support of and guidance with this project.
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