87

ORIGINAL ARTICLE

Effectiveness of the Typhoid Vi Vaccine in Overseas Travelers

from England
Karen S. Wagner, MSc,∗ Joanne L. Freedman, MPH,† Nick J. Andrews, PhD,‡
and Jane A. Jones, MSc†
∗
Immunisation, Hepatitis and Blood Safety Department; † Travel and Migrant Health Section; ‡ Statistics, Modelling and
Economics Department, Public Health England, London, UK

DOI: 10.1111/jtm.12178

See the Editorial by Watson, pp. 76–77 of this issue.

Background. Approximately 500 cases of enteric fever, caused by Salmonella enterica serovar Typhi and Paratyphi, are reported
in the UK each year. The majority are associated with travel to the Indian subcontinent. The typhoid Vi vaccine protects against
S. Typhi and is available to travelers from their general practice or private clinics. The effectiveness of this vaccine has been assessed
previously in endemic regions of the world but not in travelers.
Methods. Data from the enhanced surveillance scheme concerning persons in England aged ≥2 years who traveled from the UK
and contracted culture-confirmed enteric fever were used to calculate the effectiveness of the vaccine in travelers. A “case-case”
case–control design was used, in which patients with typhoid comprised the “cases” and those with paratyphoid acted as “controls.”
Results. The overall effectiveness of the vaccine, adjusted for age group, sex, ethnicity, birth in a typhoid-endemic country, and
year (of receipt of specimen), was 65% (95% confidence interval 53%–73%). Effectiveness did not vary across subgroups of any
of the factors in the model, but there was some evidence of waning effectiveness of the vaccine with increasing time since receipt
(trend p = 0.05).
Conclusions. The vaccine has been demonstrated to have a similar effectiveness in travelers as that found in endemic populations.
It appears to be protective in all ages, including in young children (aged 2–5 years), a finding not consistently replicated in
other studies. However, good hygiene practices are necessary in addition to vaccination to prevent infection. The “case-case”
case–control design provides a valuable method of calculating the effectiveness of this vaccine in travelers, given the availability of
paratyphoid controls, a population with similar demographics and risk exposures.

E nteric fever is caused by the bacteria Salmonella

enterica subspecies enterica serovar Typhi (S. Typhi)
and Paratyphi A, B, and C (S. Paratyphi A, B, and C).
Clinically it ranges from mild illness with low-grade
fever to severe clinical disease with abdominal dis-
comfort and multiple complications.1 The disease is
transmitted via the faecal–oral route where hygiene and
sanitation are poor. Endemic areas of the world with the
highest incidence include South Central and South East
Asia.2,3
On average, 489 laboratory-confirmed cases of
enteric fever were reported annually in the UK between
2007 and 2012; approximately half were caused by S.
Corresponding Author: Karen S. Wagner, MSc, Immunisa-
tion, Hepatitis and Blood Safety Department, Public Health
England, 61 Colindale Avenue, London NW9 5EQ, UK.
E-mail: karen.wagner@phe.gov.uk
Typhi and the other half by S. Paratyphi A (92% of
paratyphoid infections), B, and C.4
In the UK, persons >2 years of age who are travel-
ing to typhoid-endemic countries are recommended to
have a single dose of typhoid Vi vaccine.5 Reinforcing
doses may be given at 3 yearly intervals. The typhoid
Vi vaccine is composed of purified Vi capsular polysac-
charide from S. Typhi. It is available as a single vac-
cine [Typherix (GlaxoSmithKline UK, Uxbridge, UK)
or Typhim Vi (Sanofi Pasteur MSD, Maidenhead, UK),
licensed for persons ≥2 years of age], or in combination
with hepatitis A vaccine [Hepatyrix (GlaxoSmithKline
UK) or ViATIM (Sanofi Pasteur MSD), licensed for
persons ≥15/16 years of age]; both comprise 0.5 mL of
Vi vaccine, containing 25 μg of antigen.5 In addition,
an oral vaccine containing a live attenuated strain of S.
Typhi (Ty21a) [Vivotif (Crucell)] is available but com-
prises only a small proportion of UK typhoid vaccine
prescriptions (<1% between 2007 and 2012, Figure 1).

© 2014 International Society of Travel Medicine, 1195-1982

Journal of Travel Medicine 2015; Volume 22 (Issue 2): 87–93
88
Figure 1 Typhoid vaccine prescriptions dispensed in the community, UK: 2007–2012.
Previously, a whole cell vaccine was also available, but it
was withdrawn in the early 1990s (approximately 1992).
Good food-, water-, and personal hygiene practices are
recommended in addition to vaccination.6
Between 2007 and 2010, just over 1.4 million doses
of typhoid Vi vaccine were prescribed on average each
year through community primary care in the UK
(Figure 1).7 – 10 In 2011 and 2012, typhoid Vi vaccines
were affected by supply issues,11,12 resulting in annual
prescriptions decreasing to 982,556 in 2012. At the
same time, Typhim Vi vaccine was recalled because
of its potentially low potency (low antigen content)
in 16 batches, affecting some vaccines administered
between January 2011 and October 2012.13 An increase
in typhoid cases in the UK was not reported during this
period.14
The Cochrane review of vaccines for preventing
typhoid fever searched medical databases up to June
2013 and described four randomized controlled trials of
Vi vaccine in Nepal, South Africa, and China (two trials)
and two cluster-randomized controlled trials in Pak-
istan and India (all with outcomes of culture-positive
typhoid).15 However, trials have not assessed vaccine
effectiveness in travelers.16 Cumulative efficacy at
3 years, comparing typhoid vaccine to a meningococcal
bivalent polysaccharide vaccine, based on a trial (con-
ducted over 25 years ago) in Eastern Transvaal, South
Africa, of children aged 5 to 15 years was 55% [95%
confidence interval (CI) 30%–71%].17,18
This study aimed to assess typhoid Vi vaccine effec-
tiveness in travelers, to inform current travel health
advice.
Methods
Enhanced surveillance of enteric fever has been con-
ducted in England, Wales, and Northern Ireland since
J Travel Med 2015; 22: 87–93
Wagner et al.
May 2006 and is managed by the Travel and Migrant
Health Section (TMHS), Public Health England
(PHE).4 Usually, enteric fever patients first present
at hospital, from where PHE (TMHS or a regional
PHE Centre) is notified by the diagnosing clinician
or via a report from the hospital laboratory; both
typhoid and paratyphoid are notifiable infections.19
The hospital laboratory sends a specimen to the PHE
Salmonella Reference Service in Colindale for confir-
mation and typing. Reference service results are then
made available to TMHS. Patients are interviewed
by local authorities or health protection teams using
an enhanced surveillance form (containing questions
on patient demographics, symptoms, risk groups,
travel history, vaccination history, and contact and
food history for non-travel related cases), which is
sent to TMHS and reconciled with laboratory reports
in a central database. Between 2007 and 2012, on
average, 86% of confirmed cases were matched to
a completed enhanced surveillance form. Data con-
cerning travel-associated (duration of travel abroad
≤1 year) symptomatic culture-confirmed cases reported
in England from 2007 to 2012 were extracted for this
study.
In order to improve data completeness, the General
Practices (GPs) of a subset of cases from 2011 (N = 126)
were contacted by telephone to request missing vac-
cination histories. In addition, 40 more patients from
2011 (20 vaccinated, 20 unvaccinated as reported on the
surveillance form) were randomly selected and followed
up in the same way to obtain a measure of the accuracy
of vaccination histories recorded through the enhanced
surveillance scheme.
We used a case–control type design to calculate vac-
cine effectiveness whereby “cases” comprised typhoid
patients, and paratyphoid patients acted as “controls.”
Vaccine effectiveness was calculated by comparing the
Typhoid Vaccine Effectiveness in Travelers from England
ratios of cases and controls that were vaccinated (within
3 years of disease onset). We calculated the effective-
ness as one minus the odds ratio, both crude and
adjusted, using logistic regression models. Effective-
ness was also calculated for subgroups; age, sex, ethnic-
ity, birth in a typhoid-endemic country [based on the
typhoid-endemic countries listed on the National Travel
Health Network and Centre (NaTHNaC) website20 ],
and year of receipt of specimen. Likelihood ratio tests
were used to assess differences in effectiveness by sub-
group. Effectiveness was also assessed by phage type.
We calculated effectiveness by the time between
vaccination and disease onset (or specimen date if the
onset date was not known) and tested for a decline
using a test for trend in which only vaccinated patients
were included. If the exact dates of vaccination were
not stated, where possible, they were derived from other
information; those with only a year of vaccination were
assumed to have been vaccinated in the middle of the
year (2 July), or if the form stated that the patient had
been vaccinated at a pre-travel consultation for this trip,
he or she would be considered to have been vaccinated
within 1 year of disease onset.
To determine whether effectiveness was reduced as
a result of the potentially low potency of some batches
of Typhim Vi vaccine, we compared those who had
received the vaccine between January 2011 and October
2012 with those who had received the vaccine at other
times. Only those vaccinated within 1 year of onset were
included in this subanalysis to avoid confusing potency
period with time since onset.
Analyses were carried out using STATA Statistical
Software version 12.0.21
Results
A total of 2,751 symptomatic culture-confirmed enteric
fever cases were identified in England between January
2007 and December 2012, of which 2,474 (90%) were
acquired abroad. Of these, 1,279 were S. Typhi; 1,191
were S. Paratyphi; and four were mixed infections of
both organisms (excluded). An additional 297 S. Typhi
and 186 S. Paratyphi patients were excluded because
they had traveled abroad for more than a year or were
newly arriving migrants or visitors to the UK, or their
reason for travel was unknown. Of those remaining,
32/982 (3.3%) S. Typhi and 4/1,005 (0.4%) S. Paratyphi
patients were excluded because they were aged <2 years
or their age was unknown. The cases and controls
included in the study were similar in terms of known
descriptive factors, largely representing those of Indian
subcontinent ethnicity traveling to visit friends and
relatives in their countries of origin (Table 1).
Vaccine Effectiveness
One case and six controls were excluded from this anal-
ysis because they had received the oral typhoid vaccine
within 1 year of infection or at an unknown time point.
89
If the vaccine type was not stated (100/365 vaccinated
within 3 years of disease onset), it was assumed to be Vi
vaccine. Typhoid vaccination history was known (vacci-
nated within 3 years of disease onset or not) for 640/949
(67%) cases and 616/995 (62%) controls. For the 2011
data (where additional follow-up of vaccination histories
with GPs was undertaken), vaccination histories were
known for 94% (169/179) of cases and 95% (182/191)
of controls.
The effectiveness of the typhoid Vi vaccine in adults
and children ≥2 years of age resident in England and
traveling abroad from the UK was 65% (95% CI
53%–73%) (Table 2), adjusted for age group, sex, birth
in a typhoid-endemic country, ethnicity, and year.
There was no significant difference in effectiveness
by age group, sex, birth in a typhoid-endemic country,
ethnicity, year, potency period, or phage type.
There was some evidence of decreasing vaccine effec-
tiveness with time since vaccination, with effectiveness
falling from 72% (95% CI 61%–80%) in the year
immediately following vaccination to 37% (95% CI
−12% to 65%) and 56% (95% CI 21%–76%) in the
second and third years, respectively (trend p = 0.05).
Validation of Collected Vaccine Histories
Of the 20 patients that were identified as vaccinated
from their enhanced surveillance form, 16 were con-
firmed by their GP as vaccinated in the 3 years prior
to infection, three did not have typhoid vaccination
recorded in their GP notes, and one whose surveil-
lance form stated that the patient had been vaccinated
“approximately 3 years ago” was vaccinated 3.5 years
prior to the illness.
Of the 20 patients that were recorded as unvaccinated
according to their enhanced surveillance form, 19 were
confirmed by their GP as unvaccinated in the 3 years
prior to infection, and 1 was vaccinated.
The surveillance form had previously included a
question about where people obtained travel advice. Of
the confirmed enteric fever patients aged ≥2 years in
England between 2007 and 2010 who had traveled from
the UK and had received injectable typhoid vaccine
within 3 years of disease onset, 117/156 who completed
this question stated they had sought pre-travel health
advice, with 93% (104/112 with known advice source)
stating that they had sought advice from a physical
location (rather than the internet or friends/relatives).
Of these, 90 (87%) went to their GP and the remainder
(13%) went to travel clinics or other locations (eg,
occupational health or pharmacists).
Discussion
The overall effectiveness of 65% (95% CI 53%–73%)
of the typhoid Vi vaccine in travelers from England
is within the range of previous studies evaluating its
efficacy or effectiveness in populations where typhoid
is endemic.15 This study demonstrated the effectiveness
J Travel Med 2015; 22: 87–93
90 Wagner et al.

Table 1 Description of cases and controls

Cases (S. Typhi) Controls (S. Paratyphi)

Descriptive factor N = 950 N = 1,001

Mean age in years (range) 25 (2–83) 31 (2–80)

Male (%) 500 (53) 533 (53)
Ethnicity (% of those with known ethnicity)
Indian 382 (43) 325 (36)
Pakistani 247 (28) 293 (32)
Bangladeshi 102 (11) 97 (11)
White British 36 (4) 92 (10)
Other (including mixed ethnicities) 131 (15) 108 (12)
Unknown 52 86
Birth in a typhoid-endemic country (% of those with this information known) 484 (60) 457 (54)
Residency in the UK (% of those with this information known)
Since birth 84 (19) 100 (21)
0–5 years 147 (34) 88 (18)
6–15 years 132 (30) 132 (28)
16+ years 75 (17) 157 (33)
Unknown 512 524
Most common presumed country of infection* (% of those with this information known)
India 439 (46) 419 (42)
Pakistan 268 (28) 310 (31)
Bangladesh 107 (11) 100 (10)
Other/multiple destinations 135 (14) 166 (17)
Unknown 1 6
Reason for travel (% of those with this information known)
Visiting friends and relatives 825 (90) 789 (82)
Holiday 61 (7) 130 (13)
Business 17 (2) 18 (2)
Other/multiple reasons 12 (1) 27 (3)
Unknown 35 37
Median duration of travel abroad in days (range) 31 (2–304) 28 (1–365)
*This is the country of travel for cases with a single country of travel that is included in the list of NaTHNaC endemic countries.18 Patients who traveled to more than
one endemic country (dates of travel to each unclear) are recorded as having multiple destinations. For multiple destinations where specific dates of travel were available,
only those countries within the incubation period are listed as the presumed country/countries of infection. If only a non-endemic country is listed, then the infection is
presumed to be travel-associated only if no other sources of infection within the UK were found.

of the vaccine in all age groups, including children
aged 2 to <5 years. Few studies have assessed the
effectiveness of this vaccine in children under 5 years
of age and the two most recent effectiveness studies
had conflicting results for this age group at 2 years after
vaccination; the vaccine was 80% effective (95% CI
53%–91%) in children aged 2 to <5 years in India,22
but −38% effective (95% CI −192% to 35%) in this
age group in Pakistan.23 The finding of no significant
difference in effectiveness by sex, ethnicity, year, and
phage type was as expected. Those born in an endemic
country may have had some preexisting immunity from
exposure to natural infection, but this did not appear
to affect the vaccine’s performance. A difference in
effectiveness by potency period was unlikely to have
been visible in our results given the small number of
affected batches studied. Klugman and colleagues had
previously found no statistically significant difference in
protective efficacy during the first, second, and third
years following vaccination (though point estimates
showed a lower efficacy in the third year).18 Combining
results from several previous trials found an efficacy of
69% (95% CI 63%–74%) at year one (three trials),15
59% (95% CI 45%–69%) at year two (four trials),15 and
50% (95% CI −11% to 78%) in the third year (based
on the one trial by Klugman and colleagues)18,24 ; we
also found some evidence of the effectiveness decreasing
with increasing time since vaccination (the observed
fluctuation in adjusted effectiveness estimates was likely
because of sample size).
This is the first study to evaluate typhoid Vi vac-
cine effectiveness in travelers, and also to use controls
that were patients of a different disease. This design
has similarities to the indirect cohort method, docu-
mented by Broome and colleagues in their study of
pneumococcal vaccine,25 in which controls were pneu-
mococcal serotypes not included in the vaccine. It is
also similar to the test-negative case–control design
used to assess influenza vaccine effectiveness, in which
those with an influenza-like illness but who are poly-
merase chain reaction (PCR) negative act as controls.26
This method enabled assessment of the effectiveness of
a travel-related vaccine that protects against an infec-
tion not commonly seen in the UK. We were able to
draw on the large number of culture-confirmed cases
of typhoid in the national surveillance database, and

J Travel Med 2015; 22: 87–93

Typhoid Vaccine Effectiveness in Travelers from England 91

Table 2 Effectiveness of the typhoid Vi vaccine, based on typhoid cases and paratyphoid controls aged ≥2 years with a history
of foreign travel, reported in England between 2007 and 2012

Cases Controls p-Value for

(vaccinated : (vaccinated : Crude VE Adjusted VE difference in VE
Factor Sub-group unvaccinated) unvaccinated) (95% CI) (95% CI) between subgroups

Overall 118 : 522 247 : 369 66% (56% to 74%) 65% (53% to 73%) —
Age group (years) 2–4 7 : 41 10 : 14 76% (25% to 92%) 82% (20% to 96%) 0.75
5–15 34 : 104 40 : 41 66% (40% to 81%) 72% (46% to 85%)
16–49 67 : 338 154 : 271 65% (52% to 75%) 60% (43% to 72%)
50+ 10 : 39 43 : 43 74% (42% to 89%) 72% (30% to 89%)
Sex Female 69 : 239 136 : 149 68% (55% to 78%) 67% (51% to 77%) 0.53
Male 49 : 283 111 : 220 66% (50% to 77%) 62% (42% to 75%)
Birth in a typhoid- Yes 50 : 298 91 : 206 62% (44% to 74%) 60% (40% to 74%) 0.69
endemic No 60 : 162 138 : 124 67% (51% to 77%) 66% (48% to 77%)
country Unknown 8 : 62 18 : 39 72% (30% to 89%) 81% (41% to 94%)
Ethnicity White British 15 : 10 41 : 17 38% (−66% to 77%) 34% (−101% to 78%) 0.16
Non-White British 101 : 487 192 : 330 64% (53% to 73%) 66% (55% to 75%)
Unknown 2 : 25 14 : 22 87% (38% to 97%) 95% (54% to 99%)
Year of receipt of 2007 17 : 62 33 : 39 68% (34% to 84%) 69% (31% to 86%) 0.13
specimen 2008 13 : 68 23 : 53 56% (5% to 80%) 53% (−15% to 80%)
2009 18 : 77 24 : 54 47% (−6% to 74%) 22% (−74% to 65%)
2010 9 : 97 32 : 66 81% (57% to 91%) 79% (49% to 92%)
2011 41 : 128 78 : 104 57% (32% to 73%) 60% (35% to 76%)
2012 20 : 90 57 : 53 79% (62% to 89%) 78% (56% to 89%)
Time since <1 year 62 : 522† 162 : 369† 73% (63% to 80%) 72% (61% to 80%) 0.05*
vaccination ≥1 and <2 years 24 : 522 31 : 369 45% (5% to 68%) 37% (−12% to 65%)
≥2 and <3 years 21 : 522 33 : 369 55% (21% to 74%) 56% (21% to 76%)
Potency period‡ Normal potency period 40 : 522 92 : 369 69% (54% to 79%) 68% (52% to 79%) 0.57
Low potency period 22 : 522 70 : 369 78% (63% to 86%) 76% (59% to 86%)
Phage type PT E1 46 : 194 247 : 369 65% (49% to 75%) 64% (47% to 76%) 0.45
PT E9 var 27 : 98 247 : 369 59% (35% to 74%) 58% (31% to 74%)
Other PT 45 : 229 247 : 369 71% (58% to 79%) 70% (56% to 80%)
Untypable 0:1 247 : 369
CI = confidence interval; VE = vaccine effectiveness.
*Test for trend.
†Note that when looking at time since vaccination and vaccine potency, unvaccinated individuals are included in all analyses to obtain VE estimates, but p-values are
calculated only within the group of vaccinated individuals.
‡Evaluated for those with disease onset within 1 year of vaccination only.

the paratyphoid “controls” provided a population group
with similar demographics and risk exposures. Vaccine
effectiveness estimates may be subject to bias if there
are differences between cases and controls that have not
been controlled for in the model: however, given the
minimal confounding effects of the variables included
in the model, this seems unlikely.
Data recorded on surveillance forms were subject to
recall bias. However, the validation of a sample of vac-
cination histories found that the majority of patients
had the same information recorded on their enhanced
surveillance form as in their GP notes. The propor-
tion attending travel clinics for pre-travel advice (and
possibly also vaccination), from available data recorded
from 2007 to 2010, approximately matches the pro-
portion in our validation exercise who stated they had
received vaccine but did not have this recorded in their
GP notes, suggesting receipt elsewhere. The finding
that one of the 20 patients in the validation sample who
had “unvaccinated” recorded on the surveillance form
had been vaccinated according to GP records suggests
that misclassification error (which would reduce the
observed vaccine effectiveness) was small (approxi-
mately 5%).
Assumptions (based on available complete data) were
used to calculate missing dates of vaccination from
incomplete dates/other responses; this could have intro-
duced errors. However, this mainly affected allocation
to yearly categories for time between vaccination and
disease onset, for which misclassification would have
been expected to happen across categories to an equal
extent.
The “unvaccinated” group did not distinguish bet-
ween those vaccinated >3 years ago and those com-
pletely unvaccinated; vaccine effectiveness may
have been underestimated in this study if effective-
ness extended beyond 3 years (antibody responses
remain elevated for at least 3 years in non-endemic
populations27,28 and may persist for 10 years in endemic
populations29 ). Similarly, the vaccinated group did not
distinguish between those who had received only one
dose of Vi vaccine and those who had had additional

J Travel Med 2015; 22: 87–93

92
dose(s) at 3 yearly intervals. However, antibody titers
suggest that additional doses simply return antibody
levels to those achieved after primary immunization.27
The assumption that, unless stated otherwise, where
typhoid vaccine was administered it was Vi vaccine
(as opposed to oral Ty21a vaccine) seems reasonable
given that >99% of typhoid vaccines prescribed in
the UK between 2007 and 2012 were Vi vaccine. As
explained in the introduction, four different brands of
vaccine containing the Vi component were available in
the UK during the study period. It was not possible
to distinguish between them in this study, but vaccine
effectiveness would not be expected to differ between
brands.
As the typhoid vaccine does not offer complete
protection against infection and, in addition, given the
risk of paratyphoid and other food- and water-borne
infections not included in the vaccine, the need for good
hygiene should be emphasized whenever the vaccine is
administered. Patient information leaflets about typhoid
are available in four South Asian languages, as well as in
English.30
Acknowledgments
The authors gratefully acknowledge the following: Our
health protection colleagues in local PHE Centres and
the Environmental Health Officers who completed the
enteric fever enhanced surveillance forms; our col-
leagues in the PHE Salmonella Reference Service for
providing the data on laboratory-confirmed cases of
enteric fever; E. Wellington, formerly of the Travel
and Migrant Health Section, who managed the daily
administration of the enteric fever enhanced surveil-
lance and conducted telephonic follow-ups with GPs;
and M. Ramsay, R. Borrow, J. Crofts, and V. Field for
their helpful comments on the draft manuscript.
Declaration of Interests
The authors state they have no conflicts of interest to
declare.
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