Mass Vaccination Campaign against Rabies: Are Dogs Correctly Protected?

The Peruvian
Experience
Author(s): B. Chomel, G. Chappuis, F. Bullon, E. Cardenas, T. David de Beublain, M. Lombard
and E. Giambruno
Source: Reviews of Infectious Diseases, Vol. 10, Supplement 4. Research towards Rabies
Prevention (Nov. - Dec., 1988), pp. S697-S702
Published by: Oxford University Press
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REVIEWS OF INFECTIOUS DISEASES * VOL. 10, SUPPLEMENT 4 * NOVEMBER-DECEMBER 1988
? 1988 by The University of Chicago. All rights reserved. 0162-0886/88/1006-0025$02.00

Mass VaccinationCampaignAgainst Rabies: Are Dogs CorrectlyProtected?

The Peruvian Experience
B. Chomel, G. Chappuis, F. Bullon, E. Cardenas, From the Service de Maladies Contagieuses, Ecole Nationale
T. David de Beublain, M. Lombard, Veterinairede Lyon, Charbonnieres; Rh6ne-Merieux, Lyon,
and E. Giambruno and Mission Bioforce, Venissieux,France; the Division of
Field Services, Epidemiology Program Office, Centers for
Disease Control, Atlanta, Georgia, USA; and the Peruvian
Ministry of Health and the Pan American Health
Organization/OPS, Lima, Peru

In a mass vaccination campaign conducted in Peru in March 1985, 270,000 dogs (65%
of the estimated dog population) were vaccinated over the course of 1 month with an
inactivatedtissue culturevaccine.Since that time no human rabiescases have been reported;
in addition, the number of animal rabies cases has declined to only three from a previous
mean of 292 cases per year since 1980. A serologic survey was also done to determine
the immune response among randomly selected vaccinated dogs, with titers determined
3, 6, 9, and 12 months after vaccination. Twelvemonths after vaccination, 97% of the
dogs had a rabies neutralizing antibody titer of >0.5 IU/mL, and 87% had a titer of >1.0
IU/mL. Thus, this tissue culture rabies vaccine given under field conditions induced anti-
bodies that lasted for at least 1 year in 97%oof vaccinated dogs.

Urbanrabiescontinuesto be a majorthreatin many of Malta,the MissionBioforce(a Frenchtraining

countries[1].The numberof reportedrabiescases
has greatlyincreasedin Andeancountriessincethe
beginningof the 1980s.Peruis one of those coun-
trieswhererabiesis a continuingproblem(table1).
Forexample,Lima,the capitalcity of Peru,experi-
encedits largestepizooticin 1982,with the report-
ing of 1,023caninecasesand 13humancases[2, 3].
Massvaccinationcampaignshavebeen effective
in controllingrabiesin urbanareas[1].In Lima,ra-
bies was controlledby such campaignsin the early
1970s;however,becauseof thelackof adequatecon-
trol measures,the diseasereappearedin 1980and
reachedepizootic proportionsin 1982 (figure 1).
Mass vaccinationcampaignswerereintroducedin
1982-1984.Enzooticfoci persisted,however,in the
northernsuburbsof SanMartinPorresand Comas
andin the southernsuburbs.Thus,a morecompre-
hensive campaignof mass vaccinationwas con-
ductedin March1985throughthe cooperativeef-
forts of the PeruvianMinistryof Health, the Pan
AmericanHealthOrganization(PAHO),the Order
The authors thank Mission Bioforce Development for collab-
oration. M. Soulier of Rh6ne-Merieux for technical assistance,
and L. Good of the Centers for Disease Control for editorial as-
sistance.
Please address requests for reprints to Dr. B. Chomel, Divi-
sion of Field Services, Epidemiology Program Office, Centers
for Disease Control, 1600Clifton Road, Altanta, Georgia 30333.
programfortechnicians planningto workin develop-
ing countries),and the MerieuxFoundation.
Althoughmanycampaignsof massrabiesvacci-
nationhavebeenconductedin variouspartsof the
world,thereareonly limiteddataregardingthe se-
rumantibodyresponsein vaccinatedpopulationsof
dogs [4-7], especiallyin countrieswherecaninera-
biesis enzootic.Thispaperreportsthe resultsof the
1985campaignconductedin Lima-Callaoand the
serologicresponseto a tissueculture-producedvac-
cine used underfield conditions.
Materials and Methods
VaccinationCampaignand Follow-UpSurvey
A masscampaignof canineand felinevaccination
wascarriedout in Lima-Callaoin March1985,with
internationaltechnicaland financialsupportbegun
in December1984.Lima-Callaowasdividedinto 11
sectors,anda programwasplannedin whichalldogs
(v400,000) would be vaccinatedwithin 1 month.
Vaccinationcenterswereestablishedin accessible
sitessuchas marketplacesand publicsquares.The
campaignwas directedfrom the Lima Antirabies
Center,and morethan250 personstook part.One
hundredten teams,eachconsistingof one vaccina-
tor and one recorder,weredirectedby 11 supervi-
sors. In addition,each supervisorwas in chargeof

S697

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S698 Chomel et al.

1200 -
Table 1. Number of rabies cases reported in Peru, by
species, 1980-1985. 1000 -

No. of cases in indicated species

o
800
Dog
A
Other All
600- / \ -15
Year Dogs species animals Humans Z M
aHuman

878 98 976 9
0
a
400- A -10
1980
1981 1,406 134 1,540 29 200 cat
1982 1,893 183 2,076 39
118 31 ...0 0
1983 1,149 1,267 1970 1972 1974 1976 1978 1980 1982 1984
1
1986
1984 840 156 996 32
YEAR
1985 505 NA NA 28
Figure 1. Reportedrabiescases,byyear,in Lima-Callao,
NOTE. Source: Peruvian Ministry of Health. NA = data Peru (January1970through1 October1986).
not available.

overseeing the campaign in one of the 11 sectors of
Lima-Callao.
Each day from 25 Februaryto 27 March, the 110
teams began work at vaccination sites at 8 A.M.The
supervisors, in cars with loudspeakers, urged peo-
ple to bring their animals in for vaccination. That
appeal was augmented by students on summer va-
cation. Each vaccinated animal had a blue collar
placed on it, and the owner was given a vaccination
certificate. The recorder registeredthe species, sex,
age, and vaccination status (primary or booster in-
jection) of the animal.
Through international cooperative efforts, Peru
was given 600 doses of newly licensed human vac-
cine produced on Vero cells by the Institut Merieux
in Lyon, France, and approved by the World Health
Organization (WHO). This vaccine was used for
preexposure vaccination of the vaccinators. In ad-
dition, Peru received 500,000 doses of animal vac-
cine (Rabisin, Rhone-Merieux, Lyon). This vaccine
was produced with the Pasteur PV 11 strain on a
hamster embryonic cell line and was inactivated by
P-propiolactone; the adjuvant used was aluminum
hydroxide. A 1.0-mL dose was administered sub-
cutaneously to dogs. The latter vaccine has been
shown to be immunogenic, safe, and stable and to
provide immunity against rabies for 3 years [8].
Other supplies furnished by health agencies con-
sisted of 50,000 syringes, 75,000 needles, 160 insu-
lated boxes and ice packs, 500,000 vaccination cer-
tificates, and 500,000 blue collars to be placed on
vaccinated animals.
One month after the completion of the vaccina-
tion campaign (April 1985), a follow-up survey was
carried out to evaluate the ratio of dogs and cats to
humans and the number of animals vaccinated.This
surveywas conducted by PAHO, the PeruvianMinis-
try of Health, and Mission Bioforce [9]. Fifteen dis-
tricts of Lima-Callao were randomly selected, with
exclusion of the high socioeconomic districts.Blocks
wererandomly selected within each surveyeddistrict
according to the population size. In turn, 10 house-
holds in each of these blocks were selected by a clus-
ter technique (95% confidence level, 1%0precision).
The data gathered included the number of per-
sons, dogs, and cats per household; the sex of all
animals; the history of animal vaccination; and the
number of animals with a blue collar. At the begin-
ning, the number of vaccinations performed by pri-
vate veterinarians in Lima-Callao was estimated.
This number was added to the number of vaccina-
tions performed at the Antirabies Center and the
numberperformedduringthe mass campaignto give
the overall vaccination coverage.
SerologicStudy and 12-MonthSurvey:I
A survey was conducted to obtain information on
a representative sample of vaccinated dogs from
which serum specimens were collected 3, 6, 9, and
12 months after the March 1985campaign. For each
collection period, a different sample was chosen.
Twentydistricts of the city and a block within each
district were randomly selected. In each block, ev-
ery 10th house was visited. After verification of the
vaccination certificate,blood was obtained from one
household dog. A total of 10 dogs per district were
sampled. Only dogs vaccinatedduring the campaign
were included. When severaldogs were found in the
same household, only one of those vaccinated for
the first time in March 1985 was randomly selected.
Appropriate sample sizes were calculated for an

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Mass Rabies Vaccination in Peru
Table 2. Detailed questionnaire submitted to dog owners
during survey conducted 12 months after mass vaccina-
tion campaign.
Form 1: Data collected for each household
1. District
2. Block number
3. Address
4. One or more dogs presentlyin household: Yes No
5. Number of dogs
6. Number of dogs wearing a blue collar
7. Number of dogs with vaccination certificates
8. Number of new dogs acquired since March 1985
9. Number of dogs that died or disappeared after
March 1985
Form 2: Data collected for each dog from which serum sample
was collected
1. District
2. Block number
3. Address
4. Number for sample
5. Age of dog (in years)
6. Sex
7. Birthplace
8. Does dog roam in the street? Yes No
9. Is dog vaccinated against rabies? Yes No
10. Was dog vaccinated against rabies in March 1985?
Yes No
11. Was dog vaccinated for the first time during the
campaign of March 1985? Yes No
estimated antibody prevalence of >90%?in vacci-
nated dogs after 9 months and >85%oafter 1 year,
with 5%oprecision (95% confidence level). The for-
mula used for the calculation of sample sizes was
n = t2(P'q)/d2, where t = 1.96 for 95% confidence,
d = 0.05 precision (usually), p = proportion of the
target population with the characteristicbeing mea-
sured(in our study, 90% and 85%, respectively),and
q = i - p (J. V. Peavy, "Surveys and Sampling,"
lecture notes, Epidemic Intelligence Service course,
Centers for Disease Control, Atlanta, 1984). A min-
imal sample size for proper statistical analysis is 138
dogs for an antibody prevalence of 90%oand 196
dogs for an antibody prevalence of 85%.
Since dogs were randomly selected, the March
1985vaccinationmay have been either a primaryvac-
cination or a booster dose. At the time dogs were
sampled, information regardingsex, age, and vacci-
nation status (based on the owners' recall) was
recorded. A more detailed questionnaire was also
submitted to dog owners during the 12-month sur-
vey (table 2).
Rabies virus neutralizing antibody titers were de-
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S699
15- =E Dog
Cat
'
1 Otheranimal
10- -I Human
10I
/n K/
V,,' Vaccination
Campaign
b) 2^ioyyr(273,000 dogs vaccinated)
JFMAMJJASONDJFMAMJJASONDJFMAMJJASOND
1984 1985 1986
Figure 2. Impact of mass vaccinationcampaign,as
reflectedby numbersof reportedrabiescases(byspecies)
in Lima-Callao,Peru (1984-1986).
termined by the rapid-focus fluorescent inhibition
test [10].Valueswereinterpretedas follows: <0.1 IU/
mL, nonresponder; >0.1 to <0.5 IU/mL, medium
responder; and >0.5 IU/mL, good responder. (The
protective threshold accepted by WHO is 0.5
IU/mL.)
Results
Vaccination Campaign and Follow-Up Survey
Approximately 300,000 animals >3 months of age
were vaccinated in the 1-month campaign, includ-
ing 273,000 dogs (r65%o of the total estimated dog
population in Lima-Callao) and 27,000 cats. Of the
vaccinated dogs, 61% were males and 39% females;
38%0were<1 year old. Fifty-one percent of the dogs
were vaccinated for the first time, while 49% had
been vaccinated previously.
The April 1985 follow-up surveyof 1,829 selected
households establisheda dog-to-human ratio of 1:10
(1,129/11,193) and a cat-to-human ratio of 1:18
(620/11,193). The sex ratio determined in this sur-
vey was slightlydifferentfrom that for the whole vac-
cinated population: 58% of the dogs weremales and
42% females, while 54% of the cats were males and
46% females. It was estimatedthat 78% of the Lima-
Callao dog population was vaccinated: 65 00 during
the mass campaign and 13%by privatepractitioners
and at the AntirabiesCenterbetweenNovember 1984
and February 1985. The survey also revealed that 1
month after the campaign 98% of the surveyeddogs
vaccinated during this campaign were wearing blue
collars; in contrast, only 270%of the vaccinated cats
were wearing the collars.
S700 Chomel et al

Table 3. Dog sample characteristics (sex, age, and vaccination status): Lima-Callao, Peru, 1985-1986.
Sex (%) Age (%) Vaccination status (%)
Time after No. of
vaccine (mo) dogs Male Female <1 y >1 y Primary Booster

3 137 60 40 35 65 53 47
6 151 59 41 37 63 67 33
9 130 63 37 28 72 39 61
12 198 74 26 0 100 90 10

The impact of the vaccination campaign on ani- dogs werecounted in these 200 households; i.e., there
mal and human rabies is shown in figure 2. After were 1.5 dogs per household. Since 23 (8%) of the
March 1985 the number of rabies cases in dogs dogs were acquired after March 1985, 281 (92%) of
dropped dramatically; in fact, after May 1985 only them were already living in these households in
one such case was reported (in December 1985, in March 1985. However, it was reported that 35 dogs
a young puppy not vaccinatedin March).Threecases had either died or disappeared since March 1985.
were observed in cats: one in November 1985, one Therefore, 316 dogs (281+ 35) were living in the 200
in December 1985, and one (an imported case) in households in March 1985, and 11%0 had either died
1987. No other cases in dogs or cats have been or disappeared within a year.
reported to date. No cases in humans have been Fewer than 50% of dogs had blue collars, but
reported since March 1985; in contrast, there were owners produced vaccination certificates for 95?%o
eight reporteddeaths in 1983, five in 1984, and three (267 of 281). One hundred seventy-three (87%) of
in the first quarter of 1985. the dogs sampled 12 months after the campaignlived
in the same district where they were born, but 75%o
regularly roamed the streets.
SerologicStudyand 12-MonthSurvey:II
Serologic results are summarized in tables 4 and
The size of the differentdog samplesand the animals' 5. Dogs vaccinated 1 year previously had a mean an-
sex, age, and vaccination status are summarized in tibody titer of 4.33 IU/mL (table 4, figure 3), with
table 3. Blood samples were obtained from 137 dogs 97%oof these titers >0.5 IU/mL (figure3). Therewas,
3 months after vaccination, from 151 dogs after 6 however, a steady decrease in antibody titers: 64%
months, from 130 dogs after 9 months, and from of dogs had >5.0 IU/mL after 3 months (mean,
198 dogs after 12 months. (In fact, samples were ob- 11.13IU/mL), whereasonly 46% had levels this high
tained from 200 dogs after 12 months but an insuffi- after 6 months (mean, 7.96 IU/mL), 29%oafter 9
cient volume of serum was collected for testing from months (mean, 5.02 IU/mL), and 40%7after 12
two of these dogs.) Of the 198 dogs sampled after months (mean, 4.33 IU/mL) (figure 3). However,
12 months, 178 (90%) had been vaccinated for the >95% of dogs still had titers of >0.5 IU/mL after
first time during the March 1985 campaign. 12 months. There was no statistically significant
Two hundred households were visited during the
12-monthsurveyin March 1986. Three hundredfour
Table 5. Rabiesantibodytitersin dogs, by time after
vaccination:Lima-Callao,Peru, 1985-1986.
Table 4. Mean rabies antibody titers and kinetics: No. (%) of dogs with indicated
Lima-Callao,Peru, 1985-1986. titer (IU/mL)*
Time after No. <50
Antibody titer
Time after No.0 (IU/mL vaccination of
vaccination of (mo) dogs <0.5 <1.0 Total >5.0
(mo) dogs Mean CI Mean CI
3 137 2 (1.5) 11 (8) 50 (37) 87 (64)
2-3 137 1.95 1.86-2.04 11.13 8.79-13.47 6 151 4 (2.6) 23 (15) 81 (54) 70 (46)
6 151 1.60 1.53-1.67 7.96 5.96-9.96 9 130 7 (5.4) 29 (22) 92 (71) 38 (29)
9 130 1.52 1.43-1.60 5.02 3.38-6.66 12 198 6 (3) 26 (13) 119 (60) 79 (40)
12 198 1.61 1.54-1.69 4.33 2.53-6.13
* The protective threshold accepted by the World Health Or-
NOTE. CI = 95% confidence interval. ganization is 0.5 IU/mL.

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Mass Rabies Vaccination in Peru
100 - Table 6. Rabiesantibodytitersin 198dogs 12months
so-i11
80-. .. .......
60 -
5- 40-
m... .. ......
i ii
40 -
20-
3 6 9 12
AFTER
MONTHS VACCINATION
mm <0.5 IU/ML
*Meanof IU/ML
Figure 3. Rabiesantibodytiters,by timeaftervaccina-
tion, in Lima-Callao,Peru (1985and 1986).
difference (Fisher's exact test) between the primary
and booster groups after 12 months (table 6).
Moreover,no differencein antibody responserelated
to age or sex was observed between dogs that had
received a primary vaccination only and those that
had received a booster.
Discussion
This study underscoredthe excellent rabiesantibody
titers in dogs vaccinated under field conditions. One
year after vaccination only 3%7o of dogs given a pri-
mary immunization had an antibody titer of <0.5
IU/mL; 14%ohad a titer of <1.0 IU/mL. Such re-
sults are comparable to those obtained in Europe.
In France, for instance, 83?%o of the 76 dogs vacci-
nated for the first time with a similar vaccine had
titers of >0.5 IU/mL after 1 year [6]. In the booster
group, the resultsweresimilar:5?%o of dogs had titers
of <1.0 IU/mL 12 months after vaccination. Most
of the dogs given boosters in Peru had previously
been vaccinated with the same type of vaccine (F.
Bullon, unpublisheddata). Although the sample size
was small (n = 20), the data collected are compara-
ble to those reported by Toma et al. [7] in France.
Our study, however, does not confirm the report of
a low responsein dogs vaccinatedwith a similartype
of vaccine in Tunisia [5], where only 24% of 29 dogs
had titers of >0.5 IU/mL. The difference between
the two studies may be due to the methods used for
sampling and follow-up of the vaccinated dogs as
well as the number of dogs vaccinated.(In the Tunis-
ian study, the same 29 dogs were followed for 1 year,
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S701
after vaccination,by vaccinationstatus: Lima-Callao,
......... Peru, 1985-1986.
No. (%) of dogs with indicated
.5 l... ....... titer (IU/mL)*
Vaccination <1.0
status
(no. of dogs) <0.5 Total >1.0
Primary (178) 6 (3) 25 (14) 153 (86)
Booster (20) 0 (...) 1 (5) 19 (95)
* The protective threshold accepted by the World Health Or-
ganization is 0.5 IU/mL.
E3 20.5 IU/ML
while in Peru representativesamples of 270,000 dogs
were selected at different periods.)
In the Tunisian study, parasitism and malnutri-
tion werecited as possible causes for the reducedim-
mune response; we could not confirm this finding,
although parasitic infections and poor nutrition in
dogs appear to be common in Peru (F. Bullon, un-
published data). The majority of dogs vaccinated in
our study were from low socioeconomic areaswhere
such conditions exist; yet dogs in that environment
responded adequately. Even if one assumes that the
11%of dogs that died or disappeared between 1985
and 1986 had titers of <0.5 IU/mL, the rate of re-
sponse among the dogs studied was still 3.6 times
that among those studied in Tunisia (85% vs. 24%,
P <.001).
Dogs vaccinated in the field may have antibody
titerslowerthan those in dogs vaccinatedexperimen-
tally and kept underideal conditions [11].Our results
indicate that there is a <10-fold difference (one log)
between experimentallyvaccinated dogs [4, 11]and
Peruvian field dogs.
The mass vaccination campaign, conducted in a
short period (1 month), allowedus to vaccinatea high
percentageof the dog population. Moreover,in this
particular situation, the campaign had the advan-
tage of being the second in a 3-year period. Clearly
such campaigns should be carried out on a regular
basis to reduce enzootic foci of rabies, especially
when programsfor straydog control are not well es-
tablished and maintained.The vaccinationof owned
dogs and the elimination of stray dogs should al-
waysbe conducted concurrently.The health authori-
ties should take advantageof largevaccination cam-
paigns to eliminate stray dogs.
The characteristics(age and sex) of our samples,
except in the 12-month survey, are similar to those
All use subject to JSTOR Terms and Conditions
S702
reportedin 1973by Malaga[12]and in 1985by Lo-
pez in Peru.Accordingto Malaga[12],28% of the
dogs were<1 year old and 71%weremale. Lopez
[9] founda higherpercentageof youngdogs (34%
of dogs <1 year old), with 50% male. Among the
273,000dogs vaccinatedin March1985,38% were
<1 year old and 61%weremale.
The dog is the mainvectorof rabiesin Peru [2].
Massvaccinationhasnowstoppedthechainof trans-
missionof the disease;no humancases havebeen
reportedsinceApril 1985.Our studyrevealedthat
the majority(75%)of owneddogsroamthe streets.
Thisobservationjustifiesthe needfor regularrabies
vaccinationcampaignsto preventthe spread of
rabies.
Furtherstudiesin similarcountriesarenecessary
to validateandcompleteourdata.A surveyof a rep-
resentativesampleof vaccinateddogs24 monthsaf-
ter vaccinationwouldbe usefulto supportthe effi-
cacy of mass vaccinationcampaignsover a 2-year
period.
Rabiescontinuesto be a threateningpublichealth
problemin numerouscountriesin South and Cen-
tral America. Mass vaccinationcampaignshave
provedefficientin controllingrabiesin urbandogs.
Thecampaignsconductedrecentlyin Lima-Callao,
Peru,are illustrative.This studyindicatesthe high
immunogenicity of cellculture-produced
rabiesvac-
cinesunderfield conditions.The immuneresponse
of a generaldog populationto the productusedwas
excellent.
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