COURSE OF SECONDARY H UM ORAL IM M U NE
RESPONSE SH O RTLY AFTER REVACCINATION
WITH BHK-21 CELL CULTURE INACTIVATED
RABIES
VACCINE
ADJUVANTED
WITH
A LU M IN U M HYDROXIDE
neutralizing
cattle,
antibodies
and
Associate Professor
Faculdade de Medicina Veterinária e Zootecnia da USP
JOSÉ DE ANGELIS CÔRTES
Professor
Faculdade de Medicina Veterinária e Zootecnia da USP
previously
five
zebu-crossbred
bovines
reared
in
field
condition. The secondary vaccination was performed 180
inactivated rabies
Serum
samples
immunization,
were
taken
vaccine
adninistration
and
hours,
72
determination
using a commercial
vaccine prepared
and
of
in BHK-21
sequentially
at
intervals
after
7
and
neutralizing
of
14
cells.
after
0
each
(zero),
days
for
antibodies.
24
the
The
mean
neutralizing antibody titer determined for sera taken
iirmediately before the first vaccination was < 1:5, at
24 and 72 hours post-vaccination,
MARK M. RWEYEMAMU
vaccinated
interference on the humoral
immunologic response to revaccination was investigated
in
days from the first
FUMIO HONMA ITO
in
its possible
< 1:6.25;
the mean
value found at 7 days post-vaccination was 1:144 ± 51;
PhD
and 1:3,460 ± 1,329, at 14 days post-vaccination with
Laboratórios Pfizer Ltda.
mean titer of 1:58 ± 14; 24 hours after revaccination
the mean
OSSAMURO UMEHARA
BVM
Laboratórios Pfizer Ltda.
1:277
BVM
at
1:129 ± 80,
72
hours
raising forwardly to
post-revaccination,
and
increasing levels > 1:6,400 and > 1:25,600 were found
at 7 and 14 days post-revaccination,
full
RAUL MEDEIROS NETO
titer was
± 161,
anamnestic
antigen
and
the
response.
The
consequent
fall
evidenciating a
blocking
in
effect
antibody
of
levels
shortly after the revaccination was not observed.
Laboratórios Pfizer Ltda.
DOMINGOS DE LUCCA NETO
Rabies
UNTTERMS:
BVM
of
cattle;
Antibody
formation;
Immunization; Immunity of cattle
Laboratórios Pfizer Ltda.
MARIO BALTAZAR
Biologist
INTRODUCTION
Laboratórios Pfizer Ltda.
Epidemic
SILVIO ARRUDA VASCONCELLOS
Associate Professor
Faculdade de Medicina Veterinária e Zootecnia da USP
pattern
of
rabies
diagnosed by CARINI 8 (1911)
in cattle
was
first
in Santa Catarina State,
Southern Brazil, and nearly a century ago the vampire
bat-transmitted rabies
is still prevalent
in most of
South and Central American Countries from Northern A r ­
MARCIA ESTER PARREIRA VASCONCELLOS
BVM
Prefeitura Municipal de Santo André
gentina to Northern Mexico
Referring
variety of
to the vampire bats,
control methods
despite
the wide
currently available,
they
have been generally ineffective and, by and large the
non-selective
criticized
ITO, F.H.; CÔRTES, J.A.; RWEYEMAMU, M.M.; UMEHARA, 0.;
methods
by
of
bat
D.; BALTAZAR, M.;
native for controlling rabies
VASCONCELLOS,
M.E.P.
minimize
secondary
humoral
revaccination
with
immune
response
Course of
shortly
BHK-21
cell
culture
adjuvanted
with
aluminum
after
and
have
ecologists
been
14
Thus, vaccination has been used as an important alter­
MEDEIROS NETO, R.; DE LUCCA NETO,
S.A.; VASCONCELLOS,
destruction
conservationists
the
ecnonomic
in cattle,
losses
due
to
in order to
this
fatal
disease.
inactivated
To
hydroxide.
research has
achieve
this
purpose,
in
last
30
years
Braz. J. vet. Res. anim. Sci., São Paulo, v.28, n.1, p.51-7,
1991.
several
vaccine
antigen,
conducted
live
or
inactivated
vaccines
...
., . |
,.
10,17,19
commercially available in this country
'
SUMMARY: The phenomenon of "in vivo" blocking effect
of
traditionally been
the
toward the
2
development of more effective and safer vaccines
and
rabies
due
to
the
presence
of
rabies
specific
A
number
demonstrated
of
to
vaccines
be
very
have
became
experimentally
effective
for
been
cattle
52
ITO, F .H. et al.
' ' '
'
results
7,16,17
'
although
were,
in some
in
field
occasions,
conditions
very
the
disappointing
variability,
since
Based on
Insufficient
gradually
over
a
the
facts mentionned
above,
this
work
blocking
status
other
remaining
after
factors like the interference of the specific passive
5 1c 21 22 c8
maternal antibody in young animals
' ' ' '
have
"negative
phase"
antigen
been
circulation, the SN test would detect the drop in the
the
of
change
the
vaccines
25 26
antigenic variants of the virus
'
host nutrition
and
potency
results
wide range of virus doses used in the test system.
antigenic
mentionned
as
the
stimulus
possible
11,
and
cause
of
the
low
aims
to
investigate
the phenomenon of
effect
antigen
binding
protection revealed by such vaccines.
In fact, ARNOLD
antibody
et
carefulness
establishment
al.
^
(1973)
vaccinating
dams
recoimended
and revaccinating young
immunized
authors,
have
against
rabies.
calves born
According
calves possessing maternal
not be
vaccinated until
until the passive
the
age
in
from
to
seven months
immunity has wanned,
by
does
occur
and
removing
levels
for
of
as
a
an
the
serum
immune
"in vivo"
antibodies
response.
If
the
response
of
the
from
the
the
antibodies
few
days
enduring
before
the
secondary
immune
response.
these
antibodies should
of
of
its primary
the
MA TERIALS A N D METHODS
or
a booster shot
RABIES VACCINE*
should be given six months later and subsequent annual
revaccination should be adninistered cautiously.
In
case
vaccination,
of
an
immunity
A commercially produced PV-strain adapted to BHK-
following
it has been suggested that injection of a
second dose of the
detectable
enduring
from
same antigen when titer
the
primary
response
is still
results
in
reduction rather than increase in serum antibody titer
due
to removal
of
antibody
before the secondary
27
way
This phenomenon is the so-called "negative phase"
similar
to
protected
that
by
presence of high
interfere
with
^
observed
the
(1977)
in theory,
in young
calves
specific' colostral
it
is
passively
antibodies,
the
levels of circulating antibodies may
active
line
aluminum
and
rabies
hydroxide
binary
ethy leneimine
vaccine,
adjuvanted
(GUIDOLIN
given subcutaneously
et
(BEI)
al.
with
2%
1983)
was
in a single dose of 5.0 ml per
a n imal.
in complex with antigen,
immune response gets under
and according to TIZZARD
cell
inactivated
immunization
against
the
same
ANIMALS
Cattle - The bovines used
in this study were
derived
from a ranch located in the State of São Paulo, known
to be
free of
against
rabies
rabies.
Five
and not practicing vaccination
female
Zebu
cattle
of
Nelore
breed aged between 12 to 36 months were selected after
screening through the mouse SN test at 1:5 dilution.
antigen.
This "in vivo" neutralization
of controversy
and needs
is still
further
a matter
investigation
in a
Mice
- Swiss
derived
from
scientifically controlled study, especially in cattle.
maintained at
The subject
considered
is
important
if revaccination
in herds presenting
albino
a
mice
used
laboratory
Santa
Isabel
in
the
animal
- SP
SN
test
breeding
by Pfizer,
were
station
weighing
has
to be
between 10 to 14 grams and divided into groups of five
antibody titers
above
mice each.
protective levels and reared in an endemic area where
Groups of
10 mice each were used for the
CVS (Challenge Virus Standard) strain virus titration.
an emergency immunization is needed to rapidly protect
the cattle against the disease.
The
and
correlation
protection
between
against
Virus - The CVS strain 31/2 of fixed rabies virus from
neutralizing
challenge
has
antibodies
raised
some
Pan American Zoonoses Center (CEPANZO), Argentina, was
used for the SN test. The virus had been maintained in
controversies in rabies, but as quoted by ATANASIU et
mice through
al. 7 (1968)
and the LD^q (MICLDgg) determined was 10 '*'^/0.03 ml.
level
is
a relatively high neutralizing antibody
generally
accepted
as
an
evidence
Equine sera - Rabies hyperimmune serum
The evaluation of the humoral
involving
different
immunity
types
of
serum neutralization
method
known
9
CORTES; NILSSON
interpreting the
(SN)
to
be
test,
very
-
This
serum
was
kindly provided by the Butantan Institute - São Paulo,
rabies
SP, and used as the positive control serum for the SN
a worldwide
accepted
sensitive,
although
(1974) recommended precaution
results due to a high degree
in
of
test.
•Rabies
vaccine:
SP, Brazil.
Braz. J. vet. Res. anim. Sci., v.28, n. 1, p.51-7, 1991.
inoculation
in those
vaccines has usually been conducted through the mouse
assay
intracerebral
of
immunity.
experiments
two additional
RABVAC,
Pfizer
Co.Ltd.,
Guarulhos
-
53
Course o f secondary humoral im m une response sh o rtly after revaccination
Equine normal serum - Previously tested by SN test, free
1:6.25. The antibody titers corresponding to 7 th DPIV
of antibody against rabies,
the values
this foal serum was used
found
ranged
from
1:31
to
1:199,
with
a
for the preparation of the diluent at a concentration
mean titer of 1:144 ± 51. The mean SN titer found in
of 2% (V/V)
the
in distilled uater containing 1.000 IU of
Penicillin and 1.25 mg of Streptomycin per ml.
serum
1,329;
sampLes
taken
at
14th
DPIV was
1:3,460
t
indicating a mean rise in SN titer of 24 times
within a week. By the profiles of the primary hunoral
Mouse serum neutralization (SN) test - The
test
carried out
immune response,
increasing
levels of antibodies were
was the constant virus - varying serum dilution method
noted
and the procedures adopted were described by ATANASIU
antibody response than did the others,
6 , 1976.
1:504, respectively at 7 and 14 DPIV.
until
The
DPIV;
bleeding
day 180
EXPERIMENTAL PROCEDURE
14
of
confirmed
Five cattle were
given subcutaneousIy 5.0 ml of
rabies vaccine at the beginning of the experiment (day
immediately
collections
were
after
then
1s t , 3 rc*, 7 1*1 and
ns
16
presented
five animals
the
carried
presence
the
initial
sequentially
14^
day post
bleeding,
at
the
vaccination
with
Serum
SN
a mean
summarized in
blood
performed
initial
to 1:70
the
on
the
primary
from
1:26
of 1:58 ± 14, as are
Tab. 2.
samples
revaccination
titers with
out
of the remaining
titers ranged
titer
lower
i.e., 1:31 and
serum neutralizing antibodies following
immune response;
zero)
animal
taken
24
hours
following
were
slightly
increased
in
a mean
titer of
129 ± 80. At
their
this
SN
time
(DPIV). The revaccination was carried out at 1 8 0 ^ day
interval,
after the primary vaccination using the same type of
drop of two units
vaccine and dose.
of animal n s 33, and animal n s 16 maintained its titer
Bleedings
were
made
shortly
before
the
of
although
1:62,
whilst
statistically
not
significant,
a
in titer was detected in the serun
the
antibody
titers
of
other
three
actninistration of the second vaccine shot and repeated
animals
subsequently as described for the first vaccination.
values, titers corresponding to two heifers were found
Serum samples
stored at
taken
-20 °C until
at
each
bleeding
required.
After
days
thawing,
were
have
submitted to SN test. The antibody titration was run
rapidly with
twice,
mean
dilution
at
the
assessed
for
first
the
titration
second
time,
were
using
tentatively
the
two-fold
terms
of
their
absolute
From day 3 after the revaccination the levels of
the
samples not having determined the 50% end
in
to be increased 3.7 times within 24 hours.
the
sera were inactivated at 56 °C for 30 minutes and then
all
increased
serum
neutralizing
rise
in
titer
corresponding
final
50%
antibodies
the mean
to
end
titer of
was
7 th
2.14
DPR
dilutions
times.
were
but
tended
to elevate
1:277 ± 161
not
they
and the
Serum
samples
determined
were
found
their
to be
serial dilutions and the final dilution of the serum-
greater than 1:6,400, except animal n s 16 with a titer
virus mixture ranged from 1:6.25 to 1:25,600. Control
of
serum
corresponding
was
also
dilutions,
diluted
each
by
using
dilution
two-fold
was
then
serial
inoculated
1:4,525.
Similar
to
results
14th
DPR,
were
their
found
50%
end
for
sera
dilutions
were not determined but animal n s 16 with a titer of
1:4,530.
intracerebral ly into five mice each.
The mice were observed dail^ for 21 days and only
the mice found dead from the 4
were considered for
the
titer
day post inoculation
confutation,
made accordingly to REED; MUENCH ^
were
expressed
as
the
which was
DISCUSSION
(1938). The titers
reciprocal
of
dilutions
In
the
sera
of
cattle
given
a
commercially
produced rabies inactivated vaccine, detectable amount
protecting 50% of the inoculated mice.
of specific antibodies could not be found for several
days after
the
RESULTS
"lag
Although
The
of
time course of the humoral
five
cattle
enabled by
and
14
after
values
are
immune response
inactivated
bleeding at
days
respective
antibody
to
intervals
primary
in
rabies
of
vaccination
titers
of
vaccine,
not
the primary vaccination.
period",
the
followed
time course
at
daily
1,3,7
are
and
their
reported elsewhere.
neutralizing
of
to
the
intervals,
This
is known as
TIZARD
1977.
immune
response was
serun
neutralizing
antibodies were already detectable at 7 t^1 DPIV, which
zero,
surrmarized in Tab. 1. At day zero, all
according
in
accordance
to
many
of
the
previous
works
The response of cattle given a second dose of the
same vaccine six months
later was very different from
five animals were found with their SN titers < 1:5 and
the first in that it occurs much more rapidly and the
at
serum neutralizing titers reach higher levels. The so-
2nc* and
3 rc* DPIV
the
titers
determined
were
<
Braz. J. vet. Res. anim. Sci., v.28, n. 1, p.51-7, 1991.
54
ITO, F.H. et al.
called
"lag
period"
tended
to be
very
transient
or
undetectable.
that
have
investigated
vaccines.
The mean titer corresponding to this time point,
This
is
different
of
types
epidemiological
of
especially in situation when Agricultural Authorities,
i.e., 1st DPR, has increased from 58 ± 14 to 129 ± 80
field practitioners and cattle farmers must
within 24 hours,
rapidly and effectively to control
indicating that the drop in the level
of antibodies due to "in vivo" blocking effect did not
occur.
rabies
importance,
intervene
the focus of this
lethal disease.
In fact, the adjuvant contained in the vaccine
may have
influenced the processing of antigen by the
antigen sensitive cells,
release
from
the
degradation.
slowing the rate of antigen
vaccine
When
depot
and
adninistered through
(1962)
MANDELL
SVEHAG;
phenomenon of
antigen
consequent
directly
24
intravenous route, UHR et al.
and
the
20
"negative phase"
ITO, F.H.; CORTES, J.A.; RWEYEMAMU, M.M.; UMEHARA, 0.;
was
(1964)
due
reported
to
MEDEIROS NETO, R.; DE LUCCA NETO, D.; BALTAZAR, M.;
VASCONCELLOS,
the
the excess of
com
serum antibodies.
The
S.A.; VASCONCELLOS,
M.E.P.
Perfil
vacina
anti-rábica
inativada,
preparada
células BHK contendo Hidróxido de Alumínio.
antibody
levels
of
1:62
and
da
resposta imune humoral de bovinos após a revacinação
1:24,
em
Braz. J.
vet. Res. anim. Sei. , São Paulo, v . 28, n.1, p.51-7, 1991.
respectively derived from sera of animal n s 16 and n s
St
33 taken at 1
DPR, when compared to the values
RESUMO: O fenômeno do consumo de antígeno, devido à
corresponding
presença de anticorpos neutralizantes específicos para
to
those
statistically different,
of
180
DPR
indicating
"negative phase" did not occur.
clearly
However,
are
not
that
the
in spite of
a
raiva,
em
possível
bovinos
previamente
interferência
na
vacinados
resposta
e
a
sua
imunológica
the high sensitivity of the mouse SN test used in this
humoral, decorrente de revacinação, foi investigado em
experiment,
cinco bovinos mestiços azebuados, criados em condições
this
method
of
antibody
quantitation
involves assay in living system and the reactions are
de campo. A revacinação foi realizada 180 dias após a
subejected
primeira
to
a
high
degree
of
variability;
the
aplicação,
utilizando
uma
vacina
comercial
results tend to change gradually over a wide range of
inativada, preparada em células BHK-21. As amostras de
doses
soros
of
the
NILSSON
virus
(1974),
and,
as
suggested
they must be
by
CORTES;
interpreted carefully.
foram
(zero),
obtidas
24 ,
72
em
intervalos
horas,
sete
e
seqüenciais
14
dias,
de
em
0
cada
Based on the analysis of the overall results, we are
vacinação e foram submetidas à prova de neutralização
inclined in not accepting the phenomenon of "negative
em camundongos para a pesquisa de anticorpos. 0 título
phase" to occur with the vaccine used.
Another
fact
médio de anticorpos neutralizantes,
clearly demonstrated
in this study
momento
encontrado para o
imediatamente antes da primeira vacinação foi
was the velocity in the rising of the antibody titers
< 1:5,24 e 72 horas após a vacinação foi < 1:6,25; no
after the presentation of the second dose of the same
sétimo dia pós-vacinação o valor médio foi de 1:144 ±
vaccine;
the
memory
cells
as
well
as
the
effector
51; aos 14 dias pós-vacinação,
iumune response must have
os
effectively
by
dia pós-vacinação, com um valor médio de 1:58 ± 14; no
been
20
MANDEL
triggered
(1964)
horas
após
a
dose
revacinante,
um
valor
médio
de
1:129
± 80,
dose gives enduring
para 1:277 ± 161 no 3 S dia pós-revacinação,
that
to two days.
IgM
memory
synthesis
but
in
the
UHR;
has
and antibody population
IgM synthesis proceded
BAUMANN
23
(1961)
short-lasting
presence
effective anamnestic response
of
no
24
by one
duration
detectáveis
detectado
response
the
SVEHAG;
títulos
entanto,
IgM and IgG;
that
vaccine.
apresentaram
antibody synthesis is related to dose of antigen; high
consisted of
reported
the
animais
1:3.460 ± 1.329. Todos
cells of the cel I-mediated
of
high
IgG
reported
crescentes
no
7! e
no
14! dia
18 0 a
e níveis
pós-revacinação,
respectivamente,
immunologic
1:25.600,
indicando o estabelecimento de uma resposta
doses,
anamnéstica
the
IgG.
consumo
títulos
Analyzing the serum neutralizing antibody profile
do
de
plena.
Não
antígeno
e
foi
a
obervado
conseqüente
anticorpos,
a
o
1:6.400
com
valores,
is associated only with
superiores
foi
ascendendo
efeito
diminuição
imediatamente
após
e
do
nos
a
revacinação.
of animal n* 16 it seems that the rise in the level of
antibodies tended to a plateau; this could be due to
an
individual
stimulus
difference
rather
than
in responding
antigen
to an antigen
exhaustion.
The
scheme for the vaccination of young calves,
ideal
however,
is still lacking and needs further investigation.
The
anamnestic
immune
response
was
fully
confirmed, corroborating the findings of other authors
Braz. J. vet. Res. anim. Sei., v.28, n. 1, p.51 -7, 1991.
UN1TERMOS:
Raiva,
bovinos;
Anticorpos,
Imunização; Imunidade, bovinos
formação;
Course o f secondary humoral im m une response sh o rtly after revaccination
11-HUDSON,
REFERENCES
R.J.;
Physiological
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01-ABELSETH,
M.K.
An
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lmmunobiol.
ao
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for
in tissue culture.
Ser.
v.1,
Stands.,
/Apresentado
rabies
p. 367-75,
International
1966.
Symposium
on
12-INGRAM,
SABEN,
and
55
H.S.;
environmental
EMSLIE,
D.
influences
on
Vet-Bull., v.44, p . 119-28, 1974.
D.G.;
of young
SMITH,
A.N.
animals.
I.
Immunological
Review
of
the
response
literature.
Canad. vet J . , v.6, n.8, p . 194-204, 1965.
Rabies, Talloires, 1965/
13-LAWSON,
02-ABELSETH, M.K.
Bovine vaccines - Past and present.
In: BAER, G.M. The natural history o f rabies.
Academic Press, 1975.
03-ACHA,
P.N.
New York,
v.2, p . 203-19.
Epidemiologia
de
paralitica transmitida por
la
rabia
bovina
Los quiropteros.
04-ARELLAN0, S.C.; SUREAU, P.; BATALLA, D.
la
eficacia
de
la
vacuna
Bol.
WALKER,
rabies
V.C.R.;
vaccine,
CRAWLEY,
duration
cattle, dogs and cats.
of
J.F.
ERA
immunity
in
Vet Med small. Anim. Clin.,
14-LINHART,
S.B.
The biology and control of vampire
bats. In: BAER, G.M.
Evaluación
cepa
Tec. pec. M ex.,
15-MALAGA-ALBA,
A.
New
The natural history of rabies.
York, Academic Press, 1975.
antirrabica
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Recebido para publicação em 10/10/90
a f ter
serum neutralizing
vaccination
of
antibody
ca t t l e
with
i n a c t i v a t e d ra b i e s v a c c i n e . S ã o Paulo,
Animal
ti t e r s
BHK-21
cell
c u lture
1988.
Neutralizing Antibody Titers*
Number
Day 0
10
< 5
lSt D F V * *
3 rd D F V
7t h D F V
< 6.25
< 6.25
141
4,150
14thD F V
16
< 5
< 6.25
< 6.25
31
504
17
< 5
< 6.25
< 6.25
178
4,525
19
< 5
<6.25
<6.25
170
4 , 592
33
< 5
< 6.25
< 6.25
199
4,530
...
...
144
Variance
...
...
3 527
St a n d a r d d e v i a t i o n
...
...
59
M e a n s t a n d a r d err o r
...
...
26
Confidence interval
...
...
* R e c i p r o c a l of n e u t r a l i z i n g a n t i b o d y dilution,
rabies v i r u s w i t h 30 m o u s e I D ^ g / 0 . 0 3 m l
D a y Post V a c c i n a t i o n
§ C o n f i d e n c e interval,
... N o t d e t e r m i n e d
Braz. J. vet. Res. anim. Sci., v.28, n.1, p.51-7, 1991.
0! = 0.05
93 I -I 195
3, 460
2, 3 0 2,117
1, 517
678
2, 131
M
1
W
■
C-
Arithmetic mean
**
shortly before
<o
00
and
rabies
virus.
Aprovado para publicação em 16/05/91
TABLE 1 - A n t i r a b i e s
to
vaccinated
In: INTERNATIONAL CONFERENCE
with
antibody
cattle
u s i n g C V S s t r a i n o f f i xed
strain
of
in
the
Course o f secondary humoral im m une response sh o rtly after revaccination
TABLE
2
- Antirabies
serum neutralizing
antibody
ti t e r s
shortly
57
before
and a f t e r r e v a c c i n a t i o n of cat t l e at 180 days w i t h B H K - 2 1 cell
c u l t u r e i n a c t i v a t e d ra b i e s vaccine. São Paulo,
Animal
1988.
N e u t r a l i z i n g A n t i b o d y Ti t e r s *
„rd
_ th , ,
lSt D P R**
3
DPR
7
DPR
■,th . ,,
14
DPR
Nu m b e r
1 8 0 ^ day
10
67
80
308
> 6,400
> 25,600
16
62
62
79
4,525
4,530
17
67
224
356
> 6,400
> 25 , 6 0 0
19
70
259
565
> 6,400
> 25 , 6 0 0
33
26
24
80
> 6,400
> 25,600
58
129
277
26S
8,767
33 , 4 8 9
16
93
183
7
41
Arithmetic mean
Variance
Standard deviation
M e a n s t a n d a r d err o r
Confidence interval
44 I-I 72
44 I-I 209
82
116 I-I 438
* R e c i p r o c a l of n e u t r a l i z i n g a n t i b o d y dilution, u s i n g CV S st r a i n of fixed
r a b ies v i r u s w i t h 30 m o u s e I D ^ q / 0 . 0 3 m l
**
Day Post Revaccination
§ C o n f i d e n c e i n terval,
OL = 0.05
... N o t d e t e r m i n e d
Braz. J. vet. Res. artim. Sci., v.28, n. 1, p.51 -7, 1991.