PERSISTENCE DURATION OF IMMUNOGLOBULIN G ANTIBODIES TO RIFT VALLEY
FEVER VIRUS IN SHEEP AND GOATS SERA AFTER VACCINATION
By
Abdelhamid A. M. Elfadil and Emad S. Shaheen
Campaign for Control of Rift Valley Fever, Ministry of Agriculture, Jazan, Kingdom of Saudi Arabia. E-mail:
aamelfadil@yahoo.com
KEYWORDS: Rift Valley fever, Vaccination, Immunoglobulin G, Herd immunity, Control
strategies.
ABSTRACT
Duration of immunoglobulin G (IgG) antibodies to Rift Valley fever (RVF)
virus after vaccination with the live attenuated RVF Smithburn strain vaccine was
investigated in two groups (Group A and B) of sheep and goats. Also, two batches
(Batch I and II) of the same vaccine were used to compare between them. The IgGsandwich enzyme-linked immunosorbent assay (ELISA) was used to detect IgG
antibodies in serum samples of vaccinated animals. For Batch I, the percentage of IgG
positive animals significantly declined from 95% to 66.7% after the elapse of one
year, and to 50% after the elapse of four years and eight months. It would decline to
zero after six years and eleven months. For Batch II, the decline of the percentage of
IgG positive animals from 87%, which was attained at four weeks following
vaccination, to 77.3% after the elapse of one year and eight months was not
significant.
It could be concluded that the level of herd immunity induced by the live
attenuated RVF Smithburn strain vaccine significantly declines with the elapse of
years. Also, the decline of the level of herd immunity varies between different batches
of the same vaccine. Hence, efficient and cost-effective vaccination strategies for
control of RVF have been discussed.
INTRODUCTION
Herd immunity to Rift Valley fever (RVF) occurs in animals after natural
infection with the RVF virus as well as after vaccination. This immunity is
demonstrated by detection of antibodies to RVF virus in serum samples of infected or
vaccinated animals. The ELISA technique has the advantage of differentiating between
immunoglobulin M (IgM) and immunoglobulin G (IgG) antibodies to RVF virus
(Paweska et al., 2003). Since IgM antibodies persist in the blood for 4-7 weeks
following vaccination or natural infection and IgG antibodies persist for few years
(Paweska et al., 2003, Elfadil et al., 2005), immunity could be monitored by detection
of IgG antibodies. However, the duration of herd immunity after vaccination is
variable. It has been reported that the inactivated RVF vaccine confers immunity for 612months; therefore, annual vaccination is recommended (OIE, 1996). However,
conflicting reports were published about the duration of immunity after vaccination
with the live attenuated RVF vaccine (Losos 1986, OIE 1996).
In the regions of Jazan, Tahamat Asir, Tahamat Makkah and Albaha in
Southwestern Saudi Arabia, mass vaccination with the live attenuated RVF Smithburn
strain vaccine was implemented after the occurrence of RVF outbreak in 2000/2001,
and vaccination of six-month-old animals has continued thereafter. However, herd
immunity monitored in 2003 ranged from 16% to 30% in different districts of Jazan
region (Elfadil and Ali, 2006a). Hence, the issue of mass revaccination is now under
consideration. In order to implement the most efficient and cost-effective strategy to
control RVF, knowledge of the duration of herd immunity in local breeds of animals in
Southwestern Saudi Arabia after vaccination with the live attenuated RVF Smithburn
strain vaccine is essential.
This paper clarifies the duration for which IgG antibodies to RVF virus persist
in the blood of sheep and goats vaccinated with different batches of the live attenuated
RVF Smithburn strain vaccine and discusses the appropriate vaccination strategies that
could be implemented for control of RVF.
MATERIALS AND METHODS
Two groups (Group A and B) of local breed sheep and goats in an
experimental farm in Jizan district, Southwestern Saudi Arabia, were used to follow
up the duration of IgG antibodies to RVF virus after vaccination. Each animal was
marked with a numbered ear tag. Two batches (Batch I and II) of the live attenuated
RVF Smithburn strain vaccine (RSA Registered No. G 0119 Onderstepoort Biological
Products Ltd., South Africa) were used to allow comparison between them.
The first group (Group A) consisted of 20 female sheep and goats (10 sheep
and 10goats). All animals in the group were vaccinated with the live attenuated RVF
Smithburn strain vaccine (Batch I) on August 2000. These animals were followed for
disease signs and serologically tested to detect IgG antibodies to RVF virus on
September 2000 (four weeks following vaccination), September 2001, September
2003 and April 2005.
The second group (Group B) consisted of 30 female sheep and goats (8sheep
and 22 goats). All animals in the group were vaccinated with the live attenuated RVF
Smithburn strain vaccine (Batch II) on July 2003 (Elfadil et al., 2005). These animals
were followed for disease signs and serologically tested to detect IgG antibodies to
RVF virus on August 2003 (four weeks following vaccination) and April 2005.
The percentage of immune animals was measured by the percentage of IgG
positive serum samples in each test. The IgG-sandwich ELISA techniques used to
detect IgG antibodies to RVF virus was described in previous publications (Paweska et
al., 2003, Elfadil and Ali, 2006a).
Statistical analysis was performed using the one-sided F-test to investigate the
presence of significant differences between the percentages of immune animals in
different points in time after vaccination. The intercept statistic was used to determine
after how many years the level of herd immunity would decline to zero. Only data
from Group A were used to determine the intercept statistic.
RESULTS
In Group A, the percentages of IgG positive animals were 95% in September
2000 (100% in sheep and 90% in goats), 66.6% in September 2001 (55.5% in sheep
and 77.7% in goats), 64.5% in September 2003 (66.5% in sheep and 62.5% in goats)
and 50% in April 2005 (33.3% in sheep and 66% in goats). The decline of the
percentage of immune animals from 95% to 66.7% after the elapse of one year was
significant (p-value = 0.0017). This percentage of immune animals would decline to
zero after six years and eleven months.
In Group B, the percentages of IgG positive animals were 87% in August 2003
(88% in sheep and 86% in goats) and 77.3% in April 2005 (57% in sheep and 89.5%
in goats). The decline of the percentage of immune animals from 87% to 77.3% after
the elapse of one year and eight months was not significant.
DISCUSSION
Knowledge of the duration of herd immunity after vaccination with the live
attenuated RVF vaccine is essential in order to decide which vaccination strategy
could be adopted. Different vaccination strategies to control RVF may be considered
according to the situation of the disease. One strategy is mass vaccination of all
livestock in an affected region, which is usually implemented to control RVF
epidemics. Another strategy is partial vaccination, which is limited to young animals
at the age of six months after the disappearance of maternal immunity; or ring
vaccination, which is implemented at the occurred-nce of sporadic recent cases of RVF
in high-risk areas (Elfadil et al., 2006b, Elfadil et al., 2006c). Partial and ring
vaccination were implemented during the inter-epidemic phase of the disease.
The level of herd immunity conferred by vaccination partially depends upon
the type of the vaccine used. The results of this study demonstrate that there was a
difference even between different batches of the same vaccine regarding the
percentage of immune animals attained after four weeks following vaccination (95%
for Batch I versus 87% for Batch II). Moreover, the decline of the level of herd
immunity after one year was significant for Batch I (95% to 66.7%), while it was not
significant even after one year and eight months for Batch II (87% to 77.3%). These
findings should be considered when coming to the choice between different vaccines
for control of RVF.
The results of the present study demonstrate that the percentage of immune
animals significantly declines with the elapse of time. These results are consistent
with the findings of a previous study, which reported a significant decline of RVF
neutralizing antibodies from 71.7% in 1988 to 23.9% in 1989 Thiongane et al., (1991).
Also, the results are consistent with our field observa-tions on the significant decline of
herd immunity in Alarda district, which is the hardest hit by the RVF outbreak in Jazan
region, Saudi Arabia Elfadil et al., (2004), from 95% during the outbreak to 47% two
years later Elfadil and Ali, (2006a). In field observations, the decline of herd
immunity could be partly attributed to generation turn over and/or entries of new
unvaccinated animals. However, in the present study the decline in the percentage of
immune animals could be due to low sensitivity of the diagnostic test. It was reported
that time-dependent changes in the sensitivity of ELISA were clearly evident specially
for IgM-capture ELISA which was 100% sensitive 5-42 days following infection or
vaccination, and only 12.5% sensitive 3 weeks later (Paweska et al., 2003).
Although the results of the present study indicate a significant decline of the
percentage of immune animals after one year of vaccination for Batch I of the
vaccine, the decline after one year and eight months for Batch II was not significant.
Also, IgG antibodies to RVF virus were detected in 64-77.3% of vaccinated animals
after the elapse of 1-2 years and they were detected in 50% of vaccinated animals
after the elapse of four years and eight months. Moreover, it has been proved that
animals vaccinated with the live attenuated RVF vaccine were immune even after the
disappearance of antibodies from their blood suggesting other mechanism of cellular
immunity (Barnard, 1979). Also, it has been reported that the live vaccine induces
lifelong immunity against clinical disease (OIE, 1996). Considering these findings and
reports, implement-ation of mass re-vaccination to control RVF during the interepidemic phase of the disease could not be justified.
Therefore, it is recommended to implement partial vaccination with the live
attenuated RVF vaccine for young animals at the age of six months, and to implement
ring vaccination when sporadic recent serological and/or clinical cases of RVF occur
in high-risk areas. However, since the live attenuated RVF vaccine was reported to
cause abortion (Morril et al., 1987), vaccination of pregnant animals should be
avoided.
ACKNOWLEDGEMENTS: We would like to thank Drs. Sami S. M. Ali, Shehta M. Musa,
Khalid A. Hasab-Allah and Omer M. Dafa-Allah from Jazan Veterinary Diagnostic
Laboratory for performing the ELISA tests.
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