Journal of Pharmacy And Bioallied Sciences
Journal of Pharmacy And Bioallied Sciences Login  | Users Online: 1253  Print this pageEmail this pageSmall font sizeDefault font sizeIncrease font size 
    Home | About us | Editorial board | Search | Ahead of print | Current Issue | Past Issues | Instructions | Online submission

 Table of Contents  
Year : 2012  |  Volume : 4  |  Issue : 4  |  Page : 258-266  

Formulation and delivery of vaccines: Ongoing challenges for animal management

Commonwealth Scientific and Industrial Research Organisation, Division of Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia

Date of Submission06-Nov-2011
Date of Decision30-Dec-2011
Date of Acceptance24-Mar-2012
Date of Web Publication07-Nov-2012

Correspondence Address:
Lyn A Hinds
Commonwealth Scientific and Industrial Research Organisation, Division of Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0975-7406.103231

Rights and Permissions

Development of a commercially successful animal vaccine is not only influenced by various immunological factors, such as type of antigen but also by formulation and delivery aspects. The latter includes the need for a vector or specific delivery system, the choice of route of administration and the nature of the target animal population and their habitat. This review describes the formulation and delivery aspects of various types of antigens such as killed microorganisms, proteins and nucleic acids for the development of efficacious and safe animal vaccines. It also focuses on the challenges associated with the different approaches that might be required for formulating and delivering species specific vaccines, particularly if their intended use is for improved animal management with respect to disease and/or reproductive control.

Keywords: Delivery systems, domestic animals, formulation, immunocontraception, immunological adjuvants, vaccines, wildlife

How to cite this article:
Sharma S, Hinds LA. Formulation and delivery of vaccines: Ongoing challenges for animal management. J Pharm Bioall Sci 2012;4:258-66

How to cite this URL:
Sharma S, Hinds LA. Formulation and delivery of vaccines: Ongoing challenges for animal management. J Pharm Bioall Sci [serial online] 2012 [cited 2022 Jul 2];4:258-66. Available from:

In the last decade, many articles have reviewed research on the development and status of animal vaccines, especially those developed primarily for use in disease prevention for domestic animals (pets and production livestock). [1],[2],[3] This review addresses the challenges associated with formulation and delivery of such vaccines and how this assists researchers who are endeavoring to deliver vaccines for either disease management or for fertility control of wildlife. We define wildlife as animals living as wild populations. Thus, wildlife includes introduced vertebrates, which have become pest species in the natural environmental and/or agricultural landscape as well as overabundant native species that require management for conservation, disease or economic reasons in the same landscapes. Delivery of vaccines to these wild populations remains a major challenge though some progress is being made.

Successful vaccines, whether for animals or humans, induce an effective and sustained immune response, have minimal side effects and can be produced cost-effectively at a large scale. Despite these overt requirements, many of the developmental issues regarding effective delivery of vaccines are specific to the animal situation. The delivery of vaccines to domestic pets and livestock is a straightforward scenario compared to delivery to pest animals and wildlife populations. Domesticated species can generally be individually handled for vaccination, including booster immunizations. Efficient access to wildlife is problematic if the vaccine needs to be delivered as an injection. One of the difficulties for wildlife vaccination is to be able to achieve coverage of an appropriate proportion of the target population, and it may require repeated treatment over time to achieve efficacy. Oral, rather than parenteral, delivery would be ideal, but it also raises the need for the development of species specific delivery systems. These challenges along with regulatory and commercial hurdles in the development and commercialization of animal vaccines have constrained the number of commercial products developed for animals, especially for wildlife.

Domestic animal vaccines are used in order to increase food quality and productivity and to prevent and treat diseases. There is also increasing pressure from consumer groups to restrict the use of antibiotics and other drugs in domestic animals, especially in the developed world. [4] Veterinary vaccines offer many benefits over chemical drugs and antibiotics including the absence of residues in foodstuffs, lower frequency of administration, cost-effectiveness and avoidance of the selection of antibiotic-resistant, food-borne bacteria in food animals. [5] On the other hand, an important application for wildlife vaccines is elimination of infections, transmitted directly or indirectly to human beings (zoonotic diseases) or to endangered animal species. [1] One highly successful example of a vaccine for wildlife has been the development of an oral recombinant vaccinia virus, expressing the G-glycoprotein of the rabies virus. It has been widely used in northern Europe since the late 1980s to reduce the incidence of rabies in European red foxes [6],[7] and is also currently in broad use for rabies control in raccoons, gray fox and coyote in northern America. [8] In addition, fertility control of wildlife using contraceptive vaccines, which induce an immune response against a specific reproductive antigen (e.g. gonadotrophin releasing hormone, zona pellucidae proteins, sperm proteins), as an alternative method of pest management, has been researched for various invasive animal species in the recent past, and research and development is ongoing. [9],[10],[11],[12] Advances in vaccine research have started to provide not only more commercial vaccine products but also novel applications for animal uses [Table 1].
Table 1: Examples of available animal vaccines and their characteristics

Click here to view

This review describes recent research developments and ongoing challenges in the formulation and delivery of various types of antigens such as killed microorganisms, proteins and nucleic acids for the development of efficacious animal vaccines. It also provides a comparative discussion of specific vaccine delivery requirements, depending on the purpose of the vaccine and its use in different animals (livestock, domestic pets, introduced pest mammals or overabundant native species).

Types of animal vaccines

Formulation issues related to animal vaccines not only vary with the target animal population but also are significantly influenced by the characteristics of selected antigen(s) to be formulated. Vaccines can be categorized as two types, living or non-living, and these raise different issues for formulation and delivery.

Live or live-attenuated vaccines for disease control/protection

Conventionally, many of the vaccines licensed for animal use employ live or live-attenuated microorganisms as antigens. Live vaccines usually induce both cellular (e.g. cytotoxic lymphocytes) and humoral (e.g. systemic antibodies) immunity because of the ability of live microorganisms to infect target cells. [21] These vaccines can be very important for disease management, prevention and even eradication. For example, a live-attenuated vaccine, known as the "Plowright" vaccine, has been used in a vaccination program to eradicate rinderpest virus infection around the world. [22],[23],[24]

Serious safety issues, related to live or live-attenuated vaccines such as risk of residual virulence, reversion to pathogenic wild types and potential for unintended consequences if other than target species ingest the vaccines, have resulted in stricter regulatory requirements for live or live-attenuated vaccines. These requirements were highlighted during a vaccination program to control porcine respiratory and reproductive syndrome (PRRS) in Denmark. There are two main types of PRRS virus, European (Lelystad virus strain) and North American, which show 55% to 79% identity at the nucleotide level but show differences in serological cross-reactivity. [25] Following vaccination with the live-attenuated North American PRRS vaccine against the European PRRS virus type in Denmark, the vaccine virus spread within vaccinated as well as non-vaccinated herds, leaving both virus types in the Danish pig population. [26] The other issue with live or live-attenuated vaccines (e.g. against Foot and Mouth Disease, FMD) is that they can confound disease surveillance, based on serological testing of animals - false positives may result in the loss of a country's disease-free status. [27]

Non-living vaccines

Some of the disadvantages associated with live microorganism-based vaccines along with advances in novel applications in vaccinology and biotechnology have paved the way for the development and use of non-living antigens in the vaccines. Whole inactivated or killed vaccines are generally safer than live vaccines, but their inability to infect cells usually results in induction of humoral immune responses without any cell-mediated immunity, making them less effective compared to live or live-attenuated vaccines. [28] Consequently, inactivated or killed antigens usually require the addition of immunological adjuvants and multiple dosing to achieve and sustain a desired level of protective immunity. Additionally, effective oral administration of inactivated microorganisms may require incorporation of a specific protective carrier system. The necessity for immunological adjuvants, carrier systems and multiple dosing highlights the need for specific formulation strategies for these antigens. Indeed, many commercial vaccines, based on killed or inactivated microorganisms, have been successfully developed and are in use for production animals and some wildlife [Table 1].

Developments in biotechnology and molecular biology have enabled the utilization of sub-cellular subunits such as proteins, peptides, carbohydrates and nucleic acids as antigens in vaccines. DNA vaccines represent a growing theme in animal vaccination, and all aspects of DNA veterinary vaccines were recently reviewed by Redding and Weiner. [29] The identification and isolation of sub-cellular components of microorganisms, which play important roles in induction of immunity, prompted their use as safe, non-replicating antigens in vaccines. Acellular antigens, especially proteins, carbohydrates and peptides can be widely used for animal vaccinations due to their non-replicating nature, however, on their own they generally induce poor immunity. The latter can be overcome, at least in part, by conjugation of the small peptides with large immunogenic proteins (such as keyhole limpet hemocyanin), the use of suitable carrier systems and co-formulation of immunological adjuvants with the antigens. [30],[31] In addition, most of these antigens tend to be unstable under environmental conditions, such as direct exposure to high temperature, humidity and light [32],[33] and when subjected to the acidity and enzymatic activity of the gastrointestinal tract. [34],[35] Again, developments in synthetic peptide and polymer chemistry could potentially offer solutions for poor antigen stability. [36],[37]

The use of acellular antigens in vaccines has certainly flourished in the last few decades not only because of their safe profile but also because they have enabled novel applications to be investigated. One interesting application has been for reproductive control by immunizing animals against sex hormones, gametes or other key targets in the reproductive tract [Figure 1]. [38],[39],[40],[41],[42] The most studied reproductive hormone as a vaccine target is luteinizing hormone releasing hormone (LHRH), also known as gonadotrophin-releasing hormone (GnRH). [43],[44],[45],[46],[47],[48],[49],[50],[51],[52] GnRH is a small 10 amino acid peptide released from the hypothalamus in all species of mammals and has a central regulatory role in reproductive functions. Immunization against GnRH can result in immunocontraception and control of sexual behavior in both sexes [Table 1] though greater efficacy is achieved in females. Strategies to control fertility using vaccines based on gamete antigens, particularly zona pellucida proteins, have been the most widely researched. [9],[12],[42],[53],[54],[55] However, commercial successes for immunocontraceptive vaccines have been relatively few primarily because of poor immunogenicity of small peptide self antigens and difficulties in cost-effective practical delivery of the vaccines to target wildlife species. Another interesting evolution which took place with the use of acellular antigens is development of combined vaccines incorporating two or more antigens, initially used for humans and which later paved the way for numerous combined veterinary vaccines. [56]
Figure 1: Schematic representation of reproductive targets used for the development of immunocontraceptive vaccines

Click here to view

Formulation of non-living vaccines

Formulation research for antigens began about a century ago when scientists discovered that combining certain reagents, such as saponins, lecithin, aluminum compounds and killed mycobacterium with the antigen for injection could enhance the immune response against the antigen. [57],[58],[59],[60] These initial discoveries slowly led to development of immunological adjuvants and delivery systems that boost or alter immune responses to the co-administered antigen. We consider the developments in the formulation of animal vaccines under two categories: (a) use of immunological adjuvants, and (b) use of antigen delivery or carrier systems.

Immunological adjuvants

Immunological adjuvants can provide artificial signals to the immune system to initiate the immune response against a co-administered antigen. [31] In the development of a vaccine, it is important to establish the type of immune response, essential for optimal vaccine efficiency, and then select adjuvant(s) that will help to induce and enhance that type of immune response without unacceptable adverse effects. Different immunological adjuvants can induce one or more type of immune response depending on the route of administration although some of these also induce significant, undesirable side effects [Table 2].
Table 2: Examples of immunological adjuvants which enhance immune responses against acellular antigens

Click here to view

The different properties of the various adjuvants indicate the need for individual formulation strategies for particular vaccines based on (a) intended use, (b) type of immune responses required, (c) route of administration and (d) target animal population. An example highlighting the importance of formulation for an animal reproductive vaccine is the commercial failure of Vaxstrate® vaccine, which comprised a LHRH-ovalbumin conjugate, formulated with an oil emulsion adjuvant system. [74] It was used in Australia in 1990s but withdrawn a few years later due to poor sales as a result of its frequent side effects and poor efficacy in the field. [1] Many of the conventional immunological adjuvants such as Freund's complete adjuvant (FCA), bacterial toxins and non-purified crude agents (e.g. lipid A) usually induce strong stimulant effects but also frequently induce adverse effects upon administration to animals, and any vaccine incorporating these adjuvants is unlikely to be approved by regulatory authorities. [61],[75] Notwithstanding these effects, the recently registered and highly efficacious single-shot GnRH vaccine (GonaCon, USDA) uses an adjuvant comprising a Mycobacterium species, M.avium, and mineral oil (AdjuVac), [10] and it induces very limited side effects. However, newer alternative reagents, such as purified and/or receptor-specific adjuvants (e.g. monophosphoryl lipid A, ISCOMs, CpG oligonucleotides), which show moderate immune-stimulating effects, are being investigated. Many of these newer adjuvants are toll-like receptor (TLR) agonists (e.g. CpG oligonucleotides, monophosphoryl lipid A and poly (I:C)) and act by stimulating particular types of TLRs present on antigen presenting cells (APCs) such as dendritic cells situated in different lymphatic tissues. [76] Many of these newer adjuvants could be used for either mucosal or for parenteral routes of administration and are, therefore, an important consideration in formulation of an animal vaccine. Some of these adjuvants have been used successfully in commercial animal vaccines. One example is the Improvac® vaccine, a diethylaminoethyl dextran adjuvanted LHRH-protein conjugate formulation, which is used for the control of boar taint in pigs [Table 1]. [15],[77]

Antigen delivery/carrier systems

Various carrier systems have been investigated for antigen delivery, including liquid systems (e.g., emulsions), particulate delivery systems (e.g., liposomes, microparticles, nanoparticles, archaeosomes) and viral or bacterial vectors. Particulate delivery systems offer potential advantages such as co-delivery of antigen(s) and adjuvant(s), depot of antigen at the site of injection, presentation of an ordered and repetitive array of B-cell epitopes, stimulation of cell-mediated immune response against acellular antigens, and increased uptake of acellular antigens after mucosal administration. [5],[78],[79],[80] Some delivery systems such as virosomes, chitosan nanoparticles and archaeosomes also exhibit an in-built immunostimulant property, which could eliminate or reduce the requirement for any additional adjuvant in the vaccine formulation. [81],[82],[83],[84],[85],[86]

The use of a live, non-pathogenic virus or bacterium as a vector/carrier (e.g., Canarypox virus, Vaccinia virus, Fowlpox virus and Lactobacilli bacteria) [87],[88],[89] offers similar advantages to those for live vaccines, including the possibility of mucosal administration and widespread distribution to animals. However, as with live vaccines, there are regulatory and safety issues associated with replicating vectors, which are genetically modified to express foreign antigens, and prior immunity and/or induction of immunity against the vector itself may reduce efficacy. Despite such disadvantages, vector systems have been successfully used in several commercial animal vaccine products (e.g. Purevax feline rabies vaccine and RecombitekEquine West Nile Virus vaccine). [1],[90] This approach was extensively investigated for the species-specific delivery of reproductive control for introduced pest species (wild house mice, European rabbits and European red foxes) in the Australian environment and was termed viral-vectored immunocontraception, VVIC. [91],[92],[93],[94] As an example, for the wild house mouse, murine cytomegalovirus was engineered to express mouse zona pellucida 3, and it induced 100% permanent infertility within 3 weeks of an infection. However, poor transmission of the recombinant virus limited its efficacy as a disseminating product for mice. Despite concerted efforts over 10-15 years for mice, rabbits and foxes, technical difficulties precluded the full development of species-specific VVIC vaccines for field release. [95] Nevertheless, the approach still offers an excellent promise as a disseminating or non-disseminating delivery system for immunocontraceptive antigens to pest mammals.

Bacterial ghost systems have been investigated not only as vaccine candidates against their own envelope structures, but also as carrier and adjuvant vehicles for foreign acellular target antigens. [96] Bacterial ghosts are produced by protein E-mediated lysis of Gram negative bacteria (e.g. Escherichia coli, Vibrio cholerae, enterotoxigenic and enterohemorrhagic strains). [97] and show in-built adjuvant properties on both parenteral and mucosal (e.g. inhalational) administration. [98],[99] Bacterial ghosts have been assessed for their ability to deliver the zona pellucida proteins of the brush-tailed possum, a pest in New Zealand, and showed some promise. [100]

Some of the newer particulate delivery systems, such as virosomes and virus-like particles (VLPs), have been developed to retain the advantages of live viral systems but not the constraints posed by a replicating microorganism. These systems consist of one or more non-replicating viral components, such as membrane proteins for strong stimulation of immune responses against the incorporated antigen, but circumvent replication and side effects induced by other components of viruses. [2] VLPs are composed of one or several recombinantly-expressed viral proteins, which spontaneously assemble into particulate structures, resembling infectious viruses or, in some cases, sub-viral particles. VLPs have been produced for many different viruses that infect animals, such as Bluetongue virus, Nodavirus and Feline calicivirus. [101],[102],[103] They can also be used as a platform for inducing immune responses against selected antigens by incorporating antigenic epitopes by genetic fusion (chimeric VLPs) or by conjugating antigens to VLPs. [104],[105]

Virosomes are unilamellar liposomes, carrying viral envelope proteins and can be used to incorporate different types of subunit acellular antigens for delivery by mucosal or parenteral routes. [82] Virosomes have been investigated for vaccination against retroviruses, Sendai virus and Newcastle disease. [106],[107],[108] Moreover, discoveries of TLRs on antigen presenting cells (APCs) and their specific agonists have endorsed the development of cell and/or receptor specific particulate delivery systems for vaccines. [109],[110] Recently, an intensive emphasis has been given to targeting dendritic cells because of their role in detecting antigens in peripheral tissues, including vaccines at an injection site and then migrating to the T cell areas of lymphoid organs to initiate immunity. [111] These developments in targeted and novel delivery systems have opened new avenues for the development of effective but safe vaccines.

Delivery of animal vaccines

A successful vaccine requires not only careful consideration of its formulation but also an effective mechanism for its delivery to different animals, living in various environments. Delivery devices and delivery systems will vary depending on the target species (domestic, introduced pest or native wildlife), environment and scale of immunization. [Table 3] lists desirable formulation and delivery characteristics for veterinary and wildlife vaccines.
Table 3: Veterinary and wildlife vaccines: Desirable formulation and delivery characteristics

Click here to view

Various specialized parenteral delivery devices for intradermal gene gun delivery, short-distance dart delivery and long-distance ballistic vaccination have been developed and investigated for use in animal vaccination. [92],[112],[113],[114],[115] Specialized delivery systems such as biodegradable "Biobullets", made of photopolymerized PEG hydrogels, have also been investigated to make ballistic delivery efficient and feasible. [116] Ballistic delivery devices are usually air-powered rifles, which shoot the vaccine formulation into the muscle of large animal species. [5] In addition, nasal and transdermal routes of vaccination have been used for domestic animal vaccinations; for example Purevax® recombinant canarypox vectored feline leukemia vaccine has been commercialized for transdermal administration, using VET JET microneedle technology. [117],[118] These delivery systems have provided some success in vaccination of domesticated livestock and pets. For broad-scale, mass vaccination of wildlife, however, it has been accepted that parenteral vaccination generally would not be practical due to high resource requirements; thus if efficacious, oral delivery could be developed; it could be the most suitable and efficient route of vaccination.

Oral animal vaccination and research developments

The oral route of vaccine administration offers various advantages in that animals do not need to be captured for treatment, and distribution and delivery devices (e.g. bait stations) can be designed to provide target specificity. An ideal oral animal vaccine, whether for reproductive or for disease management, must be safe, species-specific, able to induce strong immune responses after one administration and must be formulated into a stable delivery system as a food bait attractive to the target animal species. The advantages of oral vaccination for wildlife have been exploited with some of the live or live virus vectored vaccines, for example, eradication of rabies in many countries using live or live-attenuated oral vaccines delivered in food baits. [119],[120],[121] However, this strategy shares the limitations of live or live-attenuated vaccines. On the other hand, poor stability of acellular antigens under environmental and gastrointestinal conditions poses serious formulation challenges in the oral delivery of acellular antigens. For successful oral delivery to wildlife, an acellular antigen should be formulated such that antigens and adjuvants are (a) protected from direct sunlight, high temperature, gastric and intestinal environments; (b) targeted to Peyer's patches in the intestinal tract; (c) effectively presented to antigen presenting cells and an immune response generated is sustained and effective.

VLPs and recombinant live dietary bacteria (e.g. Lactobacillus plantarum and Lactobacillus lactis) have been investigated as oral carriers for acellular antigens. As a vaccine-delivery vehicle, Lactobacilli effectively induces immune responses against acellular antigens by the oral route. [122] Another interesting approach has been the development of membranous or microfold cell (M-cell) targeted delivery systems, using M-cell surface targeting ligands (e.g. lectins, a monoclonal antibody targeting sialyl Lewis A). [123] Recently, many lipid and polymer-based oral food bait systems have been investigated and patented for the delivery of vaccines to wildlife. [124] However, further research is essential to achieve practical application.

The concept of using whole plant or plant fruits or seeds (e.g. rice, tomato) as an oral edible vaccine system has been suggested as a possible solution to various problems associated with vaccine delivery. [125],[126],[127] Proteins produced in transgenic plants are capable of invoking immune responses against many pathogens. [128],[129],[130],[131],[132],[133],[134] In theory, the use of plants for vaccine delivery to wildlife could overcome some of the challenges in oral delivery. However, the delivery of reproductive self-antigens expressed by transgenic plants is likely to pose a greater challenge for the induction of an efficacious immune response, particularly as their consumption may induce tolerance rather than immunity. Furthermore, apart from the likelihood that digestion and degradation of edible plant vaccines will occur in the gastrointestinal tract, safety and regulatory requirements for transgenic plants, probable contamination of human food supplies and people's attitudes to genetically modified products makes it highly unlikely that any commercial animal vaccine would be available in a transgenic plant form in the near future.

   Conclusion Top

Research developments in biotechnology and molecular biology have provided many breakthroughs in the identification of effective and safe antigens and adjuvants, which could be used for vaccination of animals to prevent spread of diseases or for other applications such as immunocontraception. In spite of these successes, commercial and field applications of animal vaccines are limited due to formulation and delivery constraints. Recent developments in the formulation and delivery of acellular antigens along with investigations of newer immunological adjuvants should enhance progress. However, it will be important to reduce production costs of the newer adjuvants, delivery systems and delivery devices to ensure commercial success. Oral delivery of vaccines to animals, particularly to wildlife and large groups of farm animals, is challenging and consolidated efforts by veterinary, wildlife, biotechnology and pharmaceutical researchers will be required for the foreseeable future.

   References Top

1.Meeusen EN, Walker J, Peters A, Pastoret PP, Jungersen G. Current status of veterinary vaccines. Clin Microbiol Rev 2007;20:489-510.  Back to cited text no. 1
2.Brun A, Bárcena J, Blanco E, Borrego B, Dory D, Escribano JM, et al. Current strategies for subunit and genetic viral veterinary vaccine development. Virus Res 2011;157:1-12.  Back to cited text no. 2
3.Shams H. Recent developments in veterinary vaccinology. Vet J 2005;170:289-99.  Back to cited text no. 3
4.Shryock TR. The future of anti-infective products in animal health. Nat Rev Microbiol 2004;2:425-30.  Back to cited text no. 4
5.Scheerlinck JP, Greenwood DL. Particulate delivery systems for animal vaccines. Methods 2006;40:118-24.  Back to cited text no. 5
6.Brochier B, Kieny MP, Costy F, Coppens P, Bauduin B, Lecocq JP, et al. Large-scale eradication of rabies using recombinant vaccinia-rabies vaccine. Nature 1991;354:520-2.  Back to cited text no. 6
7.Cross ML, Buddle BM, Aldwell FE. The potential of oral vaccines for disease control in wildlife species. Vet J 2007;174:472-80.  Back to cited text no. 7
8.Slate D, Rupprecht CE, Rooney JA, Donovan D, Lein DH, Chipman RB. Status of oral rabies vaccination in wild carnivores in the United States. Virus Res 2005;111:68-76.  Back to cited text no. 8
9.Hardy CM, Hinds LA, Kerr PJ, Lloyd ML, Redwood AJ, Shellam GR, et al. Biological control of vertebrate pests using virally vectored immunocontraception. J Reprod Immunol 2006;71:102-11.  Back to cited text no. 9
10.Fagerstone KA, Miller LA, Eisemann JD, O'Hare JR, Gionfriddo JP. Registration of wildlife contraceptives in the United States of America, with OvoControl and GonaCon immunocontraceptive vaccines as examples. Wildlife Res 2008;35:586-92.  Back to cited text no. 10
11.Fraker MA, Brown RG, Gaunt GE, Kerr JA, Pohajdak B. Long-lasting, single-dose immunocontraception of feral fallow deer in British Columbia. J Wildlife Manage 2002;66:1141-7.  Back to cited text no. 11
12.Kirkpatrick JF, Lyda RO, Frank KM. Contraceptive vaccines for wildlife: A review. Am J Reprod Immunol 2011;66:40-50.  Back to cited text no. 12
13.Jackwood MW, Saif YM. Efficacy of a commercial turkey coryza vaccine (Art-Vax) in turkey poults. Avian Dis 1985;29:1130-9.  Back to cited text no. 13
14.Moormann RJ, Bouma A, Kramps JA, Terpstra C, De Smit HJ. Development of a classical swine fever subunit marker vaccine and companion diagnostic test. Vet Microbiol 2000;73:209-19.  Back to cited text no. 14
15.Dunshea FR, Colantoni C, Howard K, McCauley I, Jackson P, Long KA, et al. Vaccination of boars with a GnRH vaccine (Improvac) eliminates boar taint and increases growth performance. J Anim Sci 2001;79:2524-35.  Back to cited text no. 15
16.Fenaux M, Opriessnig T, Halbur PG, Elvinger F, Meng XJ. A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004;78:6297-303.  Back to cited text no. 16
17.Veits J, Wiesner D, Fuchs W, Hoffmann B, Granzow H, Starick E, et al. Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc Natl Acad Sci U S A 2006;103:8197-202.  Back to cited text no. 17
18.Park MS, Steel J, García-Sastre A, Swayne D, Palese P. Engineered viral vaccine constructs with dual specificity: Avian influenza and Newcastle disease. Proc Natl Acad Sci U S A 2006;103:8203-8.  Back to cited text no. 18
19.Miller LA, Gionfriddo JP, Fagerstone KA, Rhyan JC, Killian GJ. The single-shot GnRH immunocontraceptive vaccine (GonaCon) in white-tailed deer: Comparison of several GnRH preparations. Am J Reprod Immunol 2008;60:214-23.  Back to cited text no. 19
20.Miller LA, Rhyan JC, Drew M. Contraception of bison by GnRH vaccine: A possible means of decreasing transmission of brucellosis in bison. J Wildl Dis 2004;40:725-30.  Back to cited text no. 20
21.Alexandersen S. Advantages and disadvantages of using live vaccines risks and control measures. Acta Vet Scand Suppl 1996;90:89-100.  Back to cited text no. 21
22.Baron MD, Banyard AC, Parida S, Barrett T. The Plowright vaccine strain of Rinderpest virus has attenuating mutations in most genes. J Gen Virol 2005;86:1093-101.  Back to cited text no. 22
23.Robertshaw D. Credit to Plowright for rinderpest eradication. Science 2010;330:1477.  Back to cited text no. 23
24.Plowright W. The duration of immunity in cattle following inoculation of rinderpest cell culture vaccine. J Hyg (Lond) 1984;92:285-96.  Back to cited text no. 24
25.Murtaugh MP, Elam MR, Kakach LT. Comparison of the structural protein coding sequences of the VR-2332 and Lelystad virus strains of the PRRS virus. Arch Virol 1995;140:1451-60.  Back to cited text no. 25
26.Mortensen S, Stryhn H, Søgaard R, Boklund A, Stärk KD, Christensen J, et al. Risk factors for infection of sow herds with porcine reproductive and respiratory syndrome (PRRS) virus. Prev Vet Med 2002;53:83-101.  Back to cited text no. 26
27.Pluimers FH. Foot-and-Mouth disease control using vaccination: The Dutch experience in 2001. Dev Biol (Basel) 2004;119:41-9.  Back to cited text no. 27
28.Roth JA, Henderson LM. New technology for improved vaccine safety and efficacy. Vet Clin North Am Food Anim Pract 2001;17:585-97, vii.  Back to cited text no. 28
29.Redding L, Weiner DB. DNA vaccines in veterinary use. Expert Rev Vaccines 2009;8:1251-76.  Back to cited text no. 29
30.Singh M, O'Hagan DT. Recent advances in veterinary vaccine adjuvants. Int J Parasitol 2003;33:469-78.  Back to cited text no. 30
31.Spickler AR, Roth JA. Adjuvants in veterinary vaccines: Modes of action and adverse effects. J Vet Intern Med 2003;17:273-81.  Back to cited text no. 31
32.Manning MC, Chou DK, Murphy BM, Payne RW, Katayama DS. Stability of protein pharmaceuticals: An update. Pharm Res 2010;27:544-75.  Back to cited text no. 32
33.Manning MC, Patel K, Borchardt RT. Stability of protein pharmaceuticals. Pharm Res 1989;6:903-18.  Back to cited text no. 33
34.Sharma S, Kulkarni J, Pawar AP. Permeation enhancers in the transmucosal delivery of macromolecules. Pharmazie 2006;61:495-504.  Back to cited text no. 34
35.Soares AF, Carvalho Rde A, Veiga F. Oral administration of peptides and proteins: Nanoparticles and cyclodextrins as biocompatible delivery systems. Nanomedicine (Lond) 2007;2:183-202.  Back to cited text no. 35
36.Abdel-Aal AB, Batzloff MR, Fujita Y, Barozzi N, Faria A, Simerska P, et al. Structure-activity relationship of a series of synthetic lipopeptide self-adjuvanting group A streptococcal vaccine candidates. J Med Chem 2008;51:167-72.  Back to cited text no. 36
37.Horváth A, Olive C, Karpati L, Sun HK, Good MF, Toth I. Toward the development of a synthetic group a streptococcal vaccine of high purity and broad protective coverage. J Med Chem 2004;47:4100-4.  Back to cited text no. 37
38.Cowan DP, Hinds LA. Fertility control for wildlife preface. Wildlife Res 2008;35:iii-iv.  Back to cited text no. 38
39.Holland MK, Beagley K, Hardy C, Hinds L, Jones RC. Immunocontraceptive vaccines for the control of wild animal populations: Antigen selection and delivery. In: Gagnon C, editor. Male Gamete: From Basic Science to Clinical Applications. 1st ed. St Louis: Cache River Press; 1999. pp. 493-500.  Back to cited text no. 39
40.McLaughlin EA, Aitken RJ. Is there a role for immunocontraception? Mol Cell Endocrinol 2011;335:78-88.  Back to cited text no. 40
41.McLeod SR, Saunders G, Twigg LE, Arthur AD, Ramsey D, Hinds LA. Prospects for the future: Is there a role for virally vectored immunocontraception in vertebrate pest management? Wildlife Res 2007;34:555-66.  Back to cited text no. 41
42.Hardy CM, ten Have JF, Mobbs KJ, Hinds LA. Assessment of the immunocontraceptive effect of a zona pellucida 3 peptide antigen in wild mice. Reprod Fertil Dev 2002;14:151-5.  Back to cited text no. 42
43.Fromme B, Eftekhari P, van Regenmortel M, Hoebeke J, Katz A, Millar R. A novel retro-inverso gonadotropin-releasing hormone (GnRH) immunogen elicits antibodies that neutralize the activity of native GnRH. Endocrinology 2003;144:3262-9.  Back to cited text no. 43
44.Dalin AM, Andresen O, Malmgren L. Immunization against GnRH in mature mares: Antibody titres, ovarian function, hormonal levels and oestrous behaviour. J Vet Med A 2002;49:125-31.  Back to cited text no. 44
45.Janett F, Caspari K, Thun R. Influence of immunization against GnRH on semen quality and testicular function in the adult boar. Reprod Domest Anim 2010;45:90.  Back to cited text no. 45
46.Burger D, Janett F, Vidament M, Stump R, Fortier G, Imboden I, et al. Immunization against GnRH in adult stallions: Effects on semen characteristics, behaviour and shedding of equine arteritis virus. Anim Reprod Sci 2006;94:107-11.  Back to cited text no. 46
47.Jaros P, Bürgi E, Stärk KD, Claus R, Hennessy D, Thun R. Effect of active immunization against GnRH on androstenone concentration, growth performance and carcass quality in intact male pigs. Livest Prod Sci 2005;92:31-8.  Back to cited text no. 47
48.Cook RB, Popp JD, McAllister TA, Kastelic JP, Harland R. Effects of immunization against GnRH, melengestrol acetate, and a trenbolene acetate/estradiol implant on growth and carcass characteristics of beef heifers. Theriogenology 2001;55:973-81.  Back to cited text no. 48
49.Thompson DL. Immunization against GnRH in male species (comparative aspects). Anim Reprod Sci 2000;60:459-69.  Back to cited text no. 49
50.Turzillo AM, Nett TM. Effects of bovine follicular fluid and passive immunization against gonadotropin-releasing hormone (GnRH) on messenger ribonucleic acid for GnRH receptor and gonadotropin subunits in ovariectomized ewes. Biol Reprod 1997;56:1537-43.  Back to cited text no. 50
51.Becker SE, Enright WJ, Katz LS. Active Immunization against a Gnrh-ovalbumin conjugate in female white-tailed deer. Zoo Biol 1999;18:385-96.  Back to cited text no. 51
52.Finnerty M, Enright WJ, Prendiville DJ, Roche JF. Immunization of bulls against gonadotropin-releasing-hormone (Gnrh) - growth, testes size, behavior and blood testosterone concentrations. Irish J Agr Res 1991;30:80-1.  Back to cited text no. 52
53.Li H, Piao YS, Zhang ZB, Hardy CM, Hinds LA. Molecular cloning and assessment of the immunocontraceptive potential of the zona pellucida subunit 3 from Brandt's vole (Microtus brandti). Reprod Fertil Dev 2006;18:331-8.  Back to cited text no. 53
54.Mruk DD, Wong CH, Silvestrini B, Cheng CY. A male contraceptive targeting germ cell adhesion. Nat Med 2006;12:1323-8.  Back to cited text no. 54
55.Fayrer-Hosken R. Controlling animal populations using anti-fertility vaccines. Reprod Domest Anim 2008;43:179-85.  Back to cited text no. 55
56.Desmettre P. Veterinary vaccines in the development of vaccination and vaccinology. In: Plotkin SA, editor. History of Vaccine Development. 1 st ed. New York: Springer; 2011. p. 57-65.  Back to cited text no. 56
57.Ramon G, Zoeller C. The 'associated vaccines' by unions of a toxoid and a microbial vaccine (TAB) or by toxoid mixtures. C R Seances Soc Biol Fil 1926;94:106-9.  Back to cited text no. 57
58.Glenny AT, Pope CG, Waddington H, Wallace U. Immunological notes XVII.-XXIV. J Pathol Bacteriol 1926;29:31-40.  Back to cited text no. 58
59.Freund J, Casals J, Hosmer EP. Sensitization and antibody formation after injection of tubercle bacilli and paraffin oil. Exp Biol Med 1937;37:509-13.  Back to cited text no. 59
60.Opie EL, Freund J. An experimental study of protective inoculation with heat killed tubercle bacilli. J Exp Med 1937;66:761-88.  Back to cited text no. 60
61.Claassen E, de Leeuw W, de Greeve P, Hendriksen C, Boersma W. Freund's complete adjuvant: An effective but disagreeable formula. Res Immunol 1992;143:478-83; discussion 572.  Back to cited text no. 61
62.Lambrecht BN, Kool M, Willart MA, Hammad H. Mechanism of action of clinically approved adjuvants. Curr Opin Immunol 2009;21:23-9.  Back to cited text no. 62
63.Wu HY, Russell MW. Comparison of systemic and mucosal priming for mucosal immune responses to a bacterial protein antigen given with or coupled to cholera toxin (CT) B subunit, and effects of pre-existing anti-CT immunity. Vaccine 1994;12:215-22.  Back to cited text no. 63
64.Couch RB. Nasal vaccination, Escherichia coli enterotoxin, and Bell's palsy. N Engl J Med 2004;350:860-1.  Back to cited text no. 64
65.Duewell P, Kisser U, Heckelsmiller K, Hoves S, Stoitzner P, Koernig S, et al. ISCOMATRIX adjuvant combines immune activation with antigen delivery to dendritic cells in vivo leading to effective cross-priming of CD8+ T cells. J Immunol 2011;187:55-63.  Back to cited text no. 65
66.Sun HX, Xie Y, Ye YP. ISCOMs and ISCOMATRIX. Vaccine 2009;27:4388-401.  Back to cited text no. 66
67.Kanzler H, Barrat FJ, Hessel EM, Coffman RL. Therapeutic targeting of innate immunity with toll-like receptor agonists and antagonists. Nat Med 2007;13:552-9.  Back to cited text no. 67
68.Romero CD, Varma TK, Hobbs JB, Reyes A, Driver B, Sherwood ER. The toll-like receptor 4 agonist monophosphoryl lipid a augments innate host resistance to systemic bacterial infection. Infect Immun 2011;79:3576-87.  Back to cited text no. 68
69.Casella CR, Mitchell TC. Putting endotoxin to work for us: Monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell Mol Life Sci 2008;65:3231-40.  Back to cited text no. 69
70.Rajagopal D, Paturel C, Morel Y, Uematsu S, Akira S, Diebold SS. Plasmacytoid dendritic cell-derived type I interferon is crucial for the adjuvant activity of toll-like receptor 7 agonists. Blood 2010;115:1949-57.  Back to cited text no. 70
71.Gupta K, Cooper C. A review of the role of CpG oligodeoxynucleotides as toll-like receptor 9 agonists in prophylactic and therapeutic vaccine development in infectious diseases. Drugs R D 2008;9:137-45.  Back to cited text no. 71
72.Nash AD, Lofthouse SA, Barcham GJ, Jacobs HJ, Ashman K, Meeusen EN, et al. Recombinant cytokines as immunological adjuvants. Immunol Cell Biol 1993;71:367-79.  Back to cited text no. 72
73.Heath AW, Playfair JH. Cytokines as immunological adjuvants. Vaccine 1992;10:427-34.  Back to cited text no. 73
74.Hoskinson RM, Rigby RD, Mattner PE, Huynh VL, D'Occhio M, Neish A et al. Vaxstrate: An anti-reproductive vaccine for cattle. Aust J Biotechnol 1990;4:166-70.  Back to cited text no. 74
75.Shah NM, Mangat GK, Balakrishnan C, Buch VI, Joshi VR. Accidental self-injection with Freund's complete adjuvant. J Assoc Physicians India 2001;49:366-8.  Back to cited text no. 75
76.Gnjatic S, Sawhney NB, Bhardwaj N. Toll-like receptor agonists are they good adjuvants? Cancer J 2010;16:382-91.  Back to cited text no. 76
77.Fàbrega E, Velarde A, Cros J, Gispert M, Suárez P, Tibau J, et al. Effect of vaccination against gonadotrophin-releasing hormone, using Improvac (R), on growth performance, body composition, behaviour and acute phase proteins. Livest Sci 2010;132:53-9.  Back to cited text no. 77
78.Sharma S, Mukkur TK, Benson HA, Chen Y. Pharmaceutical aspects of intranasal delivery of vaccines using particulate systems. J Pharm Sci 2009;98:812-43.  Back to cited text no. 78
79.Bachmann MF, Rohrer UH, Kündig TM, Bürki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 1993;262:1448-51.  Back to cited text no. 79
80.Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 1996;14:275-300.  Back to cited text no. 80
81.Sharma S, Mukkur TK, Benson HA, Chen Y. Enhanced immune response against pertussis toxoid by IgA-loaded chitosan-dextran sulfate nanoparticles. J Pharm Sci 2012;101:233-44.  Back to cited text no. 81
82.Bungener L, Huckriede A, de Mare A, de Vries-Idema J, Wilschut J, Daemen T. Virosome-mediated delivery of protein antigens in vivo: Efficient induction of class I MHC-restricted cytotoxic T lymphocyte activity. Vaccine 2005;23:1232-41.  Back to cited text no. 82
83.Lambkin R, Oxford JS, Bossuyt S, Mann A, Metcalfe IC, Herzog C, et al. Strong local and systemic protective immunity induced in the ferret model by an intranasal virosome-formulated influenza subunit vaccine. Vaccine 2004;22:4390-6.  Back to cited text no. 83
84.Kapczynski DR. Development of a virosome vaccine against avian metapneumovirus subtype C for protection in turkeys. Avian Dis 2004;48:332-43.  Back to cited text no. 84
85.Gonzalez RO, Higa LH, Cutrullis RA, Bilen M, Morelli I, Roncaglia DI, et al. Archaeosomes made of halorubrum tebenquichense total polar lipids: A new source of adjuvancy. BMC Biotechnol 2009;9:71.  Back to cited text no. 85
86.Krishnan L, Dennis Sprott G. Archaeosomes as self-adjuvanting delivery systems for cancer vaccines. J Drug Target 2003;11:515-24.  Back to cited text no. 86
87.Publicover J, Ramsburg E, Rose JK. Characterization of nonpathogenic, live, viral vaccine vectors inducing potent cellular immune responses. J Virol 2004;78:9317-24.  Back to cited text no. 87
88.Medina E, Guzman CA. Use of live bacterial vaccine vectors for antigen delivery: Potential and limitations. Vaccine 2001;19:1573-80.  Back to cited text no. 88
89.Mekalanos JJ. Live attenuated vaccine vectors. Int J Technol Assess Health Care 1994;10:131-42.  Back to cited text no. 89
90.Minke JM, Audonnet JC, Fischer L. Equine viral vaccines: The past, present and future. Vet Res 2004;35:425-43.  Back to cited text no. 90
91.Redwood AJ, Harvey NL, Lloyd M, Lawson MA, Hardy CM, Shellam GR. Viral vectored immunocontraception: Screening of multiple fertility antigens using murine cytomegalovirus as a vaccine vector. Vaccine 2007;25:698-708.  Back to cited text no. 91
92.Tyndale-Biscoe CH. Virus-vectored immunocontraception of feral mammals. Reprod Fertil Dev 1994;6:281-7.  Back to cited text no. 92
93.van Leeuwen BH, Kerr PJ. Prospects for fertility control in the European rabbit (Oryctolagus cuniculus) using myxoma virus-vectored immunocontraception. Wildlife Res 2007;34:511-22.  Back to cited text no. 93
94.Strive T, Hardy CM, Reubel GH. Prospects for immunocontraception in the European red fox (Vulpes vulpes). Wildlife Res 2007;34:523-9.  Back to cited text no. 94
95.Tyndale-Biscoe H, Hinds LA. Introduction - virally vectored immunocontraception in Australia. Wildlife Res 2007;34:507-10.  Back to cited text no. 95
96.Jalava K, Hensel A, Szostak M, Resch S, Lubitz W. Bacterial ghosts as vaccine candidates for veterinary applications. J Control Release 2002;85:17-25.  Back to cited text no. 96
97.Mayr UB, Walcher P, Azimpour C, Riedmann E, Haller C, Lubitz W. Bacterial ghosts as antigen delivery vehicles. Adv Drug Deliv Rev 2005;57:1381-91.  Back to cited text no. 97
98.Katinger A, Lubitz W, Szostak MP, Stadler M, Klein R, Indra A, et al. Pigs aerogenously immunized with genetically inactivated (ghosts) or irradiated Actinobacillus pleuropneumoniae are protected against a homologous aerosol challenge despite differing in pulmonary cellular and antibody responses. J Biotechnol 1999;73:251-60.  Back to cited text no. 98
99.Marchart J, Rehagen M, Dropmann G, Szostak MP, Alldinger S, Lechleitner S, et al. Protective immunity against pasteurellosis in cattle, induced by Pasteurella haemolytica ghosts. Vaccine 2003;21:1415-22.  Back to cited text no. 99
100.Walcher P, Cui X, Arrow JA, Scobie S, Molinia FC, Cowan PE, et al. Bacterial ghosts as a delivery system for zona pellucida-2 fertility control vaccines for brushtail possums (Trichosurus vulpecula). Vaccine 2008;26:6832-8.  Back to cited text no. 100
101.Di Martino B, Marsilio F, Roy P. Assembly of feline calicivirus-like particle and its immunogenicity. Vet Microbiol 2007;120:173-8.  Back to cited text no. 101
102.Stewart M, Bhatia Y, Athmaran TN, Noad R, Gastaldi C, Dubois E, et al. Validation of a novel approach for the rapid production of immunogenic virus-like particles for bluetongue virus. Vaccine 2010;28:3047-54.  Back to cited text no. 102
103.Thiéry R, Cozien J, Cabon J, Lamour F, Baud M, Schneemann A. Induction of a protective immune response against viral nervous necrosis in the European sea bass dicentrarchus labrax by using betanodavirus virus-like particles. J Virol 2006;80:10201-7.  Back to cited text no. 103
104.Raja KS, Wang Q, Gonzalez MJ, Manchester M, Johnson JE, Finn MG. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules 2003;4:472-6.  Back to cited text no. 104
105.Jegerlehner A, Tissot A, Lechner F, Sebbel P, Erdmann I, Kündig T, et al. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 2002;20:3104-12.  Back to cited text no. 105
106.Kapczynski DR, Tumpey TM. Development of a virosome vaccine for newcastle disease virus. Avian Dis 2003;47:578-87.  Back to cited text no. 106
107.Bagai S, Sarkar DP. Targeted delivery of hygromycin B using reconstituted sendai viral envelopes lacking hemagglutinin-neuraminidase. FEBS Lett 1993;326:183-8.  Back to cited text no. 107
108.Singh R, Verma PC, Singh S. Immunogenicity and protective efficacy of virosome based vaccines against newcastle disease. Trop Anim Health Prod 2010;42:465-71.  Back to cited text no. 108
109.Bandyopadhyay A, Fine RL, Demento S, Bockenstedt LK, Fahmy TM. The impact of nanoparticle ligand density on dendritic-cell targeted vaccines. Biomaterials 2011;32:3094-105.  Back to cited text no. 109
110.Grossmann C, Tenbusch M, Nchinda G, Temchura V, Nabi G, Stone GW et al. Enhancement of the priming efficacy of DNA vaccines encoding dendritic cell-targeted antigens by synergistic toll-like receptor ligands. BMC Immunol 2009;10:43.  Back to cited text no. 110
111.Steinman RM. Dendritic cells in vivo: A key target for a new vaccine science. Immunity 2008;29:319-24.  Back to cited text no. 111
112.Watkins C, Hopkins J, Harkiss G. Reporter gene expression in dendritic cells after gene gun administration of plasmid DNA. Vaccine 2005;23:4247-56.  Back to cited text no. 112
113.Torres CA, Iwasaki A, Barber BH, Robinson HL. Differential dependence on target site tissue for gene gun and intramuscular DNA immunizations. J Immunol 1997;158:4529-32.  Back to cited text no. 113
114.Olsen SC, Christie RJ, Grainger DW, Stoffregen WS. Immunologic responses of bison to vaccination with Brucella abortus strain RB51: Comparison of parenteral to ballistic delivery via compressed pellets or photopolymerized hydrogels. Vaccine 2006;24:1346-53.  Back to cited text no. 114
115.Oliveira SC, Harms JS, Rosinha GM, Rodarte RS, Rech EL, Splitter GA. Biolistic-mediated gene transfer using the bovine herpesvirus-1 glycoprotein D is an effective delivery system to induce neutralizing antibodies in its natural host. J Immunol Methods 2000;245:109-18.  Back to cited text no. 115
116.Christie RJ, Findley DJ, Dunfee M, Hansen RD, Olsen SC, Grainger DW. Photopolymerized hydrogel carriers for live vaccine ballistic delivery. Vaccine 2006;24:1462-9.  Back to cited text no. 116
117.Grosenbaugh DA, Leard T, Pardo MC, Motes-Kreimeyer L, Royston M. Comparison of the safety and efficacy of a recombinant feline leukemia virus (FeLV) vaccine delivered transdermally and an inactivated FeLV vaccine delivered subcutaneously. Vet Ther 2004;5:258-62.  Back to cited text no. 117
118.Grosenbaugh DA, Leard T, Pardo MC. Protection from challenge following administration of a canarypox virus-vectored recombinant feline leukemia virus vaccine in cats previously vaccinated with a killed virus vaccine. J Am Vet Med Assoc 2006;228:726-7.  Back to cited text no. 118
119.Grimm R. The history of the eradication of rabies in most European countries. Hist Med Vet 2002;27:295-301.  Back to cited text no. 119
120.Brochier B, Pastoret PP. Rabies eradication in Belgium by fox vaccination using vaccinia-rabies recombinant virus. Onderstepoort J Vet Res 1993;60:469-75.  Back to cited text no. 120
121.Flamand A, Coulon P, Lafay F, Kappeler A, Artois M, Aubert M, et al. Eradication of rabies in Europe. Nature 1992;360:115-6.  Back to cited text no. 121
122.Seegers JF. Lactobacilli as live vaccine delivery vectors: Progress and prospects. Trends Biotechnol 2002;20:508-15.  Back to cited text no. 122
123.Azizi A, Kumar A, Diaz-Mitoma F, Mestecky J. Enhancing oral vaccine potency by targeting intestinal M cells. PLoS Pathog 2010;6:e1001147.  Back to cited text no. 123
124.Ballesteros C, de la Lastra JM, de la Fuente J. Recent developments in oral bait vaccines for wildlife. Recent Pat Drug Deliv Formul 2007;1:230-5.  Back to cited text no. 124
125.Nochi T, Takagi H, Yuki Y, Yang L, Masumura T, Mejima M, et al. Rice-based mucosal vaccine as a global strategy for cold-chain- and needle-free vaccination. Proc Natl Acad Sci U S A 2007;104:10986-91.  Back to cited text no. 125
126.Salyaev RK, Rekoslavskaya NI, Shchelkunov SN, Stolbikov AS, Hammond RV. Study of the mucosal immune response duration in mice after administration of a candidate edible vaccine based on transgenic tomato plants carrying the TBI-HBS gene. Dokl Biochem Biophys 2009;428:232-4.  Back to cited text no. 126
127.Loza-Rubio E, Rojas E, Gómez L, Olivera MT, Gómez-Lim MA. Development of an edible rabies vaccine in maize using the Vnukovo strain. Dev Biol (Basel) 2008;131:477-82.  Back to cited text no. 127
128.Yuki Y, Tokuhara D, Nochi T, Yasuda H, Mejima M, Kurokawa S, et al. Oral MucoRice expressing double-mutant cholera toxin A and B subunits induces toxin-specific neutralising immunity. Vaccine 2009;27:5982-8.  Back to cited text no. 128
129.Hernández M, Cabrera-Ponce JL, Fragoso G, López-Casillas F, Guevara-García A, Rosas G, et al. A new highly effective anticysticercosis vaccine expressed in transgenic papaya. Vaccine 2007;25:4252-60.  Back to cited text no. 129
130.Dorokhov YL, Sheveleva AA, Frolova OY, Komarova TV, Zvereva AS, Ivanov PA, et al. Superexpression of tuberculosis antigens in plant leaves. Tuberculosis (Edinb) 2007;87:218-24.  Back to cited text no. 130
131.Zhang X, Buehner NA, Hutson AM, Estes MK, Mason HS. Tomato is a highly effective vehicle for expression and oral immunization with norwalk virus capsid protein. Plant Biotechnol J 2006;4:419-32.  Back to cited text no. 131
132.Streatfield SJ. Oral hepatitis B vaccine candidates produced and delivered in plant material. Immunol Cell Biol 2005;83:257-62.  Back to cited text no. 132
133.Lamphear BJ, Jilka JM, Kesl L, Welter M, Howard JA, Streatfield SJ. A corn-based delivery system for animal vaccines: An oral transmissible gastroenteritis virus vaccine boosts lactogenic immunity in swine. Vaccine 2004;22:2420-4.  Back to cited text no. 133
134.Tregoning J, Maliga P, Dougan G, Nixon PJ. New advances in the production of edible plant vaccines: Chloroplast expression of a tetanus vaccine antigen, TetC. Phytochemistry 2004;65:989-94.  Back to cited text no. 134


  [Figure 1]

  [Table 1], [Table 2], [Table 3]

This article has been cited by
1 The control of poultry salmonellosis using organic agents: an updated overview
Mohamed T. El-Saadony, Heba M. Salem, Amira M. El-Tahan, Taia A. Abd El-Mageed, Soliman M. Soliman, Asmaa F. Khafaga, Ayman A. Swelum, Ahmed E. Ahmed, Fahdah A. Alshammari, Mohamed E. Abd El-Hack
Poultry Science. 2022; : 101716
[Pubmed] | [DOI]
2 Estimating Abundance and Simulating Fertility Control in a Feral Burro Population
Jay V. Gedir, James W. Cain, Bruce C. Lubow, Talesha Karish, David K. Delaney, Gary W. Roemer
The Journal of Wildlife Management. 2021; 85(6): 1187
[Pubmed] | [DOI]
3 The status of fertility control for rodents—recent achievements and future directions
Integrative Zoology. 2021;
[Pubmed] | [DOI]
4 Fertility control for managing macropods – Current approaches and future prospects
Claire Wimpenny, Lyn A. Hinds, Catherine A. Herbert, Michelle Wilson, Graeme Coulson
Ecological Management & Restoration. 2021; 22(S1): 147
[Pubmed] | [DOI]
5 Nanotechnology and Animal Health
Sevda Senel
Pharmaceutical Nanotechnology. 2021; 9(1): 26
[Pubmed] | [DOI]
6 Harnessing immunological targets for COVID-19 immunotherapy
Abhishesh Kumar Mehata, Matte Kasi Viswanadh, Vishnu Priya, Vikas, Madaswamy S Muthu
Future Virology. 2021; 16(9): 619
[Pubmed] | [DOI]
7 Analysis of immune responses to attenuated alcelaphine herpesvirus 1 formulated with and without adjuvant
George C. Russell, David M. Haig, Mark P. Dagleish, Helen Todd, Ann Percival, Dawn M. Grant, Jackie Thomson, Anna E. Karagianni, Julio Benavides
Vaccine: X. 2021; 8: 100090
[Pubmed] | [DOI]
8 Effects of a Recombinant Gonadotropin-Releasing Hormone Vaccine on Reproductive Function in Adult Male ICR Mice
Ai-Mei Chang, Chen-Chih Chen, Ding-Liang Hou, Guan-Ming Ke, Jai-Wei Lee
Vaccines. 2021; 9(8): 808
[Pubmed] | [DOI]
9 Driving Adoption and Commercialization of Subunit Vaccines for Bovine Tuberculosis and Johne’s Disease: Policy Choices and Implications for Food Security
Albert I. Ugochukwu, Peter W. B. Phillips, Brian J. Ochieng’
Vaccines. 2020; 8(4): 667
[Pubmed] | [DOI]
10 Patchless administration of canine influenza vaccine on dog’s ear using insertion-responsive microneedles (IRMN) without removal of hair and its in vivo efficacy evaluation
In-Jeong Choi, Woonsung Na, Aram Kang, Myun-Hwan Ahn, Minjoo Yeom, Hyung-Ouk Kim, Jong-Woo Lim, Seong-O Choi, Seung-Ki Baek, Daesub Song, Jung-Hwan Park
European Journal of Pharmaceutics and Biopharmaceutics. 2020; 153: 150
[Pubmed] | [DOI]
11 Delivery of an inactivated avian influenza virus vaccine adjuvanted with poly(D,L-lactic-co-glycolic acid) encapsulated CpG ODN induces protective immune responses in chickens
Shirene M. Singh,Tamiru N. Alkie,Éva Nagy,Raveendra R. Kulkarni,Douglas C. Hodgins,Shayan Sharif
Vaccine. 2016;
[Pubmed] | [DOI]
12 Fertility control to mitigate human–wildlife conflicts: a review
Giovanna Massei,Dave Cowan
Wildlife Research. 2014; 41(1): 1
[Pubmed] | [DOI]
13 Protective efficacy of PLGA microspheres loaded with divalent DNA vaccine encoding the ompA gene of Aeromonas veronii and the hly gene of Aeromonas hydrophila in mice
Shanshan Gao,Na Zhao,Said Amer,Mingming Qian,Mengxi Lv,Yuliang Zhao,Xin Su,Jieying Cao,Hongxuan He,Baohua Zhao
Vaccine. 2013; 31(48): 5754
[Pubmed] | [DOI]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  In this article
    Article Figures
    Article Tables

 Article Access Statistics
    PDF Downloaded265    
    Comments [Add]    
    Cited by others 13    

Recommend this journal