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RESEARCH ARTICLE

Field testing of single-administration porcine zona pellucida contraceptive vaccines in white-tailed deer (Odocoileus virginianus)

Allen T. Rutberg A F , Ricky E. Naugle B , John W. Turner Jr C , Mark A. Fraker D and Douglas R. Flanagan E
+ Author Affiliations
- Author Affiliations

A Center for Animals and Public Policy, Tufts-Cummings School of Veterinary Medicine, 200 Westboro Road, North Grafton, MA 01536, USA.

B Humane Society of the United States, 2100 L St NW, Washington, DC 20037, USA.

C Department of Physiology and Pharmacology, University of Toledo College of Medicine, 3035 Arlington Avenue, Toledo, OH 43614, USA.

D TerraMar Environmental Research Ltd, 8617 Lochside Drive, Sidney BC V8 L 1M8, Canada.

E Division of Pharmacy, University of Iowa, College of Pharmacy, 115 S. Grand Avenue, Iowa City, IA 52242, USA.

F Corresponding author. Email: allen.rutberg@tufts.edu

Wildlife Research 40(4) 281-288 https://doi.org/10.1071/WR12117
Submitted: 30 June 2012  Accepted: 20 May 2013   Published: 18 June 2013

Abstract

Context: Many contraceptive agents have demonstrated effectiveness in wild species, most notably immunocontraceptives such as GnRH conjugates and porcine zona pellucida (PZP). The major challenge in using these agents to control deer and other wildlife populations in the field now lies with safe, effective and efficient delivery to a large-enough proportion of the population to suppress growth.

Aims: Because deer and other wildlife are typically difficult to access for treatment, contraceptives that require multiple or repeated treatments will be of limited management value. To address this constraint, we conducted a field study of white-tailed deer (Odocoileus virginianus) on Fripp Island, SC, USA, to test two different technologies for achieving single-administration, multi-year efficacy in PZP vaccines.

Methods: Between 2005 and 2010, we captured, ear-tagged and blood-sampled a total of 245 individual adult and yearling female deer. Deer were hand-injected at capture with one of two preparations of SpayVac or a combination native PZP–adjuvant emulsion plus PZP–adjuvant incorporated into lactide–glycolide polymer pellets engineered to release at 1, 3 and 12 months post-treatment. Pregnancy was determined from serum assays of pregnancy-specific protein B sampled from captured deer.

Key results: Aqueous SpayVac, and the PZP–adjuvant-containing polymer pellets manufactured through a heat extrusion (H/X) method administered simultaneously with PZP–AdjuVac or modified Freund’s complete adjuvant emulsions reduced pregnancy rates from control levels by 95–100% in the first year after treatment, and by 65–70% in the second year after treatment.

Conclusions: A single, hand-injected vaccination with SpayVac or PZP–adjuvant emulsion combined with H/X PZP pellets reduced fertility for multiple years.

Implications: Single-treatment, multi-year immunocontraceptive vaccines bring contraceptive management of wildlife populations one step closer. Future efforts should focus on improving handling and storage, developing technologies for remote delivery, and addressing remaining regulatory and management concerns.

Additional keywords: immunocontraception, PZP, SpayVac.


References

Bissonette, J. A., Kassar, C. A., and Cook, L. J. (2008). Assessment of costs associated with deer-vehicle collisions: human death and injury, vehicle damage, and deer loss. Human-Wildlife Conflicts 2, 17–27.

Boulanger, J. R., Curtis, P. D., Cooch, E. G., and DeNicola, A. J. (2012). Sterilization as an alternative deer control technique: a review. Human–Wildlife Interactions 6, 273–282.

Brown, R. G., Bowen, W. D., Eddington, J. D., Kimmins, W. C., Mezei, M., Parsons, J. L., and Pohajdak, B. (1997). Evidence for a long-lasting single administration contraceptive vaccine in wild grey seals. Journal of Reproductive Immunology 35, 43–51.
Evidence for a long-lasting single administration contraceptive vaccine in wild grey seals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXms1eqs74%3D&md5=f936e6ea140a780171d4d8c17d71543dCAS | 9373857PubMed |

Conover, M. R., Pitt, W. C., Kessler, K. K., DuBow, T. J., and Sanborn, W. A. (1995). Review of human injuries, illnesses, and economic losses caused by wildlife in the United States. Wildlife Society Bulletin 23, 407–414.

Côté, S. D., Rooney, T. P., Tremblay, J.-P., Dussault, C., and Waller, D. M. (2004). Ecological impacts of deer overabundance. Annual Review of Ecology Evolution and Systematics 35, 113–147.
Ecological impacts of deer overabundance.Crossref | GoogleScholarGoogle Scholar |

Curtis, P. D., Pooler, R. L., Richmond, M. E., Miller, L. A., Mattfield, G. F., and Quimby, F. W. (2002). Comparative effects of GnRH and porcine zona pellucida (PZP) immunocontraceptive vaccines for controlling reproduction in white-tailed deer (Odocoileus virginianus). Reproduction (Cambridge, England) Supplement 60, 131–141.
| 1:CAS:528:DC%2BD38XnsFGksL4%3D&md5=a2d47c00f87af770ba31c3e743af7825CAS |

Curtis, P. D., Richmond, M. E., Miller, L. A., and Quimby, F. W. (2008). Physiological effects of gonadotropin-releasing hormone immunocontraception on white-tailed deer. Human-Wildlife Conflicts 2, 68–79.

Deigert, F. A., Duncan, A. E., Frank, K. M., Lyda, R. O., and Kirkpatrick, J. F. (2003). Immunocontraception of captive exotic species. III. Contraception and population management of fallow deer (Cervus dama). Zoo Biology 22, 261–268.
Immunocontraception of captive exotic species. III. Contraception and population management of fallow deer (Cervus dama).Crossref | GoogleScholarGoogle Scholar |

Dunbar, B. S., Wardrip, N. J., and Hedrick, J. L. (1980). Isolation, physicochemical properties, and macromolecular composition of zona pellucida from porcine oocytes. Biochemistry 19, 356–365.
Isolation, physicochemical properties, and macromolecular composition of zona pellucida from porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXntlagsA%3D%3D&md5=00305a598606bb9a0450098b74651a9eCAS | 7352990PubMed |

Fagerstone, K. A., Miller, L. A., Killian, G. J., and Yoder, C. A. (2010). Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human–wildlife conflicts in North America. Integrative Zoology 5, 15–30.
Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human–wildlife conflicts in North America.Crossref | GoogleScholarGoogle Scholar | 21392318PubMed |

Fraker, M. A., Brown, R. G., Gaunt, G. E., Kerr, J. A., and Pohajdak, B. (2002). Long-lasting, single-dose immunocontraception of feral fallow deer in British Columbia. The Journal of Wildlife Management 66, 1141–1147.
Long-lasting, single-dose immunocontraception of feral fallow deer in British Columbia.Crossref | GoogleScholarGoogle Scholar |

Gilman, R. T., Mathews, N. E., Skinner, B. G., Julis, V. L., Frank, E. S., and Paul-Murphy, J. (2010). Effects of maternal status on the movement and mortality of sterilized female white-tailed deer. The Journal of Wildlife Management 74, 1484–1491.

Gionfriddo, J. P., Eisemann, J. D., Sullivan, K. J., Healey, R. S., Miller, L. A., Fagerstone, K. A., Engeman, R. M., and Yoder, C. A. (2009). Field test of a single-injection gonadotrophin-releasing hormone immunocontraceptive vaccine in female white-tailed deer. Wildlife Research 36, 177–184.
Field test of a single-injection gonadotrophin-releasing hormone immunocontraceptive vaccine in female white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVOnsLk%3D&md5=3a4ed4fa64f82888a396145ad7d48388CAS |

Gionfriddo, J. P., Denicola, A. J., Miller, L. A., and Fagerstone, K. A. (2011a). Efficacy of GnRH immunocontraception of wild white-tailed deer in New Jersey. Wildlife Society Bulletin 35, 142–148.
Efficacy of GnRH immunocontraception of wild white-tailed deer in New Jersey.Crossref | GoogleScholarGoogle Scholar |

Gionfriddo, J. P., Denicola, A. J., Miller, L. A., and Fagerstone, K. A. (2011b). Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey. Wildlife Society Bulletin 35, 149–160.
Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey.Crossref | GoogleScholarGoogle Scholar |

Harder, J. D., and Peterle, T. J. (1974). Effects of diethylstilbestrol on reproductive performance in white tailed-deer. The Journal of Wildlife Management 38, 183–196.
Effects of diethylstilbestrol on reproductive performance in white tailed-deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXltlWitLk%3D&md5=616138643e911a033b68dad3f5e6c876CAS |

Kirkpatrick, J. F., Liu, I. K. M., and Turner, J. W. (1990). Remotely-delivered immunocontraception in feral horses. Wildlife Society Bulletin 18, 326–330.

Kirkpatrick, J. F., Turner, J. W., Liu, I. K. M., Fayrer-Hosken, R., and Rutberg, A. T. (1997). Case studies in wildlife immunocontraception: wild and feral equids and white-tailed deer. Reproduction, Fertility and Development 9, 105–110.
Case studies in wildlife immunocontraception: wild and feral equids and white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3mt12qsw%3D%3D&md5=162f30d0145c85fb2a6171762a71a644CAS |

Liu, I. K. M., Bernoco, M., and Feldman, M. (1989). Contraception in mares heteroimmunized with pig zonae pellucidae. Journal of Reproduction and Fertility 85, 19–29.
Contraception in mares heteroimmunized with pig zonae pellucidae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7isFCqtg%3D%3D&md5=4e34e6e4b992567199616051d208e72bCAS |

Locke, S. L., Cook, M. W., Harveson, L. A., Davis, D. S., Lopez, R. R., Silvy, N. J., and Fraker, M. A. (2007). Effectiveness of Spayvac® for reducing white-tailed deer fertility. Journal of Wildlife Diseases 43, 726–730.
| 17984269PubMed |

Lyda, R. O., Hall, J. R., and Kirkpatrick, J. F. (2005). A comparison of Freund’s complete and Freund’s modified adjuvants used with a contraceptive vaccine in wild horses (Equus caballus). Journal of Zoo and Wildlife Medicine 36, 610–616.
A comparison of Freund’s complete and Freund’s modified adjuvants used with a contraceptive vaccine in wild horses (Equus caballus).Crossref | GoogleScholarGoogle Scholar | 17312717PubMed |

MacLean, R. A., Mathews, N. E., Grove, D. M., Frank, E. S., and Paul-Murphy, J. (2006). Surgical technique for tubal ligation in white-tailed deer (Odocoileus virginianus). Journal of Zoo and Wildlife Medicine 37, 354–360.
Surgical technique for tubal ligation in white-tailed deer (Odocoileus virginianus).Crossref | GoogleScholarGoogle Scholar | 17319135PubMed |

Matschke, G. H. (1977a). Antifertility action of two synthetic progestins in female white-tailed deer. The Journal of Wildlife Management 41, 194–196.
Antifertility action of two synthetic progestins in female white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlsVKhsLw%3D&md5=041162666416f139efd861999d144ba3CAS |

Matschke, G. H. (1977b). Microencapsulated diethylstilbestrol as an oral contraceptive in white-tailed deer. The Journal of Wildlife Management 41, 87–91.
Microencapsulated diethylstilbestrol as an oral contraceptive in white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXktFKhtrw%3D&md5=fbd24936ec0c1f31673da1e5a7eada85CAS |

Matschke, G. H. (1980). Efficacy of steroid implants in preventing pregnancy in white-tailed deer. The Journal of Wildlife Management 44, 756–758.
Efficacy of steroid implants in preventing pregnancy in white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktFOgu7o%3D&md5=9e790a1b09ee30869e137bf7ff7f70cbCAS |

McShea, W. J., Monfort, S. L., Hakim, S., Kirkpatrick, J. F., Liu, I. K. M., Turner, J. W., Chassy, L. M., and Munson, L. (1997). The effect of immunocontraception on the behavior and reproduction of white-tailed deer. The Journal of Wildlife Management 61, 560–569.
The effect of immunocontraception on the behavior and reproduction of white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Merrill, J. A., Cooch, E. G., and Curtis, P. D. (2003). Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer. The Journal of Wildlife Management 67, 267–279.
Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Merrill, J. A., Cooch, E. G., and Curtis, P. D. (2006). Managing an overabundant deer population by sterilization: effects of immigration, stochasticity, and the capture process. The Journal of Wildlife Management 70, 268–277.
Managing an overabundant deer population by sterilization: effects of immigration, stochasticity, and the capture process.Crossref | GoogleScholarGoogle Scholar |

Miller, L. A., Johns, B. E., and Killian, G. J. (2000a). Immunocontraception of white-tailed deer with GnRH vaccine. American Journal of Reproductive Immunology 44, 266–274.
Immunocontraception of white-tailed deer with GnRH vaccine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7lt1Gnug%3D%3D&md5=96d210d9a8970e0f0224e5177cce4499CAS | 11125787PubMed |

Miller, L. A., Johns, B. E., and Killian, G. J. (2000b). Long-term effects of PZP immunization on reproduction in white-tailed deer. Vaccine 18, 568–574.
Long-term effects of PZP immunization on reproduction in white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Miller, L. A., Crane, K., Gaddis, S., and Killian, G. J. (2001). Porcine zona pellucida immunocontraception: long-term health effects on white-tailed deer. The Journal of Wildlife Management 65, 941–945.
Porcine zona pellucida immunocontraception: long-term health effects on white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Miller, L. A., Fagerstone, K. A., Wagner, D. C., and Killian, G. J. (2009). Factors contributing to the success of a single-shot multiyear PZP immunocontraceptive vaccine for white-tailed deer. Human-Wildlife Conflicts 3, 103–115.

Naugle, R. E., Rutberg, A. T., Underwood, H. B., Turner, J. W., and Liu, I. K. M. (2002). Field testing of immunocontraception on white-tailed deer (Odocoileus virginianus) on Fire Island National Seashore, New York, USA. Reproduction (Cambridge, England) Supplement 60, 143–153.
| 1:STN:280:DC%2BD38vmtFCjtg%3D%3D&md5=bf95316fe88ad91916fedc40f0a3b94fCAS |

Ostfeld, R. S. (2010). ‘Lyme Disease: the Ecology of a Complex System.’ (Oxford University Press: New York.)

Plotka, E. D., and Seal, U. S. (1989). Fertility control in female white-tailed deer. Journal of Wildlife Diseases 25, 643–646.
| 1:STN:280:DyaK3c%2FktFSktg%3D%3D&md5=f546ca414d5e6dfba325ea04417e58f0CAS | 2509740PubMed |

Roughton, R. D. (1979). Effects of oral melengestrol acetate on reproduction in captive white-tailed deer. The Journal of Wildlife Management 43, 428–436.
Effects of oral melengestrol acetate on reproduction in captive white-tailed deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktlegs7Y%3D&md5=aa6a7f67953620acb4f4adf7b07142d7CAS |

Rutberg, A. T. (2005). Deer contraception: what we know and what we don’t. In ‘Humane Wildlife Solutions: the Role of Immunocontraception’. (Ed. A. T. Rutberg.) pp. 23–42. (Humane Society Press: Washington, DC.)

Rutberg, A. T., and Naugle, R. E. (2008a). Deer-vehicle collisions at a suburban immunocontraception site. Human-Wildlife Conflicts 2, 60–67.

Rutberg, A. T., and Naugle, R. E. (2008b). Population-level effects of immunocontraception in white-tailed deer (Odocoileus virginianus). Wildlife Research 35, 494–501.
Population-level effects of immunocontraception in white-tailed deer (Odocoileus virginianus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLnM&md5=2993fcdc96c49d9beb0945a2407cba84CAS |

Rutberg, A. T., Naugle, R. E., Thiele, L. A., and Liu, I. K. M. (2004). Effects of immunocontraception on a suburban population of white-tailed deer Odocoileus virginianus. Biological Conservation 116, 243–250.
Effects of immunocontraception on a suburban population of white-tailed deer Odocoileus virginianus.Crossref | GoogleScholarGoogle Scholar |

Turner, J. W., and Kirkpatrick, J. F. (1991). New developments in feral horse contraception and their potential application to wildlife. Wildlife Society Bulletin 19, 350–359.
| 1:CAS:528:DyaK3MXlsVGru7s%3D&md5=80f3c8714bd0b5c98165dad9f1acba66CAS |

Turner, J. W., Liu, I. K. M., and Kirkpatrick, J. F. (1992). Remotely delivered immunocontraception in captive white-tailed deer. The Journal of Wildlife Management 56, 154–157.
Remotely delivered immunocontraception in captive white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Turner, J. W., Kirkpatrick, J. F., and Liu, I. K. M. (1996). Effectiveness, reversibility, and serum antibody titers associated with immunocontraception in white-tailed deer. The Journal of Wildlife Management 60, 45–51.
Effectiveness, reversibility, and serum antibody titers associated with immunocontraception in white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Turner, J. W., Liu, I. K. M., Flanagan, D. R., Rutberg, A. T., and Kirkpatrick, J. F. (2007). Immunocontraception in wild horses: one inoculation provides two years of infertility. The Journal of Wildlife Management 71, 662–667.
Immunocontraception in wild horses: one inoculation provides two years of infertility.Crossref | GoogleScholarGoogle Scholar |

Turner, J. W., Rutberg, A. T., Naugle, R. E., Kaur, M. A., Flanagan, D. R., Bertschinger, H. J., and Liu, I. K. M. (2008). Controlled-release components of PZP contraceptive vaccine extend duration of infertility. Wildlife Research 35, 555–562.
Controlled-release components of PZP contraceptive vaccine extend duration of infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLbL&md5=0d5025cd2486ba9bc25a5e0f23b7ea83CAS |

Walter, W. D., Pekins, P. J., Rutberg, A. T., and Kilpatrick, H. J. (2002). Evaluation of immunocontraceptive adjuvants, titers, and fecal pregnancy indicators in free-ranging white-tailed deer. Wildlife Society Bulletin 30, 908–914.

Walter, W. D., Kilpatrick, H. J., and Gregonis, M. A. (2003). Does immunocontraception improve condition of free-ranging white-tailed deer? The Journal of Wildlife Management 67, 762–766.
Does immunocontraception improve condition of free-ranging white-tailed deer?Crossref | GoogleScholarGoogle Scholar |