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Frontiers in Veterinary Science 01 frontiersin.org GnRH-immunocastration: an alternative method for male animal surgical castration Chun Wang 1 , Cuiting Yang 1 , Yutian Zeng 1 and Ming Zhang 1 , 2 , 3 * 1 College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, China, 2 Key Laboratory of Livestock and Poultry Multi-Omics, Ministry of Agriculture and Rural A airs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, China, 3 Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, China Castration of male animals is intended to produce high-enhance quality of animal meat, prevent unpleasant taste, reduce aggressive behavior, and manage overbreeding. Over the years, Tranditional methods of mechanical and surgical castration have been employed over the years, but they fall short of meeting animal welfare requirements due to the associated risk of infection, pain, and stress. Immunocastration, specifically Gonadotropin-releasing hormone (GnRH)- immunocastration, targeting the hypothalamic pituitary-testis (HPT) axis, has emerged as an animal-friendly alternative to surgical castration, e ectively addressing these issues. This review seeks to systematically summarize the principles, development, current applications and challenges of GnRH- immunocastration, o ering insights into its role in promoting animal welfare. KEYWORDS immunocastration, surgical castration, male animal, animal welfare, GnRH 1. Introduction Capon production, an ancient practice dating back over 3,000 years, persists globally ( 1 3 ). While capon production constitutes a modest segment of the market, it holds signi cant

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tice dating back over 3,000 years, persists globally ( 1 3 ). While capon production constitutes a modest segment of the market, it holds signi cant growth potential due to its dustinctive sensory attributes cherished by consumers ( 4 7 ). Capon are male chickens that undergo surgicalcastration before reaching sexual maturity, a practice also applied to other male livestock like boars and rams. e objectives are to reduce unpleasant odors, increase intramuscular fat deposition, improve carcass composition and meat quality. Castration leads to androgen de ciency, hindering male secondary characteristics, such as the comb and esh hair, reducing aggressive behaviors and eliminating ghting and snorting ( 8 ). e energy consumed by capon in territorial protection, ghting, and courtship behaviors is greatly reduced compared intact rooster, making their feed energy utilization more e cient for growth and fat deposition ( 9 ). Consequently, castration enhances fat deposits and intramuscular fat content, elevating meat sensory qualities such as tenderness, juiciness, and avor ( 7 , 9 11 ). However, surgical castration also has some limitations, including postoperative complications, increased susceptibility to infections, and animal welfare concerns. Additionally, the procedure needs to be performed at an appropriate age, and the high demands on surgical skills, and other cost- e ective resources ( 12 ). In contrast, GnRH-immunocastration minimizes animal stress, reduces infection risk and complications associated with surgery, and substantially greatly improves animal welfare. Furthermore, it poses no risk of drug residue, making it easy to apply in production. Consequently, GnRH-immunocastration has the potential to be a safe alternative to surgical castration.

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residue, making it easy to apply in production. Consequently, GnRH-immunocastration has the potential to be a safe alternative to surgical castration. OPEN ACCESS EDITED BY Izhar Hyder Qazi, Shaheed Benazir Bhutto University of Veterinary and Animal Sciences, Pakistan REVIEWED BY Waseem Ali Vistro, Yangzhou University, China *CORRESPONDENCE Ming Zhang zhangming@sicau.edu.cn RECEIVED 27 June 2023 ACCEPTED 10 October 2023 PUBLISHED 31 October 2023 CITATION Wang C, Yang C, Zeng Y and Zhang M (2023) GnRH-immunocastration: an alternative method for male animal surgical castration. Front. Vet. Sci. 10:1248879. doi: 10.3389/fvets.2023.1248879 COPYRIGHT © 2023 Wang, Yang, Zeng and Zhang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. TYPE Mini Review PUBLISHED 31 October 2023 DOI 10.3389/fvets.2023.1248879

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Wang et al. 10.3389/fvets.2023.1248879 Frontiers in Veterinary Science 02 frontiersin.org 2. The comparison of di erent castration techniques for male animals Currently, various techniques for castrating male animals exist, including chemical castration, Bloodless castration, surgical castration, and immunocastration ( Table 1 ). Unlike mammals, rooster s testicles are located in the abdominal cavity, hanging ventral in the anterior part of the kidney through the mesangium and with the posterior tibial vein and aorta on both sides, which makes avian castration is more challenging than that of mammals. In the poultry industry, traditional surgical castration is performed without anesthesia or analgesic control, resulting in roosters su ering and violating animal welfare principles ( 38 ). Although geldings are banned in the EU (European Union) due to concerns about animal welfare, they are still used in traditional agricultural systems, representing a derogatory toward age-old practices ( 39 ). Surgical castration also incurs mortality rates ranging from 5 to 20%, and sometime even up to 50% ( 39 ). 3. Principles of GnRH-immunocastration Immunocastration primarily targets reproductive hormones within the HPT axis ( Figure 1 ), disrupting reproductive hormone within the HPT axis through immunological means to reduce the concentration of target hormones and achieve castration ( 29 , 40 ). GnRH is located at the upper end of the HPT axis, plays a pivotal roleinitiating and controlling the physiological functions of the entire reproductive axis ( 41 ). erefore, GnRH-immunization is the most widely used in production compared other targeted hormone immunocastration involves Animals are inoculated with GnRH vaccine, which prompts the production of speci c anti-GnRH

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compared other targeted hormone immunocastration involves Animals are inoculated with GnRH vaccine, which prompts the production of speci c anti-GnRH antibodies in the body, anda lot of anti-GnRH antibodies bind with endogenous GnRH, continuously inactivating endogenous GnRH. Consequently, GnRH-immunization leads to a decrease in luteinizing hormone (LH) and follicle stimulating hormone (FSH) secretion. Eventually, this inhibition of animal gonadal functionresults in the achievement of castration ( 42 ). 4. GnRH-immunocastration is a safe castration method in line with animal welfare Physiological doses of GnRH can signi cantly increases LH levels and slight increase FSH levels in plasma, reaching the gonads via the pituitary portal circulation, is stimulated the synthesis and secretion of gonadal steroid hormones, promoting gonadal development, gamete production, and the occurrence and TABLE 1 Comparison of four castration techniques. Item Method Surgical castration Bloodless castration Chemical castration Immunocastration Principle Cutting, and removing the gonads Rubber ring, pliers or Burdizzo castration, blocking the scrotum or spermatic cord, preventing blood ow and causing necrosis Injection of chemical drugs(Lactic acid, phenol, benzyl alcohol, etc.), causing testicular parenchymal lesions, inhibiting testicular function Using exogenous reproductive hormone targets to produce antibodies in vivo , combined with endogenous hormones, lowering testosterone levels and suppressing testicular development and spermatogenesis Characteristics It demands someone skilled in castration techniques to operate Simple and economical to operate; suitable for young animals; irreversible permanent castration Low stress, no drug residue, inexpensive, less time consuming, easy to

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mical to operate; suitable for young animals; irreversible permanent castration Low stress, no drug residue, inexpensive, less time consuming, easy to perform Suitable for both young and late production; strengthen immunity according to demand Castrated animals Pigs, Chickens, Cattle, Sheep, Foals Cattle ， Sheep Dog, Cat Pigs, Chickens, Sheep, Cattle, Mice, Horses, Deer, Cat castration e ect Irreversible, e castration is clean and thorough Irreversible, e castration is clean and thorough Irreversible; Insu cient injection or inaccurate injection site can lead to castration failure Reversible, e castration e ect is mild, and a small number of animal individuals fail to respond e ectively to antigens, resulting in immune failure Anesthesia Yes No No No Reaction Increase animal stress, produce pain, postoperative infection and cause complications Strong pain, long duration, stress response No pain No pain Side e ect Prone to postoperative bleeding, causing infection and complications Improper operation leads to cessation of blood supply to the bottom of the scrotum and secondary tissue necrosis Inaccurate injection sites can lead to degeneration of other tissues Slight redness and in ammation at the injection site Animal welfare No No Yes Yes Cost Lower Lower High High Reference ( 7 , 13 20 ) ( 21 24 ) ( 25 , 26 ) ( 27 37 )

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Wang et al. 10.3389/fvets.2023.1248879 Frontiers in Veterinary Science 03 frontiersin.org maintenance of secondary sexual characteristics. GnRH immunocastration induces a lot of GnRH-antibodies that neutralize endogenous GnRH, and the production of the antibody is a sustained biological e ect. As a result, GnRH immunocastration consistently inhibit testicular or ovarian endocrine function, reducing hormone levels and reproductive activity, and associated odors, primarily skatole and androstenone ( 43 46 ). Immunization with GnRH leads to a substantial decrease in androstenedione and testosterone in male animals ( 29 , 32 , 34 , 47 , 48 ). Consequently, European countries are advocating for GnRH-immunocastration as a surgical castration alternative, improving animal welfare. Immunocastration alleviates animal stress, reduces the risk of infection and complications associated with surgical castration, reduces pain and enhances animal welfare. GnRH-immunocastration is considered relatively safe alternative to surgical castration. 5. Current application of GnRH-immunocastration vaccine Immunocastration is not limited to pork production but is also employed in other livestock animals as an alternative to surgical castration. Its key advantage lies in eliminating pain, wound infection risks, and potential losses associated with castration ( 49 ). Now, several commercial immunocastration products have been applied in animal production ( Table 2 ). However, in Europe, Improvac is the sole product approved for commercial use in pigs., yet its market share is only 2.8% of all male pigs, despite EU approval almost a decade ago. Belgium produces about 15% of the castration vaccine in Europe, while globally, Brazil and Australia hold a market share of more than 50% ( 55 , 56 ).

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Belgium produces about 15% of the castration vaccine in Europe, while globally, Brazil and Australia hold a market share of more than 50% ( 55 , 56 ). 6. Current challenges for GnRH-immunocastration in male animals Immunocastration, o en administered using the GnRH vaccine, has undergone extensive investigation in male mammals and birds ( Figure 2 ) ( 43 , 57 61 ). Outcomes vary based on the animal species, animal age, individual response, and immunization frequency ( 62 ). GnRH plays a crucial role in regulating gonadal development and function through the pituitary gland. GnRH-immunocastration signi cantly decreases reproductive performance of male animals by inhibiting the development testes. Studies have con rmed that immunizing male animals with GnRH can cause infertility, gonadal atrophy, and changes in meat quality by directly or indirectly acting of testosterone ( 63 ). 6.1. In male mammals In mammals, the majority of research on GnRH- immunocastration has focused on male animals, and spermatogenesis is inhibited a er GnRH immunization. For example, immunizing male animals such as boars, bulls, stallions, rams, bucks, and rats with GnRH vaccine leads to the suppression of testicular, epididymal, and vas deferens development. is results in reduced sperm concentration in the testicles with low viability, constriction of the seminiferous tubules, and inhibition of spermatogonia and spermatoblast production in the deep epithelium ( 29 , 59 , 60 , 64 68 ). At present, GnRH immunocastration is the most widely used in boars. Androstenone is a male hormone that is formed in the cells of the Leydig and has a urine-like odor ( 69 ). Skatole is a metabolite of the amino acid tryptophan with a fecal odor that is synthesized by FIGURE 1 E ect of immunocastration on

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-like odor ( 69 ). Skatole is a metabolite of the amino acid tryptophan with a fecal odor that is synthesized by FIGURE 1 E ect of immunocastration on the hypothalamic pituitary-testicular axis. The vaccines: 1 6, Immunocastration vaccine targeting Kisspeptin; 7 13, Immunocastration vaccine targeting GnRH; 14 15, Immunocastration vaccine targeting LH.

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Wang et al. 10.3389/fvets.2023.1248879 Frontiers in Veterinary Science 04 frontiersin.org microbial degradation in the colon ( 44 , 70 ). Immunocastration has been shown to e ectively prevent the accumulation of boar taint in adipose tissue by reducing steroid hormone synthesis in the testes ( 45 ). However, due to the short duration of the castration e ect, the control of boars taint requires multiple doses of GnRH vaccine, and the second vaccination is o en carried out 4 6 weeks before slaughter TABLE 2 Several commercial immunocastration products on the market. Vaccine Supplier Indication/Target species Formulation Doses Reference Improvac/Valora Ceva Santé Animale, Libourne, France Immunocastration and prevention boar taint/swine Active substance: Gonadotropin releasing factor (GnRF) analog- protein conjugate +Adjuvant: 300 mg Diethylaminoethyl (DEAE)-Dextran +2 mg Chlorocresol Two subcutaneous doses, at least 4 weeks apart. ( 50 ) Bopriva Zoetis, Parsippany, NJ, United States Immunocastration, fertility control/cattle 400 g GnRH protein conjugate Two doses at an interval of 3 weeks with 1 mL Bopriva ( 51 ) Equity Zoetis Inc., Parsipanny, New Jersey, United States Control of estrus in horses and deer 300 g Iscomatrix (dipalmitoylphosphatidyl choline + Saponin Quil A + Cholesterol) + 200 g GnRH DT Two doses, at least 4 weeks apart. ( 52 ) GonaCon USDA, Pacarello, ID, United States Fertility control/white-tailed deer, wild boar, horses, feral cattle, and bison, prairie and feral dogs, feral cat both sexes GnRH protein conjugate concentration:1,000 g/mL Concholepas concholepas haemocyanin +AdjuVac ™ (mineral oil-based) +166 g/mL Mycobacterium avium concentration Single dose ( 53 , 54 ) FIGURE 2 GnRH-immunocastration e ects across diverse animals.

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mineral oil-based) +166 g/mL Mycobacterium avium concentration Single dose ( 53 , 54 ) FIGURE 2 GnRH-immunocastration e ects across diverse animals. PUFA, polyunsaturated fatty acids; WHC, water holding capacity; BW, body weight; PH, Pondus Hydrogenii.

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Wang et al. 10.3389/fvets.2023.1248879 Frontiers in Veterinary Science 05 frontiersin.org in production, and even the third dose of vaccine is required for slaughter pigs with higher age and weight to control boars odor, which increases the cost. Meat quality is increasingly valued by consumers, so male livestock are castrated in production to improve meat quality. Currently, a large number of studies have focused on the improvement of meat quality through immunocastration. GnRH immunocastration reduces the accumulation of taint compounds in adipose tissue and improves meat quality and carcass characteristics in male mammals ( 71 ). However, the latest study found that the slaughter rate of immunocastrated boars is lower than that of surgical castrated boars and intact boars, as immunocastrated boars have heavier liver and kidneys ( 72 ). e abdomen of immune castrated pigs is fatter than that of entire boars, and the lean meat rate is similar to that of surgical castrated pigs, both of which are lower than that of entire boars. erefore, to some extent, it will a ect consumers choices. Bellies from immunocastrated pigs are fatter and rmer than those from boars. In addition, although immunocastration increases intramuscular fat content and reduces polyunsaturated fatty acids, the e ect of improving intramuscular fat is still not as e ective as surgical castration, and boars that undergo surgical castration have lower polyunsaturated fatty acids ( 73 ). Similarly, studies have shown that compared to surgical castration, GnRH immunocastration improves cattle weight, but there are no di erences in beef pH, color, fat coverage, cooking loss, or tenderness ( 74 ). 6.2. In male birds e utilization and assessment of immunocastration vaccines in pigs has been extensively

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verage, cooking loss, or tenderness ( 74 ). 6.2. In male birds e utilization and assessment of immunocastration vaccines in pigs has been extensively reported ( 34 , 48 , 75 ). However, there is currently no commercially available vaccine for chickens. Recently, only three studies have investigated the use of the GnRH vaccine for immunizing roosters. Quaresma and colleagues evaluated the e ects of Improvac on the body and bone development, meat color, and composition of roosters, and found that the color parameters of Improvac birds, such as brightness, red, and hue angle, were between roosters and capons ( 5 ). In addition, i.c. Antunes et al. found that immunocastration had little e ect on the fatty acid pro le of broilers, but improved overall lipid markers in breast and leg meat to some extent, which could partially enable GnRH immunization ( 6 ). Previous studies have shown that both caponization and ovariectomy likely improve the meat quality of the breast muscle based on the objective indices of IMF, appearance (color), texture, and minor change of the fatty acid pro le; ovariectomy improves avor-related indices ( 76 ). In our study, we found that roosters inoculated with Improvac had some e ect on muscle development, but the e ect was not completely satisfactory ( 77 , 78 ). 7. Conclusions and perspective Immunocastration currently faces challenges related to immunization failure. ese challenges include signi cant variations in individual responses among immunized animals, insensitivity to antigens in some individuals, failure to elicit an immune response, or a shorter duration of immune e ect. is shorter duration leads to an increase in testosterone concentration during the recovery period compared to the previous phase, resulting in a gradual return of

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uration leads to an increase in testosterone concentration during the recovery period compared to the previous phase, resulting in a gradual return of sexual behavior. Multiple vaccinations are necessary to counter this e ect, which in turn escalates costs. Moreover, there are associated disadvantages for farmers, including increased expenses for purchasing produce and labor management, the risk of accidental self- injection by farm workers, and uncertainty regarding consumer attitudes toward meat from pharmacologically castrated animals. However, it s important to note that immunocastration o ers several advantages, such as reducing animal stress, lowering the risk of infections and complications associated with surgical castration, signi cantly improving animal welfare, and being relatively straightforward to implement in production settings. erefore, immunocastration may remain a safe alternative to surgical castration in the future. In the future development of commercial castration vaccines, particularly GnRH immunocastration vaccines for male animals, there should be an exploration of the construction of immunogens, immune dosages, immune strategies, and timing. Attention should be directed toward enhancing the e ectiveness and prolonging the duration of immune response for these vaccines. Currently, research on GnRH vaccines primarily focuses on chemical synthesis of polypeptides, dual conjugate vaccines, DNA vaccines, tandem conjugate vaccines, among others. However, these approaches have their limitations. Considering the existing challenges with GnRH gene vaccines, it s worth considering research and development of GnRH gene engineering vaccines and GnRH recombinant adenovirus vaccines in the future. In summary, the future focus of immunocastration vaccine

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ent of GnRH gene engineering vaccines and GnRH recombinant adenovirus vaccines in the future. In summary, the future focus of immunocastration vaccine development will revolve around creating products with sustained immunogenicity, easy production, and stable e ects. ese advancements could hold the key to the future of immunocastration vaccines. Author contributions CW: dra ing the manuscript. YZ and CY: provision of study materials. MZ: conceptualization and supervision. All authors contributed to the article and approved the submitted version. Funding is research was supported by National Key Research and Development Projects of China (2021YFD1600200). Conflict of interest e authors declare that the research was conducted in the absence of any commercial or nancial relationships that could be construed as a potential con ict of interest. Publisher s note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their a liated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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