98 CONTACT Muhammad-Salman Waqas salman.waqas@wsu.edu © 2023 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http:// creativecommons.org/licenses/by-nc/4.0/), permitting all non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Citation line: Clinical Theriogenology 2023, 15, 9638, http://dx.doi.org/10.58292/CT.v15.9638 Review Report Laparoscopic-assisted cryptorchidectomy in South American camelids and Nigerian dwarf goats Dane Schwartz, Muhammad-Salman Waqas, Eduardo Arroyo, Agustin Ruiz and Ahmed Tibary Comparative Theriogenology Service, Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, WA, USA Abstract Cryptorchidism is a common sexual development disorder in males with a potential hereditary origin in goats and camelids. Cryptorchid animals should be removed from breeding and castrated to eliminate male behavior. The objective of this paper is to describe the presentation and procedure of laparoscopic-assisted cryptorchidectomy in goats and South American camelids. Records of 18 Nigerian dwarf goats and 16 camelid cases that were presented to the WSU Theriogenology Services were included. Goats ranged in age from 2 months to 1 year and camelids (14 alpacas and 2 llamas) were between 15 months and 5 years of age. In goats, 15/18 (83%) were unilateral cryptorchids while 3/18 (17%) were bilateral. The right testicle was retained abdominally in 73.3% (11/15) of the unilaterally cryptorchid goats. All the camelids presented as unilateral cryptorchids with abdominally retained testis. The left testis was retained in 9/16 (56.25%) cases while the right was retained in 7/17 (43.75%). Laparoscopic-assisted cryptor- chidectomy was performed under general anesthesia in all cases. The remaining scrotal testicle was castrated using a closed tech- nique. There were no surgical complications. Ability to confirm the presence of cryptorchid testis without laparotomy, smaller incision, lesser intraabdominal manipulation, and lesser-no post/surgical complications advocate the use of this technique for cryptorchidectomy. Keywords: Goats, alpacas, llamas, testis, surgery Introduction Cryptorchidism is one of the most common congenital disor- der of sexual development in males.1 In alpacas, an abattoir study on 792 animals reported a 3% incidence of unilateral cryptorchidism (58.3% left and 41.7% right).2 Bilateral crypt- orchism is rare in camelids and has been described in an Sry- negative XX, sex reversal case in a llama with multiple congenital abnormalities.3 Monorchism, absence of one testi- cle, has been reported in alpacas and is accompanied by agen- esis of the ipsilateral kidney.2 In goats, a 3% incidence of cryptorchidism has been reported in slaughtered goats in India.4 The incidence of cryptorchidism is higher in West African dwarf goats and ranges from 33 to 66% in some regions.5–7 Nigerian dwarf goats are a popular breed as com- panion animals in the USA and one of the most common breeds to visit hospital for cryptorchidism (A Tibary, clinical observation). Cryptorchid animals produce normal levels of testosterone and display normal male behavior and mating ability.8 In one case of bilateral cryptorchidism in a dromedary camel, rut- ting, mating, ejaculation, and induction of ovulation were like normal camels although the ejaculates from the affected camel were azoospermic (A Tibary, clinical observation). Unilaterally affected males can be fertile if the descended tes- ticle is not removed. Unilateral cryptorchid Nigerian dwarf goats are fertile but show an increased percentage of sperm abnormalities.6,7 Diagnosis of cryptorchidism is based on history and clinical examination of the scrotal and inguinal regions. However, in animals displaying male-like behavior with unclear history of castration and no testicles in the scrotun or inguinal region, ultrasonographic examination and endocrine evaluation are  necessary to detect the presence of testicular tissue. Ultrasonography of the suspected cryptorchid goat or camelid has not been described thoroughly in the literature but it does allow the clinician to determine the location, size, and mor- phology of the retained testes. Endocrine diagnosis has been used mainly in camelids and is based on the response to a human Chorionic Gonadotropin (hCG) stimulation test. mailto:salman.waqas@wsu.edu http://creativecommons.org/licenses/by-nc/4.0/ http://creativecommons.org/licenses/by-nc/4.0/ http://dx.doi.org/10.58292/CT.v15.9638 Citation line: Clinical Theriogenology 2023, 15, 9638, http://dx.doi.org/10.58292/CT.v15.9638 99 At  least a twofold increase in serum testosterone concentra- tion is observed 8 h following administration of hCG (3,000 to 5,000 IU, IV) to confirm presence of testicular tissue.9–11 Cryptorchidism is suspected to be hereditary in South American camelids2,12 and Nigerian dwarf goats.7 Three cases of cryptorchidism were described in closely related males from a herd of captive vicunas.13 A high incidence of cryptor- chidism (66%) has been reported in Nigerian dwarf bucks where cryptorchid animals are used for breeding.5 Therefore, cryptorchid animals should be eliminated from breeding due to hereditary concerns. Castration also has the benefit of elim- inating male behavior and the risk for induction of ovulation in camelids8 along with the undesirable buck smell found in intact companion goats. Several surgical techniques for removal of the retained testis via laparotomy have been described.14–16 In camelids and small size goats such as Nigerian dwarfs, these techniques can be challenging and are associated with increased post-surgical complications. The objectives of this paper are to describe an ultrasonographic approach to diagnosis of cryptorchidism and a minimally invasive laparoscopic-assisted approach for cryptorchidectomy in South American camelids and goats. Material and methods Records of South American camelids (14 alpacas and 2 lla- mas) and Nigerian dwarf goats (n = 18) that presented for cryptorchidectomy to the Comparative Theriogenology ser- vice at Washington State University Veterinary Teaching Hospital were included in this retrospective study. Camelids ranged in age from 15 months to 5 years of age and goats were between 2 months and 1 year of age. All goats were acquired by owners for the purpose of serving as companion animals. Two goats were purchased as wethers and the owners became concerned when the males began to display male-like behav- ior and buck odor at 6 months of age. A bilaterally cryptorchid goat also presented which was presumed to have been cas- trated by elastic banding by the breeder at 1 week of age. All animals were in good health upon presentation. After physical examination, males were examined by transcutane- ous ultrasonography (Sonoscape® with a 5 MHz frequency lin- ear or curvilinear transducer) to determine the location of the retained testis prior to surgery. The animals were examined while in dorsal recumbency. The transducer was placed over the external inguinal ring and the entire region from the ingui- nal ring to midline was imaged on each side. Endocrine diag- nosis (hCG stimulation test) was performed in only one alpaca that had a history of castration. Total protein concen- tration and hematocrit were determined in all patients prior to surgery. For laparoscopic-assisted cryptorchidectomy, camelids were fasted for 24 h, and water was withheld for 12 h prior to surgery. Total protein concentration and hematocrit were determined in all patients prior to surgery. Anesthesia was induced with an intramuscular injection of ketamine (4 mg/ kg; Ketaset®, Zoetis, Kalamazoo, MI), xylazine (0.4 mg/kg; AnaSed®, Akorn, Lake Forest, IL) and butorphanol (0.04 mg/ kg; Torbugesic®, Zoetis, Kalamazoo, MI) in combination, intubated and maintained with isoflurane (Piramel, Talangana, India) in oxygen as needed. The patient was posi- tioned in dorsal recumbency. The abdominal area from the xyphoid process to the inguinal region was clipped and asep- tically prepared and draped for surgery. The patient was placed in Trendelenburg position to allow cranial displace- ment of the abdominal viscera, reduce the risk of damage to underlying organs, and aid in visualization of the retained testis. A 5 mm skin incision was made on the umbilical scar and a teat cannula was inserted into the abdomen for insuf- flation with carbon dioxide (CO2) to a pressure of 15 mm Hg. The same incision site was used to create a portal for the endoscope using a 10 mm diameter trocar and cannula. A second skin incision was made in the parainguinal region on the same side as the retained testis to create a new portal for insertion of an atraumatic forceps. Once the testis was located and isolated with the forceps, it was grasped at the level of the gubernaculum and brought in proximity to the body wall. The parainguinal incision was enlarged to allow exteriorization of the testis. The testis, its respective vascular cone and the gubernaculum were exteriorized. The vascular cone was transfixed with absorbable material (polyglactin 910, #0; Vicryl®, Ethicon, Guaynabo, Puerto Rico) and the testicle was excised (Figure 1). The body wall and skin inci- sion were closed in routine fashion with resorbable material. Post-surgical management includes procaine penicillin G (PenOne Pro®, VETone®, MWI, Boise, ID) 22,000 IU/kg SC SID for 3 days or ceftiofur crystallin-free acid 6.6 mg/kg SC once) and non-steroidal anti-inflammatories (flunixin meglumine 1.1 mg/kg IV SID for 2 days; Banamine®, Merck, Madison, NJ). Figure 1. Laparoscopic-assisted cryptorchidectomy, (a) place- ment of the endoscope portal over the umbilical scar, (b) placement of the forceps portal, (c) parainguinal incision for exteriorization of the testicle, (d) exteriorization of the retained testicle, (e) transfixation and removal, (f) incision site for exteriorization of the testis. http://dx.doi.org/10.58292/CT.v15.9638 100 Citation line: Clinical Theriogenology 2023, 15, 9638, http://dx.doi.org/10.58292/CT.v15.9638 Goats were fasted for 18 to 24 h. Anesthesia was induced either with ketamine (1 mg/kg IM; Ketaset®, Zoetis) xylazine (0.1 mg/kg IM; AnaSed®, Akorn) and butorphanol (0.01 mg/ kg; Torbugesic®, Zoetis) in combination or with propofol (4 mg/kg IV; PropoFlo®, Zoetis, Kalamazoo, MI ) after sedation with butorphanol (0.2 mg/kg IV; Torbugesic®, Zoetis) and midazolam (0.1 mg/kg IV; Almaject, Morristown, NJ). Anesthesia was maintained with isoflurane in oxygen after endotracheal intubation and draped as previously described. Animals were placed in dorsal recumbency, and the scrotum and ventral abdomen prepared aseptically. A 1 cm skin inci- sion was made about 4 to 6 cm lateral to midline, contralat- eral to the side of the retained testis. The abdominal cavity was insufflated with medical grade CO2 through a teat cannula prior to insertion of a 6 mm trocar and canula which served as  the laparoscope portal. The patient was placed in Trendelenburg position. A second incision was made parallel to the inguinal ring ipsilateral to the retained testis. Babcock forceps were introduced into the second portal and the testis was grasped at the level of the gubernaculum (Figure 2). The incision length was extended to allow exteriorization of the testicle. The spermatic cord was transfixed with 0 PDS suture  (Ethicon, Guaynabo, Puerto Rico), transected with Metzenbaum scissors and the testis was removed. The incision was sutured in two planes with 2-0 PDS (Ethicon, Guaynabo, Puerto Rico) to close the body wall with a simple continuous pattern and skin with an intradermal pattern. A single cruciate suture was used to close the laparoscope portal incision. The scrotal testis was castrated using a standard closed technique. For bilaterally cryptorchid cases, both testes were removed from a single paramedian incision instead of a parainguinal incision. Post-surgical management includes antibiotics (pro- caine penicillin G; PenOne Pro®, VETone®; 22,000 IU/kg SC SID for 3 days or ceftiofur crystalline-free acid; Excede®, Zoetis, Kalamazoo, MI; 6.6 mg/kg SC once) and non-steroidal anti-in- flammatories (flunixin meglumine; Banamine®, Merck; 1.1 mg/kg IV SID for 2 days). Results All camelids in this case series presented with a unilateral abdominally retained testis. Testicular identification by trans- abdominal inguinal ultrasonography was possible in all cases. All testes were in the abdominal position near the inguinal region or close to the bladder (Figure 3). The left testis was retained in nine cases (56.25%), while the right was retained in seven cases (43.75%). The surgical procedure was com- pleted in 35 ± 12 min (Mean ± SD). The animals recovered uneventfully, and no complications were reported after dis- charge from the hospital. In goats, 15 (83%) cases were unilateral and 3 (17%) were bilateral cryptorchids. Of the 15 unilateral cryptorchid cases, 11 were right (73.33%) and four were left (26.67%). All uni- laterally affected males were identified by the owner as suspect cryptorchid before presentation and diagnosis was confirmed by ultrasonography (Figure 4). In this case series there were three full brothers (2 bilateral cryptorchid, 1 unilateral crypt- orchid) and five half-brothers (all unilateral cryptorchid with Figure 2. Laparoscopic-assisted cryptorchidectomy, (a) site of placement of the endoscope portal (1) and forceps portal (2), (b) abdominal testis visualized by laparoscopy, (c) abdominal testis grasped by the gubernaculum, (d) exteriorization of the retained testicle. (e) transfixation of spermatic cord and removal. Figure 3. Transcutaneous ultrasonographic localization of the retained testis in a cryptorchid alpacas. Arrow indicated the retained testis, UB = urinary bladder. http://dx.doi.org/10.58292/CT.v15.9638 Citation line: Clinical Theriogenology 2023, 15, 9638, http://dx.doi.org/10.58292/CT.v15.9638 101 same sire). The retained testes were located intra-abdominally near the bladder and identified by transabdominal inguinal ultrasonography in all cases. The retained testis length and width were 21.8 ±2.1 mm and 18.3 ± 1.5 mm (Mean ± SD), respectively. All animals recovered uneventfully from surgery and were discharged 1 day post-operatively from the hospital. No complications were reported on follow-up calls to the owners. Discussion Cryptorchidism is not an infrequent complaint in veterinary practice. Although unilaterally cryptorchid animals may have some fertility, the consensus is to eliminate these animals from breeding population as the disorder is suspected to be heritable. Diagnosis of cryptorchidism is based on history and clinical examination in most cases with or without the use of transabdominal ultrasound. In alpacas, diagnosis of cryptor- chidism may be challenging as male-like behavior and mating are possible in males that have been castrated at an older age. In these cases, endocrine evaluation helps in differentiating between geldings displaying male-like behavior and cryptor- chid animals. The diagnosis is based on determination of serum testosterone concentration before and 8 h after admin- istration of hCG (3000 IU).9,10,13 Recently, it has been shown that determination of Anti-Müllerian hormone on a single serum sample allows diagnosis of cryptorchidism in hemicas- trated alpacas.10,17 In the present case series, endocrine testing was performed in only one alpaca as in all the other cases cryptorchidism was evident from the history (lack of castra- tion) and confirmed by percutaneous ultrasonography. In the present study, unilateral cryptorchidism in goats affected predominately the right testicle. This agrees with other reports on West African dwarf goats.5,6,14 A study of 29 small ruminant cases (20 sheep and 9 goats) found cryptor- chidism was bilateral in 27.6% of cases and unilateral in 72.4%. Among unilateral cases, the right testis was affected in 85.7% and the left testis in 14.3%.14 The study included Boer (77.8%), La Mancha (11.1%), and mixed breed (11.1%). It is not clear why cryptorchidism is predominantly right-sided. Several surgical techniques have been described for cryptor- chidectomy in camelids and goats including a parainguinal, paramedian and caudal paramedian approaches. In camelids, the parainguinal approach for cryptorchidectomy is com- mon.15,16 Caudal paramedian approach for cryptorchidectomy was also described in small ruminants less than 4 months old with 6.9 and 3.4% minor and major complications respec- tively. Finding and exteriorizing the testis using the laparot- omy technique can be challenging and require larger incisions. Additionally, a second incision is often necessary in bilaterally cryptorchid cases.14 This results in increased surgical time and risks for complications. The laparoscopic-assisted technique described here was not associated with any complications. Conclusion Laparoscopic-assisted cryptorchidectomy is a safe, quick, and effective method for cryptorchidectomy in South American camelids and Nigerian dwarf goats. It allows proper localiza- tion, manipulation, and removal of retained testicles while reducing surgical time and post-operative complications. Clients breeding Nigerian dwarf goats should be educated about the high prevalence of cryptorchidism in this breed and its potential hereditary component. Cryptorchidism may be missed by some owners during early castration by elastic banding. References 1. Amann RP, Veeramachaneni DN: Cryptorchidism in common eutherian mammals. Reproduction 2007;133:541–561. doi: 10.1530/REP-06-0272 2. Sumar J: Studies on reproductive rathology in alpacas. MS thesis, Department of Obstetrics and Gynaecology, College of Veterinary Medicine, Swedish, University of Agricultural Sciences, Uppsala, 1983. 3. Drew ML, Meyers-Wallen VN, Acland GM, et al: Presumptive Sry- negative XX sex reversal in a llama with multiple congenital anomalies. J Am Vet Med Assoc 1999;215:1134–1139. 4. Khan LA, Rghuwanshi DS, Sirsat PR, et al: Incidence of cryptorchi- dism in goats. Ind J F Vet 2008;3:74. 5. Oguejiofor CF, Ochiogu IS, Okoro OL, et al: Consequences of uni- lateral cryptorchidism on semen and sperm characteristics in West African Dwarf goats. Asian Pac J Reprod 2018;7:172–177. doi: 10.4103/2305-0500.237055 Figure 4. Transcutaneous ultrasonographic localization of the retained testis in a cryptorchid goats. Arrow indicated the retained testis. http://dx.doi.org/10.58292/CT.v15.9638 https://doi.org/10.1530/REP-06-0272 https://doi.org/10.4103/2305-0500.237055 102 Citation line: Clinical Theriogenology 2023, 15, 9638, http://dx.doi.org/10.58292/CT.v15.9638 6. Igbokwe IC, Ezeasor DN, Onwuka OS: Comparative study of the morphology of the testes and excurrent ducts system in the unilat- eral cryptorchid West African dwarf goats. Niger Vet J 2007;28:40–47. doi: 10.4314/nvj.v28i3.3565 7. Igbokwe IO, Abba Y, Geidam SU, et al: Sperm output from unilat- eral cryptorchid Sahel goats. Comp Clin Path 2014;23:819–822. doi: 10.1007/s00580-013-1695-7 8. Tibary A, Pearson LK, Anouassi A: Applied andrology in camelids. In: Chenoweth P, Lorton S: editors. Animal Andrology: Theories and Applications. Wallingford; CABI: 2014. p. 418–449. 9. Fite C, Tibary A, Reeves J, et al: Testosterone response in male alpacas (Lama pacos) following hCG administration and correla- tion with testicular weight. Theriogenology 2005;64:782. 10. Tibary A, Campbell A, Rodriguez J, et al: Urogenital surgery in camelids. Clin Theriogenol 2020;12:271–291. 11. El-Zawam A, Tibary A, Patino C: Basal levels and hCG responses of serum testosterone and estrogen in male alpacas. Front Vet Sci 2020;7:595856. doi: 10.3389/fvets.2020.595856 12. Rietschel W: Kryptorchismus beim vicunja (Lama vicugna). Tierarztliche Praxis 1990;18:459–461. 13. Perkins NR, Frazer GS, Hull BL: Endocrine diagnosis of cryptor- chidism in a llama. Aust Vet J 1996;74:275–277. doi: 10.1111/ j.1751-0813.1996.tb13773.x 14. Haig FM, Baird AN, Hawkins JF, et al: Caudal paramedian approach to cryptorchidectomy in 29 small ruminants (2011–2019). Vet Surg 2020;50:170–176. doi: 10.1111/vsu.13546 15. Parker JE, Semevolos SA: Use of a parainguinal approach for cryptorchidectomy in alpacas. J Am Vet Med Assoc 2002;220: 1835–1836. doi: 10.2460/javma.2002.220.1835 16. Garcia Pereira FL, Allen A, Anouassi A, et al: Parainguinal cryptor- chidectomy under general anaesthesia in a Bactrian camel (Camelus bactrianus). J Camel Pract Res 2004;11:103–107. 17. Ciccarelli M, Tibary A, Campbell AJ, et al: Effect of age and castra- tion on serum anti-Müllerian hormone concentration in male alpacas. Theriogenology 2018;105:174–177. doi: 10.1016/j. theriogenology.2017.09.032 http://dx.doi.org/10.58292/CT.v15.9638 https://doi.org/10.4314/nvj.v28i3.3565 https://doi.org/10.1007/s00580-013-1695-7 https://doi.org/10.3389/fvets.2020.595856 https://doi.org/10.1111/j.1751-0813.1996.tb13773.x https://doi.org/10.1111/j.1751-0813.1996.tb13773.x https://doi.org/10.1111/vsu.13546 https://doi.org/10.2460/javma.2002.220.1835 https://doi.org/10.1016/j.theriogenology.2017.09.032 https://doi.org/10.1016/j.theriogenology.2017.09.032