Theriogenology Question of the Month

Anna I. McAllister Department of Clinical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331 (Kutzler)

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Michelle A. Kutzler Department of Clinical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331 (Kutzler)

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History

A 2-year-old 54.5-kg (119.9-lb) female alpaca (Vicugña pacos) was evaluated at the Oregon State University Veterinary Teaching Hospital (OSU-VTH) because of a 5-day history of progressive stranguria, tenesmus, and signs of abdominal pain. The alpaca had been vaccinated against Clostridium tetani and Clostridium perfringens (types C and D) and dewormed with ivermectin 12 and 3 months, respectively, before the initial examination. In addition, on several occasions between 1 and 3 months before the examination, the alpaca had been naturally mated to a male with good libido and proven fertility. The owner reported that each breeding appeared abnormal because the male would remain mounted on the female for only a short time and the female had vaginal bleeding afterward.

On physical examination at the OSU-VTH, the alpaca was tachycardic, tachypneic, and afebrile; showed signs of abdominal pain; and had no vulvar discharge. Results of a CBC indicated mild anemia (PCV, 23%; reference range, 27% to 45%) and moderate leukopenia (4,690 WBCs/µL; reference range, 8,000 to 21,400 WBCs/µL), characterized with severe neutropenia (610 mature neutrophils/µL [reference range, 4,711 to 14,686 mature neutrophils/µL]; 235 band neutrophils/µL [reference range, 0 to 147 band neutrophils/µL]) and moderate eosinopenia (422 eosinophils/µL; reference range, 687 to 4,867 eosinophils/µL). Abnormalities detected with serum biochemical analyses included high creatine kinase activity (1,477 U/L; reference range, 43 to 750 U/L) and mild hyperglycemia (227 mg/dL; reference range, 88 to 151 mg/dL), hypophosphatemia (4.4 mg/dL; reference range, 5.1 to 11.5 mg/dL), hypokalemia (3.6 mEq/L; reference range, 4.1 to 6.3 mEq/L), and ketosis (β-hydroxybutyric acid concentration, 1.3 mg/dL [reference range, 0.12 to 0.75 mg/dL]; nonesterfied fatty acids concentration, 0.27 mEq/L [reference range, 0 to 0.24 mEq/L]). The alpaca's serum progesterone concentration was 0.35 ng/mL (> 1.0 ng/mL is indicative of the presence of luteal tissue).

Transrectal ultrasonographic examination of the alpaca's reproductive tract revealed an enlarged uterus that was distended (diameter, > 5 cm) with hypoechoic fluid (Figure 1). The cervix and vagina were also distended with hypoechoic fluid, a corpus luteum was present on the left ovary, and multiple small (diameter, < 10 mm) follicles were present on both ovaries. On vaginoscopic examination, the vestibule terminated at a blind end just cranial to the urethral opening and approximately 7 cm cranial to the ventral commissure of the labia (Figure 2). Firm pressure applied at the blind end with the speculum did not reveal any weak areas that could be broken down by bougienage.

Figure 1
Figure 1

Transrectal ultrasonographic image of the junction of the vagina (star), cervix (demarcated with floating cervical folds [white arrows]), and uterus (intercornual septum [black arrow] between the uterine horns is evident) in a 2-year-old 54.5-kg (119.9-lb) female alpaca (Vicugña pacos) that had been naturally mated several times between 1 and 3 months earlier and underwent ultrasonography because of a 5-day history of progressive stranguria, tenesmus, and signs of abdominal pain. The uterus, cervix, and vagina are distended with intraluminal hypoechoic fluid. The alpaca's head is to the left of the image.

Citation: Journal of the American Veterinary Medical Association 258, 2; 10.2460/javma.258.2.153

Figure 2
Figure 2

Vestibular endoscopic image of the alpaca described in Figure 1 showing the blind-pouch termination of the vaginal vestibule just cranial to the urethral opening. Dorsal is toward the upper right of the image.

Citation: Journal of the American Veterinary Medical Association 258, 2; 10.2460/javma.258.2.153

Question

What is the likely diagnosis for the reproductive abnormalities described in this alpaca?

Answer

Imperforate vagina with secondary septic hydrometrocolpos was the likely diagnosis for the reproductive abnormalities described in this alpaca.

Results

Because of the alpaca's signs of increasing severity of abdominal pain and guarded prognosis for future fertility, the owners elected euthanasia for the alpaca. After euthanasia and with the owner's permission, the lack of patency of the vaginal vestibule was confirmed postmortem with positive-contrast vestibulography. Briefly, the bladder was expressed, a Foley catheter was inserted into the vestibule, the catheter balloon was inflated, and contrast medium was injected through the catheter. A single left lateral radiographic image was obtained of the pelvic and caudal abdominal regions. Contrast medium and air were evident in the urinary bladder, and contrast medium had migrated through a ureter and into a renal pelvis (Figure 3). However, contrast medium was not evident cranially in the reproductive tract.

Figure 3
Figure 3

Left lateral postmortem positive-contrast vestibulographic image of the alpaca described in Figure 1 showing contrast medium and air in the urinary bladder (long white arrow) and contrast medium in a ureter (black arrow) and renal pelvis (short white arrow). No contrast medium is evident cranially in the reproductive tract. The alpaca's head is toward the left of the image.

Citation: Journal of the American Veterinary Medical Association 258, 2; 10.2460/javma.258.2.153

A complete necropsy was performed and revealed extensive distention of the cranial aspect of the vagina (approx 18 × 15 × 3 cm) and the left and right uterine horns (diameter, 14 and 9 cm, respectively; Figure 4). The cranial dorsal aspect of the vestibule terminated at a blind end, and there was extensive hemorrhage and hyperemia in the cranial aspect of the vestibule. Approximately 7 cm cranial to the commissure of the labia, a 2-cm-thick segment of tissue encompassed the lumen and completely separated the vestibule from the vagina. The external cervical os was hyperemic and had concentric cervical ring dilation (diameter, 3 cm). Both ovaries had multiple follicles (diameter, ≤ 2.5 mm). The left ovary also contained a corpus luteum (approx 5 × 7.5 × 10 mm) on the cranial pole.

Figure 4
Figure 4

Postmortem image of the dorsal view of the reproductive tract removed from the alpaca described in Figure 1 showing extensive distention of the cranial aspect of the vagina (approx 18 X 15 X 3 cm) and the left and right uterine horns (diameter, 14 and 9 cm, respectively).

Citation: Journal of the American Veterinary Medical Association 258, 2; 10.2460/javma.258.2.153

The dorsal aspect of the isolated reproductive tract was transected, and approximately 1 L of cloudy white, nonflocculent fluid evacuated the lumen. Cytologic evaluation of the fluid revealed high cellularity, and nearly all cells were classified as degenerated neutrophils, many of which contained rod-, cocci-, and coccobacilli-shaped bacteria. There was also a large number of extracellular bacteria present. Aerobic and anaerobic bacterial cultures of the fluid yielded a Clostridium isolate and a mixture of aerobic bacteria.

There was a large fibrous adhesion between the urinary bladder and ventral aspect of the vaginal wall, and a small number of fibrin strands adhered to the surface of the small intestines. Histologic examination of the endometrium revealed an edematous submucosa that contained moderate numbers of lymphocytes and plasma cells.

Discussion

Normal development of the female reproductive tract requires the embryological mesonephric ducts to regress and the paramesonephric ducts to develop and fuse with the urogenital sinus.1,2 Failure of the caudal paramesonephric ducts to fuse to the urogenital tubercle can result in various degrees of abnormality, including a persistent hymenal membrane and an imperforate vagina.3 Although not present in the alpaca described here, other congenital reproductive anomalies reported in camelids include hypoplastic ovaries, uterus unicornis, double cervix, and vaginal frenulum.4 In fact, congenital urogenital defects are reported much more frequently in camelids than in other species.5 There may be a heritable reason for this. For example, a total or partial imperforated vulva is believed to be heritable because the defect has been found in 2 alpaca siblings.6

During embryological development, canalization of the vagina is normally complete at birth.3 If vaginal canalization does not occur, endometrial glandular secretions will accumulate in the uterine lumen and result in hydrometrocolpos over time.7 Animals with complete mural adhesions could also have hydrometrocolpos.8 Mural adhesions are common in the reproductive tracts of female camelids following breeding trauma or dystocia.9 Although a full-thickness mural adhesion was considered as a differential diagnosis for the reproductive tract abnormalities identified in the alpaca of the present report, it was unlikely given the necropsy results and the reproductive history.

Pyometra is an accumulation of purulent fluid within the uterus. This condition develops following the functional closure of the cervix secondary to high serum progesterone concentration, rather than from a congenital anomaly. In addition, in species such as horses for which it is not uncommon for cervical adhesions to occur following trauma at parturition or cervical manipulation,10 the cervix may become completely occluded, resulting in accumulation of a large volume of purulent fluid.11 However, neutropenia and tenesmus identified in the alpaca of the present report are atypical clinical signs of pyometra in large animal species.12

Given our findings in the alpaca of the present report, we prioritized hydrometrocolpos secondary to imperforate vagina. Septic hydrometrocolpos has been reported in humans as a rare condition,13 and the route by which the hydrometrocolpos in the alpaca of the present report became septic was unknown. Ascending infection is a common route,14 and vaginal trauma during breeding could have been an inciting cause for the infection in this alpaca. However, although the alpaca had extensive hemorrhage and hyperemia in the cranial vestibule, no communication between the vestibule and vagina was identified. A hematogenous route could have occurred. Pyometra of hematogenous origin has been reported in several species but not in camelids.14

Outcome

Clostridial infections are associated with fatal third-compartment gastritis and enteritis in adult camelids.15 In the alpaca of the present report, septic clostridial hydrometrocolpos extended into acute fibrinous peritonitis and resulted in endotoxemia with signs of severe abdominal pain. Thus, given the alpaca's degree of sepsis and guarded prognosis for future fertility, surgical options (eg, vaginal cannulation, T-shaped vaginoplasty, vaginectomy, or hysterectomy) may not have been appropriate.3,16

References

  • 1.

    Cunha GR, Robboy SJ, Kurita T, et al. Development of the human female reproductive tract. Differentiation 2018;103:4665.

  • 2.

    Thomas DFM. The embryology of persistent cloaca and urogenital sinus malformations. Asian J Androl 2020;22:124128.

  • 3.

    Tan RH, Dascanio JJ. Infertility associated with persistent hymen in an alpaca and a llama. Can Vet J 2008;49:11131117.

  • 4.

    Vaughan JL, Tibary A. Reproduction in female South American camelids: a review and clinical observations. Small Rumin Res 2006;61:259281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Videla R. Camelid neonatology, in Proceedings. Mich Vet Conf 2017;1–4. Available at: michvma.org/resources/Documents/MVC/2017%20Proceedings/videla%2004.pdf. Accessed Sep 25, 2020.

    • Search Google Scholar
    • Export Citation
  • 6.

    Wilkins PA, Southwood LL, Bedenice D. Congenital vulvar deformity in 6 alpacas. J Am Vet Med Assoc 2006;229:263265.

  • 7.

    Gayle DH. Old and New World camelids. In: Noakes ED, Parkinson JT, England CWG, eds. Veterinary reproduction and obstetrics. 10th ed. London: Elsevier Saunders, 2019;670682.

    • Search Google Scholar
    • Export Citation
  • 8.

    Murray EF. Reproduction. In: Murray EF, Bravo PW, eds. Medicine and surgery of South American camelids: llama, alpaca, vicuna, guanaco. Ames, Iowa: Iowa State Press, 1998;2:381429.

    • Search Google Scholar
    • Export Citation
  • 9.

    Cebra CK, Watrous BJ, Cebra ML. Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy llamas and alpacas. Vet Radiol Ultrasound 2002;43:359366.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Arnold CE, Brinsko SP, Varner DD. Cervical wedge resection for treatment of transluminal cervical adhesions and subsequent pyometra: three clinical cases, in Proceedings. 59th Annu Meet Am Assoc Equine Pract 2013;13541357.

    • Search Google Scholar
    • Export Citation
  • 11.

    Gilbert RO. Pyometra in large animals. In: Merck veterinary manual. 2015;1–3. Available at: www.merckvetmanual.com/reproductive-system/metritis-in-large-animals/pyometra-in-large-animals. Accessed Sep 25, 2020.

    • Search Google Scholar
    • Export Citation
  • 12.

    Sheldon IM, Williams JE, Miller NA, et al. Uterine diseases in cattle after parturition. Vet J 2008;176:115121.

  • 13.

    Nagaraj BR, Basavalingu D, Paramesh VM, et al. Radiological diagnosis of neonatal hydrometrocolpos—a case report. J Clin Diagn Res 2016;10:TD18TD19.

    • Search Google Scholar
    • Export Citation
  • 14.

    Tibary A, Fite C, Anouassi A, et al. Infectious causes of reproductive loss in camelids. Theriogenology 2006;66:633647.

  • 15.

    Björklund C. Diseases and causes of death among camelids in Sweden: a retrospective study of necropsy cases 2011–2013. Swedish Univ Agric Sci 2014;65:159.

    • Search Google Scholar
    • Export Citation
  • 16.

    Tibary A, Rodriguez J, Sandoval S. Reproductive emergencies in camelids. Theriogenology 2008;70:515534.

Contributor Notes

Dr. Kutzler's present address is the Department of Animal and Rangeland Sciences, College of Agriculture Sciences, Oregon State University, Corvallis, OR 97331.

Ms. McAllister was an undergraduate student at the College of Biology, Oregon State University, Corvallis, OR 97331 when the report was written.

Address correspondence to Ms. McAllister (mcallisa@oregonstate.edu).
  • Figure 1

    Transrectal ultrasonographic image of the junction of the vagina (star), cervix (demarcated with floating cervical folds [white arrows]), and uterus (intercornual septum [black arrow] between the uterine horns is evident) in a 2-year-old 54.5-kg (119.9-lb) female alpaca (Vicugña pacos) that had been naturally mated several times between 1 and 3 months earlier and underwent ultrasonography because of a 5-day history of progressive stranguria, tenesmus, and signs of abdominal pain. The uterus, cervix, and vagina are distended with intraluminal hypoechoic fluid. The alpaca's head is to the left of the image.

  • Figure 2

    Vestibular endoscopic image of the alpaca described in Figure 1 showing the blind-pouch termination of the vaginal vestibule just cranial to the urethral opening. Dorsal is toward the upper right of the image.

  • Figure 3

    Left lateral postmortem positive-contrast vestibulographic image of the alpaca described in Figure 1 showing contrast medium and air in the urinary bladder (long white arrow) and contrast medium in a ureter (black arrow) and renal pelvis (short white arrow). No contrast medium is evident cranially in the reproductive tract. The alpaca's head is toward the left of the image.

  • Figure 4

    Postmortem image of the dorsal view of the reproductive tract removed from the alpaca described in Figure 1 showing extensive distention of the cranial aspect of the vagina (approx 18 X 15 X 3 cm) and the left and right uterine horns (diameter, 14 and 9 cm, respectively).

  • 1.

    Cunha GR, Robboy SJ, Kurita T, et al. Development of the human female reproductive tract. Differentiation 2018;103:4665.

  • 2.

    Thomas DFM. The embryology of persistent cloaca and urogenital sinus malformations. Asian J Androl 2020;22:124128.

  • 3.

    Tan RH, Dascanio JJ. Infertility associated with persistent hymen in an alpaca and a llama. Can Vet J 2008;49:11131117.

  • 4.

    Vaughan JL, Tibary A. Reproduction in female South American camelids: a review and clinical observations. Small Rumin Res 2006;61:259281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Videla R. Camelid neonatology, in Proceedings. Mich Vet Conf 2017;1–4. Available at: michvma.org/resources/Documents/MVC/2017%20Proceedings/videla%2004.pdf. Accessed Sep 25, 2020.

    • Search Google Scholar
    • Export Citation
  • 6.

    Wilkins PA, Southwood LL, Bedenice D. Congenital vulvar deformity in 6 alpacas. J Am Vet Med Assoc 2006;229:263265.

  • 7.

    Gayle DH. Old and New World camelids. In: Noakes ED, Parkinson JT, England CWG, eds. Veterinary reproduction and obstetrics. 10th ed. London: Elsevier Saunders, 2019;670682.

    • Search Google Scholar
    • Export Citation
  • 8.

    Murray EF. Reproduction. In: Murray EF, Bravo PW, eds. Medicine and surgery of South American camelids: llama, alpaca, vicuna, guanaco. Ames, Iowa: Iowa State Press, 1998;2:381429.

    • Search Google Scholar
    • Export Citation
  • 9.

    Cebra CK, Watrous BJ, Cebra ML. Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy llamas and alpacas. Vet Radiol Ultrasound 2002;43:359366.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Arnold CE, Brinsko SP, Varner DD. Cervical wedge resection for treatment of transluminal cervical adhesions and subsequent pyometra: three clinical cases, in Proceedings. 59th Annu Meet Am Assoc Equine Pract 2013;13541357.

    • Search Google Scholar
    • Export Citation
  • 11.

    Gilbert RO. Pyometra in large animals. In: Merck veterinary manual. 2015;1–3. Available at: www.merckvetmanual.com/reproductive-system/metritis-in-large-animals/pyometra-in-large-animals. Accessed Sep 25, 2020.

    • Search Google Scholar
    • Export Citation
  • 12.

    Sheldon IM, Williams JE, Miller NA, et al. Uterine diseases in cattle after parturition. Vet J 2008;176:115121.

  • 13.

    Nagaraj BR, Basavalingu D, Paramesh VM, et al. Radiological diagnosis of neonatal hydrometrocolpos—a case report. J Clin Diagn Res 2016;10:TD18TD19.

    • Search Google Scholar
    • Export Citation
  • 14.

    Tibary A, Fite C, Anouassi A, et al. Infectious causes of reproductive loss in camelids. Theriogenology 2006;66:633647.

  • 15.

    Björklund C. Diseases and causes of death among camelids in Sweden: a retrospective study of necropsy cases 2011–2013. Swedish Univ Agric Sci 2014;65:159.

    • Search Google Scholar
    • Export Citation
  • 16.

    Tibary A, Rodriguez J, Sandoval S. Reproductive emergencies in camelids. Theriogenology 2008;70:515534.

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