2022 journal article
What is your diagnosis? Coelomic fluid in an Eastern River Cooter (Pseudemys concinna concinna)
Veterinary Clinical Pathology.
author keywords: coelomic fluid; cytology; spermatozoa; turtle
MeSH headings : Animals; Rivers; Turtles
UN Sustainable Development Goal Categories
13. Climate Action
(Web of Science)
14. Life Below Water
(OpenAlex)
15. Life on Land
(Web of Science)
Source: ORCID
Added: August 20, 2022
An adult male intact Eastern River Cooter (Pseudemys concinna concinna) was presented by a good Samaritan to North Carolina State Veterinary Hospital's Turtle Rescue Team (TRT) after presumably being hit by a motor vehicle. The patient suffered from a carapace fracture of the left bridge (see Figure 2), prefemoral lacerations cranial to the left hind leg, and partial externalization of the intestines. The injuries appeared to be acute in nature. A shell repair was performed, and supportive care was initiated while the patient was dry docked. Blood work was not performed at the time of intake. Approximately 2 months following admittance, the patient was placed in water submersion due to the development of plastron pressure sores secondary to dry-docking. A week later, the patient reportedly had become very lethargic and appreciably edematous. The patient's packed cell volume (PCV) and plasma protein by refractometry at this time were 19% and 8.0 g/dL, respectively (the reference interval [RI] for related species, PCV 14%-26%, total protein 2.3-3.8 g/dL).1 Gross plasma abnormalities, such as hemolysis, were not appreciated. A coelomocentesis was performed, and approximately 35 ml of yellow, slightly cloudy fluid was removed from the coelomic cavity via fine-needle aspiration, which was then submitted for cytologic evaluation only (Figure 1); a total leukocyte count and total protein by refractometry were not performed. Low cellularity fluid with spermatozoa. The cellularity of the effusion was estimated to be low, along with low numbers of erythrocytes and few thrombocytes. Nucleated cells consisted predominantly of variably intact heterophils and macrophages. Outnumbering the leukocytes were several variably intact spermatozoa. Spermatozoa had deeply basophilic staining vermiform-shaped heads, which were elongate and tapered to a point, and variably appreciable, poorly staining midpieces and tails (Figure 2). No intracellular spermatozoa were definitively seen. No infectious agents were identified. Following water submersion and cytologic findings, the patient underwent both a computed tomography (CT) scan and coelomic laparoscopy to re-evaluate the overall extent of injuries due to trauma. The most notable finding on the CT scan included multiple severe comminuted fractures of the pelvis bilaterally, with moderate left sacroiliac subluxation and marked accumulation of coelomic fluid. While there were no obvious abnormalities in the gonads, this region was directly adjacent to the spinal luxation. The CT scan was performed without contrast. Together with the amount of coelomic fluid, any trauma to the gonads may have been inadvertently overlooked. Coelomic laparoscopy revealed a large amount of fluid with free-floating particulate matter, suspected to be plant material. Following the presumptive diagnosis of GI perforation (due to free-floating plant material), euthanasia was elected. On necropsy, a duodenal perforation and ruptured bladder, both with fibrinous adhesions, were discovered. Grossly visible gonadal trauma was not appreciated. Histopathology was not performed. Descriptive texts and images of the cytomorphology of mature turtle spermatozoa are limited.3, 4 Since cytopathology is more commonly used as a diagnostic tool in exotic and wildlife animal medicine; it is advantageous to have accessible resources with both routine and unusual findings that one might encounter as a cytopathologist. Many mammals and birds are seasonal and continuous breeders with synchronous reproductive events. In contrast, turtles located in temperate zones have a unique reproductive cycle in which spermatogenesis in male turtles is asynchronous with ovulation in the female. Spermatogenesis in the male turtle occurs episodically, starting in early summer and ending in autumn, with spermatozoa leaving the testes and entering the epididymis.5 Asynchrony of reproduction events necessitates methods for spermatozoa storage in both male and female turtles.3 In spring-breeding turtles, such as the Eastern River Cooter, spermatozoa are stored in the ductus epididymis of the male. In a study by Gist et al, spermatozoa were found in the ductus epididymis of painted turtles throughout the year, even when the testes were completely regressed in the spring.5 The spermatozoa were observed to be relatively impervious to deterioration over time (as long as 5 months), when evaluated both within and outside of the epididymis. While an official total leukocyte count and protein by refractometry was not performed, a low cellularity fluid suggestive of a transudate was considered most likely. In this case, chief uncertainties included how both the fluid and spermatozoa came to be free within the coelomic cavity. The patient was not hypoproteinemic at the time of water submersion; thus, decreased oncotic pressure was not considered to be a likely cause for the increased presence of coelomic fluid. Given that the fluid accumulation in the coelomic cavity appeared to occur simultaneously with water submersion, a postulation for the coelomic fluid was that water from the patient's enclosure had entered the coelom through the patient's wounds. The testis and epididymis are both located ventral to the kidneys and cranial to the accessory urinary bladder in the male turtle.3 Spermatozoa are a normal finding in the urine of clinically normal male turtles, as well as female turtles that have been in contact with males.6 Therefore, considerations for the presence of spermatozoa in the coelomic fluid include both traumatization to the gonads and/or contamination from the ruptured urinary bladder. An interesting observation made during the cytologic evaluation of the coelomic effusion was the relatively minimal inflammatory response. While heterophils and macrophages were present in low numbers, the spermatozoa appeared practically untouched. In small domesticated animals, the testes are considered an immune-privileged site; if exposed to surrounding tissues, a robust inflammatory response (predominantly macrophages) is anticipated (eg, sperm granuloma).2 Medications administered during the patient's hospitalization at various time points included nonsteroidal anti-inflammatory drugs (ketorolac and ketoprofen), as well as antibiotics (ceftazidime). Postulation for the lack of a significant inflammatory response includes anti-inflammatory and/or immunomodulatory effects of these medications. The timing of duodenal and urinary bladder perforations is not clear; neither plant-like material nor bacteria were observed at the time of cytologic evaluation; however, fibrinous adhesions described during necropsy suggest a degree of chronicity. Given the necessity for spermatozoa storage in both male and female turtles,3 not only traumatic mating but trauma, such as vehicular trauma, to reproductive organs in either sex may lead to spermatozoa leakage into the coelomic cavity year-round. While the presence of spermatozoa in the coelomic fluid was not a primary issue for the patient, this case allowed for the documentation of the cytologic features of spermatozoa from the Eastern River Cooter (Pseudemys concinna concinna). The authors thank Sabrina Kapp for the coordination and supervision of the patient's care. The authors have indicated that they have no affiliations or financial involvement with any organization or entity with a financial interest in, or in financial competition with, the subject matter or materials discussed in this article.