History
An approximately 2-month-old 16.1-kg (35.4-lb) castrated male Hampshire lamb developed signs of pelvic limb ataxia at 30 days after birth, which had subsequently progressed to paraplegia. The time course of the progression was not provided by the owner. The lamb was euthanized by means of an IV barbiturate overdose injection. The lamb underwent necropsy within 24 hours after euthanasia at the Michigan State University Veterinary Diagnostic Laboratory. The lamb was born on a farm that raised lambs specifically for show purposes (so-called club lambs) and was the second lamb of the herd to develop paraplegia.
Clinical and Gross Findings
At necropsy, the tail was docked at approximately the level of the fourth caudal vertebra. Ventral to the rectum, there was a soft, fluctuant, hairless swelling that measured 10 × 7 × 2 cm. On cut section, the swelling was filled with a watery, opaque, pink-brown fluid containing strands and clumps of similarly colored material.
The urinary bladder measured 19 × 10 × 7 cm and was flaccid and easily expressed manually. The urine was clear and pale yellow and contained a moderate amount of white flocculent material. The serosal and mucosal surfaces of the bladder were grossly normal. The ureters were bilaterally dilated throughout their lengths to approximately 0.5 cm in diameter. The kidneys had red to tan stippling on capsular surfaces. On cut section, each kidney had a pale tan cortex and pink-red medulla. There was marked dilation of the renal pelvises, which contained clear fluid.
From the level of the L6 vertebra and continuing caudally to the cranial aspect of the sacrum, there was subdural accumulation of a thick, creamy, yellow exudate. A sample of the exudate was obtained for aerobic microbial culture. At the level of the L1-L2 vertebral canal, there also was a 1.5 × 1.0-cm oval focus of subdural hemorrhage on the ventral aspect of the spinal cord. The spinal cord was fixed in buffered 10% formalin prior to sectioning. On transverse section, from the level of the L5 to S1 vertebrae, the spinal cord through the conus medullaris contained a central area of white to tan, creamy, granular material. The lesion measured 1.0 mm in diameter at its most cranial aspect, and caudally it expanded to efface the entire spinal cord parenchyma (Figure 1).
Photograph of transverse sections of the lumbosacral portion of the spinal cord in a 2-month-old lamb that was euthanized because of paraplegia. Serial sections reveal a lesion that has effaced the neuroparenchyma progressing in severity from the cranial (top left section is at the level of L5) to caudal (bottom right section is a sacral segment) aspect.
Citation: Journal of the American Veterinary Medical Association 256, 1; 10.2460/javma.256.1.63
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→
Histopathologic and Microbiological Findings
On histologic examination of the spinal cord at the level of the L5 vertebra, the central canal was expanded and filled with eosinophilic necrotic debris, degenerate and nondegenerate neutrophils, macrophages, and karyorrhectic debris that effaced the ependyma and dissected into the surrounding neuroparenchyma (Figure 2). At the level of the cranial aspect of the sacrum, the entire architecture of the spinal cord was replaced by necrotic debris centrally, which was surrounded by evidence of suppurative inflammation, numerous astrocytes, and concentric rings of fibroblasts and collagen. Throughout the extent of the lesion, the neuroparenchyma adjacent to the lesion had vasculature with reactive endothelium and perivascular cuffing by lymphocytes and neutrophils. There was occasional chromatolytic degeneration of neurons, numerous spheroids, and spongiosis of the white matter. The leptomeninges within the ventral median fissure were infiltrated with moderate to marked numbers of neutrophils. In the kidneys, there were multifocal areas of mild, chronic interstitial nephritis and medullary fibrosis. Within the interstitium and some tubules, there was glassy, flocculent, pale basophilic material. The urinary bladder had mild submucosal granulation tissue. Evidence of active infection in the kidneys or bladder wall was not present. Aerobic culture of a swab specimen of the subdural exudate yielded numerous colonies of Actinomyces hyovaginalis and rare mixed coliforms.
Photomicrograph of a section of the affected spinal cord of the lamb in Figure 1 at the level of the S1 vertebra. A central area of necrosis (asterisk) is surrounded by a fibrous capsule. Bordering the central area of necrosis (arrowhead) and radiating outward are concentric rings of astroglia, fibroblasts, and collagen admixed with inflammatory cells. H&E stain; bar = 200 μm. Inset—Lower-magnification view of the same section of the sacral spinal cord at the level of S1. The box outlines the region seen in the main image. The central aspect of the spinal cord is replaced by a large central area of necrosis surrounded by inflammatory cells, abscess (asterisk), and a fibrous capsule. H&E stain; bar = 800 μm.
Citation: Journal of the American Veterinary Medical Association 256, 1; 10.2460/javma.256.1.63
Morphologic Diagnosis and Case Summary
Morphologic diagnosis and case summary: severe, chronic, segmental suppurative meningomyelitis and subdural abscess with intralesional bacteria (A hyovaginalis) and bilateral hydroureter and hydronephrosis in a lamb.
Comments
For the lamb of the present report, suppurative meningomyelitis and subdural abscess formation likely resulted from an ascending infection associated with the tail dock site. However, a more commonly reported cause of pelvic limb paresis or paralysis in lambs with recently docked tails is vertebral osteomyelitis and extradural empyema with compression of the spinal cord.1–3 Bacterial infection at the site of tail docking is presumed to result in subsequent bacteremia and hematogenous spread via the vertebral veins to the vertebrae.4 In the lamb of the present report, osteomyelitis was not observed and the epidural space was grossly normal. Instead, infection was present as a subdural abscess as well as within the central area of the spinal cord. The subdural infection could be explained by direct inoculation of spinal dura mater filaments (filum durae matris spinalis), which sometimes extend into the caudal vertebrae. Given the central location of the infection within the spinal cord, it is likely that the infection arose from within the central canal. Embryologically, the spinal cord develops from the neural tube. At the rostral and caudal end of the neural tube are openings called the rostral and caudal neuropores, respectively. The rostral neuropore closes first and the neuroparenchyma enclosing the rostral neuropore becomes the lamina terminalis, whereas the caudal neuropore closes later.5 In some instances, the caudal neuropore may remain patent, allowing for communication with the subarachnoid space.6 It is possible that given the cranial location of the tail docking, bacteria may have gained direct access to the subarachnoid space or bacteria from the subdural infection may have entered the subarachnoid space. Once within the subarachnoid space, bacteria could have entered the caudal neuropore to ultimately develop into an abscess within the central canal of the spinal cord.
The large, flaccid urinary bladder likely represented a normal postmortem change. However, it is possible that it reflected lower motor neuron urinary bladder and urethral sphincter dysfunction. The sacral spinal cord segments contain the general visceral efferent fibers of the pelvic nerve, which supply the detrusor muscles and general somatic efferent fibers of the pudendal nerves, which supply the external urethral sphincter. Consequently, a lower motor neuron deficit of the urinary bladder and urethral sphincter would be anticipated owing to the location of the lesion. An explanation for the bilateral hydronephrosis and hydroureter remained uncertain. Physical obstruction to urine flow was not observed, and the urinary bladder was easily evacuated manually. It is possible that an inability to void urine owing to lower motor neuron dysfunction of the detrusor muscle resulted in a distended urinary bladder, which led to increased intravesicular pressure and secondary bilateral hydronephrosis and hydroureter. Alternatively, the bilateral hydronephrosis and hydroureter may have been consequences of prior pyelonephritis; however, supportive evidence such as damage or distortion or fibrosis of the renal pelvises was not observed. Mild chronic interstitial nephritis was present without evidence of active inflammation indicative of an active infection. The subepithelial granulation tissue in the urinary bladder wall also was mild and was unlikely to have obstructed urine outflow from the urinary bladder.
The organism isolated from the lamb's spinal cord abscess was A hyovaginalis. Originally discovered in the purulent vaginal discharge of pigs, as the name suggests,7 A hyovaginalis is still most commonly associated with pyogenic infections in pigs,8,9 but it has been isolated in a case of lymphadenitis in a goat10 and previously cultured from the abscesses of sheep.11
The lamb of the present report was owned by a club lamb breeder. Club lamb is a colloquial term for a wether lamb that is bred and raised to be shown in local clubs, such as 4-H and Future Farmers of America, and then finished and slaughtered for meat before the animal reaches maturity.12 Breeds such as Suffolk, Hampshire, and Dorsett are typically used to breed club lambs. It is common practice to dock the tails of these lambs extremely short, leaving only a few remaining caudal vertebrae to emphasize a square rump in the show ring. As a consequence of excessively short tail docking, there is an increased risk of rectal prolapse.13,14 For the lamb of the present report, excessively short tail docking may have enabled direct access of bacteria to the CNS with resultant infection. In light of the necropsy results, the owner of the farm was contacted to provide information about tail docking practices. In general, tail docking would occur when the lambs were 4 days old. In previous years, the owner had cleaned each dock site with iodine solution, but in 2017, this practice was abandoned. Current recommendations by the AVMA state that the tail should be docked no shorter than the distal end of the caudal tail fold.15 Practitioners should educate breeders about the potential morbidity and death that may result from excessively short docking of the tail in lambs.
References
1. Downey NE. Spinal abscesses as a cause of paralysis in sheep. N Z Vet J 1957;5:97–100.
2. Finley GG. A survey of vertebral abscesses in domestic animals in Ontario. Can Vet J 1975;16:114–117.
3. Marques LC, Cadioli FA, Netto AdC, et al. Abscessos em coluna vertebral de bezerros e cordeiros: aspectos neurológicos. Revista de Educação Continuada em Medicina Veterinária e Zootecnia do CRMV-SP 2004;7:8.
4. Divers TJ. Acquired spinal cord and peripheral nerve disease. Vet Clin North Am Food Anim Pract 2004;20:231–242, v-vi.
5. Noden DM, deLahunta A. Central nervous system and eye. In: The embryology of domestic animals developmental mechanisms and malformations. Baltimore: Williams & Wilkins, 1985;92–119.
6. de Lahunta A, Glass EN, Kent M. Development of the nervous system: malformations. In: Veterinary neuroanatomy and clinical neurology. 4th ed. Philadelphia: Elsevier Health Sciences, 2014;45–77.
7. Collins MD, Stubbs S, Hommez J, et al. Molecular taxonomic studies of Actinomyces-like bacteria isolated from purulent lesions in pigs and description of Actinomyces hyovaginalis sp. nov. Int J Syst Bacteriol 1993;43:471–473.
8. Aalbaek B, Christensen H, Bisgaard M, et al. Actinomyces hyovaginalis associated with disseminated necrotic lung lesions in slaughter pigs. J Comp Pathol 2003;129:70–77.
9. Reichel R, Wragg P. Isolation of Actinomyces hyovaginalis from a lung lesion in a pig. Vet Rec 2007;160:203.
10. Schumacher VL, Hinckley L, Gilbert K, et al. Actinomyces hyovaginalis-associated lymphadenitis in a Nubian goat. J Vet Diagn Invest 2009;21:380–384.
11. Foster G, Wragg P, Koylass MS, et al. Isolation of Actinomyces hyovaginalis from sheep and comparison with isolates obtained from pigs. Vet Microbiol 2012;157:471–475.
12. Savere C, Luther J. Youth market lamb project guide. Available at: www.ndsu.edu/fileadmin/4h/Animals/gbj166.pdf. Accessed Nov 8, 2017.
13. Thomas DL, Waldron DF, Lowe GD, et al. Length of docked tail and the incidence of rectal prolapse in lambs. J Anim Sci 2003;81:2725–2732.
14. Windels H. Factors causing rectal prolapse in feedlot lambs, in Proceedings. 62nd Annu Sheep Lamb Feed Day 1990;10–13.
15. Docking of lambs' tails. Available at: www.avma.org/KB/Policies/Pages/Docking-of-Lambs-Tails.aspx. Accessed Nov 8, 2017.
