History
A 4-year-old intact Nigerian Dwarf doe was presented for examination with a history of lethargy, anorexia, decreased milk production, and recumbency after kidding. Two days following parturition of 4 kids (3 healthy, 1 stillborn), the doe was evaluated for suspected metritis and treated with antibiotics and intravascular fluids by a private practitioner. Despite medical treatment, the doe continued to decline and was referred for an evaluation at the Louisiana State University School of Veterinary Medicine 5 days postpartum.
Clinical and Gross Findings
At presentation, the doe was recumbent, tachypneic, and hypothermic (35 °C). Rumen atony was noted, along with crackles and wheezes on thoracic auscultation, red mucous membranes, and ultrasonographic evidence of intrauterine fetal remnants. Blood gas analysis revealed metabolic acidosis, hyperkalemia, hypernatremia, and hyperchloremia. Treatment was initiated with insulin, dextrose, plasma, and bicarbonate. A CBC (CBC-Advia 120; Siemens Healthineers) demonstrated an inflammatory leukogram, characterized by marked neutropenia (0.2 X 109/L; reference interval, 0.7 × 109 to 7.6 × 109/L) with occasional toxic change, and an unremarkable erythrogram and thrombogram. Significant abnormalities noted on plasma biochemistry panel (Catalyst One; IDEXX Laboratories) included hyperglycemia (107 mg/dL; reference interval, 45 to 70 mg/dL) and hypoalbuminemia. Peritoneal fluid analysis revealed a total nucleated cell count of 200/µL and a protein concentration of < 2.5 g/dL.
The nucleated cells were composed predominantly of nondegenerate neutrophils with few macrophages. Clinical differential diagnoses included sepsis, Multiple Organ Dysfunction Syndrome (MODS), and Systemic Inflammatory Response Syndrome (SIRS). The doe continued to decline and was humanely euthanized due to poor prognosis.
Postmortem examination revealed marked subcutaneous edema on the ventral neck, thorax, and abdomen. The peritoneal cavity contained approximately 500 mL of serosanguinous fluid. The uterine body, urinary bladder serosa, and surrounding adipose tissue had multifocal petechiae and fibrin. The uterine serosa had multifocal to coalescing, sharply demarcated purple areas of necrosis (Figure 1), and the uterus was distended by malodorous, viscous fluid (Figure 2). The lungs were wet, heavy, and mottled purple to red, and the interlobular septa were distended by clear fluid. The main bronchi contained froth extending into the trachea.
Postmortem image of the uterus from a 4-year-old intact Nigerian Dwarf doe. The uterus was distended, more prominently in the left horn. There were several irregular dark gray to purple areas, sharply demarcated from the surrounding tissue by a bright red rim (arrowheads). Fibrin strands (arrow) were adhered to the serosa.
Citation: Journal of the American Veterinary Medical Association 262, 6; 10.2460/javma.23.12.0711
Postmortem image of the uterus from a 4-year-old intact Nigerian Dwarf doe. The left uterine horn contained large amounts of opaque, red-brown, malodorous, viscous fluid (arrowhead). The endometrial surface of the left uterine horn was irregular and dark pink to red, and the wall was thickened by dark-red fluid in the regions corresponding to the external purple areas (arrows). The right uterine horn contained moderate amounts of palepink viscous fluid (asterisk) and the endometrial surface near the base of the horn had a 1.5 X 1.0 cm dark-red focus with a pale-yellow center (inset). The intraluminal exudate also filled the uterine body.
Citation: Journal of the American Veterinary Medical Association 262, 6; 10.2460/javma.23.12.0711
Histopathologic and Immunohistochemical Findings:
Corresponding to the purple areas noted grossly in both uterine horns, there was superficial to transmural coagulative necrosis in both the caruncular and intervening regions (Figure 3). These areas were rimmed by coalescing aggregates of degenerate leukocytes amid smooth muscle bundles with dystrophic mineralization as well as by congested and variably necrotic blood vessels with occasional fibrin thrombi. Additional histologic lesions included acute pulmonary edema, mild hepatic lipidosis, splenitis, and fibrinous peritonitis.
Uterus. A—The endometrium had extensive coagulative necrosis with cellular debris and bacterial colonies at the surface. In the uterine wall, degenerate leukocytes (presumably neutrophils) border the necrotic area (arrows), amid foci of dystrophic mineralization (arrowhead; H&E stain, 1X). B—Numerous mixed bacteria were adhered to the necrotic endometrial surface (H&E stain, 40X). C—The bacteria were gram-negative short bacilli, gram-positive larger bacilli, and gram-positive chains of cocci (Gram stain, 40X). D—The larger intralesional bacilli were labeled with antibodies against Paeniclostridium sordellii (immunohistochemical stain, 40X).
Citation: Journal of the American Veterinary Medical Association 262, 6; 10.2460/javma.23.12.0711
Along the necrotic endometrial surface and mixed with degenerate inflammatory cells were moderate numbers of short gram-negative bacilli, larger gram-positive bacilli, and chains of gram-positive cocci (Figure 3). Numerous degenerate neutrophils infiltrated the subserosal stroma, which was lined by fibrin.
Immunohistochemical (IHC) staining for clostridial species (Clostridium chauvoei, Clostridium novyi, Clostridium perfringens, Clostridium septicum, and Paeniclostridium sordellii) was performed on uterine sections. The large intralesional bacilli were labeled by an antibody specific against P sordellii (Figure 3).
Morphologic Diagnosis and Case Summary
Morphologic diagnosis: Metritis, necro-suppurative, with intralesional P sordellii.
Case summary: Acute clostridial metritis with terminal exotoxemia due to P sordellii.
Comments
Postpartum metritis in does is typically predisposed by retained fetal membranes, dystocia, and multiparous births. Infectious organisms commonly associated with postpartum metritis include Coxiella burnetii, Chlamydia spp, Yersinia pseudotuberculosis, and Mycoplasma spp.1 Clostridial species were recently described as causative agents of gangrenous postpartum metritis in goats, including P sordellii (formerly Clostridium sordellii) and C perfringens.2,3 Paeniclostridium sordellii is an anaerobic, gram-positive, spore-forming bacterium that inhabits soil, sewage, and water.2,3 Two most clinically relevant virulent factors of this microorganism are lethal toxin (tcsl) and hemorrhagic toxin (tcsh).2,4 Paeniclostridium sordellii has been reported to cause gas gangrene in ruminants, umbilical infections in foals, and metritis with septic shock in humans.2,4
Clinical signs of postpartum metritis are nonspecific and include lethargy, depression, tachycardia, fetid vaginal discharge, and pyrexia.2,3 In this case, CBC and venous blood gas analysis revealed marked neutropenia, hyperglycemia, metabolic acidosis, hyperkalemia, hypernatremia, and hyperchloremia. The neutropenia was attributed to increased tissue migration and/or increased margination secondary to acute exotoxemia, and hyperglycemia was attributed to stress.
Gross findings of clostridial metritis in goats include uterine serosal petechiation, mural congestion and edema, well-delimited dark purple areas, and malodorous intraluminal exudate. Reported histologic features include transmural coagulative necrosis, circulatory leukocytosis, and occasional fibrin thrombi. Additional findings include splenic congestion, splenitis, abomasitis, enteritis, and peritonitis.2,3 Anaerobic culture of the uterus was negative in our case, possibly due to previous antibiotic therapy or sampling error for culture at necropsy; P sordellii is a strict anaerobe, and isolation can be challenging if samples are not collected and cultured immediately after death. Aerobic culture revealed heavy growth of non-hemolytic Escherichia coli and Streptococcus lutetiensis. Other case reports of clostridial metritis reported mixed infection of E coli, C perfringens, C chauvoei, C septicum, and C novyi.3 In our case, there was heavy growth of E coli and S lutetiensis on a fresh sample of spleen, while culture of a fresh lung sample yielded heavy growth of E coli. Therefore, it is possible that sepsis caused by these bacteria contributed to the death of this goat.
Clinical findings of tachycardia, tachypnea, hypothermia, and leukopenia indicated SIRS. Dysfunction of organs unrelated to the initial insult indicate secondary MODS. Histologic finding of splenitis support systemic inflammation. The doe appeared refractory to treatment and continued to decline, indicating loss of homeostatic ability and potential MODS, which is additionally supported by rumen atony and tachypnea at presentation.
Retention of placental membranes, as was observed ultrasonographically in this case, can lead to postpartum clostridial metritis in does. Bacteria and toxins interact with placental remnants during uterine involution leading to increased prostaglandin release and susceptibility to infection.2 Increased predisposition to metritis can also be due to increased stress levels and increased gestational progesterone levels.1,2 Deficient trace minerals contributing to lowered immunity can increase susceptibility to uterine infection.2 Additionally, selenium deficiencies have been implicated in herd outbreaks of retained placentas in does.5 Paeniclostridium sordellii has been isolated from the vagina of apparently healthy women, suggesting that women may be carriers. Fecal contamination during parturition could also contribute to ascending infections through the cervix.4 There are no comparable studies in goats, so it is unknown if P sordellii is associated with the normal reproductive tract or if fecal contamination is the source of uterine infection in does.
Promoting evacuation of retained placental remnants and uterine involution is justified for prevention of metritis. Treatment for retained placental remnants involves administration of oxytocin at 2-hour intervals, or 5 mg of prostaglandin IM or SC.5 If metritis is suspected, systemic antibiotics should be provided; tetanus prophylaxis is also indicated, as C tetani can potentially colonize the uterus.5 Paeniclostridium sordellii appears to be susceptible to the same antibiotic therapy as most other clostridial species, including β-lactams, clindamycin, and tetracyclines.4 In a report of clostridial metritis affecting multiple animals in different herds, no following cases were identified after treatment with a high dose of intravenous penicillin at parturition.3 Therefore, although prognosis for untreated does with clostridial metritis is poor, penicillin may be an effective treatment. Adequate selenium and trace mineral supplementation during gestation could reduce the likelihood of retained placental remnants and could boost immunity levels, decreasing the factors contributing to postpartum metritis. Kids born of affected does appear to be healthy and do not require treatment.
Acknowledgments
The authors thank the members of the Histology section at the Louisiana Animal Disease Diagnostic Laboratory/LSU Diagnostics, School of Veterinary Medicine, Louisiana State University, and of the Histology section at the California Animal Health and Food Safety Laboratory, San Bernardino branch, for their assistance.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in generation of this manuscript.
Funding
The authors have nothing to disclose.
References
- 1.↑
Schlafer DH, Foster RA. Female genital system. In: Grant Maxie M, ed. Jubb, Kennedy and Palmer's Pathology of Domestic Animals. Vol 3. Elsevier; 2016:358–464. doi:10.1016/B978-0-7020-5319-1.00015-3
- 2.↑
Gonzalez-Astudillo V, Asin-Ros J, Moore J, Uzal FA, Navarro MA. Paeniclostridium sordellii-associated peripartum metritis in goats. Vet Pathol. 2023;60(1):69–74. doi:10.1177/03009858221133506
- 3.↑
Dorso L, Chartier C, Popoff MR, Tesson C, Despres J, Uzal FA. Postpartum clostridial gangrenous metritis in 12 dairy goats in France. J Vet Diagn Invest. 2023;35(3):266–271. doi:10.1177/10406387231161508
- 4.↑
Aldape MJ, Bryant AE, Stevens DL. Clostridium sordellii infection: epidemiology, clinical findings, and current perspectives on diagnosis and treatment. Clin Infect Dis. 2006;43(11):1436–1446. doi:10.1086/508866
- 5.↑
Youngquist RS, Threlfall WR. Current Therapy in Large Animal Theriogenology. 2nd ed. Saunders/Elsevier; 2007.
