Fibrinous pleuritis associated with Streptococcus canis in a leopard cat (Prionailurus bengalensis euptilurus) (original) (raw)

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  3. v.24(5); Sep 2023
  4. 10.4142/jvs.23080

© 2023 The Korean Society of Veterinary Science

Case Report

Received March 22, 2023; Revised July 04, 2023; Accepted July 11, 2023.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Leopard cat (Prionailurus bengalensis euptilurus) is a small wild cat assessed as an endangered wildlife in Korea. There have been very few reports of their diseases. Herein, we describe fibrinous pleuritis caused by Streptococcus canis infection with excessive pleural effusion, hydropericardium, mild ascites, and liver fibrosis in a leopard cat. S. canis is a commensal microflora in domestic cats and often affects the upper respiratory tract inducing chronic and severe respiratory diseases. However, there is no literature regarding the S. canis in leopard cats. Therefore, we first report fibrinous pleuritis associated with an S. canis infection in a leopard cat.

Keywords

Gram-positive cocci; pleurisy; pleural effusion; wild cat

INTRODUCTION

Leopard cat (Prionailurus bengalensis) is a small wild cat distributed from Java island in Southeast Asia to the Amur River in Northeast Asia [1]. The range of the species was traditionally recognized as twelve subspecies, recently sunk into four [1]. The subspecies present in northeast Asia were assigned to P. b. chinesis and P. b. euptilrurus, and the latter is the only wild animal of the Felidae family that has survived in the Korean peninsula [1, 2]. The leopard cat has been designated as an endangered wildlife species in Korea. Leopard cats are small wild cats about the size of domestic cats but slender, and have longer legs with well-defined webs between their toes [3]. Their back and rounded ears are black with a central white spot, a characteristic appearance of the wild cats, which distinguishes them from domestic cats. In addition, unlike domestic cats, they are outstanding swimmers with a great affinity for water [3]. Contrary to Korea, although it has been listed as Least Concern on the International Union for Conservation of Nature Red list as it is widely distributed [4], there have been very few reports about the infectious agents of leopard cats [5, 6, 7, 8]. Moreover, these infectious agents were just confirmed through the molecular screening of pathogens using blood and tissues from free-ranging or found-dead wild cats without direct evidence of diseases. Carnivore protoparvovirus 1 and coronavirus have been detected in live-trapped and road-killed leopard cats of Taiwan [5]. There is a report about bacterial infection by arthropod vectors, such as Anaplasma spp. and hemoplasma using blood and spleen tissue of wild cats in Korea [6]. Parasitic infections with Hepatozoon felis and Clonorchiasis in leopard cats were also confirmed in Korea as incidental findings [7, 8]. Thus, information about pathologic lesions directly related to infectious agents in the species still remains scarce. Therefore, we describe the histopathological features of Streptococcus canis infection in a captive leopard cat.

CASE PRESENTATION

A male leopard cat was rescued by being caught in a net at a farm and kept at a wildlife shelter for about 4–5 years due to its inability to adapt to the wild. The leopard cat was raised with another female leopard cat, which had been saved in a different region before rescuing the male wild cat and her age was estimated to be between 8 and 9 years. Daily feed for the leopard cats in the shelter was mainly chicken meat. The male leopard cat was found dead, and a necropsy was performed for postmortem examination. Grossly, a large amount of pleural effusion was found in the thoracic cavity, with some fibrinous exudate on the lung surface and pleural membrane (Fig. 1A). Pulmonary congestion with atelectasis was seen throughout the lungs (Fig. 1B). There were no structural abnormalities in the heart except for moderate pericardial transudate (Fig. 1C). In the abdominal cavity, mild ascites was confirmed without exudate (Fig. 1D). The right kidney revealed a focal wedge-shaped pale area of infarction with atrophy of the renal parenchyma (Fig. 1E). Other organs, including the liver, did not show grossly remarkable pathologic changes, except for a mildly dilated gallbladder due to fasting (Fig. 1F). For microscopic examination, tissues were fixed in 10% neutral buffered formalin and processed in a routine manner with a graded ethanol series and xylene. The tissue samples were then embedded in paraffin wax, sectioned at 4 um, and stained with hematoxylin and eosin (H&E) and Masson’s trichrome. For the identification of bacterial infections, the pleural effusion was cultured on blood agar plates. The colonies obtained from the plates were isolated and identified through matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) spectrometry (MALDI Biotyper 3.0 software; Brucker, USA). Polymerase chain reaction (PCR) was performed with primers designed for species-specific parts of the 16S-23S rDNA intergenic spacer region and the CAMP factor gene cfg to confirm the reliability of bacterial identification by MALDI-TOF [9]. Microscopically, pulmonary congestion was observed throughout the lungs, and hemorrhage was more prominent getting near the lung surface (Fig. 2A). Fibrinous exudate, in which fibrin was mixed with cell debris, covered some parts of the lung surface, and cuboidal mesothelial cells of the lung surface were hypertrophic (Fig. 2B). Atelectasis appeared as alveolar collapse with slit-like lumina having sharp angular ends (Fig. 2C). There was no inflammatory cell infiltration, such as neutrophils, plasma cells, and lymphocytes, in the lung parenchyma. The infarction area of the right kidney showed coagulative necrosis (Fig. 2D), and mineralization was seen in some necrotic areas of the cortex. In the liver, congestion and mild fibrosis around the central veins were confirmed with atrophy of hepatocytes (Fig. 2E and F). In bacterial identification using pleural exudate, S. canis (score value: 2.224) was detected (Fig. 3). Consequently, the case was diagnosed as fibrinous pleuritis with a S. canis infection, which resulted in hydrothorax, hydropericardium, ascites, and liver fibrosis, caused by chronic profuse pleural exudate.

Fig. 1
Gross examination of the male leopard cat. (A) Enormous pleural effusion in the thoracic cavity is turbid and blood-tinged. There is fibrinous exudate on the mediastinal pleura (yellow arrow). (B) The lung is dark red and shrunken (yellow asterisk) due to pulmonary congestion with atelectasis by enormous hydrothorax. (C) Moderate transudate in the pericardium (yellow arrow). (D) Mild ascites in the abdominal cavity (yellow arrow). The effusion is transparent transudate without inflammation. (E) Cross-section of the right kidney. Focal wedge-shaped pale area of infarction (yellow arrows) with atrophy of the renal parenchyma. (F) The liver does not show any remarkable macroscopic changes except for gallbladder distension (yellow arrow) due to fasting.

Fig. 2
Histopathological examination of the lungs, the kidney, and the liver from the leopard cat. (A) Pulmonary congestion occurs throughout the lungs, and hemorrhage is more prominent near the lung surface. Fibrinous membrane covers the lung surface. H&E. (B) Higher magnification of the pulmonary surface. The exudate covering the lung surface consists of fibrin and cell debris. Cuboidal mesothelial cells on the lung surface are hypertrophic (arrow). H&E. (C) Collapsed alveoli appears as silt-like lumina. The infiltration of inflammatory cells is not seen in the lung parenchyma. H&E. (D) The infarction area of the right kidney is shown as atrophy of the parenchyma with coagulative necrosis. H&E. (E) Fibrosis with hepatocyte atrophy around the congested central vein. H&E. (F) Collagen (blue color) is confirmed in fibrotic lesions by Masson’s trichrome staining. Scale bars = 200 µm.
CV, central vein; PT, portal triads; H&E, hematoxylin and eosin.

Fig. 3
Polymerase chain reaction product from bacterial colony with two _S. canis_-specific oligonucleotide primers. S. canis is identified by amplification of S. canis 16S-23S rDNA intergenic spacer region (lane 1, 215 bp) and group G streptococcal CAMP factor gene cfg (lane 2, 238 bp). Lane M = 100 bp ladder marker (Bioneer).

DISCUSSION

S. canis is a gram-positive bacteria and common commensal microflora on the skin and mucosal surfaces of dogs and domestic cats. It is also an important opportunistic pathogen in trauma, viral infections, and immunosuppressive conditions [10]. In dogs, S. canis has been associated with numerous diseases, including severe and invasive infections such as necrotizing fasciitis, sepsis, and toxic shock syndrome [10]. In domestic cats, the streptococci can be isolated from the nasal cavity in up to 10% of cats with chronic upper respiratory infections and often cause severe inflammation, such as rhinitis, sinusitis, and pneumonia [11]. S. canis infections have also been reported in other animals and humans. The bacteria have been reported to cause mastitis in dairy herds [10]. In humans, the bacteria have been known to induce diseases such as soft tissue, urinary, and bone infections, septicemia, pneumonia, and endocarditis [12, 13]. In the present case, S. canis induced fibrinous pleuritis in the leopard cat. One study described severe pyothorax and fibrinous pleuritis with bronchopneumonia caused by S. canis infections in two domestic cats [14]. However, there are no reports of S. canis causing only pleuritis without pneumonia in domestic cats. Moreover, the other cohabiting leopard cat in this case was not affected by the infection and survived in good condition after the leopard cat died. Therefore, S. canis might exist as a commensal microflora in the leopard cat as in domestic cats and induce the disease in such as immunosuppressive conditions.

Pleuritis is caused by infectious agents which most often reach the pleura from lesions of pneumonia or abscesses in the underlying lung, or from the blood. If there is only pleuritis in the absence of pneumonia, infection from other routes including perforation of the chest wall or esophagus, lymphatic permeation or direct extension from the peritonitis have been suggested, because pleural defenses against microorganisms are much more vulnerable than those of the lung [15]. Even a few organisms reaching the pleural surfaces are apt to have serious consequences without pulmonary involvement [15]. In human, the incidence of spontaneous bacterial empyema (SBE), which is a spontaneous infection of pleural cavity in the absence of pneumonia, has been reported [16]. Although SBE of human is often occurred with peritonitis or hepatic cirrhosis with ascites, a few cases of SBE without those diseases have been reported in the literature, which are a coexistent immunosuppressive state likely predisposed them to development of SBE [16]. In the present case, S. canis may extend to the lung and pleura by direct microscopic bacterial invasion under stress or immunosuppressive condition, and induce inflammation only in the pleura because of its susceptibility.

Excessive pleural fluid by pleural inflammation may become chronic and lead to secondary atelectasis. Excessive hydrothorax may also irritate the heart and promote the hydropericardium. As pericardial fluid accumulated, the heart may be persistently compressed. Ascites is a feature of chronic liver failure and can also be associated with hypoproteinemia secondary to various causes or systemic venous congestion of the right-sided heart [15, 17]. In the present case, hepatic fibrosis and the physical body condition were not so severe as to induce hypoproteinemia. Therefore, the passive hepatic congestion related to impaired heart filling by hydropericardium may result in ascites, and furthermore, develop mild liver fibrosis with atrophy of hepatocytes around the central veins.

Renal infarction is a common lesion of localized coagulative necrosis produced by the occlusion of the renal vessels due to emboli [15]. An embolism is mainly derived from thrombi and other types of emboli, including bacteria, neoplasm, parasites, etc. [17]. In the present case, the thrombi and bacterial or other types of emboli were not directly confirmed in the renal parenchymal of the leopard cat. Therefore, it seemed difficult to determine the cause of renal infarction in this case.

The present report describes a case of fibrinous pleuritis without pneumonia, which was associated with S. canis in a captive leopard cat. Although S. canis can infect a wide range of mammals, the isolation of the bacterial species has not been documented in leopard cats. Moreover, this report shows the possibility that S. canis may be a commensal microflora in leopard cats.

Funding:This work was supported by the National Research Foundation of Korea (NRF) grand funded by the Korean government (MSIT) (No. 2020R1A2C1102143).

Conflict of Interest:The authors declare no conflicts of interest.

Author Contributions:

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