Introduction

In human medicine, a renal subcapsular abscess is defined as a suppurative process between the renal capsule and parenchyma.^1–3 A renal subcapsular abscess differs from a renal abscess in that the latter is located in the cortical or cortico-medullary parenchyma.^2–4 A renal subcapsular abscess is considered extremely uncommon in humans, and to the best of the authors’ knowledge, it is not reported in dogs.^1–3,5–7 The pathophysiology in humans has not been entirely clarified for either renal or perirenal abscess; however, the main causes seem to be related to bacterial hematogenous spread, ascending urinary tract infection (UTI), or proximity to infected area.^1,8 In dogs, the perirenal abscesses, located in the retroperitoneal space surrounding the kidney, have been reported in two cases, in association with pyelonephritis, nephrolithiasis, and bladder uroliths, and a renal abscess has been reported in a dog with diabetes mellitus.^5–7 Nephrectomy is the only treatment proposed in dogs with renal and perirenal abscesses; however, no specific recommendations are available for renal subcapsular abscesses.^5–7 This case report describes the surgical treatment of a renal subcapsular abscess with a kidney-sparing procedure in a dog with sepsis due to hematogenous spread of Staphylococcus pseudintermedius.

Case Report

An 11 yr old male Drahthaar dog was referred to the Veterinary University Hospital of the Department of Veterinary Medical Sciences, University of Bologna, Italy, for dysuria and pollakiuria. The dog had a history of recurrent lower urinary tract obstruction due to uroliths in the past 2 yr. Dysuria associated with a distended bladder was found by physical examination, and partial urethral obstruction, possibly associated with UTI, was suspected. A complete blood cell count and chemistry were performed. The complete blood cell count revealed a severe neutrophilic and monocytic leukocytosis (Table 1, T0). The chemistry profile showed a moderate increase in C-reactive protein, mild increase of transaminases, hypercholesterolemia, hypoalbuminemia with a decreased albumin/globulin ratio, and mild abnormalities of the electrolytes (Table 1, T0). Urinalysis results were consistent with UTI, and culture results were positive for S pseudintermedius (Table 1). Radiographic examination of the abdomen showed increased soft tissue opacity in the region of the left kidney. Abdominal ultrasonographic examination (US) revealed a subcapsular hypoechogenic fluid-filled lesion of 25 mm in diameter at the cranial pole of the left kidney, and a small amount of densely echogenic fluid was observed in the retroperitoneal perirenal space. A small cortical lesion was present in the right kidney, suggesting previous renal infarction. A focal hypoechoic lesion (23 mm diameter) was present in the spleen, with an infarction suspected. The gallbladder wall was slightly thickened and hyperechoic, and the gallbladder contained a moderate amount of sludge.

TABLE 1 Significant Clinicopathological Findings

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After the dog was sedated, samples of bile, retroperitoneal perirenal fluid, and renal subcapsular lesion content were aspirated with US guidance. The subcapsular lesion was completely drained, and all the samples were submitted for cytological and microbiological evaluation. The cytological examination revealed the presence of septic exudate, and S pseudintermedius was isolated in all submitted samples (Table 1, T0). The dog was hospitalized; fluid therapy and antimicrobial therapy (amoxicillin and clavulanic acid 22 mg/kg orally q 8 hr and marbofloxacin 3 mg/kg IV q 24 hr) were started on the basis of antimicrobial susceptibility results. After initial improvement, the dog re-presented for acute vomiting and anorexia after 7 days. Pain was elicited on abdominal palpation. Abdominal US confirmed the previously observed lesions and showed a focal dilation and thickening of the intestinal wall with multiple submucosal cystic formations of 7 × 10 mm and loss of layer detail. These lesions extended for about 10 cm of jejunum, and the surrounding peritoneum appeared hyperechoic. The blood tests showed that a mild anemia, persistence of neutrophilic and monocytic leukocytosis, and a decreased antithrombin activity were present (Table 1, T1). A surgical exploration of the abdomen was scheduled. After premedication with methadone (0.3 mg/kg intramuscularly [IM]) and acepromazine (10 µg/kg IM), anesthesia was induced with propofol (3 mg/kg IV) and maintained with isoflurane (0.5–2%). The intraoperative analgesia was administered with fentanyl (constant rate infusion 0.003–0.012 mg/kg IV, as needed). After surgical preparation of the ventral abdomen, xipho-pubic celiotomy was performed. A jejunal lesion, a focal marginal splenic lesion of about 2 cm with omental adhesions, and an abnormal left kidney shape with increased vascularization and decreased firmness in its cranial pole were identified during exploration. The intestine appeared focally dilated and dark in color, with omental adhesions over a length of 10 cm. The supplying mesenteric vessels were not visible owing to mesenteric thickening, and no pulse was detected. On the basis of suspicion of an ischemic intestinal lesion, the intestine was approached first. After omental adhesion resolution, enterotomy was performed to rule out the presence of a foreign body. The intestinal mucosa appeared altered by submucosal cyst-like lesions that were yellow-green in color. Enterectomy of about 25 cm of intestine and end-to-end anastomosis were performed. After changing instruments and gloves, the peritoneum covering the left kidney was incised, and the kidney was isolated (Figure 1A). A hyperemic area was observed on the kidney capsule at the cranial pole where a 3 cm fluctuant and poorly circumscribed subcapsular lesion was detected on palpation. A 22 gauge needle was inserted through the renal capsule to locate the lesion, and a small amount of viscous and brown fluid was collected. The renal capsule was incised and dissected over the palpable lesion. Because of the difficulty of finding a plane of cleavage, the abscess was incised, the exudate was aspirated, and the abscess capsule was then removed by blunt dissection, with the exception of a focal region where sharp dissection was required (Figure 1B). The abscess and the overlying renal capsule were completely excised, leaving the underlying renal parenchyma mostly intact, and the surgical site was widely irrigated. The bleeding was moderate and controlled by bipolar diathermia and the application of a hemostatic gelatin^a, kept in place by a mattress suture incorporating the remaining renal capsule (Figure 1C). Partial splenectomy was also performed using a vessel sealing device^b for the focal lesion in the most caudal portion of the spleen. The abdominal cavity was closed in the routine manner.

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The dog was hospitalized at the intensive care unit for monitoring, analgesia, and supportive care, which included antimicrobials (amoxicillin and clavulanic acid 22 mg/kg orally q 8 hr and marbofloxacin 3 mg/kg IV q 24 hr), antacids (omeprazole 1 mg/kg IV q 24 hr), and IV fluid therapy (Ringer’s lactate solution 2 mL/kg/hr). During the first 24 hr after surgery, methadone (0.1 mg/kg IM q 4 hr) was administered for pain management; subsequently, the patient was transitioned to buprenorphine (15 µg/kg IM q 8 hr). The patient’s clinical condition and blood work results remained stable (Table 1, T2), and postoperative abdominal US did not show any evidence of complications.

Nevertheless, 2 days after surgery, the dog developed edema of the right hind limb as a result of right lateral saphenous vein thrombosis, confirmed by US. Unfractionated heparin (150 UI/kg subcutaneously q 8 hr) and clopidogrel (2 mg/kg orally q 24 hr) administration was started. Clinical signs related to thrombosis improved in 4 days.

The dog was discharged 7 days after surgery, with administration of antimicrobial (amoxicillin/clavulanic acid 22 mg/kg orally q 12 hr for 7 days and marbofloxacin 3 mg/kg orally q 24 hr for 4 days) and antithrombotic therapies as prescribed during hospitalization.

Histopathologically, the renal subcapsular lesion was composed of mature fibrous connective tissue, poorly cellular and rich in collagen, consistent with an abscess capsule. Furthermore, histopathology revealed a severe neutrophilic and lymphoplasmacytic ulcerative and transmural enteritis, with abundant granulation tissue infiltrating the mesenteric adjacent adipose tissue. Thrombosis of the arteries in the mesenteric tissue, adjacent to the ulcerative lesion, was observed. A severe focal necrotizing and pyogranulomatous splenitis, with intralesional coccoid bacteria, was also observed via histopathology.

At first re-examination, 12 days after surgery, the dog’s clinical condition was good, and his urine culture was negative (Table 1, T3). One month later, the clinical condition remained good. No evidence of abdominal lesions or thrombi were noted by US, and all medications were discontinued. No symptoms had recurred at 1 yr follow-up, and the clinical condition remained good based on physical examination.

Discussion

In dogs, renal and perirenal abscesses are uncommon conditions, and few cases are reported, whereas no cases of subcapsular renal abscess have been described in the veterinary literature, to the best of the authors’ knowledge.^5–7 In the present case, the localization of the abscess was subcapsular, as the fluid was collected within a fibrous capsule between the renal capsule and parenchyma.^1,2 The pathophysiology of the renal subcapsular abscess is not clearly reported either in veterinary or in human medicine.¹ The main predisposing factors for renal and perirenal abscesses in dogs are recurrent UTIs and urinary tract obstructions, mostly due to uroliths.^5–7 In the present case, the dog had a history of urolithiasis and possibly, but not proved by previous bacterial culture, recurrent UTI. Diabetes mellitus appears to be an important predisposing factor for perirenal and renal subcapsular abscesses in humans, and it is also reported in the case of one dog with renal abscess.^1,2,7 In the case reported here, no concomitant metabolic or immunodeficiency disorders were identified. The pathogenesis of the subcapsular renal abscess in our case remains unclear. The concomitant positive culture for S pseudintermedius of the bile, urine, retroperitoneal perirenal effusion, and subcapsular renal collection and the history of the patient suggest an initial infection site, possibly ascending UTI, and subsequent sepsis with hematogenous bacterial spread and secondary lesions. S pseudintermedius is a coagulase-positive bacteria, considered the major opportunistic pathogen and the most prevalent inhabitant of the skin and mucosae of dogs.⁹ In previously reported renal and perinephric abscesses in dogs, the isolated bacteria were Staphylococcus spp. and Escherichia coli.^5,7 Furthermore, in a recent study, Staphylococcus spp. were the most common types of bacteria isolated (13.7%) in dogs with UTI, and this could support the hypothesis of ascending infection in the present case.¹⁰ In humans, bacteria isolated from subcapsular renal abscess included S aureus, E coli, Klebsiella, and Enterobacter cloacae, and Staphylococcus spp. are the most frequently isolated type of bacteria (80%) in children’s renal abscesses.^1–3 Moreover, Staphylococcus spp. are not commonly described as pathogens in the course of bactibilia in dogs, as they are not typical inhabitants of the gastrointestinal tract.^11,12 In fact, S pseudintermedius has been reported in only two cases of bactibilia in dogs, probably consequent to hematogenous spread, as it was assumed in our case.^11,12 In our case, the spleen was not submitted for culture; however, coccoid bacteria inside the excised granuloma were observed on performing histopathology. In the few human reported cases, the clinical signs of subcapsular renal abscess are nonspecific and included fever and flank pain.^1,3,8 In the present case, the only clinical signs reported by the owner were dysuria and pollakiuria, probably due to UTI. Laboratory evaluation revealed an inflammatory state characterized by neutrophilic and monocytic leukocytosis and increased C-reactive protein, as has already been reported for humans with renal subcapsular abscess.¹ US and computed tomography are recommended to correctly identify and then localize the lesion.^1–3 Cytology and culture of the renal lesion samples collected under US guidance are recommended.^6,7 In humans, renal subcapsular hematoma and abscess have similar appearance on computed tomography scan, and only cytology of the content might discriminate between the two lesions.^1,6,7 Nephrectomy is the only treatment described for dogs for renal or perirenal abscess.^5–7 This approach has been elected because of severe damage to the kidney parenchyma or the deep location of the lesion.^5–7 In human medicine, especially in pediatric patients, a conservative approach, such as image-guided percutaneous drainage associated with antimicrobial therapy, is the treatment of choice for renal and perirenal abscess, and it has been reported in a case of renal subcapsular abscess.^2,3,8 Furthermore, laparoscopic excision of a subcapsular abscess has been reported once.¹ In our case, as a first attempt, the purulent content was drained under US guidance, and antimicrobial therapy was instituted, guided by culture and sensitivity tests. The conservative treatment was useful to stabilize the patient; however, it was not successful in resolving the infection. Indeed, surgery was subsequently necessary because of the persistence of renal lesions and the development of septic secondary lesions.

Complete surgical excision of the subcapsular abscess was feasible because of the circumscribed subcapsular location and the almost normal appearance of the underlying renal parenchyma. After the removal of the abscess and the renal capsule, a hemostatic sponge was applied to better control the parenchymal bleeding. Hemostatic sponge implanting into infected sites is usually not recommended, as it may act as a nidus of infection.¹³ However, in this case the abscess was completely excised without major surgical field contamination, and no postoperative complication relating to the hemostatic sponge was identified.

On the basis of clinical, surgical, and histological findings, the focal intestinal lesion was considered the result of a mesenteric vascular occlusion.¹⁴ In dogs, mesenteric vascular disorders can be linked to mechanical, inflammatory, and/or traumatic causes and hypercoagulability.^14,15 Arterial thrombosis, thromboembolism, venous thrombosis, or occlusive vasculitis are the reported causes of ischemic intestinal lesions, and they have rarely been reported in veterinary literature.^14,15 Neither traumatic events nor mechanical causes were detected in the present case, and we postulate that the vascular injury may be due to the spread of septic thrombo-emboli.^15,16 The inflammatory and/or hypercoagulable state, promoted by sepsis, and the presence of the subcapsular abscess were more likely responsible for mesenteric ischemia in this dog.^15,16 In fact, according to the literature, inflammatory states including intra-abdominal infections, peritonitis, and biliary infection/inflammation are considered predisposing factors, and they were all reported in our case.^15,16 The hypercoagulable state is reported in humans as a predisposing factor to mesenteric vein thrombosis, and it may be linked to antithrombin deficiency, as detected in our case.¹⁵ In the present case, blood culture was not performed; however, the positivity to Staphylococcus spp. of all the samples collected, including bile, was considered indicative of sepsis. Sepsis is consistently listed as an underlying cause of thrombosis in dogs, and antithrombotic therapy should be considered when hypercoagulability is demonstrated or if other risk factors for thrombosis exist.^17,18 In this case, hyperfibrinogenemia was not detected, and unfortunately no thromboelastometry was performed; however, the septic condition was demonstrated.

Splenic abscess and pyogranuloma are uncommon disorders in dogs, but they are frequently associated with systemic diseases.^19,20

Conclusion

The present study describes a subcapsular renal abscess surgically treated, preserving the kidney in a septic dog with severe thromboembolic complications. Ischemic intestinal and splenic pyogranulomatous lesions, rarely reported entities in veterinary literature,^15,19,20 were also addressed successfully with surgery. Hematogenous spread of S pseudintermedius was the main suspected cause, as the presence of bacteria was documented in different locations; however, the initial infection site could not be determined.