Resolution of nonurine transudative pleural effusion in a cat after removal of a hydronephrotic kidney

Maura E. Duffy Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Andrew J. Specht Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Ahmira R. Torres Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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May-li Cuypers Veterinary Mobile Endoscopy and Diagnostics, Belleair Bluffs, FL 33770.

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Abstract

CASE DESCRIPTION A 3-year-old spayed female Bengal cat was evaluated because of a history of bilateral pleural effusion and hydronephrosis of the right kidney.

CLINICAL FINDINGS Cytologic analysis of a pleural fluid sample revealed characteristics of a pure transudate with a high percentage of lymphocytes. Results of fluid biochemical testing were not consistent with urine or chyle. Serum biochemical analysis and echocardiography yielded no evidence of hypoalbuminemia or high hydrostatic pressure secondary to cardiac disease. Abdominal ultrasonography revealed hydronephrosis of the right kidney and hydroureter of the right ureter.

TREATMENT AND OUTCOME Exploratory laparotomy with nephrectomy of the right kidney was performed. At the time of surgery, there was no evidence of communication between the retroperitoneal space and thoracic cavity. No other treatments were performed. No evidence of pleural fluid accumulation was detected 1 week after surgery, and no recurrence of clinical signs associated with pleural effusion was observed for > 1 year after surgery.

CLINICAL RELEVANCE Transudative, or nonchylous lymphatic, pleural effusion secondary to intra-abdominal disease, but independent of a low plasma protein concentration, is uncommon in veterinary medicine. This case emphasized that urinary tract obstruction should be considered as a differential diagnosis for cats with pleural effusion when more common disorders are not identified. Even without evidence of direct communication between the abnormal kidney or retroperitoneal space and the pleural space, removal of the hydronephrotic kidney appeared curative.

Abstract

CASE DESCRIPTION A 3-year-old spayed female Bengal cat was evaluated because of a history of bilateral pleural effusion and hydronephrosis of the right kidney.

CLINICAL FINDINGS Cytologic analysis of a pleural fluid sample revealed characteristics of a pure transudate with a high percentage of lymphocytes. Results of fluid biochemical testing were not consistent with urine or chyle. Serum biochemical analysis and echocardiography yielded no evidence of hypoalbuminemia or high hydrostatic pressure secondary to cardiac disease. Abdominal ultrasonography revealed hydronephrosis of the right kidney and hydroureter of the right ureter.

TREATMENT AND OUTCOME Exploratory laparotomy with nephrectomy of the right kidney was performed. At the time of surgery, there was no evidence of communication between the retroperitoneal space and thoracic cavity. No other treatments were performed. No evidence of pleural fluid accumulation was detected 1 week after surgery, and no recurrence of clinical signs associated with pleural effusion was observed for > 1 year after surgery.

CLINICAL RELEVANCE Transudative, or nonchylous lymphatic, pleural effusion secondary to intra-abdominal disease, but independent of a low plasma protein concentration, is uncommon in veterinary medicine. This case emphasized that urinary tract obstruction should be considered as a differential diagnosis for cats with pleural effusion when more common disorders are not identified. Even without evidence of direct communication between the abnormal kidney or retroperitoneal space and the pleural space, removal of the hydronephrotic kidney appeared curative.

A 3-year-old spayed female Bengal cat was brought to an emergency clinic because of dyspnea and tachypnea of < 12 hours' duration. Physical examination revealed an increase in respiratory rate and effort and pale mucous membranes. Thoracic radiography revealed bilateral pleural effusion. A CBCa and serum biochemical analysis revealed only a few mild abnormalities, which were not considered clinically important. Thoracocentesis yielded 290 mL of clear fluid. Refractometer reading of the fluid sample indicated a low protein concentration (< 2.0 mg/dL), and no cells were detected via in-house cytologic examination. The cat was given furosemide (1.6 mg/kg [0.7 mg/lb], IM) and cefovecin sodium (8 mg/kg [3.6 mg/lb], SC) and was discharged from the hospital with furosemide (1 mg/kg [0.45 mg/lb], PO, q 12 h) pending response and reevaluation by the primary veterinarian. After thoracocentesis, respiratory rate and effort had improved, and no other abnormal clinical signs had been noted.

Three days later, the cat was brought back to the primary veterinarian for recheck examination. Results of serum biochemical analysis, CBC, and urinalysis were unremarkable, except for a urine specific gravity of 1.014 (isosthenuria). Results of a combination ELISA testb for FeLV antigen and FIV antibody were negative. Echocardiography revealed no cardiac abnormalities, but pleural effusion was noted during this procedure.

Thoracocentesis was performed again, and a small sample of pleural fluid was submitted to a reference laboratoryc for analysis. The sample was straw colored, with a refractometer reading equal to a specific gravity of 1.007 or protein concentration of < 2.0 g/dL; total nucleated cell count was estimated as < 1,000 cells/μL. The fluid was classified as a transudative effusion. Microscopic evaluation of the fluid sample revealed few erythrocytes, and nucleated cells were predominantly small lymphocytes (99%) with the remainder (1%) consisting of neutrophils and large mononuclear cells. Fluid cholesterol concentration was 3 mg/dL (reference range, 82 to 218 mg/dL), and fluid triglycerides concentration was 21 mg/dL (reference range, 20 to 90 mg/dL).

Abdominal ultrasonography revealed hydronephrosis of the right kidney, with most of the renal architecture replaced with anechoic fluid. A diffusely dilated right ureter was also detected as well as a small amount of retroperitoneal fluid.

Twelve days after the initial evaluation at the emergency clinic, the cat was brought to the University of Florida Small Animal Hospital for further evaluation and treatment. Physical examination revealed a mild increase in respiratory effort, unremarkable thoracic auscultation findings, and a markedly enlarged right kidney. All values obtained in a renal-specific serum biochemical analysis were within reference limits. A urine sample was obtained via cystocentesis and submitted for microbial culture; results after 3 days of culture were negative. Thoracic radiography and abdominal ultrasonography were repeated, revealing findings similar to those identified previously, including severe hydronephrosis of the right kidney and hydroureter of the right ureter, with mild perinephric fluid accumulation (Figures 1 and 2). Additional findings included a mild, bilateral cranioventral alveolar pulmonary pattern consistent with atelectasis and a small volume of peritoneal fluid.

Figure 1—
Figure 1—

Sagittal ultrasonographic image of the right kidney of a 3-year-old spayed female Bengal cat. Notice the severe hydronephrosis with almost complete loss of normal tissue architecture. The image was obtained transabdominally with an 8- to 5-MHz broadband microconvex transducer.

Citation: Journal of the American Veterinary Medical Association 251, 1; 10.2460/javma.251.1.80

Figure 2—
Figure 2—

Transverse ultrasonographic image of the same right kidney as in Figure 1. Pockets of perinephric fluid are visible. The image was obtained transabdominally with an 8- to 5-MHz broadband microconvex transducer.

Citation: Journal of the American Veterinary Medical Association 251, 1; 10.2460/javma.251.1.80

Thoracocentesis was performed, yielding 150 mL of clear fluid. Fluid analysis revealed no important changes in fluid characteristics. Results of minimal biochemical testing of a pleural fluid sample included a creatinine concentration of 1.2 mg/dL (serum concentration, 1.4 mg/dL), potassium concentration of 3.5 mEq/L (serum concentration, 4.3 mEq/dL), and triglycerides concentration of 21 mg/dL. A pleural fluid sample was submitted for microbial culture; results after 5 days of culture were negative. No peritoneal or retroperitoneal fluid sample was obtained. Furosemide treatment was discontinued.

Exploratory laparotomy and nephrectomy of the right kidney were performed the following day (13 days after initial evaluation). Laparotomy revealed that the right ureter had a fibrous band and narrowing just cranial to the urinary bladder, and dilation of the ureter ceased at that level. There was no evidence of direct communication between the retroperitoneal space and thoracic cavity on direct visual inspection, but no contrast or other imaging tests were performed to further evaluate this.

Urinalysis performed 1 day after surgery revealed a urine specific gravity of 1.053, a pH of 6.5, a few calcium oxalate crystals, and otherwise unremarkable sediment. The cat recovered uneventfully and was discharged from the hospital 2 days after surgery with buprenorphine for analgesia. Histologic evaluation of the removed kidney and ureter revealed hydronephrosis and severe ureteral distension with no other clinically important abnormalities.

The cat was returned for reevaluation 1 week following surgery. The owner reported that the cat had returned to its normal health status. Findings of physical examination were unremarkable for a patient that had undergone laparotomy and nephrectomy. Thoracic radiography was performed, revealing nearly complete resolution of the pleural effusion and atelectasis. There had been no return of clinical signs and no evidence of return of pleural effusion 17 months after surgery.

Discussion

Several potential causes exist for fluid accumulation in the pleural space. For most fluids classified as pure transudates or protein-poor transudates, the primary mechanism includes a change in the hydrostatic or oncotic gradient between capillaries and interstitial spaces, an increase in permeability of the endothelium or mesothelium, or loss of effective lymphatic drainage.1 Development of protein-poor transudative pleural effusion secondary to a primarily intra-abdominal disease is well described in both human and veterinary medicine, but most cases are related to diseases that alter plasma oncotic pressure, such as liver failure, glomerulonephritis, and protein-losing enteropathies.1–4

Rarely, intra-abdominal diseases independent of low oncotic pressures (eg, renal or perirenal abscesses, urinary tract obstructions, hydronephrosis, acute pyelonephritis, hepatic diseases, or ovarian masses) can cause transudative pleural effusions in humans.5–9 Most cases of transudative pleural effusion secondary to urinary obstruction in humans are suspected to occur secondary to accumulation of urine in the pleural space and generally occur ipsilateral to the ureteral obstruction.10–13 A few reports8,10,14,15 also exist of nonurine transudative pleural effusion in humans secondary to urinary obstructions or hydronephrosis without evidence of cavity communication. The suspected mechanism for fluid accumulation in cases without evidence of cavity communication is impaired drainage of the transdiaphragmatic descending lymphatic vessel. This is suspected to occur because of retroperitoneal pressure or inflammation but is difficult to prove in clinical cases.

In veterinary medicine, a few case reports16–19 exist of urinothorax secondary to trauma or urinary disorders. All those reports confirm the presence of urine in the pleural space and a substantiating fluid-to-blood creatinine concentration ratio. In most patients, a communication between the abdominal and thoracic cavities is identified. A report20 also exists of nonurine transudative pleural effusion secondary to a connection with a perinephric pseudocyst in a cat. Some of the renal disease processes that can result in pleural effusion in humans, such as urinary obstruction, infection, or acute renal failure, have been reported to produce localized extrarenal (retroperitoneal or subcapsular) accumulation of fluid in dogs, and accumulation of perirenal fluid has also been reported (but not characterized) in cats with ureteral obstruction.21–23 Results of thoracic imaging were not reported for any of these patients, and therefore, it is unclear whether any of them may have also had pleural fluid accumulation.

In the cat of the present report, a protein-poor transudative pleural effusion developed that resolved after nephrectomy of a hydronephrotic kidney. To the authors' knowledge, this is the first veterinary report of naturally occurring nonurine transudative pleural effusion secondary to hydronephrosis without evidence of a fistula or nephropleural communication. The most common causes of protein-poor transudative pleural effusion in cats (low capillary oncotic pressure due to hypoalbuminemia and high capillary hydrostatic pressure secondary to cardiac disease) were excluded on the basis of clinicopathologic and echocardiographic findings. Radiographic evaluation failed to identify evidence of any other likely intrathoracic cause of the pleural effusion, although without thoracic CT or contrast imaging techniques such as lymphangiography, small mass lesions or lesions associated with the lymphatics might have been missed. However, given the fairly unremarkable findings of postoperative thoracic radiography and lack of recurrence of fluid accumulation without additional treatment, these other possibilities appeared unlikely explanations for the fluid.

Urinothorax was also excluded as a diagnosis in the cat of the present report on the basis of the results of limited biochemical analysis. Diagnostic criteria to confirm presence of urinothorax include characterization of pleural fluid as a transudate and a fluid-to-blood creatinine concentration ratio > 1.0.5 Other common features of urinothorax effusions include low pleural fluid glucose concentration, low pH (< 7.3), and high lactate dehydrogenase activity11 In case reports10,12,14 of humans with urinothorax, the condition is often diagnosed or excluded on the basis of pleural fluid lactate dehydrogenase activity, glucose concentration, or pH and infrequently confirmed with the fluid-to-blood creatinine concentration ratio. However, no affected patients had a ratio < 1.0. In the cat of the present report, the fluid-to-blood creatinine concentration ratio was 0.85, making urinothorax unlikely.

The effusion in this cat was not classified as chyle because the limited biochemical evaluation revealed a pleural fluid triglycerides concentration less than reported cutoff values (91 or 100 mg/dL, depending on source1,24,25) for differentiating between chylous and nonchylous fluids. Given the predominance of small lymphocytes, it was possible that this finding indicated extravasation of fluid from lymphatic vessels that do not drain the intestines; however, the fluid protein concentration was lower than would be expected for lymph.

In the only previous case report20 of a nonurine transudative pleural effusion secondary to renal or perinephric disease in a cat, a direct connection was identified by scintigraphy between a perinephric pseudocyst and pleural space and was confirmed by laparotomy. Serial ultrasonographic evaluation of the abdomen in that cat had failed to reveal the communication prior to surgery. In reported human cases of nephropleural or nephrobronchial fistulas, the diagnosis of the fistula was often missed on standard radiographic and ultrasonographic evaluations13,26–29; renal angiography, retrograde pyelography, or technetium Tc 99m scintigraphy were used to obtain the diagnosis. Although no scintigraphy or contrast imaging was performed for the cat of the present report, surgical exploration failed to identify communication between the peritoneal or retroperitoneal space and the thorax. Lack of fistula identification and the characteristics of the pleural effusion supported the possibility of an alternative mechanism of effusion accumulation beyond direct communication.

Pleural effusion in the cat had almost completely resolved by 1 week after unilateral nephrectomy and had apparently not redeveloped by 17 months after this procedure. Although we could not be certain that a relationship truly existed between the surgery and resolution of the pleural effusion, the clinical response of the cat was similar to that reported for human cases of nonurine transudative pleural effusion secondary to urinary obstruction after correction of the urinary disease.8–10,14,30 If the pleural fluid accumulation was not secondary to the unilateral hydronephrosis, pleural fluid would likely have reaccumulated after surgery because this was the only new treatment instituted at our hospital for the cat. Although reports exist of spontaneous resolution of pleural effusion, the only reports31–33 involving cats or dogs pertain to idiopathic chylothorax.

When considered in combination with findings in humans with similar diseases and another cat with a perinephric pseudocyst, the present report of nonurine transudative pleural effusion secondary to hydronephrosis in a cat without apparent direct communication between retroperitoneal and pleural spaces emphasizes that certain intra-abdominal, and particularly renal, conditions should be considered as differential diagnoses for pleural effusion in cats when more common disorders are not identified. The pathophysiologic mechanism underlying development of transudative pleural effusion in the cat was unclear, and it would be interesting in future similar cases to use scintigraphy with or without contrast imaging to further elucidate the possible mechanisms. Although the number of reported cases is few, it appears that the positive clinical outcome achieved in the cat was typical of that obtained with nephrectomy, relief of urinary obstruction, or treatment of underlying urinary disease in humans with similar disease.8–10,14,30

Footnotes

a.

IDEXX ProCyte Dx hematology analyzer, IDEXX Laboratories Inc, Westbrook, Me.

b.

IDEXX SNAP FeLV/FIV Combo, IDEXX Laboratories Inc, Westbrook, Me.

c.

ANTECH Diagnostics, Irvine, Calif.

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