Introduction

Pericardial congenital anomalies are rare in dogs and cats. A peritoneopericardial diaphragmatic hernia (PPDH) is the most common of these congenital anomalies and has a prevalence of 0.015% in dogs.¹ In dogs and cats, there is no direct communication after birth between the thoracic and peritoneal cavities; a PPDH is almost always congenital and not related to a trauma in companion animals.^2–4 Conversely, in humans, because the diaphragm forms a part of the pericardial sac, traumatic PPDHs are more frequent than congenital hernias are, although the latter are also encountered in humans.⁵ Abnormal development of the transverse septum, resulting in either a gap in the ventral portion of the diaphragm or an unusually thin ventral diaphragmatic tissue that ruptures, is the most commonly accepted initial cause of this anomaly.⁶ In dogs, an association between a PPDH and other congenital abnormalities is rare and has been reported in the literature in only 11 dogs and two cats.^7–15

Pericardial cystic lesions have been anecdotally reported in dogs and cats as potential congenital abnormalities observed concomitantly with a PPDH.^8–10,14,15 Cysts and cyst-like lesions, also known as “pseudocysts,” are distinct abnormalities and must be differentiated. A “cyst” is defined as a closed sac or capsule containing a liquid or semi-solid substance, lined with endothelium, epithelium, or mesothelium depending on its origin.^14,16 “Pseudocysts” are considered to be cyst-like lesions that lack an epithelial, mesothelial, or endothelial lining. These structures are also referred to as “cystic hematomas” when chronic bleeding is observed in the cyst-like lesion.^9,10,16 Cysts and pseudocysts are commonly confused in descriptions of pericardial cyst-like lesions in the veterinary literature. In humans, true pericardial cysts are rarely described and usually do not cause any clinical signs.¹⁷ In dogs, true pericardial cysts are extremely rare; to our knowledge, they have been reported in only two cases.^9,13 Indeed, most of the pericardial cyst-like lesions diagnosed in dogs are pseudocysts. The association between PPDHs and pericardial pseudocysts remains anecdotally reported in dogs, although it is somewhat more common than the association between PPDHs and pericardial cysts.^9,10,14 This association has also been observed in two cats, in one of which the pseudocyst was observed via computed tomography (CT).^8,15

This case report is the first to present a CT finding of a PPDH associated with a pericardial pseudocyst in a dog. To our knowledge, this is also the first case report describing a cholecystopexy after lobectomy of the right medial lobe and quadrate lobes of the liver in a dog.

Case Report

A healthy 4 mo old spayed female golden retriever weighing 17 kg was referred to a teaching and referral hospital for correction of a PPDH. The referring veterinarian diagnosed a 10-cm long cranial abdominal wall hernia and had attempted to correct it during an elective spaying 6 days earlier. The dog had exhibited no clinical signs since its adoption 2 mo earlier. During the surgery, the veterinarian suspected a PPDH. He also observed abnormal soft tissue structures and adhesions at the level of the abdominal wall hernia. He elected to spay the dog and not to correct the PPDH or resect the abnormal tissues. The abdominal cavity and the cranial abdominal wall hernia were closed.

On presentation, the dog was alert and responsive but mildly lethargic. A 7-cm long, firm, and nonpainful mass was palpable in the cranial abdomen, dorsal to the surgical wound. Muffled cardiac sounds were heard on the right side without any cardiac murmur or arrhythmia. No other abnormality was detected. The results of a complete blood count and blood chemistry tests were unremarkable except for a mild hyperphosphatemia attributed to the young age of the patient. An echocardiographic examination revealed that part of the liver had herniated into the pericardial cavity and the presence of a large fluid-filled structure, suspected to be adherent to the pericardium, causing an incomplete and intermittent collapse of the right atrium, confirming the diagnosis of PPDH. A CT examination was elected to better characterize the fluid-filled structure and the extent of the PPDH. Transverse 1.25-mm images of the thorax and the abdomen were acquired helicoidally^a before and after the intravenous administration of an iodinated contrast medium^b (Figures 1A, B). Communication between the peritoneal cavity and the pericardial sac through a central 4-cm wide defect in the ventral portion of the diaphragm was observed, consistent with a congenital peritoneopericardial hernia. The right medial and quadrate lobes of the liver, as well as the gallbladder, were displaced through the PPDH into a severely dilated pericardial sac. A large L-shaped structure with a multilobular cyst-like appearance occupied the ventral aspect of the right cranial abdomen, displacing the adjacent organs. The cranial portion of this cyst-like structure also protruded into the pericardial sac, medial to the gallbladder. The appearance of the content was suggestive of fluid with a low cell count and/or low protein level (average attenuation of between 8 and 12 Hounsfield units), and no contrast enhancement was noted. A concurrent umbilical hernia with a similar cyst-like component was also visible. A significant amount of iatrogenic free gas and a moderate level of effusion were present in the peritoneal cavity and the pericardial sac. These observations were consistent with an iatrogenic pneumoperitoneum and sterile peritonitis, secondary to the previous laparotomy conducted for spaying (less than 7 days before). The heart was completely shifted to the left by the abnormal pericardial content but appeared otherwise normal. In the cranial mediastinum, the thymus was clearly delineated due to the young age of this patient. Sternal lymphadenomegaly was present, presumably due to lymphatic drainage of the peritoneal effusion via the cranial sternal lymph node, secondary to the previous laparotomy.¹⁷

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A surgery was elected to explore the abdominal cavity and correct the PPDH. During the laparotomy, fibrinous adhesions between some of the abdominal contents and the cranial abdominal wall at the level of the previous surgical incision were observed, which were most likely secondary to the iatrogenic sterile peritonitis caused by the previous laparotomy. An elliptical incision around this area was performed to allow better visualization, which revealed adhesions between the cystic mass and the abdominal wall. An extension of the cystic structure through the PPDH was visually suspected (Figure 1C). Blunt dissection of the peritoneal cystic lesion was initiated, and continuity with a second cystic structure located in the pericardial cavity was confirmed. These cystic structures were subsequently removed from the peritoneal and pericardial cavities after blunt dissection. The cyst-like structure was resected en bloc with the isolated portion of the cranial abdominal wall. Upon gross examination, both cysts were found to be part of a single 17 cm x 8 cm x 7 cm (length x width x height) lobulated cyst-like structure, adherent to the pericardium and the cranial abdominal wall and located in both in the pericardial and peritoneal cavities, communicating through the PPDH. Most of the right medial and quadrate hepatic lobes and the gallbladder had herniated into the pericardial cavity through the PPDH. The central division of the liver and the gallbladder were dissected free of the pericardium and were reduced in the peritoneal cavity. Most of the liver parenchyma of the central division of the liver was dark and indurated and was therefore considered nonviable. In contrast, the gallbladder and the cystic duct appeared healthy and well vascularized. The gallbladder was bluntly dissected from the fossa and the central division of the liver was resected using a thoraco-abdominal stapling device^c. Mild hemorrhage was controlled using two hemoclips^d and a hemostatic sponge^e. A cholecystopexy was then performed on the diaphragm, 5 cm lateral to the right of the linea alba, using four simple interrupted sutures (polydioxanone 4-0^f) (Figure 1D). The PPDH was closed using a simple interrupted suturing pattern (nylon 2-0^g). Before tightening the last interrupted suture, a 10 French red rubber catheter was placed in the pericardial cavity to drain the pneumopericardium. Exploration of the abdominal cavity did not reveal any other abnormality, and, after lavage using warm saline, the linea alba was closed using a simple continuous suturing pattern except for the most cranial 5 cm portion of the incision, which was closed using a simple interrupted suturing pattern^g. Great consideration was given to visualize and appose the external rectus sheath because of its strength-holding nature and to ensure that no fat or portions of the peritoneum were entrapped during suturing. The standard subcutaneous and skin closures were performed. Postoperative recovery was uneventful. The cyst-like structure and the right medial hepatic lobe were submitted for histopathological examination. Three days after the surgery, a defect located in the area of the cranial abdominal wall closure was palpated. A surgical exploration revealed a dehiscence of the cranial abdominal closure, caudal to the most cranial of the simple interrupted sutures and extending more than 5 cm to the umbilicus. Abdominal exploration revealed the intact closure of the PPDH and intact cholecystopexy with a patent cystic duct and extrahepatic biliary tract. Surgical closure of the abdominal wall was performed using only simple interrupted sutures^g. Incorporation and apposition of the external rectus sheath was by far the most important factor for abdominal closure to prevent a second abdominal wall dehiscence. To allow for precise visualization and distinction from the peritoneum, mild dissection of the external rectus sheath was performed at both edges of the abdominal wound and then the rectus sheath was sutured using an appositional suturing pattern. Routine closure of the subcutaneous layer and skin was performed. The dog was discharged 2 days after the second surgery with tramadol (3 mg/kg PO q 8 hr) prescribed for 7 days and amoxicillin-clavulanate^h (12.5 mg/kg PO q 12 hr) prescribed for 2 wk.

Histological analysis revealed that the cyst-like structure was adhered to the skin and the subcutaneous skeletal muscle and was lined with a layer of fibrous stroma and granulation tissue that was up to 1.5 cm thick without identifiable endothelial or mesothelial cells (Figure 2A). A small amount of fibrin was present in the lumen, and the fluid had a low-protein content (24.8 g/L). All of these findings were compatible with a pericardial pseudocyst rather than a pericardial cyst. The architecture of the liver was diffusely effaced by the presence of large numbers of vascular channels of up to 1 mm in diameter and a proliferating biliary epithelium supported by a fibrovascular stroma that extended into and replaced the adjacent hepatocytes completely obliterating the limiting plate (Figure 2B). Rare remnants of hepatic chords and islands of surviving hepatocytes were present. The liver lesion was compatible with a diffuse portal dysplasia with severe hepatic atrophy, most likely due to an ischemic lesion that had destroyed the hepatic parenchyma and caused proliferation of the connective tissue and the biliary epithelium in the portal tracts.

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Two months later, the dog was presented for a follow-up evaluation. The dog was functioning very well and did not show any clinical signs. Upon palpation, the abdominal wall appeared to be normal. The owners reported that the dog had a much higher activity level than before the surgical correction of the hernia and that they did not realize how lethargic the dog had been before surgery. The biochemical results were within the normal ranges except for a mild hyperphosphatemia, which was considered normal for a dog of such a young age. Abdominal ultrasonography showed that the gallbladder was still attached to the diaphragm and was patent. A follow-up phone call with the owner 1 yr postoperatively revealed that the dog was acting completely normally and did not show any clinical signs or consequences related to the affection or the surgical intervention.

Discussion

A PPDH associated with a pericardial pseudocyst is rare in dogs. To our knowledge, this is the first report of a CT description of this condition as well as the first clinical report of a cholecystopexy in a dog after resection of the central division of the liver. In dogs, a PPDH has been associated with other congenital abnormalities, such as concurrent umbilical hernias, cranial abdominal wall defect, sternal deformities, congenital heart diseases, and chylothorax, and it has also been associated with several liver abnormalities in cats.^3,6–12 Pericardial pseudocysts are rare and they have already been associated with a PPDH.^{8–10,13–15} These structures can also be reported as cystic hematomas. The clinical signs of pericardial pseudocysts are related to compression of the cardiac chambers and impaired cardiac filling in dogs younger than 3 or 4 yr of age.^9,14 The etiopathogenesis of pericardial pseudocysts in small animals is uncertain, but these lesions are almost always connected to an intraabdominal fatty pedicle, which could have entered the pericardial cavity through a small PPDH or could have been a vestigial remnant and are often adherent to the apex of the pericardium,.^9,14 This phenomenon suggests that a pericardial pseudocyst could be the result of entrapment of the omentum or the falciform ligament in the pericardial sac through a PPDH during development and thus would not be a true cyst.^1,9 Moreover, histopathological examinations have revealed that cyst-like structures are generally lined with a layer of fibrous stroma and granulation tissue without identifiable endothelial or mesothelial cells.^9,10,14 Therefore, almost all of the pericardial cystic structures that have been described should be considered pseudocysts or cystic hematomas rather than true congenital pericardial cysts. Pericardial cysts and pseudocysts have a different pathogenesis and must be clearly differentiated.^9,10,14 Four types of true congenital pericardial cysts have been described in humans, including coelomic, lymphadenomatous, bronchial, and teratomatous cysts.^9,14 Histologically, the wall of these cysts is lined with mesothelial or endothelial cells.⁹ The true pericardial cysts that are typically observed in humans are not attached to the pericardium by abnormal fatty tissue or a sternopericardial ligament, which has also been reported for a pericardial cyst in one dog.⁹ Pericardial cysts are very rare in dogs, and the majority of pericardial cystic structures are most likely pseudocysts or cystic hematomas.⁹ There are only two reports of a true coelomic pericardial cyst in dogs. The reports described a thin-walled unilocular cyst surrounding a cavity filled with liquid, with a wall composed of mesothelial cells overlaid by a fibrous connective-tissue stroma. Anomalous development of the pericardial mesoderm was proposed to explain the development of the two pericardial cysts reported.^9,13 The case presented here concerned a pseudocyst, characterized by a fibrous wall lacking a lining of mesothelial cells. This case demonstrated that the denomination of a pericardial “cyst” in various previous reports was partially inappropriate and that these structures would be better described as “pericardial pseudocysts” or “pericardial cystic hematomas” because their histological features are more compatible with granulation tissue than real endothelium, and they are almost always associated with a patent or closed PPDH.

In the case presented here, the cyst-like structure was thin-walled and multilobulated, measuring 17 cm x 8 cm x 7 cm and containing 500 mL of a transparent fluid (a transudate with 24.8 g/L of proteins), attached to a small amount of subcutaneous connective tissue. The gross characteristics of this cystic structure were similar to those of a congenital lymphangiomatous cyst in humans and were not similar to a cystic hematoma.⁹ However, histopathological examination of this cystic lesion showed that it was surrounded by granulation tissue and not by an endothelium as a pericardial cyst should be. These observations led us to conclude that despite the gross characteristics of a pericardial cyst (thin wall and transparent fluid), this structure was most likely a pseudocyst in the early phase of formation caused by tissue strangulation through the PPDH, in which the definitive characteristics of a cystic hematoma were not present at the time of diagnosis because of the young age of the patient. We hypothesize that this lesion would have evolved into a cystic hematoma. The fluid in a pseudocyst is initially translucid secondary to vascular obstruction of the herniated omentum or falciform ligament through the PPDH. Intrapseudocyst hemorrhaging due to repeated trauma from heart beats will induce the formation of a hematoma and thus bloody fluid, as reported in previous case series.^9,14

In humans, pericardial cystic lesions are diagnosed using CT, transthoracic and transoesophageal ultrasonography, or MRI.¹⁸ In dogs, the diagnosis of PPDH and pericardial pseudocyst is generally reached using thoracic radiology or cardiac ultrasonography.^9,14 However, identifying the herniated organs and assessing a pericardial pseudocyst using these imaging modalities can be difficult. Recently, CT was used in a cat to better characterize the evolution of a pericardial cystic structure that developed after a PPDH repair.¹⁵ In our dog, cardiac ultrasonography allowed the detection of a fluid-filled structure adherent to the epicardium as well as some portion of the liver, helping to confirm the diagnosis of PPDH. However, it was difficult to make a precise description of the fluid-filled structure using this technique, the appearance of which was most compatible with the gallbladder (some parts of the liver were herniated), a cystic structure, or the stomach. Additionally, the extension of this mass could not be adequately assessed using this technique. Considering the preoperative planning, CT allowed a better evaluation of the extent of the lesion, the herniated organs, and the size of the hernia ring and was diagnostic for the pericardial pseudo-cyst.

To our knowledge, this is the first case report describing a cholecystopexy in a dog that required hepatic central division resection. The gross aspect of the parenchyma led to the intraoperative decision to resect these lobes. The surgeon elected to preserve the gallbladder due to its viability, the patency of the cystic duct, and the age of the dog. Because the gallbladder is located between the right medial lobe and the quadrate lobe of the liver, it was necessary to release the gallbladder from the gallbladder fossa before resecting the central division of the liver. Thus, the gallbladder would not have had any support after the lobectomy, and the decision to perform a cholecystopexy was reached. The literature contains a few reports of cholecystopexy in humans, and this technique has been performed experimentally in small animals.^19–23 To our knowledge, this is the first report of a cholecystopexy in a clinical case involving a small animal. In a paper describing liver lobectomy techniques for dogs, Covey suggested attaching the gallbladder to the diaphragm or to the left medial liver lobe with two interrupted sutures to prevent its volvulus when removing the central division of the liver.²¹ However, that study was conducted using cadavers. The attachment between the right medial lobe and the quadrate lobe of the liver, which form the gallbladder fossa, is substantial, making it more technically demanding to perform the lobectomy of the right medial lobe.²¹ Other authors have recommended performing a cholecystectomy after the complete resection of the central division of the liver.²³ The histological examination revealed severe hepatic atrophy and dilatation of the sinusoids. As a potential complication, vascular and lymphatic congestion leading to fluid retention could result in the formation of a cyst, which, concurrently with hepatic parenchyma atrophy, could predispose the patient to recurrent liver infections.^8,12 It is possible that reducing the herniated lobes would decrease the risk of cyst formation. However, a liver lobectomy was elected based on the gross aspects of the liver (dark and indurated). During the revision surgery, 3 days after the correction of the PPDH, the cholecystopexy was found to be intact, and the patency of the cystic duct and extrahepatic biliary tract was confirmed. At follow-up, an abdominal ultrasonography and biochemical profile were obtained, and no signs of cholestasis were observed. A telephone interview 1 yr later revealed that the dog was entirely normal and did not exhibit any clinical signs related to the disease or to the cholecystopexy. In our opinion, a cholecystopexy appears to be a valuable procedure when the central division of the liver is removed because it limits the risk associated with a freely movable gallbladder, such as gallbladder volvulus, secondary obstruction and necrosis, or gallbladder herniation.^20,21

Conclusion

This case report describes an unusual lesion associated with PPDH in a dog, a pericardial pseudocyst. Pericardial pseudocysts should be differentiated from pericardial cysts because these lesions have a different pathogenesis. Surgical planning is an important factor in the treatment of PPDH, and the selection of CT as the diagnostic imaging technique appears to be appropriate. In this case, cholecystopexy to the diaphragm proved to be a safe, functional, and effective technique for stabilizing the gallbladder after the hepatic central division lobectomy to prevent volvulus of the gallbladder.