A rare case of solitary intrahepatic splenosis following splenectomy in a dog

Abstract

A 9-year-old spayed female mixed breed dog weighing 6.8 kg with a history of previous splenectomy for hemangiosarcoma 4 years earlier was referred for a hepatic mass lesion. Although the dog did not have a clinical sign, a computed tomography revealed a solitary mass in the left medial lobe of the liver. Spleen-like tissue was observed on needle core biopsy of the mass, leading to the diagnosis of intrahepatic splenosis. Therefore, hepatic lobectomy of the left medial lobe of the liver was performed. Histopathological evaluation of the excised tumor confirmed the diagnosis of intrahepatic splenosis. No further development of splenosis was detected on CT performed 217 days after the surgery. The dog died of suspected aspiration pneumonia without any event or clinical signs related to intrahepatic splenosis on postoperative 272 days. The cause of the intrahepatic splenosis observed in this dog was unknown; however, hematogeneous dissemination and autoimplantation of splenic tissue via the portal venous flow was speculated. This case shows the utility of needle core biopsy for the preoperative diagnosis of splenosis. The intrahepatic splenosis in this case was considered to have developed as a long-term sequelae after splenectomy, as in humans.

Splenosis is defined as the autoimplantation of splenic tissue to various other tissues following splenectomy, abdominal trauma, or splenic rupture [5]. Splenosis results from the autotransplantation and seeding of splenic tissue, secondary to splenectomy or traumatic splenic rupture [13]. Two mechanisms developing splenosis are indicated. One is that splenic implants are spread throughout peritoneal cavity or serosal surfaces of abdominal viscera [13]. Another developmental mechanism is that splenic tissue seeded through the splenic vein to the portal vein [8]. In humans, splenosis reportedly occurs in a variety of tissues, such as the serosal surface of the small or large bowel, peritoneum and mesentery, although it only rarely occurs in the liver [9]. Splenosis in dogs is reportedly very rare, with only a few previous reports [8, 10,11,12,13]. Contrast enhanced ultrasonography, computed tomography (CT) or magnetic resonance imaging are used to diagnose splenosis [1, 4, 15]. While ultrasonography is used to confirm the diagnosis of splenosis in humans, there are no definitive diagnostic methods in dogs. Thus, none of the previously reported cases of splenosis in dogs were diagnosed preoperatively [8, 10,11,12,13]. Although there are no reports about the prognosis of splenosis in humans, it does not seem to be poor. However, since four of the six dogs reported with splenosis were euthanized or died and the other dog only survived for a short period, the short-term prognosis of splenosis in dogs is expected to depend on the site of splenosis [8, 10,11,12,13]. This is the first report regarding the preoperative diagnosis of intrahepatic splenosis that was surgically resected. This report describes the post-surgical follow-up of a dog with intrahepatic splenosis.

A 9-year-old spayed female mixed breed dog weighing 6.8 kg was referred to Yamaguchi University Animal Medical Center for detailed examination of a liver mass (on day 1). The dog had undergone splenectomy for splenic hemangiosarcoma 4 years earlier at the referring veterinary hospital, at which time there was no evidence of splenic rupture. Since the resected spleen had been diagnosed with hemangiosarcoma accompanying hematoma on histopathological examination, she had received the anticancer drug, doxorubicin, postoperatively. The client had recognized no obvious symptoms before the dog’s current presentation, although a liver mass with a mixed echo pattern in the left medial lobe (approximately 3 cm) had been found on ultrasonography examination at the referring veterinary hospital 10 days prior to the first visit to Yamaguchi University Animal Medical Center. Physical examination revealed no abnormalities, although blood tests revealed hyperammonemia (95 µg/dL), but with normal hepatic enzyme levels. Prothrombin time and activated partial thromboplastin time was within normal limits (5.4 sec and 13.6 sec). Ultrasonography showed an approximately 4 cm mass with a mixed echogenic pattern in the left medial lobe of the liver (Fig. 1A). This tumor was approximately 4 cm in diameter. Blood flow to the mass was not abundant (Fig. 1B). Thoracic and abdominal radiographs revealed no metastasis to the thorax or abdomen. Since the dog had a history of hemangiosarcoma, the mass was considered to be possible metastasis of hemangiosarcoma. If the mass was metastasis of hemangiosarcoma, hemorrhage risk by biopsy was considered high. However, because blood flow in the mass was not abundant on ultrasonography and the coagulation times was normal, the risk of hemorrhage was judged low. For a definitive diagnosis, CT and biopsy of the mass were performed under general anesthesia. CT revealed a polycystic mass in the left medial lobe of the liver, with no metastasis or abnormalities in other tissues. Iopamidol (Iopamidol 370, Fuji Pharma Co., Tokyo, Japan) was used as contrast medium and was administered at a dose of 1.5 mL/kg (555 mg iodine/kg) via the cephalic vein. The injection time was fixed at 10 sec. The arterial phase (15 sec after the start of the injection), the portal venous phase (40 sec after the start of the injection), and the delay phase (120 sec after the start of the injection) scans were performed. Contrast-enhanced CT showed a slightly enhanced effect of the mass in the portal vein phase as compared to the arterial phase (Fig. 2). The biopsy of the mass was performed by needle core biopsy (TEMNO Evolution^® Biopsy Device, 14G, 11 cm, Merit Medical Japan, Tokyo, Japan). No adverse event such as intraabdominal hemorrhage was observed after the biopsy procedure.

Fig. 1.

Abdominal ultrasonography on day 1. A. A mass with mixed echo pattern (arrow) was observed in the left medial lobe of the liver on ultrasonography. B. Blood flow in the mass was not abundant.

Fig. 2.

Computed tomography on day 1. A. A polycystic mass (arrow) was observed in the left medial lobe of the liver. B. Arterial phase. C. Portal vein phase.

Histopathological evaluation of the biopsy specimen revealed that the mass was consisted with spleen-like tissue (Fig. 3A), associated with hematoma (Fig. 3B). Based on the history of splenectomy and histopathological findings, intrahepatic splenosis was diagnosed. Hepatic lobectomy was planned in order to prevent the ruptured of the mass.

Fig. 3.

Pathological evaluation of the biopsy specimen of the mass in the left medial liver lobe. A. The mass shows spleen-like tissue composed of the white pulp (lymphoid follicles) and the red pulp (sinusoidal structures containing blood) (H&E stain, Bar=100 μm). B. The mass lesion contains hematoma, with a lot of hemorrhagic blood and less mesenchymal tissue. Hemosiderin-laden macrophages are scattered (arrows) (H&E stain, Bar=50 μm).

Seven days after the first visit, hepatic lobectomy of the left medial lobe of the liver was successfully performed (Fig. 4). Although other parts of liver and other parts of abdomen was examined grossly at the time of surgery, other lesions were not observed. The dog was discharged on day14, following an uneventful recovery. Postoperatively, the excised mass was fixed in 10% formalin for histopathological examination. Evaluation showed that the mass had a spleen-like tissue, with the white and red pulps (Fig. 5A). Hemosiderin-laden macrophages were scattered suggesting hemorrhage in the mass (Fig. 5B). No tumor was found in the left medial lobe of the liver. Based on these results, the mass was diagnosed as intrahepatic splenosis. CT performed on days 50 and 217 showed no new mass in the thorax or abdomen, and the results of blood tests were also normal. The dog continued to be asymptomatic until the day 279, when the dog died of aspiration pneumonia at the referring veterinary hospital.

Fig. 4.

Intraoperative findings. The mass (dashed line) was observed in the left medial lobe of the liver.

Fig. 5.

Histopathological evaluation of the resected specimen. A. Adjacent to the liver tissue (arrowhead), a mass lesion showing spleen-like tissue are present. Arrows indicate the white pulp (H&E stain, Bar=200 μm). B. The red pulp in the mass lesion contains hemosiderin-laden macrophages (arrows) (H&E stain, Bar=25 μm).

In humans with intrahepatic splenosis, since 95% of the patients had a history of splenectomy and 67% had a history of a ruptured spleen, splenectomy and ruptured spleen are considered to be risk factors for splenosis [5, 14]. In the previous reports of splenosis in dogs, four of the seven dogs had a history of both ruptured spleen and splenectomy, two had no history of either, and the history was not described in the seventh case [8, 10,11,12,13]. The dog in the present report had a history of splenectomy without splenic rupture. Although the number of cases is very small, since four of the seven dogs with splenosis had a history of ruptured spleen and splenectomy [8, 10,11,12,13], it is suggested that splenectomy and ruptured spleen are also related to splenosis in dogs, as in humans. Since the white and red pulps were observed in the left medial lobe of the liver by histopathology, this case was diagnosed as an intrahepatic splenosis. Previous report was presumed that traumatic splenic ruptured tissue seeded to the liver with splenic tissue through the splenic vein to the gastrosplenic vein and into the portal vein [8]. In this case without ruptured spleen, intrahepatic splenosis may have been caused by splenic tissue entering the splenic vein and passing into the portal vein, not by seeding ruptured spleen. Therefore, when a hepatic mass is observed in a dog with a history of splenectomy and ruptured spleen, intrahepatic splenosis should be included in the differential diagnosis.

Previous studies of splenosis in dogs only described their short- and medium-term follow up, and none of the previous cases were followed up for the long term as in the present case [10, 11, 13]. The prognosis is likely to be poor in cases of disseminated splenosis [8, 12, 13]. Previous cases that underwent complete excision of seeded splenosis showed only short- to medium-term survival [10, 13]. In addition to being a solitary intrahepatic splenosis, our case underwent complete resection, and experienced a long-term survival than other cases without any clinical signs. This case suggests that the prognosis of splenosis depends on the site of occurrence and solitary intrahepatic splenosis, and might be good in cases of complete resection.

Splenosis is an uncommon disease even in humans, and is diagnosed preoperatively by various examinations [1, 2, 4, 15]. However, the methods of effective preoperative diagnosis in dogs have not been indicated. In a previous report, it was not possible to definitively diagnose intrahepatic splenosis by fine needle aspiration [10]. Preoperative diagnosis of an ectopic spleen is difficult, and the definitive diagnosis is generally made using postoperative histopathology [6]. This could also be the case for splenosis. In addition to no complication such as hemorrhage by needle core biopsy, the dog in the present case was diagnosed with intrahepatic splenosis by preoperative histopathological evaluation of needle core biopsy. It is the first report in a dog that needle core biopsy can be preoperatively diagnosed. Our experience suggests that needle core biopsy might be possible to be useful to definitive diagnosis for intrahepatic splenosis when the dog has coagulation system within normal limits and no abundant blood flow in intrahepatic splenosis. Thus, if needle core biopsy is possible, it should be performed to definitive diagnosis of intrahepatic splenosis.

Although Kutara et al. reported the case of a dog with splenosis in whom contrast-enhanced CT showed enhanced effect in the arterial phase [10], our dog showed a slightly enhanced effect in the portal vein phase. This difference suggests that it might be difficult to diagnose intrahepatic splenosis by contrast-enhanced CT. Although that study by Kutara et al. used a 16-slice multidetector CT scanner, we had access to a 64-slice multidetector CT scanner [10]. The dose of Iopamidol used in our patient was also lower than previously reported [10]. These differences may have contributed to the disparity in the results of contrast-enhanced CT.

In humans, splenosis reportedly develops a long time after splenectomy [3, 7]. One of the dogs in a previous report developed intrahepatic splenosis 5 years after splenectomy [12]. The dog in the present case developed intrahepatic splenosis 4 years after splenectomy. This suggests that intrahepatic splenosis in dogs likely develops as a long-term sequelae of splenectomy, as in humans.

In conclusion, splenosis in dogs is very rare, and cases of intrahepatic splenosis in the absence of a ruptured spleen may result from seeding through the splenic vein into the portal vein. The prognosis of solitary intrahepatic splenosis may be good in cases of complete resection. The dog in this report represents the first case of preoperative diagnosis of this condition. Additionally, needle core biopsy is useful for confirming the diagnosis of splenosis. This case suggests that splenosis might develop in the long term after splenectomy in dogs, as in humans.

CONFLICT OF INTEREST

The authors declare no potential conflicts of interest with respect to the research, authorship, and publication of this article.