Soft tissue sarcoma at the site of a previous laparoscopic-assisted gastropexy in a dog

Abstract

An 8-year-old, spayed female, Doberman pinscher dog was presented to the Ontario Veterinary College Health Sciences Center for evaluation of a large subcutaneous mass on the right cranial ventral abdomen. Computed tomography localized a 6 × 7 cm soft tissue mass to the site of a laparoscopic-assisted gastropexy performed 3 years earlier. Body wall resection with wide surgical margins was performed. Histological evaluation identified the mass as a grade III soft tissue sarcoma with clean surgical margins. To the authors’ knowledge, this report is the first to detail a case of a soft tissue sarcoma that is suspected to have originated at and/or infiltrated into tissues that were previously incised during a surgical procedure.

Key clinical message:

Based on this case, there is a possibility of a clinical correlate to the feline injection site sarcoma in the canine species.

Introduction

Soft tissue sarcomas are mesenchymal cell tumors which represent approximately 15% of all cutaneous and subcutaneous tumors in dogs (1). They most often occur in middle-aged and older dogs with large breed dogs being overrepresented (2). The term soft tissue sarcoma is a broad term which represents tumors of many soft tissues including fibrosarcoma, peripheral nerve sheath tumor, liposarcoma, myxosarcoma, malignant mesenchymoma, leiomyosarcoma, rhabdomyosarcoma, synovial cell sarcoma, and lymphangiosarcoma (1). Although histologically each type appears relatively distinct, the behavior of these tumors as a whole is often similar as they are locally invasive with a rate of metastasis up to 40%, which is positively correlated with histologic grade (2,3). Diagnosis of a soft tissue sarcoma is best done with histology since mesenchymal cells do not exfoliate well; however, spindle cells identified on cytology from fine-needle aspirate that lack differentiating features such as osteoid or chondroid matrix, can suggest a soft tissue sarcoma (3). Histological evaluation is necessary to confirm the diagnosis of soft tissue sarcoma and provide the grade that is needed for prognosis and for planning adjuvant therapy (1). The cure rate of soft tissue sarcoma with chemotherapy or radiation therapy alone is poor and surgical resection with wide margins gives the best chances of survival (2). Marginal resection has higher rates of recurrence, with grade III marginally resected soft tissue sarcoma recurring ~75% of the time (3). If margins are not clean on histological evaluation of the mass, radiation therapy or re-excision are commonly recommended since radiation therapy is most effective on microscopic disease rather than when gross tumor tissue is present (1). Since resection is the best treatment option for these tumors, diagnostic imaging is paramount to planning and for assessing the degree of local invasion and/or metastasis.

For most soft tissue sarcoma cases, the etiology is not often identified and the overall pathway of tumorigenesis remains unclear (3). There have been reports of soft tissue sarcoma associated with foreign bodies, trauma, implants, and parasitic infections (1).

Case description

An 8-year-old, 33.5 kg, spayed female, Doberman pinscher was presented to the referring veterinarian for a large subcutaneous mass on the right cranial ventral abdomen. The mass corresponded to the site of a laparoscopic-assisted gastropexy performed 3 y before presentation. An abdominal ultrasound examination was performed which localized the mass to the subcutaneous tissues with suspected invasion of deeper tissues. The mass was solid with minimal vascularity, and no lymph-adenopathy was noted. An incisional biopsy and histology revealed a grade II soft tissue sarcoma with a mitotic index of 14 figures/10 high power fields (HPF).

The dog was referred to the Ontario Veterinary College Health Sciences Centre (OVCHSC) for further evaluation. At the time of presentation to OVCHSC the owner noted that the mass had grown 10 times its size since initial appearance with 1/3 of this growth occurring during the previous week. The soft tissue sarcoma was 7 × 6 × 6 cm and located in the subcutaneous tissues at the level of the right third mammary gland and extending laterally from the midline. The mass was firmly attached to the underlying tissues with a 1-cm scar in the superficial tissues from the previous incisional biopsy. The dog was eating and drinking normally with no other signs of illness. Upon physical examination, all vital signs were within normal limits. Surgical resection with wide margins was planned with curative intent. Prior to surgical removal, staging and planning were scheduled the following week with a computed tomography (CT) scan of the abdomen and thorax.

The dog underwent routine general anesthesia for CT of the thorax and abdomen (16 slice detector, GE Lightspeed; GE Healthcare, Milwaukee, Wisconsin, USA). Imaging parameters were 0.625 mm slice thickness, 50 cm field of view, helical mode, 1 s rotation time, 120 kV, and 220 mA. Iodinated contrast medium was administered (Iopamidol 300 mgI/mL, Isovue; Bracco Imaging Canada, Anjou, Quebec) at 2 mL/kg body weight, IV, for a post-contrast abdomen scan. The thoracic CT was unremarkable with no evidence of pulmonary nodules. The abdominal scan revealed a large soft tissue dense mass centered on the right rectus abdominus muscle, at the level of the right cranial abdominal mammary gland (Figure 1). The mass was isodense (56 HU) to the adjacent rectus abdominus muscle with a few small central hypodense (26 HU) regions. There was moderate peripheral contrast enhancement (106 HU) of the mass, slightly less than the gastric wall (133 HU), with minimal (61 HU) central contrast enhancement. The few small central hypodense regions noted pre-contrast did not contrast-enhance, consistent with necrosis. The mass extended ventrally into the subcutaneous tissues, and dorsally into the wall of the pyloric antrum at the site of a previous laparoscopic-assisted gastropexy. The mass abutted the mucosa of the stomach but did not extend through it and did not extend into the peritoneal cavity. The mass was approximately 5.8 × 6.6 × 5.8 cm, with the portion of the mass invading the gastric wall being approximately 2.5 cm in diameter. The right inguinal lymph node was mildly enlarged (8.7 mm thick) compared to the left inguinal lymph node (2.8 mm).

Figure 1.

Multiplanar reconstructed CT images of the body wall mass including sagittal plane (A), transverse plane (B), and dorsal plane (C). The large soft tissue dense mass (*) is centered on the right rectus abdominus muscle and extends ventrally into the subcutaneous tissues, and dorsally into the stomach (white arrows) through the previous gastropexy site, without perforating the mucosal layer of the pyloric antrum, seen best on B and C. A bolus is applied to the skin for radiation therapy planning, seen on all images.

Body wall resection, required for surgical resection of the mass, was performed 6 d after the CT scan (Figures 2A, B). The body wall mass was resected with 3 cm margins which required distal ostectomy of 4 ribs and a partial gastrectomy at the site of the gastropexy, and resulted in a large body wall defect (Figure 2C). A thoracic drainage catheter (MILA thoracic drainage catheter; MILA International, Florence, Kentucky, USA) was placed in the thorax and a closed suction drain was placed in the abdomen before closure of the surgical site. Two layers of polypropylene mesh (Bard Mesh; C.R Bard, Queensbury, New York, USA) were used to cover the defect and sutured in place using 2-0 Prolene (Ethicon, Sommerville, New Jersey, USA) suture in multiple simple continuous patterns (Figure 2D).

Figure 2.

Intraoperative images of the body wall mass resection, gastrectomy, and closure. A — pre-operative image of the ventral abdominal body wall revealing a large subcutaneous mass (arrow) at the level of the right cranial abdominal mammary gland. B — Surgical excision of the mass (arrow) that can be seen through the peritoneum, with pyloric antrum attached to the body wall (arrowhead) at the previous gastropexy site. C — Large defect in the body wall following mass removal and partial rib resection. The gastrectomy site is also seen in C (arrow). D — Closure of the body wall defect using a polypropylene mesh (*) sutured to the body wall, before skin closure.

The mass was submitted for histopathological evaluation. Gross examination of the sample revealed a 6 × 6 × 7 cm ovoid mass. The total sample measured 12 cm long, 9 cm wide, and 6 cm deep from skin surface to stomach. On cut section the mass was solid and firm with several 1 to 5 mm multifocal areas of necrosis that affected less than 5% of the tissue. The mass was focally invasive into the skeletal muscle and gastric wall. Upon histological examination of the sections, the mass was located largely within the subcutaneous tissue with focal extension into the skeletal muscle, body wall, and tunica muscularis of the stomach (Figure 3). The mass was well-demarcated and partially encapsulated, composed of mesenchymal cells intermixed with eosinophilic collagen bundles. There were several small aggregates of lymphocytes at the periphery of the tumor and a small number of individual intermixed lymphocytes. There was 4-fold anisocytosis and anisokaryosis, small foci of necrosis, and a mitotic index of 22 cells/10 HPF. A diagnosis of soft tissue sarcoma was made. The mass appeared to have originated in the subcutaneous tissue with focal invasion through the body wall at the site of the gastropexy and into the tunica muscularis of the stomach. A grade of III was assigned to the soft tissue sarcoma in accordance with the Dennis et al (4) grading scheme. The possibility of an inflammatory or scar-origin for the soft tissue sarcoma was considered in this case due to the location of the soft tissue sarcoma and the specificity as to which tissues were invaded during growth, given the history of laparoscopic-assisted gastropexy.

Figure 3.

A soft tissue sarcoma originating in the subcutis of the ventral abdomen at the site of a prior gastropexy invades the adhesion and stomach wall. A — Neoplastic cells consist of sheets and streams of spindle cells, with multifocal areas of necrosis (arrow). B — Foci of lymphocytes are present at the periphery of the neoplastic tissue (arrow). C — There are frequent mitotic figures (arrows) in the mass. D — Neoplastic cells invade the tunica muscularis of the stomach but do not extend past the submucosa (N — Neoplasm; M — Gastric mucosa; SM — Submucosa).

The dog recovered well from surgery and was discharged 3 d after surgery. At the time of suture removal, 14 d after surgery, multiple small subcutaneous masses were observed at the right flank and shoulder. These were marginally excised the following day and were also consistent with a grade III soft tissue sarcoma. At the time of recheck 1 mo after surgery, restaging of the dog’s thorax was performed and radiographs revealed multifocal pulmonary nodules consistent with metastatic disease. At the time of submission of the manuscript 7 mo after surgery, the dog was clinically doing well.

Discussion

The etiology of many soft tissue sarcomas is unclear and they primarily arise spontaneously, similar to many other neoplasms (3,5). As outlined by Okada et al (6), there are at least 5 etiologies of neoplasia. These include spontaneous replication errors, carcinogenic substance exposure, genotoxic substance exposure, radiation exposure, and viral oncogene activation. An additional factor that should be included in this list is the role of inflammation and wound healing in tumorigenesis (6). It was discovered as early as 1940 in human medicine that healing and scar formation preceded the development of certain cancers (6). This was initially discovered in lung cancer in humans, in whom cancer had formed around a scar, and was subsequently named scar cancer (6). Furthermore, gastrointestinal tumor recurrence after resection was most often found at the site of the previous anastomosis along the incision, which further corroborates the role of inflammation in the development of some cancers (6). Desmoid tumors, lipomas, and lymphoma have also been linked to patients with previous trauma such as car accidents (7). Interestingly, the composition of the fibrous tissue formed in healing is different in tumor-associated fibrosis than fibrosis not associated with tumors, in that tumor-associated fibrosis is largely mediated by collagen type III, as opposed to types I and IV that are normally observed (6).

An association of inflammation with cancer has also been made in animals (8). The most largely described inflammation-induced soft tissue sarcoma is the feline injection site sarcoma (FISS) (9). Thought to be linked to the feline leukemia virus (FeLV) and rabies vaccinations, or vaccinations with aluminum adjuvants, FISS occurs in 2.1/10 000 cats in the United States (5). Various terms have been used to describe neoplasms at sites of prior inflammation/healing which include, injection-site sarcoma, inflammatory sarcoma, scar tissue sarcoma, and foreign-body sarcoma (6). Although the inflammatory stimuli among these differ, the same underlying inflammatory pathway is common among them. The basic pathway of inflammation begins with proliferation and cellular infiltration, followed by fibrosis (5). As stated before, the collagen type that makes up the fibrous tissue is different with tumor-associated fibrosis, which localizes the transformation from inflammation to neoplasia during the healing process (6).

Vascellari et al (10) conducted a comparative study in dogs contrasting the histology of injection site sarcomas to spontaneous sarcomas and identified a few key differences. Primarily, most injection site sarcomas in dogs were high grade and all showed lymphocytic infiltration largely at the periphery of the tumor. Contrasting this, dogs with spontaneous sarcomas showed perivascular infiltrate within the tumor but no inflammatory infiltrate around it. Furthermore, the histology of a feline injection site sarcoma was found to be more similar to the dog’s inflammation-induced sarcoma, than other sarcomas in dogs (11). For this reason, it is proposed that the mechanisms of injection/inflammation-induced sarcomas are distinct from those of other etiologies.

The pathway of inflammatory sarcomagenesis has been shown in dogs to a lesser degree since injection-site sarcomas in dogs appear to be less common than in cats (8). Although a surgically induced sarcoma has not been reported, there are a few reports of microchip-induced sarcomas in dogs (12). Prior to these cases, this had only been demonstrated in laboratory rats (13). Additionally, in rats, bioglass, dye, and plastic implants have all been associated with tumor formation (5). Perhaps the closest related event to this case would be 1 case of a cat which developed a soft tissue sarcoma around the site of deep non-absorbable suture (14). This dog’s sarcoma follows many of the behaviors seen in inflammatory sarcomas. Firstly, it is a high-grade soft tissue sarcoma; secondly, there is lymphocytic infiltrate at the periphery of the neoplasm rather than perivascularly, as one would expect in a spontaneous sarcoma. During a laparoscopic-assisted gastropexy, only the seromuscular layer of the stomach is incised (15). At the body wall, an incision is made through the skin, subcutaneous, and abdominal muscle layers (15). This incision is used to briefly exteriorize the pyloric antrum before suturing the seromuscular layer of the stomach to the transversus abdominus muscle layer of the body wall (15). The technique used in this surgery is important to this case since it correlates identically with the tissues invaded by the soft tissue sarcoma which developed 3 y later. On histological evaluation, it was confirmed that the tumor stopped at the tunica muscularis of the stomach, and invaded the body wall into the subcutaneous tissue. For these reasons, it is highly suggestive that the gastropexy healing process played some role in the formation of this dog’s soft tissue sarcoma.

The relationship between inflammation and sarcomagenesis is still largely unknown; however, as more cases appear, the causal relationship becomes stronger (3). It is important to understand the risks of tumor formation and monitor patients, particularly those which have a previous history or predisposition to neoplasia. Regular monitoring of the surgery site in the years after surgery may help with early identification of soft tissue sarcoma and increase the likelihood of successful wide margin resection. The management of soft tissue sarcomas is dependent on the degree of growth and invasion at the time of presentation, since the ability for wide margins dictates the likelihood of recurrence or the need for adjunct radiation therapy (2). With increased monitoring at the site in the years after surgery, more cases may be detected and treated successfully. CVJ