Cervical Expanding Hematomas in Dogs: Five Cases

Introduction

Hematoma is defined as a localized collection of blood, usually clotted, in an organ, space, or tissue, due to a break in the wall of a blood vessel.¹ A hematoma’s size usually stabilizes quickly by equalization of intravascular and extravascular (i.e., tissue) pressures before it spontaneously resorbs, leaving a persistent, fibrous scar.² In some instances, as sometimes described in humans, hematoma formation is followed by slow expansion of the encapsulated mass.³⁴ To the authors’ knowledge, expanding subcutaneous, encapsulated hematomas other than aural hematomas have not been described in the veterinary literature. The present report describes five cases of subcutaneous cervical hematomas.

Case Reports

Five dogs were presented to the Alfort National Veterinary School from December 1998 to December 1999 for a dorsally located, gradually expanding, subcutaneous cervical mass [Figures 1, 2]. Signalment, history, and clinical signs are detailed in Table 1. Dogs were nonrelated. There were four males and one female. All were young at the time of admission (i.e., 3 to 8 months) and were in good general condition. Duration of clinical signs prior to presentation ranged from 1 to 28 days. The masses had initially shown rapid growth over an 8- to 12-hour period, followed by gradual expansion over the next few days or weeks. One dog (case no. 2) underwent a cervical dog-bite injury. In the other cases, only minor traumatic events were recorded. Physical examination in each case revealed a soft, subcutaneous cervical mass, nonadherent to deeper tissues. The skin overlying the mass appeared otherwise normal.

Differential diagnoses included congenital diseases such as meningocele, myelomeningocele, persistence of embryonic lymph sacs or thymic branchial cysts, and acquired diseases such as hygromas, hematomas, abscesses, or neoplasia. Fine-needle aspiration (FNA) of the masses revealed a serosanguineous fluid with a density ranging from 1.229 to 1.416 and a protein concentration ranging from 3.5 to 5.2 g/dL. The fluid did not clot when left to stand. The total volume of fluid was not known in any cases, because no total aspiration was realized. Cytopathological examination of the fluid showed predominantly red blood cells and a few macrophages [Figure 3]. No abnormal cells or pathogen was observed. Bacterial growth in aerobic and anaerobic culture media was negative in all cases [Table 2]. One case (case no. 1) had had previous FNA of the mass by the referring veterinarian, who did not register the total volume of fluid he removed. Recurrence was noted within the next 12 hours. These observations ruled out congenital diseases, hygromas, or abscesses and were suggestive of hematomas. Complete blood count and coagulation profile were within reference physiological ranges, ruling out coagulation disorders [Table 3].

Considering the large size of the masses, their location, and the loose aspect of the neck skin, en-bloc surgical resection was decided in all cases. The surgical procedure was the same for all dogs. After premedication with diazepam^a (0.2 mg/kg body weight, intravenously [IV]), animals were induced with thiopental^b (10 mg/kg body weight, IV) and maintained by administration of halothane^c (1.5%) in 100% oxygen at a flow rate of 1 liter per minute. Lactated Ringer’s solution^d infusion (20 mL/kg body weight per hour) was administered IV perioperatively. A broad-spectrum antibiotic, cephalexin^e (30 mg/kg body weight), was administered IV preoperatively because of the anticipated length of the surgical procedure. Animals were positioned in ventral recumbency, and prior to surgery, skin tension and elasticity were assessed. A large area of skin was prepared for aseptic surgery, should a skin flap be necessary for wound closure.⁵ En-bloc surgical resection of the mass along the dorsal tension line was performed, removing a 1-cm, disease-free tissue margin around abnormal tissues [Figure 4]. In all cases, swelling was located on the dorsal tension line, and the elliptical incision was parallel to it. Fluid was encapsulated within a dense fibrous tissue with an abundant peripheral vascularization. Few blood clots were observed within the fluid. The mass was easily separated from deeper tissues by combined blunt and sharp dissections. The surgical site was flushed with sterile physiological saline, and the wound was primarily closed along the dorsal tension line incorporating Penrose^f (case nos. 1, 2, 5) or closed suction^g (case nos. 3, 4) drains by a combination of walking sutures and subcutaneous continuous pattern of polyglactin 910.^h The skin was closed with a simple-interrupted pattern using polyamid.ⁱ Active drainage was chosen when the size of the dead space and bleeding during surgery were significant. Drain exits were protected with a well-padded bandage that was changed daily. Morphine^j (0.1 mg/kg body weight, q 4 hours) and cephalexin^e (15 mg/kg body weight, bid) were administered subcutaneously postoperatively for 2 and 8 days, respectively. Postoperative drainage was maintained for 2 to 4 days [Figure 5]. Sutures were removed 12 to 15 days after surgery. No complications were encountered, and no recurrence was noted 15 to 27 months after surgery.

Resected masses were submitted for histopathological examination. Macroscopic examination revealed well-demarcated, divided cavities [Figure 6]. A peripheral wall of dense tissue encircled a central space containing red blood cells and fibrinoid material. The outer zone of the wall was dense, collagenous tissue with a few inflammatory cells and primarily iron-laden macrophages, plasma cells, lymphocytes, and neutrophils. The midzone was made of loose connective tissue, and the inner layer was composed of granulation tissue with numerous, newly formed blood vessels [Figures 7, 8]. Histopathological characteristics were compatible with encapsulated hematomas.³⁴⁶

Discussion

Hematomas are usually the result of a traumatic event, either through surgery or by accident, or secondary to a coagulation disorder such as hemophilia. Inherited or acquired clotting abnormalities should always be suspected when hematomas, filled with unclotted blood, form with minimal movement or trauma, especially in dogs predisposed to inherited coagulation disorders.² Coagulation profile results were within reference ranges for the five cases of this report, making trauma the most probable etiology. Although major trauma was only reported once (case no. 2), minor trauma was reported in all cases in the days preceding appearance of the mass. Case nos. 1, 3, and 5 were frequently grabbed by the scruff of the neck by their owners, and case nos. 1 and 4 had been vaccinated subcutaneously in the cervical area a few days (days 15 and 5, respectively) prior to mass occurrence. In each case, skin traction may have damaged a direct cutaneous artery, explaining initial blood accumulation in the subcutaneous tissues.⁷⁸

Hematomas are usually self-limiting. Once the pressure in the tissue space exceeds the pressure in the bleeding vessel and cavity of the hematoma, bleeding usually ceases and the hematoma size becomes static.² With time, fibrin strands become organized, and fibrous tissue forms in the region of the clot.² When a large quantity of blood accumulates, hematomas become encysted and may subsequently show a tendency to expand slowly. This was observed in the cases of this report, where a first period of rapid expansion was followed by slow but noticeable expansion of the mass over the next few days or weeks.

A similar clinical situation is described in humans as chronic expanding hematomas (CEH). Different mechanisms in humans have been proposed to explain the gradual expansion of these lesions. Capsule formation is induced by blood breakdown and liquefaction, which activates vasoactive substances. The breakdown products derived from erythrocytes, hemoglobin, leukocytes, and other solid blood elements induce mild, continuous inflammation, which causes increased permeability of the vascular wall and bleeding from altered or damaged dilated microvessels beneath the fibrous capsule in the granulation tissue.³⁴⁶⁹ When injecting blood in the subcutaneous tissue of rats, Labadie and Glover demonstrated that for a volume >12 mL, the larger the amount of blood injected, the greater the likelihood of subsequent enlargement.⁹ Glucocorticoids prevented their development, which is suggestive of an underlying inflammatory etiology.⁹ In this study, the hematoma expansion was large in each dog, probably because of the remarkably loose skin on the dorsal aspect of the neck, which allowed accumulation of a great amount of blood.¹⁰ Although hematomas in case nos. 1, 2, and 4 presented a slower expansion rate after a few days, they all eventually became chronic, as in humans.³⁴⁹

In humans, CEH appear as firm, painless, circumscribed, slowly expanding masses, growing sometimes over years and often simulating neoplasms.³⁴ Well-documented studies report cases of subcutaneous, paracecal, scrotal, intramuscular, corpus luteum, renal, or rectus abdominis hematomas after intra-abdominal surgical procedures, herniorrhaphy, or trauma.³⁴⁹ Other locations such as brain, spinal column, median nerve, bone, retroperitoneum, and spleen have also been reported. The veterinary literature mentions cases of aural, penile, or intra-abdominal hematomas.^7811–13 Increasing size of the chronic hematoma results in progressive clinical signs, depending on location. In this study, apart from the large dorsal subcutaneous deformation, clinical examination was unremarkable. Pain upon mass palpation was recorded in only two cases.

Cervical hematomas must be differentiated from other cervical masses resulting from congenital diseases such as meningocele, meningomyelocele, persistence of embryonic lymph sacs, and thymic branchial cysts or acquired diseases such as abscesses, hygromas, hematomas, and neoplasias.

Persistence of embryonic lymph sacs or thymic branchial cysts was ruled out in the cases of this report by the patients’ age, the dorsal location of the masses, and the macroscopic and cytopathological appearance of the fluid sampled. Persistence of embryonic lymph sacs, which has been described as the result of an interruption in the development of lymphatic system in two calves, affects younger animals and contains aqueous fluid.¹⁴ Thymic branchial cysts, previously described in dogs, are vestiges of the fetal branchial arch.¹⁵ They are located in the subcutaneous tissues of the neck, contain a mucinous acellular fluid, and develop in middle-aged to older animals.¹⁵¹⁶ Furthermore, histopathological analysis typically reveals an inner, pseudostratified ciliated epithelium, which is different from the granulation tissue observed in CEH.¹⁵

Biochemical, cytopathological, and bacteriological analyses of the fluid obtained by FNA in the cases of this report ruled out meningocele or meningomyelocele, hygromas, and abscesses. In all five reported cases, fluid was grossly reddish-brown in color and showed a specific gravity and total protein concentration ranging from 1.229 to 1.416 g/dL and from 3.5 to 5.2 g/dL, respectively. This is similar to other documented cases of hematoma in which total protein content typically ranges from 2.5 g/dL to a value equal to the total protein concentration of blood.² Fluid samples collected from cases of meningocele or meningomyelocele have lower specific gravity and total protein concentration (ranging from 1.004 to 1.006 g/dL and from 2.5 to 3.5 g/dL, respectively); this is also true for fluid samples from hygromas (total protein content ranging from 1.0 to 1.5 g/dL).¹⁷

Cytopathological examinations of fluid retrieved from a hematoma usually show a predominance of red blood cells and a few macrophages containing erythrocytes or hematoidin.²³¹⁸ These characteristics were observed in the five cases reported here. A low neutrophilic population and negative bacterial cultures ruled out abscesses.⁴

When blood clots are abundant, FNA may give poor results.² Ultrasonographic evaluation of the swelling can then be used to differentiate a hematoma from other lesions, such as neoplasia, abscess, or cyst, according to its ultrasonographic characteristics.¹¹¹⁹ In these cases, ultrasonography was not considered because of the accurate results of the cytopathological examination. In human and equine surgery, computer-assisted tomography allows distinction between hematomas and other soft-tissue masses because of their multicompartmentalized structure and their computed tomographic (CT) appearance, which vary within the lesion and over time.³¹⁹ Nevertheless, ultrasonography or CT could be indicated preoperatively to assess the noninvolvement of deeper tissues.

Histopathological analysis of these masses showed an inner layer of granulation tissue, which is distinct from the typical epithelial inner layer of hygromas.²⁰ Furthermore, histopathology ruled out neoplasia and allowed a definitive diagnosis of encapsulated hematoma.

In human esthetic surgery, endoscopic treatment of recent hematomas using standard equipment for suction-assisted lipoplasty is advocated.²¹ Suction evacuation and accurate hemostasis are performed without the need for open surgery.²¹

Surgery is recommended for large or increasing hematomas that may become painful as a result of fibrosis.^36–82122 Elimination of blood clots and fluids is obtained by incision and drainage. When hematomas are well demarcated, an en-bloc resection with good hemostasis of the vessel-rich capsule gives good results.²³⁶²³ In the five presented cases, the specific location of hematomas and the resulting dramatic skin expansion precluded conservative treatment by drainage and pressure bandages. Aspiration followed by a pressure bandage had given poor results in case no. 1. As in reports of human cases, en-bloc resection was successful.³⁴⁶ Primary wound closure was possible because of previous skin expansion by the mass. Walking sutures helped in reducing tension at wound edge and, together with drains, in obliterating dead space. En-bloc resection could probably have been avoided if the disease was treated earlier. A current study is investigating the efficacy of closed-suction drains as a sole treatment for dogs presented at the beginning of clinical signs. Use of glucocorticoids, as proposed for aural hematomas, could be interesting in combination with drainage, as inflammation was identified on histopathological examination.⁷

Conclusion

Cervical expanding hematoma is a clinical entity, which, in the authors’ experience, develops most commonly in young, large-breed dogs. A traumatic event, even minor, resulting in traction on loose, cervical, subcutaneous tissues and rupture of a cutaneous artery is a possible etiology for the disease, as no coagulation disorders could be evidenced. Further studies on a larger series of dogs are nevertheless necessary to confirm this hypothesis. This entity must be added to the differential diagnosis of dorsal cervical masses in the dog and resembles CEH in humans. Diagnosis relies upon FNA and histopathological examination of the resected mass. En-bloc surgical resection associated with short-term postoperative drainage carries an excellent prognosis.

Acknowledgments

The authors thank Drs. P. Moissonnier and V. Mentre for their advice in reviewing this article.