Introduction

Hematopoietic neoplasia is common in dogs, with canine non‐Hodgkin lymphomas (cNHLs) representing more than 80% of all hematopoietic cancer.¹ cNHLs encompass a heterogeneous group of diseases with distinct biological behavior, highly dependent on the subtype and extent of systemic distribution.² cNHLs commonly arise within lymphoid tissues; however, extranodal involvement is observed as part of systemic tumor progression or a solitary form, with cutaneous and alimentary lymphoma being the most common and best characterized.³

cNHL of the skeletal muscle is rare and is described in four veterinary patients, both singly^4–6 and in conjunction with cutaneous infiltration.⁷ In humans, it is similarly rare, accounting for <1% of extranodal lymphomas, and is postulated to occur in three ways: as part of disseminated disease, extension from bone or lymph nodes, or rarely as primary extranodal disease arising from histologically undetectable aberrant lymph nodes.^8,9

In humans, the characteristics of skeletal muscle lymphoma at MRI are described in detail^9–11; however, the MRI findings associated with lymphoma of the skeletal muscle have not been previously reported in dogs. This report describes the MRI features of a case of cytologically confirmed lymphoma of the skeletal muscle and correlates them with those from the medical literature to establish the similarities and differences and determine any unique features associated with this pathology in the dog.

Case Report

A 9 yr old neutered male English mastiff presented with a 3 wk history of recurrent stranguria. He had visited the referring veterinary practice with hematuria 12 mo previously and was diagnosed with and successfully treated for a urinary tract infection.

On presentation, he was overweight (body condition score: 7/9), subdued, and reluctant to walk. He had pelvic limb ataxia and mild proprioceptive deficits bilaterally, worse in the right pelvic limb. The remainder of the neurological examination, including spinal reflexes, was deemed unremarkable, prioritizing a thoracolumbar (T3–L3) neurolocalization. The urinary bladder was distended and tender when palpated; no other abnormalities were identified. Complete hematology, electrolytes, and biochemistry were normal. A urinary catheter was passed with ease and the bladder drained; urinalysis was unremarkable and urine bacterial culture sterile.

Abdominal radiographs were normal. Ultrasonography of the abdomen was performed at the authors’ institution and showed mild unilateral left-sided adrenomegaly. This was considered unrelated to the clinical signs. There was no lymphadenopathy.

To investigate the ataxia and proprioceptive deficits, MRI of the thoracolumbar and lumbosacral spine was performed with a 1.5 T MRI scanner^a. Turbo spin echo T2-weighted (T2W) images were acquired in dorsal, sagittal, and transverse planes. Fat-suppressed (mDixon) T2W images were acquired in the dorsal plane. Gradient echo (Fast field echo) images were acquired in the transverse plane. T1-weighted (T1W) images were acquired in the sagittal and transverse plane before and after IV gadobutrol (0.1 mmol/kg)^b. Fat-suppressed (T1W-mDixon) images were acquired in the sagittal and transverse plane after gadobutrol^b injection.

On T2W images of the lumbosacral spine, an expansile, ill-defined lesion of intermediate signal intensity to fat and muscle was noted within the bulbospongiosus muscle and compressing the penile urethra (Figures 1A, 2A). Further imaging was thereafter centered on this lesion. On fat-suppressed images, adjacent perineal subcutaneous fat had a loose, honeycomb-like, T2W hyperintense appearance. On precontrast T1W images, the bulbospongiosus muscle was enlarged and ill defined (Figures 1B, 2B; white arrow). Following gadobutrol injection, there was heterogeneous contrast enhancement of the lesion with areas of reduced enhancement centrally (Figures 1C, 2C; white arrowhead). Enhancement also extended in a finger-like fashion into the adjacent subcutaneous fat. (Figure 1D; double arrowheads). The urethra was moderately dilated proximal to the lesion. (Figures 1A, C; open arrow). Involvement of the bulb of the penis and corpus spongiosum was considered unlikely based on these images, but without images orientated perpendicularly to the plane of the urethra, directly adjacent to the lesion, this possibility was not completely excluded.

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Additionally, there was generalized reduced T2W hyperintensity within multiple nuclei pulposi, multiple intervertebral disc protrusions with minimal spinal cord compression, and marked ventral spondylosis deformans at the lumbosacral junction. Modic type 2 changes were detected within multiple vertebral bodies. Multiple small cysts were observed within both renal cortices, and the left adrenal gland was mildly enlarged. None of these findings were considered related to the urinary tract signs or ataxia.

Ultrasonography of the perineum and penile urethra was performed to facilitate fine-needle aspiration of the lesion. This showed a hypoechoic infiltration of the bulbospongiosus muscle, compressing but not invading the urethra, and hyperechoic perilesional fat.

Based on these findings, differential diagnoses for the mass included primary or metastatic neoplasia and inflammatory/immune-mediated myopathy. Ultrasound-guided aspirates were performed to further characterize the lesion, and cytological examination revealed a monomorphic population of discrete round cells, consistent with a lymphoma of high-grade morphology.¹² A diagnosis of presumed extranodal lymphoma arising from the bulbospongiosus muscle was proposed and extensive staging offered to the client to confirm the solitary location and to further classify the lymphoma subtype. However, further procedures and treatment options were declined.

Discussion

This is the first report describing the MRI features of lymphoma infiltrating the skeletal muscle in the dog. Although lymphoma in this patient's bulbospongiosus muscle resulted in stranguria secondary to extramural urethral compression, solitary lymphoma of the skeletal muscle is very rare in humans and dogs and is therefore an uncommon cause of stranguria in the dog.

In humans, MRI provides the most detailed classification of skeletal muscle lymphoma, and it is reported with variable characteristics.¹⁰ It is frequently T1W-isointense or hyperintense to uninvolved muscle and of high or mid-signal intensity between fat and skeletal muscle to uninvolved muscle on T2W sequences.^8,9 Short tau inversion recovery sequences demonstrate lesions hyperintense to unaffected adjacent muscle.¹⁰ Following IV contrast injection, heterogeneous enhancement was the most common feature described in 24 human cases of skeletal muscular lymphoma.⁸ Suresh and Lee also describe infiltration of the adjacent subcutaneous fat with “fibroadipose septa” and involvement of adjacent subcutaneous and muscle compartments.^8,11 The MRI findings in this case were strongly correlative with these features, most notably the comparable signal changes and digitate signal alteration in adjacent tissue compartments. Although not confirmed histopathologically, these could reflect the fibroadipose septa described by Suresh and Lee, and we hypothesize that similar pathophysiology and disease course underlie the imaging features in the dog.

The role of advanced imaging in diagnosing muscle disease is not widely documented in dogs. It has been postulated by Platt and others that myopathies resulting in an inflammatory response cause redistribution of tissue water within muscle (muscle edema), prolonging the relaxation time and therefore altering the signal intensity, and a similar pathophysiology is implicated in the signal changes observed in this case.¹³ A “muscle edema pattern” is reported to be sensitive for detecting diffuse disease within muscle, but its specificity is poor and must be supported by biopsy as denervation, rhabdomyolysis, and central necrosis associated with tumors and myositis have a similar appearance, especially if relying on T2W sequences alone.¹³ It can be difficult to distinguish edema from fat on turbo spin echo T2W sequences without fat suppression, and fat-suppressed images may provide additional diagnostic information in these cases.¹³

Ultrasonography findings also corresponded to those reported in the medical literature, notably, a solid, heterogeneous, predominantly hypoechoic mass with an irregular or ill-defined margin.¹⁴ However, these findings are also nonspecific, further reiterating the need for confirmatory cytological evidence of suspected pathology.¹⁵

Lee et al. stipulate correlative histopathology, absence of systemic nodal disease, and muscle lesions preceding abnormalities within bone marrow for a confirmatory diagnosis of NHL of the skeletal muscle in humans.¹¹ Although no criteria have been proposed in veterinary oncology, a similar approach should be used to differentiate between primary extranodal disease and progression of systemic lymphoma to an extranodal site. In humans, MRI can be used for staging,¹⁶ and a study by Feeney et al. using 3.0T out-of-phase MR pulse sequences in dogs permitted successful identification of abnormal marrow in dogs with myelodysplastic syndrome, but this technique is not used routinely in veterinary patients.¹⁷ Infiltration of the urinary tract by lymphoma has also been previously described in dogs¹⁸ and humans¹⁹ as a consequence of systemic disease and as solitary extranodal disease. It is possible that the primary extranodal site in this patient was within the urinary tract and infiltration of the muscle occurred subsequently. However, the absence of intramural pathology at ultrasonography and MRI reduce the index of suspicion for this disease course.

No definitive cause was established for the ataxia in this case, although it is feasible that the gait abnormalities described were a result of pain or discomfort associated with the primary lesion described. Unfortunately, the owner declined further investigation in this case, preventing definitive exclusion of infiltration at any other site. However, the lack of regional and distant lymphadenopathy at MRI and ultrasonography, the correlative MRI features, the ultrasonography findings, and the laboratory test results support a primary lymphoma of the skeletal muscle.

Conclusion

To the authors’ knowledge, this is the first report of the MRI features of skeletal muscle lymphoma in an atypical location in a dog, causing partial urethral obstruction and recurrent stranguria. Infiltration of lymphoma within the skeletal muscle had intermediate signal intensity to muscle and fat on T2W imaging and was isointense to unaffected muscle on precontrast T1W imaging. Contrast enhancement was heterogeneous and there was digitate signal alteration within perilesional fat. Ultrasonography confirmed a hypoechoic lesion within the muscle, with adjacent hyperechoic fat. These imaging findings, although nonspecific, are strongly correlative with those described in the medical literature for primary extranodal lymphoma of skeletal muscle, providing support to the validity of MRI in assisting with diagnosis of this condition in the dog.