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Abstract

Objectives

Primary nasal tumours in cats are rare, with lymphoma being the most common feline nasal tumour, followed by adenocarcinoma. Although CT can reliably detect feline nasal tumours, there are no specific CT features that identify each tumour type. To our knowledge, there have been no reports describing MRI findings, including diffusion-weighted imaging (DWI), for nasal lymphomas and adenocarcinomas in cats. Therefore, this retrospective study aimed to evaluate the MRI findings of nasal lymphoma and adenocarcinoma, including qualitative and quantitative analysis of DWI.

Methods

MRI examination was performed on seven cats with histologically confirmed lymphoma and on two with adenocarcinoma. The MRI protocol included T2-weighted imaging (T2WI), T1-weighted imaging (T1WI) and DWI. Apparent diffusion coefficient (ADC) values were measured using DWI. Contrast agent was not used in one cat with lymphoma.

Results

Of the cats with lymphoma, three (43%) were iso- and hyperintense on T2WI, seven (100%) were isointense on T1WI, five (83%) exhibited mild heterogeneous enhancement, including a prominent region of non-enhancement on post-contrast T1WI, and seven (100%) cats exhibited hyperintensity on DWI. The median ADC values were 0.45 × 10⁻³ mm²/s (range 0.37–0.53 × 10⁻³ mm²/s). For adenocarcinoma, two (100%) were iso- and hyperintense on T2WI, two (100%) were isointense on T1WI, two (100%) exhibited marked heterogeneous enhancement on post-contrast T1WI and two (100%) were isointense on DWI. The median ADC values were 1.08 × 10⁻³ mm²/s (range 0.88–1.27 × 10⁻³ mm²/s). The median ADC values of lymphoma tended to be lower than adenocarcinoma (P = 0.056).

Conclusions and relevance

Determining ADC value and tumours with a large area of non-enhancement may be helpful in differentiating nasal lymphoma from nasal adenocarcinoma.

Keywords

Apparent diffusion coefficient ADC biopsy diffusion-weighted imaging DWI MRI

Introduction

Although primary feline nasal tumours are rare, around 90% of them are malignant tumours, based on histopathological criteria.^1–3 Among primary feline nasal tumours, lymphoma (70%) is the most common, followed by adenocarcinoma (13%) and squamous cell carcinoma.^3–6 Most nasal tumours exhibit local invasion and, rarely, distant metastasis.³ Cats with nasal tumours are more likely to be euthanased than those without tumour-related disease.⁵

There is a difference in treatment strategy and response for cats with lymphoma or adenocarcinoma.⁷ Adenocarcinomas exhibit a moderate response to radiation therapy, with a median survival time of 330 to 382 days.^7–9 In comparison, survival times in cats with feline nasal lymphoma range from 8 months to >4 years, without a significant difference between cats treated with radiation therapy only, chemotherapy only or a combination of both.^5,10,11 Cats with lymphoma experience longer survival times than those with adenocarcinoma.⁵ Therefore, we believe that differentiating lymphoma from adenocarcinoma is important for designing appropriate treatment strategies and prediction prognoses.

For definitive diagnosis of nasal tumours, histopathological analysis is the primary method.⁵ A false-negative diagnosis of malignant tumour occurs as a result of low cellularity in the adenocarcinoma and well-differentiated lymphoma.¹² A recent study reported that some cases of feline nasal lymphoma are misdiagnosed as carcinoma when immunohistochemical methods are not used.¹³

CT is used to detect feline nasal tumours.^1,2,4 CT features of nasal tumour include soft tissue or fluid accumulation in the sphenoid or frontal sinuses, and osteolysis of the paranasal bones, nasal septum (the maxilla or ethmoid, orbital lamina) and turbinate destruction associated with a soft tissue attenuating mass with extension into the orbits, nasopharynx or facial soft tissues.^1,2,4,14 Seventy-five percent of nasal tumours exhibit heterogeneous enhancement.¹ However, there are no specific CT features that characterise different tumour types.^2,4

MRI yields better tissue contrast without the ionising radiation and beam-hardening artefacts of CT.¹⁵ Although conventional MRI, including T2- and T1-weighted imaging (T2WI and T1WI, respectively), is often performed to detect nasal tumours in dogs, some cases of nasal tumour are missed.¹⁶ To our knowledge, there exist no reports describing specific MRI features that identify tumour type. On MRI, diffusion-weighted imaging (DWI) delivers microstructural information by measuring the macromolecular motion of intra- and extracellular water, which is influenced by cell density.^17–19 Apparent diffusion coefficient (ADC) values are measured using DWI.¹⁸

We previously reported the utility of ADC values to diagnose intracranial and nasopharyngeal lymphomas.^20,21 In two cats with nasopharyngeal polyps, ADC values were higher than in a cat with nasopharyngeal lymphoma.²¹ There are no reports describing the utility of ADC values in nasal tumours. In the present study, we evaluated MRI findings, including qualitative and quantitative analysis of DWI, of nasal lymphoma vs adenocarcinoma.

Materials and methods

The present retrospective case series considered all cats with suspected nasal tumour that underwent CT examination at our institution between 2014 and 2019. Of these, the study population included those with a histopathological diagnosis of nasal tumour using the closed suction technique and had undergone MRI examination. Cats with multiple tumours or the presence of apical abscess(es) were excluded.

For MRI, the cats were anaesthetised using intravenous propofol (Intervet); anaesthesia was maintained using isoflurane and oxygen. MRI examination was performed using a 1.5 Tesla system (Brivo MR355; GE Healthcare Japan) with the cats lying in sternal recumbency. A flex coil was wrapped around the head for signal reception. MRI was carried out using the following sequences: (1) transverse fast-spin echo T2WI (repetition time [TR]/echo time [TE], 4600/120 ms; thickness, 3.5 mm; spacing, 0.7 mm; number of excitations [NEX], 3; field of view [FOV], 140 mm; and matrix, 480 × 480); (2) transverse spin echo (SE) T1WI (TR/TE, 350/13 ms; thickness, 3.5 mm; spacing, 0.7 mm; NEX, 4; FOV, 140 mm; matrix 320 × 320; and flip angle, 90°); (3) transverse single-shot SE-type echoplanar imaging (EPI) DWI (TR/TE, 3700/88 ms; thickness, 3.5 mm; spacing, 0.7 mm; b-value, 1000 s/mm²; NEX, 4; FOV, 150 mm; and matrix 64 × 64); (4) transverse SE post-contrast T1WI after administration of gadolinium-diethylenetriamine penta-acetic acid (DTPA) 0.2 ml/kg (Magnevist; Bayer). Diffusion-weighted gradients were applied in three directions (x, y and z). ADC distribution was demonstrated on an ADC values colour map created with Functool version 7.4.03 (GE Healthcare).

Two observers were blinded to the final diagnoses at the time of MRI evaluation, and all images were assessed in random order. The MRI findings were recorded by consensus. Location of the tumour (unilateral or bilateral) and the infiltration site of the lesion were documented. MRI signal intensity of nasal tumours on T2WI and T1WI were subjectively compared between the tumour and cerebral white matter. The signal intensity of the tumour on T2WI and T1WI was graded as iso- or hyperintense. If the tumour included an iso- and hyperintense lesion, it was defined as iso- and hyperintense. Measurement of signal intensity from fluid accumulation areas of the nasal cavity was avoided. Fluid accumulations were defined as isointense to cerebrospinal fluid on T2WI and T1WI without contrast enhancement. Contrast enhancement was assessed subjectively on post-contrast T1WI as mild/moderate or marked and homogenous or heterogenous.

On DWI, signal intensity of the tumour was subjectively compared between the tumour and the cerebral white matter. The intensity of the tumour on DWI was graded as iso- or hyperintense. Three regions of interest (ROIs) of at least 10 mm² were manually drawn to include the lesion and exclude fluid accumulation areas to calculate ADC values of the nasal tumours on the ADC colour map: the mean values of these images were then calculated. The ADC was measured in random order three times, with at least a 2-week interval to avoid potential bias, and mean ADC values were calculated.

Statistical analysis

Statistics were analysed using R version 2.12.1 (R Development Core Team, 2010). A Mann–Whitney U-test was performed to test the difference in ADC values between lymphoma and adenocarcinoma. P values <0.05 were considered statistically significant.

Results

CT examination was performed on 362 cats and nine cats met the final criteria for inclusion in the present study. MRI was performed only for cases in which the owner’s consent was obtained. The nasal tumours included lymphomas (n = 7) and adenocarcinomas (n = 2). All nasal tumours were histopathologically diagnosed using the closed suction technique.

Among the cats with lymphoma (n = 7), two were castrated males, one was an intact male and four were spayed females, with a median age of 9 years (range 7–14 years). The breeds of the cats were mixed (n = 6) and Persian (n = 1). Based on MRI findings, five (71%) were unilateral. The sites of extranasal infiltration included the retrobulbar space (n = 5), nasopharynx (n = 6), facial soft tissues (n = 2) and intracranial cavity (n = 1). On MRI findings for lymphoma, three (43%) were iso- and hyperintense and four (57%) were hyperintense on T2WI; on T1WI, seven (100%) were isointense. Post-contrast T1WI was performed in six cases. Contrast agent was not used in one (14%) cat owing to lack of permission from the owner. On post-contrast T1WI, five (83%) exhibited mild heterogeneous enhancement, including a prominent region of non-enhancement. One (17%) exhibited mild homogeneous enhancement. On DWI, seven (100%) cats exhibited hyperintensity (Table 1). The median ADC values of lymphoma were 0.45 × 10⁻³ mm²/s (range, 0.37–0.53 × 10⁻³ mm²/s) (Figure 1). A representative example of lymphoma is shown in Figure 2.

Table 1

MRI findings of nasal lymphoma and adenocarcinoma

Lesion features	Lymphoma (n = 7)	Adenocarcinoma (n = 2)
Lesion location
Bilateral	2 (29)	0 (0)
Unilateral	5 (71)	2 (100)
Lesion infiltration
Retrobulbar space	5 (71)	2 (100)
Nasopharynx	6 (86)	2 (100)
Facial soft tissues	2 (29)	0 (0)
Intracranial cavity	1 (14)	1 (50)
T2WI
Iso- and hyperintense	3 (43)	2 (100)
Hyperintense	4 (57)	0 (0)
T1WI
Isointense	7 (100)	2 (100)
Post-contrast T1WI*
Mainly non-enhancing and mildly heterogeneous	5 (83)	0 (0)
Mildly homogeneous	1 (17)	0 (0)
Markedly heterogeneous	0 (0)	2 (100)
DWI
Hyperintense	7 (100)	0 (0)
Isointense	0 (0)	2 (100)

Data are n (%)

Post-contrast T1WI was performed in six cases of lymphoma

T2WI = T2-weighted imaging; T1W1 = T1-weighted imaging; DWI = diffusion-weighted imaging

Figure 1

Apparent diffusion coefficient (ADC) value of lymphoma and adenocarcinoma. The median ADC values of lymphoma tended to be lower than adenocarcinoma (P = 0.056)

Figure 2

Representative example of lymphoma (arrowhead) on (a) T2-weighted imaging (T2WI), (b) T1-weighted imaging (T1WI), (c) post-contrast T1WI, (d) diffusion-weighted imaging (DWI) and (e) an apparent diffusion coefficient (ADC) map. The nasal lymphoma exhibits mild heterogeneous enhancement, including a prominent non-enhancement region on (c) post-contrast T1WI and (d) hyperintensity on DWI. The median ADC was 0.45 × 10⁻³ mm²/s

In the two cats with adenocarcinoma, one was a castrated male and one was a spayed female, with a median age of 14.5 years (range 14–15 years). The breed of these cats was mixed. Based on MRI findings, two (100%) were unilateral. The site of extranasal infiltration included the retrobulbar space (n = 2), nasopharynx (n = 2) and intracranial region (n = 1). On MRI findings of adenocarcinoma, two (100%) were iso- and hyperintense on T2WI, two (100%) were isointense on T1WI, two (100%) exhibited marked heterogeneous enhancement on contrast-enhanced T1WI and two (100%) were isointense on DWI (Table 1). The median ADC values of adenocarcinoma were 1.08 × 10⁻³ mm²/s (range 0.88–1.27 × 10⁻³ mm²/s). The median ADC values of lymphoma tended to be lower compared with adenocarcinoma (P = 0.056, Figure 1). A representative example of adenocarcinoma is shown in Figure 3.

Figure 3

Representative example of adenocarcinoma (arrowhead) on (a) T2-weighted imaging (T2WI), (b) T1-weighted imaging (T1WI), (c) post-contrast T1WI, (d) diffusion-weighted imaging (DWI) and (e) an apparent diffusion coefficient (ADC) map. The nasal adenocarcinoma exhibits marked heterogeneous enhancement on (c) post-contrast T1WI and (d) isointensity on DWI. The median ADC was 1.08 × 10⁻³ mm²/s

Discussion

In nasal tumours, destruction of the maxillary turbinates and nasal discharge are commonly detected.^3,4 This study demonstrated iso- and hyperintensity on T2WI in feline nasal lymphoma and adenocarcinoma. Tumours and discharge in the nasal cavity may mix and cause several signal intensities on MRI. In this study, all adenocarcinomas showed marked heterogeneous enhancement. Adenocarcinomas originate from the superficial respiratory epithelium.³ Adenocarcinoma is classified as acinar, cystic, mucinous or papillary according to their morphology. Depending on the morphological subtype of adenocarcinoma, tumours include variously sized cystic structures and various amounts of extracellular mucin.³ These histopathological features may cause marked heterogeneous enhancement. Unfortunately, we did not assess the morphological subtypes of adenocarcinoma in the present study. Gadolinium-DTPA is distributed throughout the extracellular fluid compartment.²² Therefore, enhancement is dependent on the volume of interstitial spaces in the tumour. Because nasal lymphoma is a highly cellular type of tumour,^3,11 interstitial spaces in the tumour may be narrowed. The malignant lymphocytes infiltrate the margins of the tumour or the area around blood vessels.¹¹ In humans, lymphoma surrounds and compresses blood vessels.²³ These features may cause a large area of non-enhancement in the lymphoma. Further study is therefore needed to assess the relationship between histopathological and post-contrast findings.

DWI reflects the macromolecular motion of intra- and extracellular water.¹⁷ DWI can be used for qualitative evaluation of lesions.²⁴ In feline nasal tumours, highly malignant tumours have necrosis.³ Tumour necrosis and cystic tumour components affect diffusion.^25,26 ROI placement has the potential to influence DWI signal intensity. DWI signal intensity is influenced by T2WI.²⁷ ADC distribution, which is measured using DWI, permits the quantitative evaluation of tissue microstructure and pathophysiological states without the influence of T2WI.¹⁸ The previously reported ADC values of lymphoma were 0.57 × 10⁻³ mm²/s and 0.46 × 10⁻³ mm²/s.^20,21 This study showed that the median ADC for cats with nasal lymphoma was similar to that previously reported in feline lymphoma. The ADC value of cats with nasal lymphoma tended to be lower than that of adenocarcinoma. Therefore, a low ADC may be a specific feature of lymphoma. However, studies investigating ADC values of other tumours are scarce; as such, further study is needed in this regard.

Image distortion in DWI is common.²⁸ DWI is very sensitive to magnetic field inhomogeneities caused by the air–tissue interface.²⁹ In humans, sinonasal DWI is affected by these magnetic field inhomogeneities.³⁰ Therefore, if the nasal tumour is small, DWI may be distorted by air in the nasal cavity. In humans, distortion of sinonasal DWI is reduced using parallel imaging and multishot and readout-segmented EPI.³⁰ Further study is needed to detect appropriate techniques to reduce the distortion of nasal tumour on DWI.

Frequently detected unilateral lesions and infiltration sites of nasal tumours, including nasopharynx, retrobulbar space and facial soft tissue, of the present study support those of other similar investigations.^2,4 Intracranial infiltration was detected in one case of lymphoma and one case of adenocarcinoma. In cats, erosion of the cribriform plate is not a specific feature of nasal tumours, and not a predictive finding to differentiate specific tumours.^2,4 However, in nasal lymphomas and carcinomas, the presence of cribriform plate destruction is a negative prognostic finding for radiation therapy.^31,32 In nasal tumours, the incidence of erosion of the cribriform plate is 18–40%.⁴ In humans, bone destruction detected on MRI is identified by the alteration of the bone by the invading tumour.³³ In canine nasal tumours, detection of a midline shift by intracranial infiltration of the nasal tumour is a negative prognostic finding for radiation therapy.³⁴ MRI provides superior resolution of intracranial lesions than CT.³⁵ Therefore, we believe that MRI is a useful modality with which to assess intracranial infiltration of nasal tumours.

This study has some limitations. First, this study included a small number and unequal distribution of cats with nasal lymphoma and adenocarcinoma. Other types of nasal tumour, such as squamous cell carcinoma, were not assessed. Second, this study was retrospectively designed. Histopathological features were not assessed in each tumour. As such, further study is needed to evaluate MRI findings, including post-contrast findings and ADC values, in a larger population of cats with nasal tumours.

Conclusions

ADC measurement and a large area of non-enhancement in the tumour may be helpful for differentiating nasal lymphoma from adenocarcinoma. Further studies are needed to evaluate MRI findings in a larger population of cats with nasal tumours.

Footnotes

Acknowledgements

We thank the staff of the Veterinary Medical Center of Osaka Prefecture University and Kinki Animal Medical Training Institute for their help with the manuscript and care of the patients.

Accepted: 15 May 2020

Conflict of interest

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

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

This work involved the use of non-experimental animals only (including owned or unowned animals and data from prospective or retrospective studies). Established internationally recognised high standards (‘best practice’) of individual veterinary clinical patient care were followed. Ethical approval from a committee was therefore not necessarily required.

Informed consent

Informed consent (either verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work (either experimental or nonexperimental animals) for the procedure(s) undertaken (either prospective or retrospective studies). No animals or humans are identifiable within this publication, and therefore additional informed consent for publication was not required.

ORCID iDs

Toshiyuki Tanaka

Hideo Akiyoshi

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MRI findings,including diffusion-weighted imaging,in seven cats with nasal lymphoma and two cats with nasal adenocarcinoma

Abstract

Objectives

Methods

Results

Conclusions and relevance

Keywords

Introduction

Materials and methods

Statistical analysis

Results

Discussion

Conclusions

Footnotes

Acknowledgements

Conflict of interest

Funding

Ethical approval

Informed consent

ORCID iDs

References