Preliminary study of CT features of intermediate- and high-grade alimentary lymphoma and adenocarcinoma in cats

Abstract

Case series summary

The ultrasonographic findings of many feline intestinal tumours are similar. This study evaluated the CT features of intermediate- and high-grade alimentary lymphoma and adenocarcinoma in cats. CT was performed on six cats with adenocarcinoma and 14 cats with lymphoma. Comparisons between tumour types were conducted, focusing on CT features, including obstruction (present or absent), growth patterns of lesions (symmetry or asymmetry), layering enhancement (present or absent), location of the lesion, number of lesions (solitary or multiple), lymphadenopathy (present or absent), location of lymphadenopathy, pulmonary metastasis (present or absent) and maximum thickness (mm) of the lesion. The cats with adenocarcinoma (n = 5/6 [83%]) experienced intestinal obstruction significantly more often than cats with lymphoma (n = 0/14 [0%]; P = 0.0004). Layering enhancement was observed significantly more often in cats with adenocarcinoma (n = 6/6 [100%]) than in cats with lymphoma (n = 1/14 [7%]; P = 0.0002). Lymphadenopathy was detected significantly more often in cats with lymphoma (n = 14/14 [100%]) than in cats with adenocarcinoma (n = 2/6 [33%]) (P = 0.003). In cats with lymphoma, the intestine (12.1 ± 3.9 mm) was significantly thicker than that in cats with adenocarcinoma (6.4 ± 2.3 mm; P = 0.005).

Relevance and novel information

To the best of our knowledge, no reports have described the characteristics of feline intestinal tumours using CT. Layering enhancement was observed in cats with intestinal adenocarcinomas. No layering enhancement was observed in alimentary lymphoma in cats, but enlarged regional nodes were noted. Lesions with lymphoma were thicker than those with adenocarcinoma. These findings may help differentiate between adenocarcinomas and lymphomas.

Keywords

Duodenum intestinal tumour jejunum lymphadenopathy

Introduction

The most common intestinal neoplasms in cats include lymphoma, adenocarcinoma and mast cell tumours.¹ Alimentary lymphoma is the most common intestinal neoplasm in cats (55%), followed by adenocarcinoma (32%) and mast cell tumours (4%).² In cats with adenocarcinoma, surgical resection is the treatment of choice as it improves survival time, even in those with metastasis.^3,4 In cats with alimentary lymphoma, the combination of surgical resection and chemotherapy has not demonstrated improved survival time vs chemotherapy alone.^5–7 Therefore, differentiation of intestinal tumours is beneficial in determining the best treatment option.

In veterinary medicine, abdominal ultrasonography is a conventional method for diagnosing intestinal tumours.⁸ Thickened walls and loss of layering are highly predictive of focal intestinal neoplasia in cats.^1,9 Intermediate- and high-grade lymphoma most commonly occur as solitary, hypoechoic intestinal masses with transmural loss of layering,^10,11 while adenocarcinoma appears as circumferential bowel wall thickening with transmural loss of normal ultrasonographic wall layers and regional lymphadenopathy.^1,8 Alimentary lymphoma and adenocarcinoma often involve regional lymph nodes, making them large and rounded.^1,12 The ultrasonographic characteristics of segmental alimentary lymphoma are difficult to differentiate from adenocarcinoma.⁸

In human medicine, CT is used for the evaluation of intestinal diseases.^13–15 CT is useful for tumour detection and preoperative staging, as well as evaluation of nodal involvement and distant metastases.¹³ The morphological features of CT imaging allow accurate prediction of tumour histology.^13–15 In cats, mesenteric ischaemia and duplication are among a few of the limited intestinal diseases investigated using CT.^16–18 To the best of our knowledge, no reports have described the characteristics of feline intestinal tumours on CT. This study aimed to evaluate the CT findings associated with intestinal lymphoma and adenocarcinoma in cats.

Case series summary

This was a retrospective case series. All cats with intestinal tumours that underwent CT examination at our institution between 2015 and 2020 were included. The final inclusion criterion required confirmation of cancer by histopathological or cytological samples from an intestinal tumour or enlarged lymph nodes. Criteria for exclusion included metastatic lymphadenopathy from a tumour of another origin or the presence of multiple tumour types.

Whole-body CT studies, including the head, neck, limbs, thorax and abdomen, were performed using a multidetector 16-slice CT scanner (SOMATOM Scope [Siemens] or Activion16 [Canon Medical Systems]) in the helical scan mode according to our previous protocol.¹⁹ A contrast-enhanced study was performed on the abdomen in the early phase (20 s after the injection of contrast medium) and the delayed phase (60 s). Image analyses were performed according to our previous report using commercially available DICOM image viewing software (OsiriX 4.1.2, 32 bit; Pixmeo).¹⁹

The following CT parameters were recorded: obstruction (present or absent); growth patterns of lesions (symmetry or asymmetry); layering enhancement (present or absent); location of the lesion; number of lesions (solitary or multiple); lymphadenopathy (present or absent); location of lymphadenopathy; pulmonary metastasis (present or absent); and maximum thickness (mm) of the lesion.

Intestinal obstruction was diagnosed when the proximal loops were distended and the distal loops were collapsed.²⁰ The layering enhancement was considered present or absent, depending on whether there was a layering of the intestinal wall mucosa and the outer intestinal wall in the postcontrast image.

Lymphadenopathy was indicated when either lymph node length or width was longer than the mean normal size.^21,22 The length (mm) and width (mm) of enlarged lymph nodes were measured on transverse, sagittal or dorsal reconstructions, depending on their orientation.²¹ If two or more enlarged lymph nodes were noted in a single case, the mean length and width of the largest lymph nodes were calculated. Pulmonary metastasis was defined as a soft tissue density nodule detected in a pulmonary window (window level −600 HU; window width 1500 HU).

As described elsewhere, we measured the maximum thickness (mm) of the lesion from the luminal mucosal surface of the inner intestinal wall to the outer serosal surface of the intestinal wall.²³ Cross-sectional images of the affected regions were obtained in transverse, sagittal or dorsal reconstructions, depending on the tumour orientation. Mean ± SD lesion thickness was calculated. The measurement of the maximum thickness (mm) of the lesion is shown in Figure 1.

Figure 1

To measure the maximum thickness of intestinal tumours, cross-sectional images were obtained based on (a) transverse, (b) sagittal or (c) dorsal reconstructions, depending on the orientation of the tumour. The thickness of intestinal tumours was measured from the luminal mucosal surface to the outer serosal surface of the affected regions (arrow)

Statistical analyses were performed using commercially available software (R version 2.12.1, R Development Core Team, 2010). The normality of quantitative CT data distributions was assessed using the Shapiro–Wilk test, which indicated that parametric testing was required. The differences in qualitative parameters between adenocarcinoma and lymphoma were assessed using Fisher’s exact test. For quantitative CT parameters, the differences between adenocarcinoma and lymphoma were assessed using a t-test. Statistical significance was set at P <0.05.

A total of 29 cats met our initial criteria; of these, 20 met the final conditions for analysis. Six cats were diagnosed with adenocarcinoma (30%) and 14 with lymphoma (70%). Adenocarcinoma was diagnosed in one case (17%) using fine-needle aspiration (FNA) and five cases (83%) using excisional biopsy. All lymphoma diagnoses (100%) were based on the FNA findings.

The group of cats with adenocarcinoma consisted of a neutered male (n = 1), an intact male (n = 1), spayed females (n = 3) and an intact female (n = 1). Mean ± SD age was 11.2 ± 3.7 years. The group of cats with lymphoma consisted of neutered males (n = 8), an intact male (n = 1) and spayed females (n = 5). Mean ± SD age was 10.1 ± 2.5 years.

Comparisons between the tumour types and qualitative CT features are summarised in Table 1. Cats with adenocarcinoma experienced intestinal obstruction significantly more often than cats with lymphoma (P = 0.0004).

Table 1

Comparisons between tumour type and qualitative CT features

CT features		Adenocarcinoma (n = 6)	Lymphoma (n = 14)	P
Obstruction	Present	5/6 (83)	0/14 (0)	0.0004*
	Absent	1/6 (17)	14/14 (100)
Growth patterns	Symmetry	5/6 (83)	12/14 (86)	1
	Asymmetry	1/6 (17)	2/14 (14)
Layering enhancement	Present	6/6 (100)	1/14 (7)	0.0002*
	Absent	0/6 (0)	13/14 (93)
Number of lesions	Solitary	6/6 (100)	10/14 (71)	0.27
	Multiple	0/6 (0)	4/14 (29)
Lymphadenopathy	Present	2/6 (33)	14/14 (100)	0.003*
	Absent	4/6 (67)	0/14 (0)
Pulmonary metastasis	Present	0/6 (0)	1/14 (7)	1
	Absent	6/6 (100)	13/14 (93)

Data are n (%)

P <0.05

All cases of adenocarcinoma and lymphoma had wall-thickening lesions. Adenocarcinomas and lymphomas tended to show symmetric lesions. In all six (100%) cases of adenocarcinoma, the layering enhancement was well defined, and the mucosa showed gradually increasing enhancement. In one case (7%) of lymphoma, layering enhancement was observed. Cats with adenocarcinoma demonstrated layering enhancement significantly more often than cats with lymphoma (P = 0.0002). In the group of cats with adenocarcinoma, all cases had solitary lesions. The lesion was detected in three cases in the jejunum and three cases at the ileocaecal junction. In the group of cats with lymphoma, four patients had multiple lesions. Lesions were detected in 11 cases in the jejunum, three cases at the ileocaecal junction and two cases at the duodenum. Representative CT images of intestinal adenocarcinoma and lymphoma are shown in Figure 2.

Figure 2

Representative CT images of intestinal adenocarcinoma in (a) precontrast, (b) early-phase postcontrast and (c) delayed-phase postcontrast, and representative CT images of alimentary lymphoma in (d) precontrast, (e) early-phase postcontrast and (f) delayed-phase postcontrast. There was an enhancement of the intestinal wall mucosa (arrowheads) and a lesser enhancement of the outer intestinal wall in the postcontrast image (b,c). Adenocarcinomas showed layering enhancement. Alimentary lymphoma showed no layering enhancement (arrows) with enlarged regional lymph nodes (*)

The cats with lymphoma demonstrated lymphadenopathy significantly more often than cats with adenocarcinoma (P = 0.003). In adenocarcinoma, lymphadenopathy was detected in 2/6 cases (33%). In two cases of adenocarcinoma with lymphadenopathy, the jejunal lymph node was enlarged in two cases (100%) and the sternal lymph node in one case (50%). Lymphadenopathy was detected in all 14 cases (100%). In 14 cases of lymphoma with lymphadenopathy, the jejunal lymph node was enlarged in 12 cases (86%), the hepatic lymph node in two cases (14%), the ileocaecal lymph node in one (7%) and the sternal lymph node in seven (50%). The distribution, length and width of the enlarged lymph nodes in adenocarcinoma and lymphoma are summarised in Table 2.

Table 2

Distribution, length and width of enlarged lymph nodes in adenocarcinoma and lymphoma

Lymph node	Adenocarcinoma (n = 2)	Lymphoma (n = 14)
Jejunal	n = 2	n =12
Length (mm)	11.8 ± 3.1	26.7 ± 12.4
Width (mm)	7.1 ± 2.5	15.6 ± 9.3
Hepatic	n = 0	n = 2
Length (mm)		20.5 ± 0.7
Width (mm)		11.5 ± 2.1
Ileocaecal	n = 0	n = 1
Length (mm)		23
Width (mm)		17
Sternal	n = 1	n = 7
Length (mm)	15.7	19.5 ± 6.5
Width (mm)	8.3	11.3 ± 2.4

Data are mean ± SD

Pulmonary metastasis was detected in one cat with lymphoma. Nodules of unequal sizes were found throughout the lung lobes. Pulmonary metastasis was diagnosed cytologically using FNA.

The mean thickness of the adenocarcinomas and lymphomas were 6.4 ± 2.3 mm and 12.1 ± 3.9 mm, respectively. In cats with lymphoma, the intestines were significantly thicker compared with cats with adenocarcinoma (P = 0.005; Figure 3).

Figure 3

Mean intestinal wall thickness of adenocarcinoma and lymphoma cases. Intestinal walls were significantly thicker in lymphoma cases compared with adenocarcinoma cases (*P <0.05). The bar represents the SD

Discussion

In this study, both adenocarcinoma and lymphoma demonstrated a specific enhancement pattern of intestinal lesions. On contrast CT, the mucosal layer of a normal intestinal wall displays high attenuation in animals with early phase.²⁴ In the delayed phase, there is a washout of contrast in the mucosa and prolonged homogeneous enhancement of the outer intestinal wall.²⁴ Adenocarcinoma originates from the glandular epithelium in the crypts of Lieberkühn and spreads via the intramural or submucosal lymphatics.²⁵ Severe desmoplastic reactions and muscular hypertrophy are features of adenocarcinomas.²⁶ Distinct hypertrophy and hyperplasia of the muscular layers are seen in 78% of intestinal adenocarcinomas even when not involved with the tumour.²⁶ The histopathological features may influence the layering enhancement in adenocarcinomas.

In the histopathological classification system, alimentary lymphoma is considered mucosal (confined to the mucosa) or transmural (mucosa and additional layers).²⁷ Histopathological findings of high-grade alimentary lymphoma are similar to those of transmural disease.^2,5 In transmural lymphoma, the mucosal lamina propria is effaced and the submucosa is heavily infiltrated.²⁸ In advanced transmural lymphoma, the coalescence of the lymphocytic infiltrate obliterates the muscularis propria and spreads to the serosa and adjacent mesentery, leading to mass formation.²⁸ Absence of layering enhancement in lymphoma may be influenced by the transmural infiltration.

Compared with adenocarcinoma, in this study lymphoma showed no intestinal obstruction and greater thickness. Lymphoma causes partial stenosis of the intestinal lumen, but it usually does not cause complete obstruction.¹ Adenocarcinoma grows outward or inward toward the bowel lumen, producing an annular constricting band with minimal outward enlargement.⁸ Therefore, intestinal carcinoma often causes the development of a mechanical ileus due to luminal stenosis, which is less common with lymphoma.¹ Mechanical ileus causes severe, acute clinical signs, and adenocarcinoma can often be diagnosed at a stage of minimal outward enlargement. In contrast, lymphoma may tend to be diagnosed at a later stage with more outward growth. For this reason, the intestinal thickness may be greater in lymphoma than in adenocarcinoma.

Adenocarcinoma most frequently occurs at the ileocaecal junction, followed by the jejunum and ileum.³ The most common sites of lymphoma are the small intestine,^12,29 but the preferred segment depends on molecular clonality.²⁸ High-grade alimentary lymphoma is invariably of B- or T-cell origin.² T-cell lymphoma is most common in the ileum and jejunum.^30,31 B-cell lymphomas affect the stomach, caecum and colon.^2,28 Unfortunately, we did not assess the molecular clonality. Owing to the site of lymphoma, alimentary lymphoma in this study may be of T-cell origin.

High-grade alimentary lymphoma is usually a symmetric wall-thickening lesion, in contrast to adenocarcinomas, which usually have asymmetric wall-thickening lesions.⁸ In this study, both lymphoma and adenocarcinoma tended to have symmetrical wall-thickening lesions. Further studies are needed to assess the relationship of growth patterns between lymphoma and adenocarcinoma.

Alimentary lymphoma is characterised by infiltration of the gastrointestinal tract by neoplastic lymphocytes, with or without regional lymph node involvement.^2,6 Involved lymph nodes are commonly enlarged.¹ The most frequent metastasis sites of adenocarcinoma are the regional lymph nodes, peritoneum, liver and lung.³ Sixty percent of cats with adenocarcinoma had metastases detected at the time of diagnosis.³ Compared with cats with adenocarcinoma, cats with lymphoma had various enlarged regional lymph nodes. In cases of lymphoma, enlarged jejunal lymph nodes tended to be larger than those in adenocarcinoma cases. Enlarged hepatic and ileocaecal lymph nodes were remarkably large in lymphoma, compared with those in healthy cats.²¹ Statistics were not available because of the uneven number of cases for each tumour, but enlarged regional lymph nodes may have a bulkier appearance in alimentary lymphoma than in those in adenocarcinoma.

The sternal lymph nodes receive drainage from the pars sternalis and thoracic duct, which drain from the pars costalis and pars lumbalis, making them responsible for draining all material from the peritoneal cavity.³² Sternal lymphadenopathy can be caused by various neoplastic, inflammatory and haematological diseases.³³ In cats, enlarged sternal lymph nodes are associated with lymphoma, melanoma, biliary carcinoma, mammary carcinoma, renal transitional cell carcinoma and feline infectious peritonitis.³³ Lymphoma is the most common neoplasia associated with enlarged sternal lymph nodes.³³ In this study, cats with alimentary lymphoma and adenocarcinoma showed enlarged sternal lymph nodes. Owing to the uneven number of cases of adenocarcinoma, further studies are needed to assess the frequency of enlargement of the sternal lymph node in adenocarcinoma.

In adenocarcinoma, pulmonary metastases are not commonly reported at the time of diagnosis.^4,25 To our knowledge, pulmonary metastasis of alimentary T-cell lymphoma has been reported as a case report;³⁴ pulmonary metastasis was detected in one case of lymphoma. Although pulmonary metastases of alimentary lymphoma are uncommon, pulmonary metastases may not be a factor in ruling out alimentary lymphoma.

This study has some limitations. First, it included only a small and uneven number of intestinal tumours, including lymphomas and adenocarcinomas, but not mast cell tumours. Secondly, all lymphoma cases were diagnosed using cytology. It can be difficult to differentiate lymphoma from mast cell tumours using cytology because gastrointestinal mast cell tumours often have few granules.³⁵ Further studies should be performed to evaluate the CT findings in a larger population of cats with intestinal tumours, including those with mast cell tumours, by histopathological diagnosis.

Conclusions

In cats, intestinal adenocarcinomas show enhanced layering. Alimentary lymphoma showed no layering enhancement with enlarged regional lymph nodes. Lesions affected by lymphoma were thicker than those with adenocarcinoma. These findings may help differentiate between adenocarcinomas and lymphomas, allowing for the most appropriate treatment options for each cancer.

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: 30 August 2021

Conflict of interest

The authors declare 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

The work described in this manuscript involved the use of non-experimental (owned or unowned) animals. Established internationally recognised high standards (‘best practice’) of veterinary clinical care for the individual patient were always followed and/or this work involved the use of cadavers. Ethical approval from a committee was therefore not specifically required for publication in JFMS. Although not required, where ethical approval was still obtained, it is stated in the manuscript..

Informed consent

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

ORCID iD

Toshiyuki Tanaka

Hideo Akiyoshi

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