Canine ovarian diseases are rare, partly due to early spaying (6,10). The most common ovarian diseases are cystic ovarian disease and ovarian tumors (10). Ovarian neoplasms comprise 0.5% to 1.2% of all canine tumors (6). Ovarian tumors tend to occur in older dogs except for teratomas, which usually affect young dogs (6,10). There is no breed predisposition, but bulldogs and boxers appear to be at a higher risk (16). Ovarian tumors are commonly classified into three types by the cell origin: epithelial cell, sex cord-stromal cell, and germ cell (13,15). Epithelial cell tumors include adenoma, adenocarcinoma, and cystadenoma (6,13). Sex cord-stromal cell tumors include granulosa cell tumors and Sertoli–Leydig cell tumors (18). Germ cell tumors include dysgerminoma and teratoma (13). Approximately 50% of ovarian tumors originate from epithelial cells, followed in order by sex cord-stromal cells and germ cells (11,16,17). Most ovarian tumors are unilateral, and the left ovary is more frequent than the right (17). Approximately 30% of adenocarcinoma and Sertoli-Leydig cell tumors occur bilaterally (10). Ovarian neoplasms should not be excluded from dogs that have undergone an ovarian resection. The remains of the ovary can cause granulosa cell tumors (20).

The clinical findings of ovarian tumors vary depending on the tissue of origin. Most epithelial cell tumors are asymptomatic until a space-occupying mass forms (13). Ovarian tumors may be enormous. Therefore, most dogs with the tumor exhibit abdominal distension, and the mass are palpable on a physical examination. Vaginal bleeding, pyometra, and cystic endometrial hyperplasia are also commonly observed with ovarian tumors (1).

Ovarian tumors often metastasize. One study found that ovarian teratoma showed 50% metastasis, and 48% in adenocarcinoma, usually in the form of carcinomatosis, which is an invasion into the peritoneum and may be accompanied by a large amount of malignant peritoneal fluids (9,17). Distant metastases to the kidneys, adrenal glands, lung, bone, and mediastinal lymph nodes have been reported (10).

Radiography and ultrasonography may help determine the origin of an ovarian mass. When the ovary enlarges, the ligament of the ovary elongates, which causes medial displacement of the adjacent organs on radiographs, not ventral displacement. They may also result in ventral deviation of the caudal pole of the kidney (19). Ultrasonography mainly provides detailed images of the tumor structure. The origin of ovarian tumors can be determined by the appropriate location based on an association with an adjacent uterine horn and being caudal to the kidneys (19). On the other hand, the origin may be difficult to determine owing to the enormous size of the ovarian mass, and with metastases occurring, there may be limitations in diagnosis using only radiography and ultrasonography. As an advanced study, computed tomography (CT) is needed to find the exact origin of the tumor and evaluate metastasis.

Ovarian tumors have similar clinical, radiological, and ultrasonic characteristics (12). CT and MRI are used widely as the main diagnostic tools in human medicine to identify the specific image characteristics of some ovarian tumors, metastasis, and preoperative evaluation (12). CT and MRI may provide useful information for characterizing ovarian masses as non-neoplastic or neoplastic, and in the latter case, as benign or malignant (8,12).

Some studies on the ultrasonographic features of canine ovarian masses, but CT information is often very scarce (6,20). This paper describes the CT imaging features of canine ovarian masses.

Patient selection

Web-based hospital databases from Chungnam National University Animal Hospital, Ian Animal Medical Imaging Center, and Kangwon National University Animal Hospital were searched for ovary, ovarian, ovarian tumor, and ovarian mass between April 2016 and September 2020. The above search was limited to female dogs who had undergone an abdominal CT examination with contrast administration. The cases were excluded if histology was inconclusive or not performed.

Data recorded

The patient signalments, history, physical examination, CT findings, and histopathologic results were reviewed for each dog.

The thoracic and abdominal CT examinations were performed to diagnose and obtain evidence of metastases. The patients were positioned in sternal or dorsal recumbency and were maintained with isoflurane or sevoflurane inhalation anesthesia. The CT instruments (Alexion_{TM, TOSHIBA, Canon Medical Systems, Japan; SOMATOM^TM, Siemens, Germany) were applied. The CT parameters were selected according to each patient’s condition, and approximately 120-130 kilovoltage peak, 100-150 milliampere-seconds, and 1-2.5 mm slice thickness were used. Intravenous (IV) iodinated contrast medium, iohexol (Omnipaque^®, GE healthcare Ireland, Ireland), was then administered with a dose of 600 mgI/kg. After injecting the contrast medium, the artery, portal, and delay phases were scanned. The sagittal and dorsal plane images in the soft tissue window were reconstructed. Using Vitrea workstation version 7 (Vitrea^®, Vital Images, Minnetonka, Minnesota), maximum intensity projection (MIP) reconstruction was carried out to confirm the connectivity between the intra-abdominal tumor and the ovarian artery and to make the origin of the tumor more precise.}

CT interpretation

One reader with two years of experience in veterinary medical imaging with a diagnostic imaging viewer (Zetta Pacs, Taeyoung Soft CO., LTD, Korea) evaluated the CT images. For each lesion, the following parameters were recorded: maximal diameter (mm), the side where the ovarian mass occurred, pre-contrast images attenuation, degree of contrast enhancement, the changes in the uterus, presence of ascites or pleural effusion, carcinomatosis, and distant metastasis.

The measurements of the maximal diameter were made on the transverse plane. The larger side was measured if the mass was bilateral. The morphological characteristics of each abnormal ovary were identified and recorded. Mass attenuation in Hounsfield units (HU) was measured using a soft tissue window of a pre-contrast image on a transverse plane, drawing a region of interest (ROI) along the margin of the mass at the randomly picked three different transverse slices. A mean of these three measurements was calculated. Because soft tissue is 20 to 40 HU, it was judged subjectively that a lower value indicated a smaller composition of soft tissue and more cystic structures. The contrast enhancement of the mass was evaluated by subtracting the pre-contrast value from the post-contrast attenuation values. The mass was considered contrast-enhanced if the difference in CT values was more than 20 HU. This study recorded cases where uterine changes, such as pyometra, hydrometra, and endometrial hyperplasia, were observed together. Cases of metastasis to the peritoneum and distant metastasis to other organs, lymph nodes, lungs, and bones were also confirmed (2).

Sixteen dogs that met the search criteria were identified. Of these sixteen dogs, six dogs met the inclusion criteria and were included in this study. The other ten dogs were excluded because of a lack of histopathologic results. On the other hand, out of the 10 dogs excluded, a dog with a strong suspicion for adenocarcinoma from the peritoneal fluid examination was included, and seven dogs were used.

Table 1 lists the patients’ signalments, clinical signs, and histopathologic findings. The breeds of the patients were three Maltese dogs, one Yorkshire terrier, one Jindo dog, one poodle, and one dachshund. The age of the dogs ranged from seven to 15 years (mean: 10.7 years). The weight range was from 2.6 to 25 kg. The clinical signs at present included abdominal distention (two dogs), lethargy (one dog), mammary gland mass (two dogs), mastitis (one dog), and no clinical signs (one dog). Of the seven ovarian masses, three were identified on the right, two were on the left, and two were bilateral.

Table 1 . Summary of the signalment and histopathology in seven dogs with ovarian masses.

Dog no.	Breed	Gender	Age (years)	Body weight (kg)	Clinical signs	Side	Histological diagnosis
1	Maltese	F	8	3	Lethargy	Right	Adenocarcinoma
2	Maltese	F	9	4.15	Abdominal distension	Left	Adenocarcinoma
3	Poodle	F	12	4.5	Abdominal distension	Bilateral	Adenocarcinoma suspected
4	Yorkshire terrier	F	14	2.64	Mastitis	Left	Granulosa cell tumor
5	Maltese	F	15	4.9	Mammary gland mass	Right	Granulosa cell tumor
6	Dachshund	F	13	5.6	No clinical sign	Right	Sex cord stromal tumor
7	Jindo dog	F	7	25	Mammary gland mass	Bilateral	Ovarian cyst

F, female intact..

Table 2 lists the CT characteristics of the ovarian masses. Examples of epithelial cell tumors (Fig. 1), granulosa cell tumors (Fig. 2), and ovarian cysts (Fig. 3) are shown in each figure. All ovarian diseases were identified reliably by their ovarian artery and connectivity, and a MIP reconstruction has made this easier (Fig. 1G).

Table 2 . CT characteristics of the ovarian masses.

	Epithelial cell tumor (n = 3)	Sex cord tumor (n = 3)	Ovarian cyst (n = 1)
Mean value of maximal diameter (range)	57.59 mm (42.53-69.37)	51.31 mm (31.70-74.51)	66.00 mm
Side	Right 1/3	Right 2/3	Bilateral 1/1
	Left 1/3	Left 1/3
	Bilateral 1/3
Mean value of mass attenuation (range)	39.37 HU (35.00-43.57)	37.71 HU (33.71-40.97)	13.85 HU
Contrast enhancement	3	3	0
Uterine changes	2/3	1/3	0/1
Peritoneal effusion	2/3	0/3	0/1
Pleural effusion	1/3	0/3	0/1
Carcinomatosis	2/3	0/3	0/1
Distant metastasis	2/3	3/3	0/1

Figure 1. CT images of ovarian epithelial cell tumor. (A) Transverse pre-contrast CT image of a right ovarian adenocarcinoma in dog 1. (B) Delayed phase image of post-contrast. (C) Dog 2, transverse pre-contrast image of a left ovarian epithelial cell tumor, which was ambiguous between adenocarcinoma and adenoma. (D) Delayed phase image of post-contrast. (E) Dog 3, transverse pre-contrast image of bilateral ovarian adenocarcinoma suspected. (F) Delayed phase image of post-contrast. (G) Maximum intensity projection reconstruction image of bilateral ovarian adenocarcinoma suspected in dog 3. The connection between the tortuous ovarian artery and the tumor was seen more precisely.

Figure 2. CT images of ovarian sex-cord stromal cell tumor. (A-B) Transverse pre- and post-contrast (delayed phase) CT images of left ovarian granulosa cell tumor in dog 4. The tumor was predominantly solid with a hypodense necrotic region. (C-D) Transverse pre- and post-contrast (delayed phase) CT images of right ovarian granulosa cell tumor in dog 5. (E-F) Transverse pre- and post-contrast (delayed phase) CT images of right sex cord-stromal tumor in dog 6.

Figure 3. CT images of an ovarian cyst. (A) Doral pre-contrast CT image of bilateral ovarian cysts in dog 7. (B) In post-contrast (delayed phase), there was little contrast enhancement.

A large-sized adenocarcinoma of the right ovary was observed in dog 1, and the lesion was composed of cysts and solids, showing a clear contrast enhancement effect (Fig. 1A, B). Furthermore, metastasis to the peritoneum, sternal and cranial mediastinal lymph nodes, and severe peritoneal and pleural effusions were observed with pyometra. The left ovarian mass in dog 2 was a large adenocarcinoma, substantially composed of soft tissue, and pyometra were observed (Fig. 1C, D). Dog 3 has a soft tissue density bilateral ovarian tumor with an irregular margin, showing heterogeneous and distinct enhancement (Fig. 1E, F). In addition, the metastasis to sternal and visceral lymph nodes and peritoneum were observed and accompanied by a large number of ascites. Through the peritoneal fluid examination, the tumor was strongly suspected of adenocarcinoma. Dog 4 has an oval-shaped granulosa cell tumor derived from the left ovary occupying the entire abdominal cavity. The mass was predominantly solid and showed homogeneous parenchyma with severe enhancement (Fig. 2A, B) and metastasis to sternal lymph nodes. Dog 5 was presented with a round-shaped right ovary granulosa cell tumor. The CT characteristics of this ovarian neoplasm were cystic and solids, unlike other sex cord-stromal tumors (Fig. 2C, D), and the sternal lymph node showed metastatic change. In dog 6, the diameter of the right ovarian sex cord-stromal tumor was 74.51 mm, the largest size of any other tumor, and the mass showed severe enhancement with mainly solid components (Fig. 2E, F). In addition, endometrial hyperplasia and metastasis to the sternal lymph node were observed. Dog 7 had ovarian cysts on both with a low percentage of soft tissue and mild enhancement (Fig. 3).

The main goal of this study was to describe the CT characteristics of ovarian masses in seven dogs. A few studies have been performed on ovarian diseases in female dogs using CT over the last few decades (1).

Normal ovaries have a small size, measuring up to 25 mm depending on the dog’s size and phase of the reproductive cycle (6,20). When affected by a neoplasm or cystic disease, the size can vary considerably and usually increase in size (6). In this study, the ovarian masses ranged from 31.70 to 74.51 mm in diameter. The granulosa cell tumor had the smallest average diameter. Differential diagnoses should be made between the tumors and cystic ovarian disease because ovarian tumors often contain multiple cystic structures (8). Many researchers have stated that it is difficult to establish a clear definition and morphological characteristics of an ovarian tumor because various characteristics and patterns appear as the disease progresses (3,9,15).

Ovarian tumors often occur unilaterally, and the left ovary is more frequent than the right (5,17). Five out of seven ovarian tumors (two epithelial cell tumors, three sex cord tumors) affected the unilateral ovary: three affected the right, and two affected the left ovary. In a previous study, including 63 dogs, ovarian lesions were found more frequently in the left ovary (5). No specific conclusion could be drawn because of the limited number of canine patients used in this study.

Human medicine has several reports of features in CT and MRI of ovarian tumors (8,12). The higher proportion of the solid, the more likely the neoplasm is to be malignant (12,14). The morphological features that are more likely to be benign tumors include a diameter of less than 4 cm, entirely cystic components, a wall thickness of less than 3 mm, a lack of internal structure, and the absence of ascites and invasion to the peritoneum or adenopathy (12). Most ovarian tumors in this study appeared to be a mixed texture of soft tissue and cystic structures. The differences in morphological characteristics of CT between the three groups were unclear. The HU value for soft tissue is 20-40 and 0 for water. Accordingly, a lower HU value of the tumor indicated a higher proportion of cystic components. There were no significant differences in the HU value between epithelial cell tumors and sex-cord stromal cell tumors. Only one patient with an ovarian cyst showed relatively low HU values, which is consistent with earlier studies that entirely cystic components are most likely to be benign lesions (12). Only a benign neoplasm showed mild contrast enhancement because of the slight soft tissue composition, while six malignant neoplasms showed moderate to severe contrast enhancement.

Uterine abnormalities with pyometra or cystic endometrial hyperplasia were detected by CT in three dogs. In particular, sex cord-stromal cell tumors may present as vaginal bleeding, pyometra, or an unusual frequency of estrus related to endometrial hyperplasia, presumably because of the excessive estrogenic steroid production by tumor tissues (4). Unlike previous studies, only one out of three (33.3%) patients with sex cord-stromal tumors had endometrial hyperplasia. Two out of three (66.6%) patients with epithelial cell tumors had pyometra, with a higher probability of uterine change. On the other hand, this study included a small population making it difficult to identify the tendency between the uterine changes and ovarian tumor types.

The presence of ascites was detected in the malignancy by CT with two epithelial cell tumors; one also had pleural effusion. The hypodense fluid was filled around the abdominal organs and ovarian masses, and carcinomatosis was also suspected. The findings of the peritoneal fluid may be associated with peritoneal dissemination, and a careful assessment of metastasis should be carried out if pleural effusion or ascites are identified (14). Even among the ovarian masses, malignancy was more frequent than benign masses, and distant metastases were identified in five out of six ovarian malignant tumor patients. This shows that ovarian tumors have a very high metastasis rate, suggesting that the CT test is essential.

The MIP reconstruction projects the voxel with the highest attenuation value on every view throughout the volume onto a 2D image (7). This is used most widely to produce angiographic images (7). If the ovarian mass occurs bilaterally, the origin can be estimated relatively quickly through the location or clinical symptoms of the patient when confirmed by ultrasound. On the other hand, it may be challenging to identify the origin if it is unilateral and huge. MIP reconstruction is beneficial in a diagnosis by clearly and intuitively showing the connection between the tortuous ovarian artery and mass.

This study had several limitations. Only a small number of cases were included in this study because all ovarian mass cases did not perform CT scans or a biopsy. Statistical analysis was not performed due to the small population size.

In conclusion, the present study describes the CT features of ovarian masses in seven ovarian masses subdivided into three types. The results may help veterinarians evaluate the appearance of ovarian masses with CT. A CT examination is essential for identifying malignant ovarian tumors more frequently and observing distant metastasis. Using MIP reconstruction will be of great help in evaluating the origin. The differences in the morphological characteristics of CT between the three groups were unclear. Because the association between the soft tissue composition ratio and malignancy in the ovarian tumor parenchyma was confirmed, CT may enable certification diagnosis or signally narrow the range of differential diagnoses using the HU value of the ovarian mass or the degree of contrast enhancement. The characterization of ovarian masses may help distinguish benign and malignant tumors, avoiding improper management.

Further studies involving larger patient numbers, comparing the characteristic of each tumor type, and MR image features would help refine the clinicians’ diagnostic accuracy with this group of diseases.

The authors have no conflicting interests.