Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Acta Veterinaria Scandinavica https://doi.org/10.1186/s13028-022-00638-x RESEARCH Open Access Anatomic, computed tomographic, and ultrasonographic assessment of the lymph nodes in presumed healthy adult cats: the abdomen, pelvis, and hindlimb Mauricio Tobón Restrepo1,2* , Rosa Novellas1 , Adrià Aguilar1, Xavier Moll1 and Yvonne Espada1    Abstract Background: The computed tomography (CT) and ultrasonography (US) features of lymph nodes of the abdomen, pelvis, and hindlimb in healthy cats are poorly described in the current literature. A prospective anatomic and refer- ence interval study was therefore performed. The lymph nodes of six feline cadavers were identified, and dimensions were measured (length, width, and height). The lymph nodes from 30 healthy adult cats were identified and meas- ured using CT (pre- and postcontrast) and US. The identification and dimensions of the separate lymph nodes were compared between imaging techniques and the anatomic study. Results: The identification of lymph nodes was most frequent in CT, and the dimensions were overall larger than those identified and measured in US and the anatomic study. The caudal epigastric and sacral lymph nodes were not identified in the anatomic study. The ischiatic, lumbar aortic, internal iliac, and caudal epigastric lymph nodes were not visualized in US. The height presented the main statistical differences among techniques. The lymph nodes were mainly homogeneous in pre- and postcontrast CT and US images. Some lymph nodes showed a hyperattenuating periphery with a hypoattenuating center (on pre- and postcontrast images) and a hypo-/isoechoic periphery with a hyperechoic center, representing the hilar fat. The lymph nodes were commonly elongated and rounded except for the jejunal lymph nodes, which had an irregular shape. Conclusions: The assessment of most of the abdominal, pelvic, and hindlimb lymph nodes in the cat is feasible using CT and US, with CT performing best. Factors like the amount of adipose tissue and contrast administration subjec- tively improved the lymph node visualization and assessment. The measurements and features reported are proposed as reference values. Keywords: Abdominal, Computed tomography, Feline, Lymph nodes, Imaging Background The abdominal lymph centers in the cat are divided into parietal and visceral groups as in dogs [1, 2]. The pari- etal group has four lymph centers (lumbar, iliosacral, *Correspondence: matores79@gmail.com inguinofemoral, and ischiatic), and the visceral group 2 has three lymph centers (celiac, cranial and caudal mes- Present Address: Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 108, 3584 enteric) [3, 4]. Previous studies regarding the ultrasono- CM Utrecht, The Netherlands graphic assessment of the abdominal cavity in the cat Full list of author information is available at the end of the article reported that the most frequently identified lymph nodes © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 2 of 25 from the visceral group are the gastric, hepatic, pancrea- xiphoid process in the linea alba with a 24-scalpel blade. ticoduodenal, jejunal, ileocecal, and colic lymph nodes; The incision was continued caudally with Mayo scissors and from the parietal group are the medial iliac and the until the pubic bone. Afterward, the abdominal muscles superficial inguinal lymph nodes [5]. The lymph nodes were cut following the costal arch until the spine. Then, less frequently identified in the visceral group are the blunt dissection of the abdominal lymph nodes was per- splenic and caudal mesenteric lymph nodes, and in the formed with special care in not tearing any great vessels. parietal group are the lumbar aortic, renal, internal iliac Then, the skin was removed from the hindlimbs with an (formally called hypogastric [4]), sacral, and caudal epi- incision in the cranial aspect of the thigh until the talus. gastric lymph nodes [5, 6]. The peripheral lymph nodes After that, the incision surrounded the talus, and the of the abdomen are described as fusiform and slender in skin was pulled off. The lymph nodes were searched fol- shape with ultrasonography (US). When compared with lowing the previous anatomic descriptions [3, 5, 9]. The surrounding fat tissue, they appeared slightly rounded, lymph nodes were measured using a manual dial cali- with regular margins and hypoechoic. Deep abdominal per (Vernier 0–150 mm/0.02 high precision). The length lymph nodes were described as more rounded and elon- was defined as the largest dimension in the craniocau- gated in shape, slightly hypoechoic to the surrounding dal plane. For the lymph nodes of the cranial mesenteric peritoneum, and with regular margins [5, 7]. The iliofem- lymph center, the length was measured following a paral- oral and the popliteal lymph centers have been identified lel direction with the gastrointestinal tract or the jejunal as the two lymph centers for the cat’s hindlimb [3]. In vessels. The height was obtained at the thickest point in ultrasound, the popliteal lymph node is described as an the dorsoventral plane, and the width was measured at oval or rounded node of variable size (short axis range of the thickest point in the mediolateral plane. A short-to- 2.8–6.5 mm; long axis range of 4.3–12.0 mm) [8]. long axis ratio was calculated with the length and height There is scarce literature about the normal computed to determine the shape. As previously described, a lymph tomographic appearance of the abdominal lymph nodes node was classified as rounded when the short-to-long in the cat. In dogs, abdominal lymph nodes have been axis ratio was > 0.5, and elongated when the short-to-long described as homogeneously attenuating structures axis ratio was ≤ 0.5 [2, 10]. Multilobular lymph nodes commonly elongated in shape. Some lymph nodes were that did not fit the ratio were classified as miscellaneous. slightly irregular or relatively more hyperattenuating in The number, anatomical landmarks, shape, and size of the periphery than centrally before and after contrast lymph nodes per lymph center were recorded. administration due to the presence of fatty tissue in the hilus [2]. Imaging study To the authors’ knowledge, studies comparing the iden- Clinically healthy cats older than 1 year were prospec- tification, dimensions and features of abdominal and tively recruited from October 2013 to July 2015. All ani- hindlimb lymph nodes between gross dissection, CT, and mals belonged to staff, students, and hospital clients at US are lacking. the Fundació Hospital Clinic Veterinari of the Universi- The aims of this study were: (i) to describe the features tat Autònoma de Barcelona. The owner’s writing consent of the abdominal, pelvic, and hindlimb lymph nodes in was obtained for all the included cats. Clinically healthy CT and US in a group of healthy adult cats, and (ii) to status was determined based on physical examination compare the identification and dimensions of the lymph (performed by AA and XM), biochemical profile [glucose, nodes from the abdomen and hindlimb obtained with total proteins, cholesterol, calcium, potassium, alanine- US and CT in a group of healthy adult cats with those amino-transferase (ALT), gamma-glutamyl-transferase obtained from an anatomic study. (GGT), creatinine, urea], complete blood count, fast test to rule out feline immunodeficiency virus antibod- Methods ies and feline leukemia virus antigens, and a polymerase Anatomical study chain reaction test for Bartonella sp. as described pre- Cadavers of cats referred to the pathology department viously by the authors [11]. To perform CT and US, the of the Universitat Autònoma de Barcelona from January patients underwent sedation using midazolam (0.2 mg/ 2013 to June 2015 were prospectively included. Exclu- kg) (Midazolam 15 mg/3 mL, Normon, Spain), butorpha- sion criteria were: time of death > 24 h, age < 1-year, and a nol (0.4 mg/kg) (Torbugesic 10 mg/mL, Zoetis, Madrid, cause of death due to inflammatory or neoplastic condi- Spain), and ketamine (5 mg/kg) (Imalgene 100 mg/mL, tions. The cadavers were included if owner consent was Merial, Barcelona, Spain). Anesthesia was induced and obtained. maintained with Isoflurane (1.5–5% dosage 100% O ­ 2 at The dissections were performed by one author (MTR). 4 L/min) (Isoflurane, Abbott Laboratories, Berkshire, A small incision was made immediately caudal to the UK). CT and US images were acquired and reviewed by Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 3 of 25 a Ph.D. candidate/veterinarian (MTR) under the supervi- as the distance from the medial to the lateral border, and sion of a board-certified veterinary radiologist (RN) and a height was defined as the distance from the ventral to the radiology professor (YE). dorsal border in each position. The highest values were used for the statistical analysis. The short-to-long axis Computed tomography ratio was calculated in each lymph node using the higher A whole-body CT scan was performed with the cats value of height divided by the value of length obtained in positioned in dorsal recumbency with the forelimbs and the multiplanar reconstruction. The shape was then clas- hindlimbs along the sides. Dorsal recumbence was per- sified according to the ratio in the same way as explained formed for optimal image comparison between CT and in the anatomic study. A 2–4 ­mm2 circular/oval region US and the anatomical study in which the cadavers were of interest (ROI) was placed over the same cranial, mid- helical CT-scanner ­(GE® Brivo CT 385, Madrid, Spain). in a similar position. Scans were performed in a 16-slices dle, and caudal transverse slices (where width and height measurements were performed) to calculate attenuation Images are acquired in a soft tissue algorithm before (Hounsfield units) values. Attenuation measurements Iopromide (300 mgI/mL) ­(Ultravist® 300 mg/mL, Bayer and after intravenous administration of 600 mg/kg of were performed in both pre- and postcontrast images. Mean values for attenuation pre- and postcontrast were mL) ­(Scanlux® 300 mg/mL, Sanochemia pharmazeutika, Pharma AG, Berlin, Germany) or Iopamidol (300 mgI/ calculated using the three previously obtained measures. As in previously reported studies, lymph nodes attenu- Neufeld/Leitha, Austria) via the cephalic vein. Technical ation was compared with the surrounding muscles and details were: slice thickness of 0.625 mm, interval thick- was classified as isoattenuating, slightly hypoattenuat- ness of 0.625 mm, collimation pitch of 1.25 mm, 120 kV, ing (slightly less attenuating and homogeneous), hypoat- 50–90 mA, and matrix of 512 × 512. In this study, the tenuating (markedly less attenuating and homogeneous), assessment of the abdominal cavity to identify the lymph hyperattenuating and heterogeneous (single or multiple nodes was performed following anatomic references areas of different attenuation within the lymph node). and available literature [3, 4, 11, 16]. Using multiplanar On postcontrast images, the attenuation was classified reconstruction on CT images, the lymph nodes along the as homogeneous, mildly heterogeneous (small, multiple intestinal tract (e.g., colic lymph node) or along the great areas of varying contrast enhancement), heterogeneous vessels of the abdomen (e.g., medial iliac lymph node) (large, multiple areas of varying contrast enhancement), were numbered from oral to aboral and from cranial to and peripheral enhancement (contrast enhancement in a caudal, respectively. The jejunal lymph node at the medial ring-like distribution with a hypoattenuating center). or dorsal aspect of the jejunal vessels was numbered as one and at the lateral or ventral as two. The most ventral Ultrasonography ileocecal lymph node was numbered as one and the dor- Ultrasonographic examination was performed in all cats sal as two. All these indications were also used during the after the CT scan with the maintenance of general anes- US examination and in the anatomic study to accurately thesia. The animals were positioned in dorsal recum- compare the different lymph nodes. bency (similar to CT), and the hair of the abdomen and The CT dimensions and features of each identi- the caudal aspect of each stifle was clipped. B-Mode ­Xvision® (Firenze, Italy) ultrasound machine with a fied lymph node were performed following previously ultrasonography was performed using an Esaote Mylab70 described methods for measuring and comparing CT images [2, 9, 11]. All recollected data were recorded using 4–13 MHz frequency linear transducer. Settings on the Electric® Healthcare). an image archiving and communication system software machine were adjusted to optimize image acquisition for Acoustic coupling gel (Transonic ­gel®, Telic, Barcelona, (Centricity PACS-IW, General ­ each patient, including depth, focus, gain, and frequency. Measurements were performed as previously described for dogs [2, 9]. Two previously reported methods were Spain) was generously applied to ensure adequate skin- used to determine the length; (1) calculated length: mul- transducer contact. tiplying the number of transverse images that contained For the sagittal plane, the transducer was placed with the lymph node by the slice thickness; and (2) multiplanar the guide pointing cranial and parallel to the spine. An reconstruction-length (MPR-length): a sagittal image of image including the largest measurement of the lymph the lymph node at its maximal dimension was generated node was recorded. For the lymph nodes of the cranial with multiplanar reconstruction, an electronic caliper mesenteric lymph center (e.g., jejunal, colic, ileocecal), was placed from the cranial to the caudal border to meas- the image for the sagittal plane was performed following ure the length of the lymph node. Width and height were a parallel direction to the longitudinal axis of the intes- measured in transverse images at the cranial, middle, and tines or blood vessels. Measurement in this image was caudal aspects of the lymph nodes. The width was defined performed using an electronic caliper from the cranial to Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 4 of 25 the caudal border (long axis) of the lymph node and was sp. (3/4) and feline immunodeficiency virus antibodies defined as length. In the same image, a second measure- (1/4), resulting in a final study sample of 30 presumed ment made perpendicularly to the first one at the point of clinically healthy cats. The average age was 3.7 years the maximum thickness (ventral to dorsal) was defined as (range 1.5–17), and the average weight was 4.4 kg (range the height (short axis). As for the anatomic study and the 3.0–7.0). Twenty-nine cats were domestic short-hair, and CT images, the short-to-long axis ratio was calculated for one cat was a Persian. The study population consisted of each lymph node and used to determine the shape. For 16.7% males (n = 5), 20.0% neutered males (n = 6), 30.0% the transverse image of the lymph node, the transducer females (n = 9), and 33.3% neutered females (n = 10). was rotated 90° with the guide towards the patient’s right Table 1 shows the frequency of identification of lymph side to select then an image that contained the largest nodes per technique. Tables 2, 3 and 4 summarizes the portion of the lymph node. A measurement was per- mean and standard deviation for the length, width, and formed from medial to lateral in this image and was con- height together with the results of the statistical com- sidered the width. parisons among techniques. Additional file 1 shows the For each lymph node, echogenicity was recorded as attenuation values (Hounsfield units) of the lymph nodes. hypoechoic, isoechoic, hyperechoic, or heterogeneous Additional file 2 summarizes the echogenicity of the when compared to surrounding fat tissue. The presence lymph nodes, and Additional file 3 summarizes the shape of a hyperechoic central line that corresponded with the of the lymph nodes per technique. hilus was also recorded. The shape of each lymph node was evaluated following the same criteria as in CT. Mar- Lymph center description gins were defined as smooth or irregular. Celiac lymph center (Lymphocentrum celiacum) Gastric lymph nodes: In the anatomic study, one round Statistics or ovoid lymph node was found in the omentum of the Statistic tests were selected by one of the authors (MTR) gastric lesser curvature (Fig. 1A). A fair amount of fat and a statistician (OC). Data were digitalized using tissue covered the lymph node in most cases. On CT Microsoft Excel (Microsoft Office Excel, 2010, USA). images, one or two lymph nodes were observed in close Statistical analyses were performed using the free avail- contact with the left gastric vein at the gastric lesser cur- able statistics software R (R version 3.2.3, 2015-12-10), vature (Fig. 1C, D). On the US images, the transducer Copyright ©, the R foundation for statistical comput- was placed parallel to the spine immediately caudal to ing). Descriptive statistics (frequency, mean, median, the xiphoid process and then moved slightly to the left and standard deviation) of lymph nodes identification, until an image with the liver to the left of the screen and attenuation values in pre- and postcontrast images, echo- the stomach to the right was obtained (Fig. 1B). One or genicity, and measurements were calculated. Wilcoxon two lymph nodes were in the omentum of the lesser gas- Signed Rank Test was used to compare the pair distribu- tric curvature, in the fat tissue between the liver and the tion between the calculated length and the MPR-length stomach. A hyperechoic central line was visible in 33.33% obtained of the lymph nodes on CT images, as well as of the identified gastric lymph nodes. MPR-length, height, and width between CT and US. Hepatic lymph nodes: In the anatomic study, it was Mann–Whitney U test was used to compare the pair located at the porta hepatis, dorsal, and slightly to the left distribution of the lymph nodes measurements (MPR- of the portal vein (Fig. 2A). On the CT transverse images, length, width, and height) between CT and anatomy; and these lymph nodes were frequently identified dorsally between US and anatomy. Each measurement was com- and slightly to the left of the portal vein (Fig. 2B–D). On pared individually for each lymph center and not for the US images, these were identified by placing the trans- whole sample of identified lymph nodes (No Post-Hoc ducer parallel to the spine and caudally to the xiphoid corrections were used). A P value < 0.05 was considered process, fanning slightly from right to left lateral. These statistically significant. lymph nodes were located on the left side of the portal vein. A hyperechoic central line was visible in 6.60% of Results the lymph nodes. Anatomic study: six feline cadavers were included. Two Splenic lymph nodes: This lymph node was embed- cats died of heart failure, two of kidney failure, one due ded in the fat tissue of the splenic hilus adjacent to the to poisoning, and one of unknown cause. The average splenic vein on both the anatomic study and CT images age was 6.8 years (range 1–16). The breed includes five (Fig. 3A, C, D). Ultrasonographically, the splenic vein domestic short-hair and one British long-hair cat. was the main landmark to localize the lymph node. Imaging study: Thirty-four cats were recruited, but four When identified, this was adjacent to the vein in the were excluded due to a positive test result for Bartonella fat tissue of the splenic hilus, close to the head of the Table 1 Frequency of lymph node identification in each technique Lymph center Lymph node Frequency Lymph center Lymph node Frequency CT US Anatomy CT US Anatomy n % n % n % n % n % n % Celiac Gastric 1 28 93.33 27 90.00 5 83.33 Lumbar Right renal 7 23.33 2 6.67 2 3.33 Gastric 2 6 20.00 2 6.67 0 0.00 Left renal 4 13.33 0 0.00 2 33.33 Tobón Restrepo et al. Acta Veterinaria Scandinavica Hepatic 22 73.33 20 66.67 5 83.33 Iliosacral Right medial iliac 28 93.33 30 100.00 5 83.33 Splenic 23 76.67 23 76.67 2 33.33 Left medial iliac 28 93.33 30 100.00 5 83.33 Pancreaticoduodenal 29 96.67 29 96.67 6 100.00 Right internal iliac 19 63.33 0 0.00 1 16.67 Cranial mesenteric Jejunal 1 30 100.00 30 100.00 6 100.00 Left internal iliac 19 63.33 0 0.00 0 0.00 Jejunal 2 28 93.33 28 93.33 5 83.33 Right sacral 8 26.67 1 3.33 0 0.00 (2022) 64:18 Jejunal 3 14 46.67 15 50.00 4 66.67 Left sacral 4 13.33 0 0.00 0 0.00 Jejunal 4 0 0.00 0 0.00 3 50.00 Inguinofemoral Right Superficial inguinal 28 93.33 28 93.33 4 66.67 Ileocecal 1 27 90.00 30 100.00 6 100.00 Left superficial inguinal 1 28 93.33 29 96.67 4 66.67 Ileocecal 2 27 90.00 24 80.00 4 66.67 Left superficial inguinal 2 1 3.33 0 0.00 0 0.00 Colic 1 27 90.00 21 70.00 6 100.00 Right superficial caudal epigastric 1 26 86.67 0 0.00 0 0.00 Colic 2 15 50.00 0 0.00 6 100.00 Right superficial caudal epigastric 2 4 13.33 0 0.00 0 0.00 Colic 3 9 30.00 0 0.00 4 66.67 Right superficial caudal epigastric 3 1 3.33 0 0.00 0 0.00 Colic 4 5 16.67 0 0.00 4 66.67 Left superficial caudal epigastric 1 26 86.67 0 0.00 0 0.00 Colic 5 4 13.33 0 0.00 2 33.33 Left superficial caudal epigastric 2 2 6.67 0 0.00 0 0.00 Caudal mesenteric Caudal mesenteric 1 29 96.67 10 33.33 5 83.33 Ischiatic Right ischiatic 6 20.00 0 0.00 1 16.67 Caudal mesenteric 2 14 46.67 0 0.00 4 66.67 Left ischiatic 3 10.00 0 0.00 1 16.67 Caudal mesenteric 3 5 16.67 0 0.00 2 33.33 Popliteal Right popliteal 29 96.67 30 100.00 6 100.00 Caudal mesenteric 4 2 6.67 0 0.00 1 16.67 Left popliteal 29 96.67 29 96.67 6 100.00 Lumbar Lumbar aortic 1 4 13.33 0 0.00 3 50.00 Lumbar aortic 2 0 0.00 0 0.00 2 33.33 Lumbar aortic 3 0 0.00 0 0.00 1 16.67 Page 5 of 25 Table 2 Mean and standard deviation for length, width, and height of the lymph nodes of the celiac and cranial mesenteric lymph centers Lymph Celiac Cranial mesenteric center Lymph Gastric 1 Gastric 2 Hepatic Splenic Pancreatico- Jejunal 1 Jejunal Jejunal Jejunal Ileocecal Ileocecal Colic 1 Colic 2 Colic 3 Colic 4 Colic 5 node duodenal 2 3 4 1 2 Lengthmm CT- 6.34 4.48 9.14 5.08 7.20 (2.18) 34.50 (7.80) 23.60 12.10 – 7.82 (2.52) 7.44 (2.76) 12.58 8.63 6.88 4.76 5.80 (2.42) Calc (2.62) (0.74) (3.26) (1.63) (7.20) (3.40) (4.00) (2.49) (3.25) (1.16) CT- 6.58 6.12 9.03 5.33 6.38 (1.82) 36.97 (5.42) 26.73 13.80 – 7.38 (2.21) 7.1 (1.96) 11.86 7.57 5.98 4.06 5.20 (3.52) MPR (3.18) (3.91) (2.77) (2.01) (4.75) (2.50) (3.71) (2.51) (1.92) (0.77) US 5.99 4.00 6.15 5.41 5.76 (1.49) 25.05(6.19) 17.87 10.00 – 7.13 (2.65) 6.55 (1.92) 8.14 – – – – (2.05) (0.28) (2.32) (2.03) (7.74) (2.34) (2.39) Anat- 8.56 – 10.84 4.35 5.60 (3.06) 45.30 26.78 11.08 18.67 5.78 (2.37) 5.10 (0.88) 15.68 8.75 6.85 6.70 4.85 (2.89) omy (6.45) (2.17) (2.62) (10.83) (12.45) (1.50) (18.58) (10.59) (3.62) (1.45) (3.07) Tobón Restrepo et al. Acta Veterinaria Scandinavica MPR A** A* A* A* vs. Calc CT- A* A* A* A* A* MPR vs US (2022) 64:18 CT- B* MPR vs Anat US vs B** B* Anat Width mm CT 3.30 3.23 3.89 4.12 6.05 (1.79) 9.55 (4.44) 9.58 10.25 – 5.37 (1.54) 7.57 (9.06) 5.94 5.09 4.58 5.40 4.20 (1.68) (1.06) (1.11) (1.67) (1.32) (4.91) (3.06) (3.02) (1.91) (1.50) (1.79) US 4.87 3.50 5.33 3.80 5.77 (2.13) 10.93 (5.23) 15.27 8.68 – 6.36 (2.84) 5.96 (2.32) 7.44 – – – – (1.16) (2.40) (1.95) (1.31) (6.04) (4.69) (3.38) Anat- 3.14 – 4.20 2.65 2.55 (1.05) 7.90 (3.50) 5.40 3.75 3.67 2.95 (0.91) 3.45 (1.05) 3.05 4.08 3.48 3.40 3.55 (1.77) omy (1.05) (2.02) (1.20) (1.31) (0.71) (1.80) (0.63) (1.57) (1.12) (0.89) CT vs A** A* US CT vs B** B* B* B* B** B* Anat US vs B* B** B* B* B* B** B* Anat Heigth mm CT 3.04 3.43 4.48 3.55 4.31 (1.36) 6.27 (2.58) 5.78 8.53 – 3.80 (1.20) 6.41 (9.8) 5.35 3.70 2.87 3.36 3.30 (1.00) (1.27) (0.86) (1.62) (1.38) (1.70) (4.11) (2.98) (1.53) (0.92) (1.47) Page 6 of 25 Table 2 (continued) Lymph Celiac Cranial mesenteric center Tobón Restrepo et al. Acta Veterinaria Scandinavica Lymph Gastric 1 Gastric 2 Hepatic Splenic Pancreatico- Jejunal 1 Jejunal Jejunal Jejunal Ileocecal Ileocecal Colic 1 Colic 2 Colic 3 Colic 4 Colic 5 node duodenal 2 3 4 1 2 US 2.50 3.10 2.92 2.53 3.17 (0.94) 4.42 (1.55) 4.23 4.38 – 3.06 (1.01) 2.94 (0.59) 3.68 – – – – (0.72) (0.28) (0.77) (0.94) (1.07) (1.75) (1.29) (2022) 64:18 Anat- 1.1 (0.14) – 2.44 1.5 (0.71) 1.1 (0.64) 2.50 (1.87) 1.55 1.55 – 1.35 (0.39) 1.47 (0.57) 1.23 1.35 1.30 1.20 1.45 (0.21) omy (1.55) (1.05) (0.24) (0.46) (0.49) (0.47) (0.18) CT vs A* A* A** A* A* A** A* US CT vs B** B* B* B** B* B* B* B** B** B* B* B* B* Anat US vs B** B** B* B* B* B** B** Anat The statistical comparison among techniques is shown CT: computed tomography, US: ultrasonography, Anat: Anatomy, NC: not calculated, SD: standard deviation, CT-MPR: multiplanar reconstruction-length, CT-Calc.: calculated-length *P-value < 0.05, **P-value < 0.01, (A) Wilcoxon signed-rank test, (B) Mann–Whitney U test Page 7 of 25 Table 3 Frequency, mean and standard deviation for length, width, and height of the lymph nodes of the caudal mesenteric, lumbar, and iliosacral lymph centers Lymph Caudal mesenteric Lumbar Iliosacral center Lymph Caudal Caudal Caudal Caudal Lumbar Lumbar Lumbar Right Left Right Left Right Left Right Left sacral node mesenteric mesenteric mesenteric mesenteric aortic 1 aortic 2 aortic 3 renal renal medial medial internal internal sacral 1 2 3 4 iliac iliac iliac iliac Length mm CT- 11.37 (4.60) 9.44 (4.27) 10.24 (5.01) 12.80 (0.42) 4.25 – – 9.20 9.25 16.52 17.04 7.96 8.08 5.58 5.65 (1.72) Calc (1.87) (2.97) (2.55) (4.78) (7.03) (2.14) (1.88) (2.24) CT- 10.34 (4.50) 8.98 (4.44) 10.88 (6.26) 13.05 (0.49) 3.93 – – 9.30 8.80 17.85 17.52 8.17 8.66 5.09 4.65 (1.38) MPR (1.55) (3.87) (2.20) (4.85) (4.11) (2.65) (2.60) (2.48) US 10.00 (2.22) – – – – – – 8.10 – 10.27 11.62 – – 5.20 (NC) – (1.70) (3.56) (3.46) Tobón Restrepo et al. Acta Veterinaria Scandinavica Anat- 7.34 (4.99) 7.52 (2.23) 6.80 (5.09) 6.70 (–) 3.57 5.40 4.50 (–) 11.40 8.65 12.48 13.28 12.00 6.70 (NC) – – omy (2.02) (3.25) (8.77) (4.60) (6.58) (4.74) (NC) MPR vs. Calc (2022) 64:18 CT- MPR vs US CT- B** MPR vs Anat- omy US vs Anat- omy Width mm CT 5.14 (2.21) 5.37 (2.36) 6.38 (2.22) 6.45 (2.05) 2.17 – – 4.64 3.30 3.46 3.31 4.25 4.07 4.76 4.72 (1.72) (0.92) (1.61) (1.29) (1.25) (1.00) (1.91) (1.81) (1.83) US 7.77 (2.69) – – – – – – 6.10 – 4.64 4.12 – – – – (2.69) (1.72) (1.33) Anat 3.12 (0.73) 3.12 (0.75) 4.00 (1.70) 4.00 (NC) 1.70 1.95 2.00 (NC) 3.10 2.30 (NC) 3.82 2.88 4.70 (NC) 4.40 (NC) – – (0.72) (0.35) (0.42) (1.08) (0.73) CT vs US CT vs B** Anat- omy US vs Anat- omy Page 8 of 25 Table 3 (continued) Lymph Caudal mesenteric Lumbar Iliosacral center Lymph Caudal Caudal Caudal Caudal Lumbar Lumbar Lumbar Right Left Right Left Right Left Right Left sacral node mesenteric mesenteric mesenteric mesenteric aortic 1 aortic 2 aortic 3 renal renal medial medial internal internal sacral 1 2 3 4 iliac iliac iliac iliac Tobón Restrepo et al. Acta Veterinaria Scandinavica Heigth mm CT 3.51 (1.44) 3.53 (1.55) 3.62 (1.82) 4.30 (1.27) 1.82 – – 3.31 2.95 2.42 2.60 3.10 3.73 2.09 2.17 (0.84) (1.13) (1.07) (1.38) (0.65) (1.16) (1.50) (1.71) (0.67) US 3.50 (0.98) – – – – – – 3.25 – 3.45 3.28 – – 2.00 (NC) – (0.64) (1.34) (0.84) (2022) 64:18 Anat- 1.66 (0.64) 1.82 (1.20) 1.90 (0.42) 1.90 (NC) 0.87 1.30 (NC) 0.90 (NC) 1.15 1.30 1.40 1.56 2.50 (NC) – – – omy (0.58) (0.21) (0.42) (0.87) (0.88) CT vs US CT vs B* B* Anat- omy US vs Anat- omy The statistical comparison among techniques is shown CT: computed tomography, US: ultrasonography, NC: not calculated, SD: standard deviation, CT-MPR: multiplanar reconstruction-length, CT-Calc.: calculated-length * P-value < 0.05, **P-value < 0.01, (A) Wilcoxon signed-rank test, (B) Mann–Whitney U test Page 9 of 25 Table 4 Frequency, mean and standard deviation for length, width, and height of the lymph nodes of the inguinofemoral, ischiatic, and popliteal lymph centers Lymph Inguinofemoral Ischiatic Popliteal center Lymph node Right Left Left Right Right Right Left Left Right Left ischiatic Right Left popliteal superficial superficial superficial superficial superficial superficial superficial superficial ischiatic popliteal inguinal inguinal 1 inguinal 2 caudal caudal caudal caudal caudal epigastric 1 epigastric 2 epigastric 3 epigastric 1 epigastric 2 Length mm CT-Calc 9.24 (3.03) 8.81 (4.14) 6.90 12.25 (5.56) 7.83 (3.87) 13.80 (NC) 13.71 (5.35) 15.00 (0.85) 4.92 (1.65) 5.63 (0.65) 8.24 (1.93) 8.14 (2.35) CT-MPR 9.03 (3.17) 8.12 (3.23) 9.90 (NC) 12.55 (6.98) 7.53 (5.16) 12.70 (NC) 13.37 (5.38) 16.25 (1.63) 4.58 (1.28) 4.63 (0.50) 8.02 (1.78) 8.49 (2.30) US 7.25 (1.75) 7.21 (2.28) – – – – – – – – 7.73 (2.36) 7.88 (2.35) Anatomy 13.60 (5.62) 13.05 (5.33) – – – – – – 3.20 (–) 3.30 (–) 7.37 (2.28) 6.63 (1.82) MPR vs. Tobón Restrepo et al. Acta Veterinaria Scandinavica Calc MPR-CT 9.24 (3.03) 8.81 (4.14) 6.90 12.25 (5.56) 7.83 (3.87) 13.80 (NC) 13.71 (5.35) 15.00 (0.85) 4.92 (1.65) 5.63 (0.65) 8.24 (1.93) 8.14 (2.35) vs US MPR-CT vs Anatomy (2022) 64:18 US vs Anatomy Width mm CT 6.88 (2.53) 6.76 (2.95) 6.90 (NC) 5.80 (1.96) 4.30 (0.82) 6.90 (NC) 5.72 (1.95) 5.60 (2.4) 4.05 (0.76) 3.73 (0.91) 6.29 (1.65) 5.97 (1.25) US 6.19 (3.11) 5.43 (1.82) – – – – – – – – 5.99 (1.26) 6.05 (1.32) Anatomy 3.45 (1.69) 3.27 (1.49) – – – – – – 2.00 (NC) 6.00 (NC) 4.45 (2.52) 4.10 (1.80) CT vs US CT vs B* Anatomy US vs Anat- B* tomy Heigth mm CT 3.21 (1.14) 3.04 (1.28) 4.20 (NC) 3.88 (1.25) 3.83 (1.95) 5.90 (NC) 3.83 (1.35) 5.00 (0.85) 2.42 (0.63) 2.50 (0.1) 5.11 (1.83) 5.42 (1.45) US 2.72 (0.90) 2.67 (0.62) – – – – – – – – 4.99 (1.24) 5.11 (1.36) Anatomy 1.27 (0.72) 1.27 (0.70) – – – – – – 1.00 (NC) 1.00 (NC) 1.58 (0.93) 1.67 (1.04) CT vs US CT vs B** Anatomy US vs B** Anatomy The statistical comparison among techniques is shown CT: computed tomography, US: ultrasonography, NC: not calculated, SD: standard deviation, CT-MPR: multiplanar reconstruction-length, CT-Calc.: calculated-length * P-value < 0.05, **P-value < 0.01, (A) Wilcoxon signed-rank test, (B) Mann–Whitney U test Page 10 of 25 Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 11 of 25 Fig. 1 Gastric lymph node. A Image of the dissection showing its localization (arrow) in the lesser omentum (LO) of the stomach (S), near the pylorus (P). B Ultrasonographic image showing an elongated gastric lymph node (between cursors) with an isoechoic center and a hypoechoic periphery, located between the stomach (S) and the liver (L). C, D CT images indicating the localization of an isoattenuating gastric lymph node (arrow) in the lesser omentum in the precontrast image (C) and with a homogeneous contrast enhancement pattern in the postcontrast image (D). A second lymph node (arrowhead) is partially visible dorsally, between the stomach (S) and the spleen (Sp). The liver (L) and pylorus (P) are indicated spleen (Fig. 3B). The appearance of the splenic lymph area, surrounded by a hypoechoic ring and a thin hyper- node was commonly hypoechoic (47.83%). However, a echoic rim at the periphery. center isoechoic to the mesenteric fat within a hypo- echoic periphery was identified in 34.78% of the lymph Cranial mesenteric lymph center (Lymphocentrum nodes and was classified as heterogeneous. A hypere- mesentericum craniale) choic central line was identified in 26.70% of the lymph Jejunal lymph nodes: In the anatomic study, one to four nodes. jejunal lymph nodes were identified. Three cadavers pre- Pancreaticoduodenal lymph nodes: In the anatomic sented four lymph nodes, and one, two, or three lymph study, it was located adjacent to the cranial pancrea- nodes were found in one cadaver each. These lymph ticoduodenal vessels at the cranial duodenal flexure nodes were located along the jejunal vessels just proxi- (Fig. 4A). On the CT images, one pancreaticoduodenal mal to the origin of the ileocolic artery. At least two large lymph node was seen ventral to the cranial portion of jejunal lymph nodes with an elongated shape were identi- the duodenum on the right side of the abdomen (Fig. 4C, fied in each animal (Fig. 5A). In the CT images, one to D). On the US images, one pancreaticoduodenal lymph three jejunal lymph nodes were frequently (93.3%) identi- node was always found on the right side, slightly caudal fied at the dorsal and ventral aspects of the jejunal vein and ventral to the pylorus and cranial duodenal portion (Fig. 5C, D). Three jejunal lymph nodes were found in 15 (Fig. 4B). In 37.93% of the identified pancreaticoduode- cats, two in 13 cats, and only one lymph node in two cats. nal lymph nodes, heterogeneous echogenicity was noted, On the US examination, the ileocolic junction was used characterized by a central isoechoic to the mesenteric fat as a landmark. Once it was located, the transducer was Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 12 of 25 Fig. 2 Hepatic lymph node. A Image of the dissection showing the localization of the lymph node (arrow) in the porta hepatis, near the portal vein (P). The liver (L) and gallbladder (GB) are indicated. B Ultrasonographic image showing the hepatic lymph node (between cursors) in the porta hepatis. The liver (L) and a partially visible portal vein (P) are indicated. C, D CT images indicate a slightly hypoattenuating hepatic lymph node (arrow) in the precontrast image (C) and with homogeneous contrast enhancement in the postcontrast image (D). It is located normally at the dorsomedial aspect of the portal vein (P) and ventromedial to the caudal vena cava (asterisk). The liver (L) and the spleen (Sp) are indicated directed caudal and to the center of the abdomen until in six cats. The main landmark in finding the ileocecal visualizing the jejunal vein. The jejunal lymph nodes lymph nodes was the ileocolic junction. An image of this were located on each side of the vein. Four jejunal lymph with a sagittal plane of the ileum was obtained, and then nodes were identified in one cat, three in 16 cats, two in a slight movement to the right lateral side of the patient 11 cats, and one lymph node in one cat. A hyperechoic allowed their visualization (Fig. 6B). A hyperechoic cen- central line was visible in only 5.20% of the jejunal lymph tral line was visible in 5.50% of the lymph nodes. nodes. Colic lymph nodes: In the anatomic study, three and Ileocecal lymph nodes: In the anatomic study, two five colic lymph nodes were found in two cadavers. Addi- lymph nodes were observed in four cadavers, and only tionally, two and four lymph nodes were seen in one one was seen in two cadavers. They were in the ileoce- cadaver each. The colic lymph nodes were located in cal ligament along the ileocecal vessels, one on each the mesocolon, near the ascending and transverse colon side between the ileum and the cecum (Fig. 6A). On the (Fig. 7A). At least two lymph nodes were bigger and more CT images, two ileocecal lymph nodes were identified elongated than the rest, normally one near the ascending in 26 cats and only one in two cats. The anatomic land- colon and one within a group of nodes located near the mark for these lymph nodes was the ileocolic junction. transverse colon. On the CT images, the identification of On transverse slices, they were identified slightly caudal one, two, three, four, and five colic lymph nodes was pos- to the junction in a dorsal and ventral position between sible in twelve, six, four, one, and four cats, respectively. the ileum and cecum (embedded in the adipose tissue of These lymph nodes were seen along the colonic blood the ileocecal ligament) (Fig. 6C, D). On the US images, vessels (Fig. 7C, D). Multiplanar sagittal reconstructions two lymph nodes were identified in 24 cats and only one were helpful in the localization of these lymph nodes. On Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 13 of 25 Fig. 3 Splenic lymph node. A Image of the dissection showing its localization (arrow) in the splenic hilus along the splenic vein (SV). The spleen (Sp) is partially visible. B US image showing the splenic lymph node (between cursors) at the splenic hilus. The spleen (Sp) and a partially visible splenic vein (asterisk) are indicated. C, D CT images indicating the localization of the splenic lymph node (short arrow), which is slightly hypoattenuating with a hypoattenuating center in the precontrast image (C) and showing slightly heterogeneous contrast enhancement (D). The splenic vein (long arrow), the pancreas (P), and the spleen (Sp) are indicated US images, only one colic lymph node could be success- slightly ventral to the descending colon and dorsolateral fully identified in 21 cats and was not seen in 9 cats. This to the left aspect of the urinary bladder (Fig. 8C, D). On lymph node was close to the ileocolic junction (Fig. 7B). the US assessment, only one lymph node was identified In order to distinguish it from the ileocecal lymph nodes, in 10 of the 30 cats located between the bladder and the the transducer was displaced medially from the ileocolic descending colon (Fig. 8B). A hyperechoic central line junction instead of laterally. A hyperechoic central line was visible in 3.30% of these lymph nodes. was visible in 6.70% of these lymph nodes. Lumbar lymph center (Lymphocentrum lumbale) Caudal mesenteric lymph center (Lymphocentrum Lumbar aortic lymph nodes: In the anatomic study, one, mesentericum caudale) two, and three small rounded lymph nodes were seen in One to four caudal mesenteric lymph nodes were iden- one cadaver each. These lymph nodes were located along tified in the cadavers of the anatomic study. Two lymph and between the aorta and caudal vena cava (Fig. 9A). nodes were present in one cadaver. One, three, and four On CT images, one lumbar aortic lymph node was found lymph nodes were found in one cadaver each. These in three cats, and two were found in two cats. The pres- lymph nodes were located along the caudal mesenteric ence of fat tissue around the aorta and caudal vena cava vessels (Fig. 8A). On CT images, one lymph node was in these five cats gave enough contrast to differenti- seen in 14 cats; two, three, and four lymph nodes were ate these lymph nodes from the surrounding soft tissue found in nine, three, and two cats, respectively. These attenuating structures such as the large vessels or hypax- lymph nodes were seen on transverse images located ial musculature. However, the localization of the lumbar Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 14 of 25 Fig. 4 Pancreaticoduodenal lymph node. A Image of the dissection showing the localization of the pancreaticoduodenal lymph node (arrow) near the pancreas (P) and the duodenum (arrowhead). B US image showing a heterogeneous, rounded pancreaticoduodenal lymph node (between cursors), between the duodenum (arrowhead), pancreas (P), and the liver (L). C, D CT images indicate the localization of a rounded pancreaticoduodenal lymph node (arrow), which is isoattenuating with a hypoattenuating center in the precontrast image (C) and with peripheral homogeneous contrast enhancement in the postcontrast image (D). The liver (L), gall bladder (GB), duodenum (arrowhead), portal vein (asterisk), stomach (S), and spleen (Sp) are indicated aortic lymph nodes on CT images was dorsal to the aorta and extended cranially until the deep circumflex iliac rather than between the aorta and the caudal vena cava vessels (Fig. 10A). On the CT images, the lymph nodes (Fig. 9B–D). The lumbar aortic lymph nodes were not were identified in 28 cats bilaterally. The location of these identified ultrasonographically in any of the cats. lymph nodes was as described in the anatomic study, and Renal lymph nodes: In the anatomic study, the left more specifically, extending from the cranial end-plate of and right renal lymph nodes could be identified only in the seventh lumbar vertebra (L7) until the cranial end- two cadavers. These small and rounded lymph nodes plate of the first sacral vertebra (S1) (Fig. 10C, D). Some were seen in close contact with the renal vessels. On lymph nodes were very thin in their mid-portion, pre- CT images, both renal lymph nodes were identified in senting a bilobed shape. Ultrasonographically, both right five cats, and only the right was seen in two cats. These and left medial iliac lymph nodes were identified in all lymph nodes were located dorsal and slightly cranial to the cats with a similar location as described in the cadav- each renal vessel. On the US images, only the right renal ers and on CT (Fig. 10B). A hyperechoic central line was lymph node was seen in two cats adjacent to the junction identified in 18.30% of these lymph nodes. of the renal vein with the caudal vena cava. Internal iliac lymph nodes: Right and left internal iliac lymph nodes were found only in one cadaver, along Iliosacral lymph center (Lymphocentrum iliosacrale) the internal iliac vessels. On the CT images, these sin- Medial iliac lymph nodes: In the anatomic study, one gular lymph nodes were visualized in 17 cats bilaterally. right and one left medial iliac lymph node were identified Additionally, unilaterally one right and one left lymph in five cadavers. These singular lymph nodes were located node were identified in two cats each. These lymph slightly dorsal and lateral to the external iliac arteries nodes were located at the ventrolateral aspect of the Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 15 of 25 Fig. 5 Jejunal lymph nodes. A Image of the dissection showing the localization of the jejunal lymph node (arrow) in the mesentery along the jejunal vessels (JV). The jejunal loops (J) are indicated. B US image showing a miscellaneous shaped, hypoechoic jejunal lymph node (between cursors). The jejunal vessels (asterisk) are partially seen. C, D CT images in dorsal reconstruction indicating the localization of the jejunal lymph nodes (arrows) seen isoattenuating in the precontrast image (C) and with homogeneous contrast enhancement in the postcontrast image (D). The jejunal loops (J), colon (Co), stomach (S), spleen (Sp), pancreas (P), and urinary bladder (UB) are indicated first sacral vertebra (ventral to the sacral wings) along Inguinofemoral lymph center (Lymphocentrum the internal iliac vessels in contact with the body of inguinofemorale) the ilium (Fig. 11). On US assessment, the internal iliac Superficial inguinal lymph nodes: In the anatomic study, lymph nodes were not identified in any of the cats. the right and the left superficial inguinal lymph nodes Sacral lymph nodes: These lymph nodes were not were identified in four cadavers. The location of these identified in the anatomic study. On CT images, the lymph nodes was cranial to the inguinal canal in contact right and the left sacral lymph nodes were identified in with the external pudendal vessels and embedded in fat two cats. Only the right sacral lymph node was identi- tissue (Fig. 12A). On CT images, the right and left super- fied in six cats, and only the left was identified in two ficial inguinal lymph nodes were identified in 24 cats. cats. These lymph nodes were in the midline at the ven- Additionally, one right, one left, and one right and two tral aspect of the sacrum. On US assessment, one right left lymph nodes were seen in one cat each. These lymph sacral lymph node was visualized in one cat, only in the nodes were located slightly caudal and dorsal to the junc- sagittal plane, allowing the measurement of the length tion between the external pudendal and caudal epigastric and the height. A transverse image was not possible to vessels, ventral to the pubic bone (Fig. 12C, D). On the obtain due to its caudal position in the pelvic cavity; US assessment, singular right and left superficial ingui- therefore, the width was not provided. nal lymph nodes were identified in 28 cats and in one Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 16 of 25 Fig. 6 Ileocecal lymph nodes. A Image of the dissection showing the localization of the ileocecal lymph nodes (arrow) near the ileocolic junction, along the ileocolic vessels (asterisk). The ileum (I), cecum (Cc), and colon (Co) are indicated. B US image showing two elongated and hypoechoic ileocecal lymph nodes (between cursors) between the ascending colon (Co) and ileum (I). C, D CT images indicating the localization of the ileocecal lymph node (arrows), which is isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D). The colon (Co), ileum (I), jejunal loops (J), right (RK) and left (LK) kidneys, and spleen (Sp) are indicated cat only on the left side. They were visualized in the adi- anatomic study (Fig. 14C, D). The ischiatic lymph nodes pose tissue cranioventral to the pubic bone (Fig. 12B). A were not visualized with US. hyperechoic central line was visible in 21.80% of these lymph nodes. Popliteal lymph center (Lymphocentrum popliteum) Superficial caudal epigastric lymph nodes: This group The right and left popliteal lymph nodes were identi- of lymph nodes was identified in 26 cats only on CT fied in all the cadavers. These nodes were embedded in images. One right and occasionally three (in 5/26), and the adipose tissue located in the caudal aspect of the sti- one left and occasionally two (in 2/26) lymph nodes were fle joint, in contact with the medial aspect of the lateral identified. The location of these lymph nodes was along saphenous vein (Fig. 15A). On CT images, both popliteal the caudal epigastric vessels in the subcutaneous adipose lymph nodes were identified in 29 cats. On the US assess- tissue of the ventrolateral abdominal wall (at the level of ment, the right and left popliteal lymph nodes were iden- the 6th–7th lumbar vertebrae) (Fig. 13). tified in 29 cats, and only the left was seen in one cat. In the imaging study, the popliteal lymph nodes were Ischiatic lymph center (Lymphocentrum ischiadicum) located in the adipose tissue of the caudolateral aspect of Ischiatic lymph nodes: The right and left ischiatic lymph the stifle joints (Fig. 15B–D). nodes were found in one cadaver. These rounded nodes were located at the base of the tail, partially covered by Statistical analysis the gluteofemoralis muscle and embedded in adipose tis- Computed tomography showed a higher frequency of sue (Fig. 14A, B). On the CT images, the ischiatic lymph lymph node identification when compared to US and nodes were found in one cat bilaterally. Additionally, five anatomy (Table 1). cats presented only the right, and two cats presented only The lymph nodes dimensions measured on CT, US, the left lymph node. The location was as described in the and gross dissection during the anatomic study showed Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 17 of 25 Fig. 7 Colic lymph node. A Image of the dissection showing the localization of the colic lymph node (arrow) near the ascending colon (Co) and ileum (I). B Doppler US image showing the colic lymph node (among cursors), blood flow can be seen in the mesenteric vessels. C, D CT images indicating the localization of the colic lymph node (arrow), which is isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D). The colon (Co), ileum (I), jejunal loops (J), right (RK) and left (LK) kidneys, and spleen (Sp) are indicated differences when compared to each other using the of the lymph node on the right side showed statistically Wilcoxon signed-rank test (CT and US) and the Mann– significant differences between CT and anatomy. Whitney U test (CT, US, and Anatomy) (Tables 2, 3, The width of the lymph nodes in the anatomic study and 4). was often lower than the measurements obtained by CT In this study, the MPR-length on CT images showed and US. Statistical significant differences were observed a better reflection of the dimensions of the abdomi- for the pancreaticoduodenal, the second and third jeju- nal lymph nodes during the anatomy study. There- nal, the ileocecal, the first colic, and the left ischiatic fore, the MPR-length was chosen to compare between lymph nodes. The width of the gastric lymph node on US techniques. The comparison of the MPR-length of the was higher compared to CT and anatomy, and the differ- lymph nodes showed few differences with US and anat- ences were statistically significant. The width of the right omy mainly with lymph nodes from the celiac and cra- medial iliac lymph node in anatomy was slightly higher nial mesenteric lymph center. The length of the hepatic than on CT, being statistically significant. lymph nodes obtained with US was statistically sig- The height was the measurement that showed more nificantly lower when compared to CT and anatomy. statistically significant differences among the three tech- Additionally, the length of the jejunal lymph nodes was niques. The height of the gastric, the splenic, the pan- almost 10 mm higher on CT than on US, and this dif- creaticoduodenal, the jejunal, the left superficial inguinal, ference was statistically significant. The length of both and the ileocecal lymph nodes was statistically signifi- ileocecal lymph nodes in anatomy was lower com- cantly higher on CT and US than in the cadavers. Besides pared to CT and US, showing statistical significance. that, it was statistically different from anatomy height Although the length of the medial iliac lymph nodes in measurements. The height on CT was also statistically CT was higher than in anatomy and US, only the length significantly higher than on US. Additionally, the height Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 18 of 25 Fig. 8 Caudal mesenteric lymph node. A Image of the dissection showing the localization of the caudal mesenteric lymph node (arrow) near the descending colon (Co) along the caudal mesenteric vessels (CM). B US image showing the caudal mesenteric lymph node (between cursors) near the descending colon (Co). C, D CT images indicating the localization of the caudal mesenteric lymph node (arrow), which is isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D). The descending colon (Co) and the urinary bladder (UB) are indicated of the hepatic, the colic (except the most caudal), the fat with a more hypoechoic periphery and a hypere- first caudal mesenteric, and the right medial iliac lymph choic rim; therefore, they were classified as heterogene- nodes was statistically significantly higher on CT than ous. Mainly the gastric, the splenic, the medial iliac, the with anatomy. superficial inguinal, and the popliteal lymph nodes pre- Most of the lymph nodes were isoattenuating or sented a higher percentage of heterogeneous echogenic- slightly hypoattenuating to the surrounding muscula- ity than the other lymph nodes (Additional file 2). ture (Additional file 1). A negative mean Hounsfield unit An elongated shape was commonly found in the lymph was obtained in the left renal and lumbar aortic lymph nodes of this study, however, rounded (hepatic, splenic, nodes. However, these lymph nodes were tiny, and most pancreaticoduodenal, and popliteal lymph nodes) and of them had a hypoattenuating center and were classi- miscellaneous (jejunal, medial iliac, and ileocecal lymph fied as heterogeneous. After contrast administration, nodes) shapes were also present (Additional file 3). most of the lymph nodes showed homogeneous contrast enhancement. However, the renal lymph nodes (right: n Discussion 4/7 = 57.14%; left: n 3/4 = 75.00%) were frequently pre- The identification of almost all the lymph centers of senting a heterogeneous attenuation, followed by the the abdomen, pelvis, and hindlimb was possible dur- splenic (n 5/23 = 21.74%) and both right and left pop- ing gross dissection in the anatomic study. However, liteal (n 5/29 = 17.24% each) lymph nodes. A peripheral accurate assessment of some lymph nodes (e.g., lumbar contrast enhancement was present in eight (n 23) lymph aortic, sacral, and caudal epigastric lymph nodes) was nodes, being more frequent for the splenic lymph nodes. not achieved because of their similar appearance to the In ultrasound, the majority of the lymph nodes were surrounding fat tissue. A dyeing procedure was not per- hypoechoic, followed by isoechoic. A small percentage formed before the dissection because the animals were showed a center that was isoechoic to the mesenteric presented for post-mortem examination within 24 h of Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 19 of 25 Fig. 9 Lumbar aortic lymph nodes. A Image of the dissection showing the localization of the lumbar aortic lymph node (arrow) between the abdominal aorta (Ao) and the caudal vena cava (asterisk). The psoas (Ps) muscles are indicated. B–D CT images indicating the localization of the lumbar aortic lymph node (arrow) in the sagittal plane seen with heterogeneous contrast enhancement with a hypoattenuating central area postcontrast (B) and in the transverse plane seen slightly hypoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D). The psoas (Ps) muscles, aorta (Ao), caudal vena cava (asterisk), and right (RK) and left (LK) kidneys are indicated death. In our study, the mean length of the abdominal length of the abdominal and hindlimb lymph nodes but lymph nodes in the anatomic study was smaller than the their width and height as well. reports in the literature. Previous anatomic descriptions A previous study reported the CT features of the reported a length range for the abdominal lymph nodes abdominal lymph nodes in healthy cats [17]. However, of 1 cm to 8 cm. However, that study included cats from the paper refers to each lymph node in the abdomen as 7 days to 10 years old, resulting in 33.3% of cats under the lymph centers. In our study, a clear definition of each 1 year old [16]. Previous studies reported statistically sig- lymph center and its representative lymph nodes is made. nificant differences in the size of lymph nodes when com- Also, in the mentioned study, the dimensions and fea- paring young versus adult animals because of the active tures from several lymph nodes per location (e.g., three production of lymphoid cells at a young age [13, 14]. or more jejunal lymph nodes) were combined to pro- The lymph nodes of the abdomen, pelvis, and hindlimbs vide the mean values. In our study, a description of the in dogs have been well documented in the anatomy books number of lymph nodes per location was provided. This and assessed using CT and US [1, 2, 4, 10, 15]. In cats, the may explain the difference in length and width (smaller anatomic locations, landmarks, drainage areas, and the values in the previous study) when compared to the number of lymph nodes per lymph center have been well lymph nodes in our study. Additionally, it only reports documented in anatomy studies [3, 4, 16, 12]. However, the length and width, but there is no clarity on how these in those anatomic references, mostly the length of lymph measurements were obtained or the landmarks used to nodes was reported. In our study, we report not only the differentiate each group of lymph nodes. Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 20 of 25 Fig. 10 Medial iliac lymph nodes. A Image of the dissection showing the localization of the medial iliac lymph node (arrow) along the aortic trifurcation (asterisk) and the external iliac vessels (EI). The psoas muscles (Ps) and descending colon (Co) are indicated. B US image showing a hypoechoic medial iliac lymph node (between cursors) with a fusiform shape located ventral to the psoas (Ps) muscles. C, D CT images indicating the localization of the medial iliac lymph nodes (arrows) in the dorsal plane, which is isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D), around the aortic trifurcation (asterisk) between the external iliac vessels (EI) and the psoas (Ps) muscles. The descending colon (Co) is indicated Fig. 11 Internal iliac lymph nodes. A, B CT transverse images indicating the localization of isoattenuating internal iliac lymph nodes (arrows) in the precontrast image (A) that show homogeneous enhancement in the postcontrast image (B). The lymph nodes are located near the medial aspect of the ilium (I), ventral to the sacrum (S1), and along the internal iliac vessels (asterisk). The colon (Co) and the urinary bladder (UB) are indicated Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 21 of 25 Fig. 12 Superficial inguinal lymph nodes. A Image of the dissection showing the localization of the superficial inguinal lymph nodes (arrow) along the external pudendal vessels (asterisks). B US image showing a heterogeneous superficial inguinal lymph node (between cursors) embedded in the inguinal adipose tissue (asterisks). C, D CT transverse images indicating the localization of the superficial inguinal lymph nodes (arrows), which is isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D). The pubis (asterisk) is indicated A description of the ultrasonographic characteristics contrast medium as part of a thoracic duct lymphog- of the lymph nodes in the abdominal cavity was previ- raphy in cats using CT [8]. The US features were not ously published [5]. In that study, the visualization of the provided, but their measurements were similar to those medial iliac, jejunal, pancreaticoduodenal, splenic, and in the present study. lumbar aortic lymph nodes in the cat was reported with Few statistical differences were found regarding the a frequency between 60 and 100% [5]. In contrast, the length of the lymph nodes among techniques. The ileocecal, colic, and gastric lymph nodes were also identi- hepatic and jejunal lymph nodes were shorter on US fied with a high frequency in this study. Additionally, the than in the other techniques. We hypothesized that caudal mesenteric lymph node was also more frequently the presence of gas in the stomach and intestinal loops, identified in our study than in the previously published the location (hepatic lymph node), and a miscellaneous study [5]. The lumbar aortic, internal iliac, left sacral, and shape (jejunal lymph nodes) could have influenced the left renal lymph nodes were not visualized on US images achievement of a correct acoustic window to obtain the in our study, but they were identified in a previous study whole length of these lymph nodes. Similar limitations [5]. We hypothesize that this could be due to the lack of have been reported in dogs [18]. The mean length of the contrast between these small structures and the tissues lymph nodes on US in our study showed some differ- between the aorta and caudal vena cava. The use of real- ences from those previously reported [5]. The hepatic time compound imaging US in the previous publication, and caudal mesenteric lymph nodes in our study were which produces a higher border definition and soft tissue longer. Additionally, the pancreaticoduodenal and right contrast compared with B-Mode, might have increased sacral lymph nodes in our study were shorter. The cause their ability to depict these lymph nodes [5]. for these differences remains unclear, but the sam- The popliteal lymph node was assessed in one study ple size, demographic characteristics of included cats, during ultrasound-guided intranodal injection of Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 22 of 25 Fig. 13 Caudal epigastric lymph nodes. A–D CT transverse (A and B) and dorsal (C and D) images indicating the localization of the caudal epigastric lymph nodes (arrows) in precontrast (A and C) and postcontrast (B and D) images along the caudal epigastric vessels (asterisk). In A and B, mammary tissue is indicated (arrowheads) fasting period, the scanning planes, and the interob- The attenuation and Hounsfield Units of the lymph server variability might have been contributing factors. nodes in this study before contrast administration was The width and height of the lymph nodes obtained consistent with the descriptions and values reported for in the anatomic study were shorter than in the imaging dogs [2] and the medial retropharyngeal lymph nodes in techniques. Some of them showed statistical differences, healthy cats [9]. In our study, some of the lymph nodes mainly for the pancreaticoduodenal, jejunal, ileocecal, in the abdominal cavity (splenic and renal) and in the and colic lymph nodes. We hypothesized that the lack of hindlimb (popliteal) showed a nodal periphery isoat- blood perfusion and the loss of fluids after death could tenuating or slightly hypoattenuating to the musculature; contribute to these differences. meanwhile, the center of the node was hypoattenuat- The height was the most variable measurement ing. This appearance has been reported for abdominal between CT and US. A possible explanation is that the lymph nodes in dogs [2, 15, 19], and has been observed relative orientation of the lymph nodes is likely to be by these authors for the sternal and axillary lymph nodes influenced by patient position, scanning plane used in healthy cats, and is produced by the presence of a fatty for the assessment, and filled intestinal loops and peri- hilus [11]. After contrast administration, a homogene- stalsis that could induce displacement in a ventrodor- ous contrast enhancement was more frequently visual- sal or lateral direction of the lymph nodes. All the cats ized. In the lymph nodes with a fatty hilus, a peripheral in this study were positioned in dorsal recumbency for enhancement was observed. This phenomenon is due to the acquisition of the CT images. However, avoiding an the presence of vascularized nodal tissue in the periph- oblique orientation of the abdominal lymph nodes in CT ery; meanwhile, the hilus had less vascularized fat tissue. transverse images was challenging. Similar limitations The lymph nodes of the abdomen, pelvis, and hindlimb have been described in dogs [2]. were more frequently hypoechoic or isoechoic to the Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 23 of 25 Fig. 14 Ischiatic lymph node. A, B Images of the dissection showing the localization of the ischiatic lymph node (arrow) deep to the gluteofemoralis muscle (GF). C, D CT transverse images indicating the localization of the ischiatic lymph node (arrow) seen isoattenuating in the precontrast image (C) and with homogeneous enhancement in the postcontrast image (D), deep to the gluteofemoralis (asterisk) muscle. A coccygeal vertebra (Cc) is indicated surrounding tissue. Similar descriptions have been than neoplastic or inflammatory diseases was challeng- reported for dogs [18]. The presence of a hyperechoic ing, resulting in a small sample size in the anatomic center, especially in the popliteal lymph nodes, was most study. The use of ink solutions or other staining proce- likely due to fat in the hilus (a feature also visible in CT). dures in the cadavers was not performed, which could This hyperechoic center was different from the described have assisted in the differentiation of the lymph nodes hyperechoic central line. This line was thin and well- from the surrounding fat tissue during dissection, espe- defined, corresponding to the description of the hilus [6, cially in the sublumbar region and for the superficial 7, 9, 20]. inguinal lymph nodes. The animals used in the imaging The shape of the lymph nodes in this study is similar study were assessed with US immediately after the CT to previously reported shapes for dogs [6, 7, 14, 18, 21]. scan. Therefore, the analysis of the CT images was not The lymph nodes that presented a rounded shape were performed at the same time as the US examination, mak- smaller and had regular margins. The shape could be ing an exact correlation in the number of lymph nodes compared with the image in CT, being the same in all the identified with both techniques challenging. In some of cases. In previous reports, rounded lymph nodes in com- the patients, a period of apnea during the whole-body CT bination with increased size, loss of the hilus, and echo- scan was difficult to achieve, and movement artifact was textural changes were suggestive of malignancy [10, 22, present, especially in the cranial abdomen. This artifact 23]. The rounded lymph nodes in our study were small, reduced the identification of the lymph nodes, mainly regular, and homogeneous and were considered nor- from the celiac lymph center. All the cats included in this mal since all the included cats were healthy according to study were fasted to avoid complications during anesthe- physical examination and blood tests. sia; however, some of them presented gas and feces in The present study included several limitations. The the colon that may have reduced the visualization of the search for feline cadavers with a cause of death other lymph nodes of the lumbar and iliosacral lymph centers Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 24 of 25 Fig. 15 Popliteal lymph nodes. A. Image of the dissection showing the localization of the popliteal lymph node (arrow) in the caudo-proximal aspect of the stifle joint. B. US image showing a heterogeneous (hyperechoic central area compatible with the hilus) popliteal lymph node (between cursors) caudally to the gastrocnemius muscle (G). C - D. CT images indicating the localization of the popliteal lymph nodes (arrows) seen as heterogeneous with isoattenuating periphery and hypoattenuating center in the precontrast image (C) with homogeneous peripheral enhancement in the postcontrast image (D). The gastrocnemius (G) muscles are indicated. on US due to the gas and fecal material reverberation and Supplementary Information distal acoustic shadowing artifacts. The online version contains supplementary material available at https://​doi.​ org/​10.​1186/​s13028-​022-​00638-x. Conclusions Additional file 1. Computed tomography characteristics of the lymph The identification of the lymph nodes of the abdomen, nodes of the abdomen, pelvis, and hindlimb of healthy cats. pelvis, and hindlimb is excellent with both imaging tech- Additional file 2. Ultrasonographic features of the lymph nodes of the niques when compared with node identification during abdomen, pelvis, and hindlimb in healthy cats. gross dissection. The length of the lymph nodes is more Additional file 3. Distribution of the different shapes of the lymph nodes in each technique according to the short-to-length axis ratio. challenging to assess with US than with CT, where mul- tiplanar reconstruction can be used. The lymph nodes were more frequently isoattenuating to surrounding Acknowledgements The authors want to thank the staff member and owners of the cats of the musculature in CT. However, some of them showed a hospital clinic veterinari of the Autonomous University of Barcelona for hypoattenuating center corresponding to a fatty hilus. allowing their pets to participate in this study. The authors acknowledge Dr. Frequently, the abdominal and hindlimb lymph nodes Oriol Camps for his support in the statistical analysis of the present study. The authors thank Dr. Stefanie Veraa for the English language correction of this were hypoechoic or isoechoic. An elongated shape with manuscript. regular margins was most frequently visible except for the jejunal, medial iliac, and ileocecal lymph nodes that Prior publication Data have not been published previously. showed a miscellaneous shape and the hepatic, splenic, pancreaticoduodenal, and popliteal lymph nodes that Author contributions were rounded. This study can be used as an anatomic and MTR, RS, and YE contributed to the conception and study design. MTR, RN, AA, XM, and YE contributed to the acquisition of data. MTR performed the analysis imaging reference while comparing the size of abdominal and interpretation of data and drafted the manuscript. All authors revised the lymph nodes in cadavers, US, and CT examinations, as submitted manuscript. All authors read and approved the final manuscript. well as provide a detailed description of the lymph cent- ers in CT and US. Tobón Restrepo et al. Acta Veterinaria Scandinavica (2022) 64:18 Page 25 of 25 Funding nodes in presumed healthy adult cats: the head, neck, thorax, and fore- The first author of this study (MTR) received financial support by a Ph.D. limb. J Anat. 2021;239:264–81. https://​doi.​org/​10.​1111/​joa.​13429. scholarship from the Colombian government & Departamento Administrativo 12. Sugimura M, Kudo N, Takahata K. Studies on the lymphonodi of cats: III. de Ciencia, Tecnología e Innovación (COLCIENCIAS). Grant program: Becas Macroscopical observations on the lymphonodi in the abdominal and Francisco José de Caldas, 2010. pelvic cavities. Jpn J Vet Res. 1958;6:69–88. http://​hdl.​handle.​net/​2115/​ 1729. Accessed 1 Oct 2013. Availability of data and materials 13. Burns GO, Scrivani PV, Thompson MS, Erb HN. Relation between age, The datasets obtained and analyzed during the current study are available body weight, and medial retropharyngeal lymph node size in apparently from the corresponding author on reasonable request. healthy dogs. Vet Radiol Ultrasound. 2008;49:277–81. 14. Krol L, O’Brien R. Ultrasonographic assessment of abdominal lymph nodes in puppies. Vet Radiol Ultrasound. 2012;53:455–8. Declarations 15. Rossi F, Patsikas MN, Wisner ER. Abdominal lymph nodes and lymphatic collecting system. In: Schwarz T, Saunders JH, editors. Veterinary com- Ethics approval and consent to participate puted tomography. Ames: Wiley-Blackwell; 2011. p. 371–9. The ethical committee of the Universitat Autònoma de Barcelona (reference 16. Sugimura M, Kudo N, Takahata K. Studies of lymphonodi of cats: II. Macro- #CEAAH 2255 of September 2013) approved this study. A written owner con- scopical observations on the lymphonodi of the body surfaces, thoracic sent of all the patients was obtained before inclusion in the study. and pelvic limbs. Jpn J Vet Res. 1956;4:101–12. http://​hdl.​handle.​net/​ 2115/​1694. Accessed 1 Oct 2013. Consent for publication 17. Perlini M, Bugbee A, Secrest S, Scott SC. Computed tomographic Not applicable. appearance of abdominal lymph nodes in healthy cats. J Vet Intern Med. 2018;32:1070–6. Competing interests 18. Agthe P, Caine AR, Posch B, Herrtage ME. Ultrasonographic appearance of The authors declare that they have no competing interests. jejunal lymph nodes in dogs without clinical signs of gastrointestinal dis- ease. Vet Radiol Ultrasound. 2009;50:195–200. https://​doi.​org/​10.​1111/j.​ Author details 1740-​8261.​2009.​01516.x. 1 Departament de Medicina I Cirurgia Animals, Facultat de Veterinària, Univer- 19. Kneissl S, Probst A. Comparison of computed tomographic images of sitat Autònoma de Barcelona, Travessera dels Turons, 08193 Bellaterra, Spain. normal cranial and upper cervical lymph nodes with corresponding E12 2 Present Address: Department of Clinical Sciences of Companion Animals, plastinated-embedded sections in the dog. Vet J. 2007;174:435–8. Faculty of Veterinary Medicine, Utrecht University, Yalelaan 108, 3584 CM Utre- 20. Tobón Restrepo M. Ultrasound of the abdominal cavity, lymph nodes and cht, The Netherlands. large vessels. In: Novellas Torroja R, Dominguez Miño E, Espada Gerlach Y, Martínez Pereira Y, Tobón Restrepo M, editors. Diagnostic ultrasound in Received: 18 November 2021 Accepted: 2 August 2022 cats. Zaragoza: Servet editorial- Grupo Asís Biomedia S.L.; 2015. p. 211–29. 21. Llabres-Diaz FJ. Ultrasonography of the medial iliac lymph nodes in the dog. Vet Radiol Ultrasound. 2004;45:156–65. https://​doi.​org/​10.​1111/j.​ 1740-​8261.​2004.​04026.x. 22. 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Choose BMC and benefit from: phography in cats by popliteal lymph node iohexol injection. Vet Radiol Ultrasound. 2012;53:174–80. https://​doi.​org/​10.​1111/j.​1740-​8261.​2011.​ • fast, convenient online submission 01892.x. • thorough peer review by experienced researchers in your field 9. Nemanic S, Nelson NC. Ultrasonography and noncontrast computed • rapid publication on acceptance tomography of medial retropharyngeal lymph nodes in healthy cats. Am J Vet Res. 2012;73:1377–85. • support for research data, including large and complex data types 10. Nyman HT, Kristensen AT, Skovgaard IM, McEvoy FJ. Characterization of • gold Open Access which fosters wider collaboration and increased citations normal and abnormal canine superficial lymph nodes using gray-scale • maximum visibility for your research: over 100M website views per year B-mode, color flow mapping, power, and spectral doppler ultrasonogra- phy: A multivariate study. Vet Radiol Ultrasound. 2005;46:404–10. 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