CARDIOLOGY AND RESPIRATORY SYSTEM ORIGINAL WORK

CT-guided fine-needle aspiration and tissue-core biopsy of lung lesions in the dog and cat M. Vignoli(1), G. Gnudi(2), P. Laganga(1), M. Gazzola(3), F. Rossi(1), R. Terragni(1), M. Di Giancamillo(4), B. Secchiero D(4), S. Citi(5) , A. M. Cantoni(3) , A. Corradi(3)

SUMMARY Diagnosis of pulmonary lesions on the basis of history and physical examination is often challenging. Diagnostic imaging is therefore of paramount importance in this field. Radiology has traditionally been considered the elective diagnostic procedure for these diseases. Nonetheless it is often not possible to differentiate inflammatory/infectious lesions from neoplastic disease. A correct cyto-histopathological diagnosis is therefore needed for an accurate diagnosis and subsequent prognostic and therapeutic plan. In human medicine, CT and CT-guided biopsy are indicated in the presence of lesions which are not adequately diagnosed with other procedures. In the present study 38 dogs and 11 cats, of different sex, breed and size, underwent either CT-guided lung fine-needle aspiration (FNA), tissue-core biopsy (TCB) or both. Clinical examination, haematology and chest radiography were performed on all animals. In this study 46 samples out of 56 were diagnostic (82.14%). Ten cases, either due to uncertainty or because only blood was aspirated, were considered non diagnostic. Sixteen out of 49 cases showed complications (32.6%). Pneumothorax was seen in 13 cases and mild haemorrhage in three cases. No major complications were encountered. Key words: Computer Tomography, CT, tissue-core biopsy, fine-needle aspiration, lung lesions, dog, cat.

Introduction

needle aspiration or tissue core biopsy of intrathoracic masses adjacent to the thoracic wall have been described in human medicine [6, 7] as well as in veterinary medicine [3]. Furthermore, the use of the Doppler examination allows the evaluation of the lesion vascularisation [3]. In human medicine, CT and CT-guided biopsies are indicated in the presence of lesions which cannot be adequately diagnosed with other procedures [8-17]. In veterinary medicine, some studies have been published on the CT-guided biopsy of the brain with stereotactic devices [18-20], while the description of free hand technique CT-guided biopsy in animals is still limited [3-5, 21-28] and few details and results are available regarding sensitivity of the technique. In one study, the accuracy of the CT-guided biopsy in bone and soft tissue associated diseases was described; TCB had an accuracy of 100% both for inflammatory/infectious and neoplastic

Diagnosis of pulmonary lesions on the basis of history and physical examination is often challenging. Diagnostic imaging is therefore of paramount importance in this field. Radiology has traditionally been considered the elective diagnostic procedure for these diseases. Nonetheless it is often not possible to differentiate inflammatory/infectious lesions from neoplastic disease. A correct cyto-histopathological diagnosis is therefore needed for an accurate diagnosis and subsequent prognostic and therapeutic plan [1, 5]. Other imaging modalities such as Fluoroscopy, Ultrasonography (US), Computerized Tomography (CT) and Magnetic Resonance (MRI) have to be considered as to the possibilities they offer to the interventional radiologist in taking take guided biopsy samples [3, 4, 8]. US-guided fine

(1) Veterinary Clinic dell’Orologio – Sasso Marconi (BO), Italy (2) Section of Radiology and Diagnostic Imaging, Dpt. of Animal Health - University of Parma, Italy (3) Pathology Unit, Dept. of Animal Health - University of Parma, Italy (4) Section of Clinical and Experimental Radiology – University of Milan, Italy (5) Department of Veterinary Clinic – University of Pisa, Italy Address correspondence and reprint requests to Dr. Massimo Vignoli Via Gramsci 1/4 –I- 40037 Sasso Marconi (BO) E-mail: [email protected]

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CT-guided fine-needle aspiration and tissue-core biopsy of lung lesions in the dog and cat - M. Vignoli

1a

1b

1c Fig. 1 a, b, c Dobermann, male, 7 year old, in right lateral recumbency. CT of the thorax after contrast medium administration with a soft tissue window (WW 300, WL 35). The slice where to biopsy is chosen (a). Then measurements from the skin to the lesion at different depth are taken (b). Based on this information, the guide is inserted within the lesion and the position is checked with further slices from the same area. Streak artifacts due to the metal are visible (c). Final diagnosis: Adenocarcinoma. were studied under general anaesthesia and monitored during the procedure. The CT examinations were performed to assess the extent of the lesion, to diagnose eventual metastases, and to take an aimed biopsy. The pieces of equipment used were a spiral CT in Sasso Marconi (BO)1) and Milan2), and third generation CT in Pisa3). The gantry was never tilted and the slice thickness was 3-5 mm depending the size of the lesion. The CT was repeated after i.v. contrast medium4) administration at the dose of 400800 mg/kg, depending the size of the animal. The CT study was reviewed with lung (WW 1500, WL – 550) and soft tissue (WW 300-350, WL 35-40) windows, and then, with the same soft tissue window, the biopsy was performed. In some cases, to decrease the streak artefacts, a bone window (WW 20004000, WL 450) was obtained. For FNA a 90 mm long, 21 gauge (G) spinal needle5) was used. For the TCB, a 14 G guide with stylet and stopper and a 16 G spring loaded automated needle, with 23 mm of excursion6) were used. Both the guide and the automated needle were calibrated at one cm. The technique has been modified from previously described techniques [23, 26]. All the animals were positioned in a manner offering easiest access to the lesion based on its location as seen on thoracic radiographs.

diseases, while with FNA the accuracy was 75%, with an overall mean accuracy of 94% [25]. In another study, the overall mean accuracy was 95.7% (100% TCB and 83.3% FNA) [26]. In two recent reports on the CT-guided biopsy of the intra-thoracic lesions, an accuracy of 65% for FNA and 83% for TCB [29], and 82% for FNA, was shown [4]. The latter was a preliminary study on CT-guided FNA and did not take into account TCB. The purpose of this study is to assess the percentage accuracy of diagnostic samples and complications of CT-guided FNA and TCB in the lung lesions of the dog and cat.

Materials and methods A retrospective study on 49 animals, 38 dogs and 11 cats of different breed, sex and size, underwent free hand technique CT-guided biopsy of the lung. Forty-four FNA and 12 TCB were performed. Only a single specimen was taken from each lesion, in order to limit the possible complications. Seven dogs underwent both FNA and TCB. All the cats underwent FNA. The choice of technique (FNA or TCB) was mainly based on the size of the lesion. Before the procedure, all the animals underwent blood and urine examinations. Thoracic radiography was always performed before CT examination. All the animals

A surgical preparation was done before the CT study. After the CT study was completed, an assessment of the location and extent of the lesion and the selection of the target plane was carried out. The target plane was chosen in an area with significant changes in order to obtain viable tissue samples. Areas suspected to be necrotic (with no contrast enhancement) and large vessels were avoided. Then the CT table was moved to the target plane, as indicated by the laser light in the gantry. In this plane, the site for insertion of the needle was subjectively chosen and marked with a sterile radiopaque metal marker. Subsequently, additional slices in the area of the marker were

1) GE Pro-Speed Power Spiral CT, Bologna, Italy 2) Philips PQ2000S Spiral CT, Milano, Italy 3) GE CT MAX third generation CT, Pisa, Italy 4) Omnipaque, Amersham Health, Milano, Italy 5) Ago spinale, Artsana. Cuneo, Italy 6) Angelo Franceschini, S.Lazzaro (BO), Italy

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(Fig. 3 a, b). Benign lesions such as abscesses, cysts or granulomas were diagnosed in eight cases (six dogs and two cats) (Fig.4 a, b, c).

Discussion The CT of the thorax is a very sensitive, but not very specific method, even with the use of contrast media [4]. In a study on five cats, Henninger (2003) showed that the density of the lesion measured with Hounsfield Units is not specific for a neoplastic disease versus an inflammatory disease and that contrast medium does not give differential enhancement [27]. Therefore a biopsy is needed to establish a final diagnosis. In this study, the percutaneous CT-guided biopsy was used to obtain a diagnostic sample in 46 out of 56 biopsy samples, with an overall mean accuracy of 82.1%. Tidwell and Johnson (1994), reported four lung and one cranial mediastinal biopsies. All the samples, four evaluated for cytology and three for histopathology, were diagnostic [22]. One study has reported an accuracy of 65% for FNA and 83% for TCB [29]. In human medicine, the diagnostic accuracy of the core biopsy under CT guidance is reported as high, between 88% [16] and 95% [17], with similar results for FNA, 85% [14]. It has been reported in the literature that carcinomas exfoliate better than sarcomas [2, 3], and since most of the malignancies in the lung are carcinomas, this may explain why there is a high accuracy with CT-guided FNA. The localization of the needle tip in the percutaneous CT-guided biopsy has been considered the key point for the success of the procedure. It is of paramount importance to differentiate between the true tip of the needle from the impression of a false tip, which is visible when the CT scan comprises only the angled needle [5]. It has been reported that the “low density” artifact visibile immediately adjacent to the distal part of the tip of the needle may create a false positive impression; therefore the correct position of the needle must be determined by evaluating the shape and the distinct nature of the tip rather than the “low density” artifact [21]. The choice of biopsy needle and the position of the animal depends on the localisation, dimension and distance from the

Fig.2. Same dog as in Fig. 1. Lung window: a mild to moderate pneumothorax was present in the post biopsy image (d). acquired to measure the distance from the skin to the proximal and distal borders of the lesion and to the area to biopsy. Those measurements facilitated the choice of correct depth and angle of insertion of the needle. The CT table was moved out of the gantry so that the spinal needle (for FNA) or the metallic guide (for TCB) could be placed and advanced to the preset distance and angle following a skin incision. The position of the spinal needle/guide tip was evaluated with additional images and the needle placement was corrected when necessary before the lesion was sampled. For FNA, once the needle was in a correct position, the stylet was retracted and suction with a syringe was applied. For TCB, when the metallic guide was considered to be in a correct position, the stylet was retracted and the automated needle inserted within the guide to the lesion and a tissue-core biopsy was obtained (Fig. 1a, b, c). Further images were taken in the area of the lesion in order to check for complications. All the animals were clinically monitored after the procedure for two to 24 hours depending on clinical signs and the severity of any complications.

Results The tip of the needle was visualized within the lesion in all the patients. The diagnosis was reached in 46 out of 56 samples (Tab. 1). Thirty five of 44 FNA (79.5%) and 11 of 12 TCB (91.7%) were diagnostic. Nine of 44 FNA were considered not diagnostic because only blood was aspirated. One TCB was not diagnostic because only fibrous tissue was recovered. In the same dog, the FNA was diagnostic for carcinoma. The overall mean accuracy was 82.1%. Sixteen out of 49 cases showed complications (32.6%). Mild to moderate pneumothorax was present in 12 cases, and one severe pneumothorax was present after a TCB, however this did not require any surgical intervention. Pneumothorax was present after five FNA (11.4 %) and eight TCB (66.7%) (Fig.2). The deeper the lesion, the more severe the pneumothorax, with a range of two to seven centimetres. However, in some deep lesions, no pneumothorax was visible. In three cases, a mild haemorrhage was present in deep lesions, with collapse of the dependent lung. Neoplastic lesions were detected in 31 cases (25 dogs and six cats). Thirty were carcinomas and one malignant histiocytosis

Fig. 3 a, b. Crossbreed, female, 12 year old. CT of thorax in sternal recumbency and with a soft tissue window (WW 300, WL 40). After contrast medium administration a large mass in the left caudal lung lobe is shown with a non-homogenous enhancement (a). Biopsy phase. The guide is inserted within the lesion. Streak artifact are visibile (b). Final diagnosis: Adenocarcinoma.

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CT-guided fine-needle aspiration and tissue-core biopsy of lung lesions in the dog and cat - M. Vignoli

Table 1: CT-procedure and results of 38 dogs and 11 cats with toracic lesions. Cases number 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

Signalement: breed, age in years (y), sex (M: male; F: female) Miniature Poodle, 10 y, F Miniature Poodle, 11 y, F Bouvier de Flandres, 7 y, F Boxer, 11 y, M Brittany Spaniel, 9 y, F Griffon Kort., 10 y, M Mix, 10 y, F Mix, 10 y, M Mix, 11 y, F Mix, 14 y, F Bernese Mountain, 8 y, M German Shepherd, 10 y, F German Shepherd, 11 y, M Pekingese, 11y, F Pointer, 13 y, F Rottweiler, 9 y, M Siberian Husky, 12 y, F Schnauzer, 9 y, F English Setter, 8 y, F German Shepherd, 7 y, M Mix, 9 y, M Mix, 12 y, M Mix, 7 y, F Mix, 10 y, M German Shepherd dog, 11 y, M Mix, 9 y, F Mix, 14 y, M Labrador Retriever, 17 y, M Mix, 4 y, F Boxer 9 y, M Boxer, 8 y, M Weimaraner, M 18 m Mix, 12 y, F Bernese Mountain, 7 y, M

Location of the lesion in the lung lobe Right middle Right caudal Left caudal Left caudal Right cranial Right caudal Left caudal Right middle Right caudal Left caudal Right middle Left caudal Left caudal Left caudal Left caudal Right caudal Right cranial Right middle Right caudal Right cranial Right cranial Right caudal Left cranial Right middle Right middle Left cranial Left caudal Right caudal Right accessory Right middle Left caudal Left caudal Left caudal Left caudal

35 Dobermann, 12 y, M Right caudal 36 Airdale terrier, 12 y, M Right caudal 37 Labrador Retriever, 9 y, F Left caudal 38 Bernese Mountain, 8 y, M Right middle 39 European Shorthair cat, 13 y, F Left caudal 40 European Shorthair cat, 8 y, M Left cranial 41 European Shorthair cat, 9 y, M Left cranial 42 Persian cat, 13 y, M Right caudal 43 Persian cat, 9 y, F Right caudal 44 Siamese cat, 15 y, M Left caudal 45 Persian cat, 13 y Right caudal 46 European Shorthair cat, 14 y, F Left cranial 47 European Shorthair cat, 13 y, M Right caudal 48 European Shorthair cat, 18 y, M Right caudal 49 European Shorthair cat, 15 y, M Left caudal TCB = Tissue-core biopsy; FNA = Fine-needle aspiration.

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Biopsy technique* FNA FNA FNA TCB FNA FNA FNA FNA FNA TCB FNA FNA FNA FNA FNA FNA FNA FNA FNA FNA FNA TCB FNA FNA FNA FNA FNA +TCB FNA FNA + TCB FNA + TCB FNA FNA FNA + TCB FNA + TCB FNA + TCB TCB FNA +TCB TCB FNA FNA FNA FNA FNA FNA FNA FNA FNA FNA FNA

Histological/Cytological diagnosis Carcinoma Non-diagnostic Carcinoma Carcinoma Carcinoma Carcinoma Carcinoma Non-diagnostic Carcinoma Carcinoma Malignant histiocytosis Carcinoma Carcinoma Carcinoma Non-diagnostica Abscess Granuloma Non-diagnostic Abscess Carcinoma Non-diagnostic Carcinoma Carcinoma Carcinoma Carcinoma Carcinoma Carcinoma Abscess Carcinoma Abscess Non-diagnostic Abscess Carcinoma FNA: Carcinoma TCB: Non-diagnostic Carcinoma Carcinoma Carcinoma Carcinoma Carcinoma Cyst Non-diagnostic Carcinoma Non-diagnostic Carcinoma Carcinoma Carcinoma Abscess Non-diagnostic Carcinoma

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Fig. 4 a, b, c. Domestic short hair cat, female, 15 year old. CT of the thorax in sternal recumbency and with a lung window (WW 1500, WL – 550). A small nodule, about 1 cm in diameter is visible in the right caudal lung lobe (a). Measurements (b) and phase of the biopsy (c) are visible. Final diagnosis: Granuloma. skin surface of the lesion [3]. In the present study, 21-G spinal needle was used for FNA. A fine needle has been recommended in order to avoid aspiration of blood [3]. For TCB, a 14-G calibrated guide with stylet was employed, which functioned as a support for the 16-G calibrated automated needle. Indeed, the length of the automated needle and the weight of the handle of the needle did not allow direct biopsy. The use of different techniques (FNA or TCB) was chosen mainly based on the size of the lesion, considering the 23 mm of extension of the automatic needle. Because of this, we did not consider it possible to take a TCB in lesions smaller than 4 cm. We observed some complications including three mild haemorrhages and 12 cases of mild to moderate pneumothorax. Only one severe pneumothorax was seen after a TCB and none of them required surgical intervention. Most of the complication were seen after TCB, probably due to the larger size of the guide compared to that of the needle used for FNA and the depth of the biopsy lesions. However, with some deep lesions neither haemorrhage nor pneumothorax was observed. Those complications were not related to the size of the lesion. In one study it was reported that the deeper the lesion, the more severe the pneumothorax was likely to be, but no clinical manifestations were noted in that study [29]. Since passage through more lung tissue accurs to get into a deeper lesion, we can speculate that this could be the reason for the higher number of pneumothorax complications seen with deep lesions. However we still cannot explain why the biopsy in some deep lesion did not create any pneumothorax. In one case, dog n° 34, Tab. 1, the severe pneumothorax created was probably the cause of not being able to obtain a diagnostic sample. In the same case the FNA was diagnostic for carcinoma. In human medicine, pneumothorax is the most common complication of percutaneous CT-guided lung biopsy and ranges from 8 to 61% [30, 31]. In one study on 289 patients, it was reported that application of a thoracic drain was necessary in 14% of the cases. In the same study it was reported that deeper lesions, which require a wider trajectory angle, were risk factors for pneumothorax [30]. In another study it was reported that the transthoracic needle biopsy can be performed with high-diagnostic yield in patients with iatrogenic stable pneumothorax caused by other procedures, such as CT-

guided biopsy, US-guided biopsy or transbronchial lung biopsy [32]. The respiratory movements did not cause problems during the procedure. However, it is important not to move the animal during the procedure to avoid loosing the target which necessitates restarting the examination. In this study the animals were positioned in different modes of recumbence with the goal being to reach the lesion more easily on basis of lesion localization obtained by radiography. However, it is our opinion that lateral recumbency should be avoided, if possible, because metastases may be missed due to partial collapse of the dependent lung. Another option is to position the animal in ventrodorsal or dorsoventral recumbency in order to examine for metastases, and then reposition the animal in lateral recumbency to obtain the biopsy. The latter method however, which includes a retake of the scout views and scanning against the mass involves a longer examination time and an additional injection of contrast medium. The i.v. administration of non-ionic iodinated contrast medium, can give useful information. Indeed, the enhancement of the lesion allows the operator to biopsy viable tissue and to avoid large vessels [4, 22, 26]. CT allows better evaluation of the extent of the lesion than US or fluoroscopy [4, 26], particularly in lesions surrounded by gas, as opposed to in US [3, 26]. The CT is a more sensitive technique to examine for metastases when compared to fluoroscopy and conventional radiology [4]. Some disadvantages of CT compared to other techniques are reported, however [3, 26]. The time for the whole procedure is variable depending on the size, location of the lesion, experience of the radiologist and CT machine available. With a spiral CT the whole procedure (scanning and biopsy) takes from 5 to 30 minutes. In conclusion, CT-guided biopsy is a safe and accurate technique. The only limitation we observed is when a lesion smaller than 4 cm is biopsied with the automated needle. CT is useful for examination of areas that are difficult to reach with other techniques, especially in lesions surrounded by gas. Moreover, within the same examination, it is possible to assess the possible presence of metastases.

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CT-guided fine-needle aspiration and tissue-core biopsy of lung lesions in the dog and cat - M. Vignoli

Acknowledgements

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The authors would like to acknowledge the contribution of SPINNER Consortium of the University of Bologna (European Union, Emilia-Romagna Region, Ministry of the Work and Social Politics)

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