Tissue Effects of Salivary Gland Fine-Needle Aspiration Does This Procedure Preclude Accurate Histologic Diagnosis?

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1 Anatomic Pathology / FINE-NEEDLE ASPIRATION TISSUE EFFECTS Tissue Effects of Salivary Gland Fine-Needle Aspiration Does This Procedure Preclude Accurate Histologic Diagnosis? Perkins Mukunyadzi, MD, 1 Ricardo H. Bardales, MD, 2 Hal E. Palmer, MD, 3 and Michael W. Stanley, MD 2 Key Words: Fine-needle aspiration; Salivary gland masses; Infarction; Hemorrhage; Histologic diagnosis; Complications Abstract Recent reports have alluded to various tissue effects secondary to fine-needle aspiration (FNA), particularly infarction observed in resected salivary gland masses, precluding accurate histologic diagnosis. Our experience with the use of 25-gauge needles indicates otherwise. We retrospectively reviewed 94 resected salivary gland masses previously sampled by FNA, looking for infarction, hemorrhage, needle track tumor seeding, and fibrosis. We assessed the significance of these complications and their impact on the histologic diagnosis. The median interval from FNA to excision was 25 days. Variable degrees of infarction and hemorrhage were present in 7 cases (7%) and 9 cases (10%), respectively. Infarction ranged from 5% to 80% (average, 20%), while hemorrhage averaged less than 20% of the material on the tissue sections. Significant infarction was present in acinic cell carcinomas (3/7), but histologic diagnosis was not compromised, and tissue alterations were absent. We conclude that FNA of salivary gland lesions using 25-gauge needles is safe and does not significantly alter the histologic diagnosis. The tissue effects observed did not preclude accurate diagnostic interpretation in any case. Fine-needle aspiration (FNA) is used widely in the initial workup and diagnosis of both palpable and deep-seated masses. Salivary glands are among the commonly aspirated locations in the head and neck area. Complications and clinical side effects that have been ascribed to this procedure are minimal, as long as very fine (23- to 25-gauge) needles are used. 1 Various tissue effects and changes to the lesion itself also have been addressed in case reports and small series. These include tumor infarction, needle track tumor seeding, intratumoral hemorrhage, and squamous metaplasia. 2-6 Rare cases of spontaneous infarction in some salivary gland tumors not subjected to preoperative FNA also have been reported. 7 Some reports have alluded to a high occurrence of these tissue effects in FNA of the salivary gland masses, leading to changes that would impair the histologic diagnosis of the subsequent surgical resection material Our experience, with exclusive use of 25-gauge needles, has been otherwise, showing that the incidence of clinical complications and tissue effects is low and of minor degree. This study of a large number of cases was conducted to evaluate the frequency and impact of tumor infarction, hemorrhage, and other FNA-related tissue alterations on subsequent histologic interpretation of surgical specimens. Materials and Methods In this retrospective study, we looked at salivary gland FNAs performed at the University of Arkansas for Medical Sciences and the Central Veterans Health Care System Hospitals. Little Rock, for a 4-year period ( ). Twenty-five-gauge needles were used in all the FNA procedures. We identified 94 FNA cases that had follow-up Am J Clin Pathol 2000;114:

2 Mukunyadzi et al / FINE-NEEDLE ASPIRATION TISSUE EFFECTS surgical resections. The H&E-stained surgical slides from resection specimens were reviewed and correlated with FNA samples from each case. The surgical tissue slides were assessed for the following parameters: tumor infarction, intratumoral hemorrhage, substantial fibrosis or granulation tissue, needle track seeding by tumor cells (malignant neoplasms), and overall diagnostic adequacy of the material. The extent of infarction and hemorrhage was estimated semiquantitatively as a percentage of the submitted material on the glass slides, with an average estimate given in cases with more than 1 slide. Fibrosis and granulation tissue were scored as present (if deemed clinically significant) or absent. Needle track seeding was scored as present only if there was irrefutable evidence of the presence of tumor cells along the path of the needle, usually accompanied by a linear track lined by granulation tissue. Finally, an overall assessment was made to determine whether the cases that displayed one or more of the tissue effects of FNA were sufficiently compromised to affect or prevent accurate histologic interpretation of the surgical specimen. Results Clinical Data, Cytologic Diagnosis, and Histologic Findings Ninety-four FNAs were followed by subsequent resection of the salivary gland lesion. Among these, 26 (28%) were malignant (1 case showing a Warthin tumor and malignant lymphoma was counted as malignant) and 68 (72%) were benign. The average interval between FNA and Table 1 Salivary Gland Lesions Showing FNA-Related Tissue Complications * resection was 25 days. Table 1 summarizes the cytologic and histologic findings in 15 cases with hemorrhage or infarction in resection material. Surgical evaluation of the resected material showed that varying degrees of infarction and hemorrhage were present in 7 cases (7%) and 9 cases (10%), respectively. The parotid gland was the location most frequently involved by tumor, both benign and malignant, as well as the location demonstrating the highest number of FNA-related tissue changes. Of the 15 cases that showed FNA complications, 13 (87%) were in the parotid gland; 6 cases (40%) and 8 cases (53%) demonstrated tumor infarction and hemorrhage, respectively. A single case of acinic cell carcinoma from the parotid gland showed both infarction Image 1 and hemorrhage. Infarction and focal hemorrhage also were present separately in the 2 malignant tumors from the submandibular gland. Up to 80% of the resected malignant salivary gland tumor was found to be infarcted in 2 cases of acinic cell carcinoma, 1 each from the parotid and submandibular glands, but this did not interfere with accurate histologic diagnosis in these cases. Of the tumors showing infarction, 4 (4%) of 94 were malignant and 3 (3%) were benign. Hemorrhage was seen in 3 malignant (3%) and 6 benign (6%) tumors. There was no significant difference between malignant and benign tumors in showing FNArelated complications. Areas of infarction in cases of mucoepidermoid carcinoma and benign mixed tumor are shown in Image 2 and Image 3, respectively. Intratumoral hemorrhage averaged 20% in the 9 cases (10%) in which this was a complication of FNA. In all the cases, hemorrhage was focal and of minor degree and did not preclude histologic interpretation of the surgical slides Image 4. The acinic cell carcinoma that demonstrated marked necrosis in 1 slide also contained areas of hemorrhage Case No./ Infarct Hemorrhage Interval to FNA Sex/ Age (y) Site of Tumor (%) (%) Excision (d) Diagnosis Surgical Diagnosis 1/M/46 Parotid BMT BMT 2/M/34 Parotid BMT BMT 3/M/77 Parotid < Warthin tumor Warthin tumor 4/F/62 Submandibular Positive Acinic carcinoma 5/F/79 Parotid Positive MEC 6/M/81 Parotid Positive Acinic carcinoma 7/M/46 Parotid 40 <10 30 Negative Acinic carcinoma 8/M/65 Parotid BMT BMT 9/M/47 Parotid BMT BMT 10/F/66 Parotid Negative Monomorphic adenoma 11/M/90 Submandibular 0 <10 9 SCC SCC, metastatic 12/M/72 Parotid Negative Warthin tumor 13/M/33 Parotid Negative Chronic sialadenitis 14/M/59 Parotid 0 <10 25 Negative Warthin tumor 15/F/60 Parotid 0 <10 26 Melanoma Melanoma BMT, benign mixed tumor; FNA, fine-needle aspiration; MEC, mucoepidermoid carcinoma; SCC, squamous cell carcinoma. * None of 94 total cases of resected salivary gland masses showed fibrosis, granulation tissue, abscess formation, or needle track seeding by malignant cells. 742 Am J Clin Pathol 2000;114:

3 Anatomic Pathology / ORIGINAL ARTICLE Image 1 (Case 6) Marked post fine-needle aspiration necrosis in an acinic cell carcinoma (H&E, 40). However, viable tumor was present in other slides (inset, H&E, 200). Image 3 (Case 1) Benign mixed tumor (pleomorphic adenoma) showing post fine-needle aspiration infarction (H&E, 40). involving about 20% of the tissue area. Small foci of hemosiderin deposition, representing remote hemorrhage, were noted in some cases in which the resection of the lesion was done 2 or more weeks after the FNA. There was no substantial fibrosis, granulation tissue, or squamous metaplasia in any case. A single case (case 6) demonstrated focal minor fibrosis of less than 5% of the submitted material. There were no cases showing needle track seeding by tumor cells in the 26 malignant tumors. Image 2 (Case 5) Post fine-needle aspiration infarction in a case of mucoepidermoid carcinoma (H&E, 100). Image 4 (Case 9) Intratumoral hemorrhage after fine-needle aspiration in a benign mixed tumor (H&E, 40). Discussion The use of FNA as a first-line diagnostic procedure in the evaluation of palpable lesions in different regions of the body is practiced widely in many centers where the expertise is available. In the head and neck area, salivary gland masses commonly are diagnosed by FNA. 10 Several case reports describe FNA-related tissue effects and complications associated with the recent increase in FNA procedures. 10 The Am J Clin Pathol 2000;114:

4 Mukunyadzi et al / FINE-NEEDLE ASPIRATION TISSUE EFFECTS most commonly reported tissue effect is tumor necrosis, but other complications include hemorrhage, vascular proliferation, fibrosis, and metaplastic changes. 4,10-12 Although the frequency of FNA-related tissue changes might be expected to rise with the increasing number of aspirations, we found post-fna frequencies of 7% and 10% for tumor necrosis and hemorrhage, respectively. When malignancy of the tumor is considered, the numbers decrease to 4% infarction and 3% hemorrhage in malignant tumors and 3% infarction and 6% hemorrhage in benign tumors. However, in all the cases, these tissue changes did not preclude accurate histologic diagnosis. In a study of FNA changes in benign lymph nodes, Behm et al 13 similarly concluded that the resulting alterations were minor and did not interfere with histologic assessment of the excised lymph node. It seems that consistent use of 25-gauge needles in aspiration results in fewer complications, yet provides adequate material for cytologic diagnosis. At our institution, we perform an average of 2 passes on a single mass. In occasional situations, additional aspirations may be necessary if the immediate slide evaluation demonstrates insufficient material or if special studies are required. We suspect that the reported cases with significant post-fna infarction and hemorrhage in the salivary gland lesions were a result of the use of larger bore needles, 2 but this information often is lacking in published studies. Infarction is a pathologic change that results from inadequate blood supply. Several mechanisms may be responsible for causing FNA-associated tumor necrosis. The postulated mechanisms include direct traumatic injury to the microvascular supply, thus disrupting blood flow to the tumor and inducing thrombosis. The ultimate result is ischemia and tumor infarction. Chan et al, 4 Pinto et al, 9 and Ersoz et al 14 hypothesize that tumors rich in mitochondria have high energy demands and are more susceptible, adding to the effects of FNA. Vascular lesions or organs such as the thyroid gland are at greater risk for infarction and hemorrhage after FNA. 9,14,15 Fibrosis or granulation tissue formation after FNA is a potential complication of the healing process because of tissue injury. However, there are few reports in the literature in which fibrosis is documented as a serious tissue complication after FNA or a cause of diagnostic difficulties. 2 Proliferation of endothelium or myofibroblasts and granulation tissue potentially could be confused with vascular tumors such as angiosarcoma. 16,17 Prominent fibrosis and granulation tissue were not present in our cases, unlike in some case reports on FNA of the thyroid gland and lymph nodes. 17,18 Absence of any substantial fibrosis or granulation tissue formation may be because FNA with 25-gauge needles is minimally traumatizing and does not cause substantial tissue damage, as might be the case with larger gauge needles Table 2. Squamous metaplasia and necrotizing sialometaplasia are rare complications. Florid squamous metaplasia in salivary glands could be confused with mucoepidermoid or squamous cell carcinoma. 7,19 However, lack of cytologic atypia in metaplastic epithelium and correlation of surgical material with FNA cytology should lead to the correct diagnosis. Needle track seeding by tumor cells is a complication that is either extremely rare or difficult to demonstrate. There are few reports in the literature of proven secondary spread of tumor cells along the needle track following FNA or causing pseudocapsular invasion. 8,16 None of our patients with malignant tumors demonstrated needle track seeding by tumor cells. Still, the importance of tumor seeding after FNA is controversial, as is the importance of causing metastasis in an operational field by spillage during surgery for treatment of a malignant neoplasm. The biology of tumor spread and metastasis seems to relate more to complex interactions among the tumor cells, among the stroma, and induction of angiogenesis, rather than to the mechanical events during procedures. The mere presence of tumor cell deposits along the needle path after FNA may not necessarily indicate tumor spread. Instead, pathologists need to recognize the diagnostic challenge that this can Table 2 Published Studies of Fine-Needle Aspiration of Various Organs in Which Substantial Tissue Changes Were a Potential Diagnostic Problem in Resected Specimens Reference Organ Studied Needle Gauge Gottschalk-Sabag and Glick 3 Salivary gland (parotid) Not indicated Palma et al 2 Salivary gland (parotid) 22 (18 in 1 case) Batsakis et al 10 Salivary glands 22 Tabbara et al 8 Breast 22 Lee et al 23 Breast 21 and 22 Ersoz et al 14 Thyroid 23 Pinto et al 9 Thyroid Not indicated Tsang and Chan 18 Lymph node Am J Clin Pathol 2000;114:

5 Anatomic Pathology / ORIGINAL ARTICLE pose, as such cells could be misinterpreted as representing invasion. 23 A careful search for the linear array of these cells along the needle path and absence of any adjacent stromal desmoplastic reaction will help avoid the wrong diagnosis. We conclude that FNA of salivary gland masses using 25-gauge needles is a safe and reliable procedure for cytologic diagnosis and causes minimal tissue effects that do not preclude histologic diagnosis on subsequently excised specimens. From the Departments of Pathology, 1 Central Arkansas Veterans Healthcare System and the 3 University of Arkansas for Medical Sciences, Little Rock, AR, and 2 Pathology and Laboratory Medicine, Hennepin County Medical Center, Minneapolis, MN. Presented in part at the 47th Annual Scientific Meeting of the American Society of Cytopathology, Sacramento, CA, November Published in abstract form in Acta Cytol. 1999;43:123. Address reprint requests to Dr Mukunyadzi: Dept of Pathology, Slot LR/113, Central Arkansas Veterans Healthcare System, 4300 W 7th St, Little Rock, AR References 1. Stanley MW, Lowhagen T. Fine Needle Aspiration of Palpable Masses: Stoneham, MA: Butterworth-Heinemann; 1993: Palma SD, Simpson RHW, Skalova A, et al. Metaplastic (infarcted) Warthin s tumour of the parotid gland: a possible consequence of fine needle aspiration biopsy. Histopathology. 1999;35: Gottschalk-Sabag S, Glick T. Necrosis of parotid pleomorphic adenoma following fine needle aspiration: a case report. Acta Cytol. 1995;39: Chan JKC, Tang SK, Tsang WYW, et al. Histologic changes induced by fine-needle aspiration. Adv Anat Pathol. 1996;3: Davies JD, Webb AJ. Segmental lymph-node infarction after fine-needle aspiration. J Clin Pathol. 1982;35: Kini SR. Post-fine-needle biopsy infarction of thyroid neoplasms: a review of 28 cases. Diagn Cytol. 1996;15: Layfield L, Reznicek M, Lowe M, et al. Spontaneous infarction of a parotid gland pleomorphic adenoma: report of a case with cytologic and radiographic overlap with a primary salivary gland malignancy. Acta Cytol. 1992;36: Tabbara SO, Frierson HF Jr, Fechner RE. Diagnostic problems in tissues previously sampled by fine-needle aspiration. Am J Clin Pathol. 1991;96: Pinto RGW, Couto F, Mandreker S. Infarction after fine needle aspiration. a report of four cases. Acta Cytol. 1996;40: Batsakis JG, Sneige N, EL-Naggar AK. Fine-needle aspiration of salivary glands: its utility and tissue effects. Ann Otol Rhinol Laryngol. 1992;101: Dardick I, Jeans MTD, Sinnot NM, et al. Salivary gland components involved in the formation of squamous metaplasia. Am J Pathol. 1985;119: Skalova A, Starek I, Michal M, et al. Malignancy-simulating change in parotid gland oncocytoma following fine needle aspiration: report of 3 cases. Pathol Res Pract. 1999;195: Behm FG, O Dowd GJ, Frable WJ. Fine-needle aspiration effects on benign lymph node histology. Am J Clin Pathol. 1984;82: Ersoz C, Soylu L, Erkocak EU, et al. Histologic alterations in the thyroid gland after fine-needle aspiration. Diagn Cytopathol. 1997;16: Jayaram G, Aggarwal S. Infarction of thyroid nodule: a rare complication following fine needle aspiration. Acta Cytol. 1989;33: LiVolsi VA, Merino MJ. Worrisome histologic alterations following fine-needle aspiration of the thyroid (WHAFFT). Pathol Annu. 1994;29(2): Tsang K, Duggan MA. Vascular proliferation of the thyroid: a complication of fine-needle aspiration. Arch Pathol Lab Med. 1992;116: Tsang WYW, Chan JKC. Spectrum of morphologic changes in lymph nodes attributable to fine-needle aspiration. Hum Pathol. 1992;23: Lam KY, Ng IOL, Chan GSW. Palatal pleomorphic adenoma with florid squamous metaplasia: a potential diagnostic pitfall. J Oral Pathol Med. 1998;27: Moloo Z, Finley RJ, Lefcoe MS, et al. Possible spread of bronchogenic carcinoma to the chest wall after a transthoracic fine needle aspiration biopsy: a case report. Acta Cytol. 1985;29: Roussel F, Dalion J, Benozio M. The rise of tumoral seeding in needle biopsies. Acta Cytol. 1989;33: Mighell A, High AS. Histological identification of carcinoma in 21 gauge needle tracks after fine needle aspiration biopsy of head and neck carcinoma. J Clin Pathol. 1998;51: Lee KC, Chan JKC, Ho LC. Histologic changes in the breast after fine needle aspiration. Am J Surg Pathol. 1994;18: Am J Clin Pathol 2000;114: