Fine-needle aspiration cytological diagnosis of neck masses.

Fine Needle Aspiration Acta Cytologica 2015;59:68–76 DOI: 10.1159/000371412

Received: June 11, 2014 Accepted after revision: December 5, 2014 Published online: February 11, 2015

Fine-Needle Aspiration Cytological Diagnosis of Neck Masses Mohammad Javad Ashraf a Hanieh Raad a Negar Azarpira a, d Bijan Khademi b Mahmood Shishegar b Behrooz Gandomi b Sezaneh Hagpanah e Pourya Adibi c Departments of a Pathology, b Otolaryngology and c Anesthesiology, d Transplant Research Center, and e Hematology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract Background: Fine-needle aspiration (FNA) is a simple, safe, inexpensive, and acceptable method for diagnosing masses, especially at superficial areas. Therefore, we decided to evaluate the accuracy of FNA cytological diagnosis in nonthyroidal, nonsalivary gland neck masses and compare the results with histopathological diagnosis. Materials and Methods: In this retrospective study, all cases with FNA cytological diagnosis of nonthyroidal, nonsalivary gland neck masses from April 2009 to July 2013 were retrieved. The procedure was done by pathologists, and all cytological and histopathological slides of the existing 46 cases were reviewed by 3 pathologists. The values of sensitivity (SN), specificity (SP), positive predictive value (PPV), negative predictive value (NPV), and diagnostic accuracy were calculated. Results: SN, SP, PPV, NPV, and accuracy in this study were 79, 100, 100, 73, and 86%, respectively. We had 6 false-negative and no false-positive cases. Conclusion: The FNA procedure is a reliable method as the first step for the diagnosis of nonthyroidal, nonsalivary gland neck masses. To increase the diagnostic value of cytology, careful examination of all cytological slides, repetition of the FNA procedure and good history taking are helpful. © 2015 S. Karger AG, Basel

© 2015 S. Karger AG, Basel 0001–5547/15/0591–0068$39.50/0 E-Mail [email protected] www.karger.com/acy

Introduction

Fine-needle aspiration (FNA) technique was first described by Martin and Ellis in 1930, with the use of narrow-gauge needles for the sampling of tumors at available anatomic areas [1, 2]. The neck is an accessible superficial area that allows FNA of lesions of the thyroid, salivary gland, lymph node, soft tissue, and cysts. Tissue biopsy is the gold standard method required for the diagnosis of neck masses [3]. However, open biopsy can be accompanied by complications such as scarring, neurovascular injuries, longer recovery time, and bleeding. Also, incisional biopsy needs general anesthesia, especially for children [3, 4]. In contrast to open biopsy, FNA procedure has many advantages. It is inexpensive, available, well tolerated, quick, repeatable, and simple. This technique is relatively safe and can be used as the first diagnostic method. Additionally, complications such as ecchymosis, hematoma, draining sinus tract, and pneumothorax have rarely been reported [3, 5]. Many studies have been done to evaluate the sensitivity (SN) and specificity (SP) of FNA procedure in neck masses and compare its accuracy (ACC) with open biopsy [3, 5–8]. The reported SN on thyroid and salivary gland mass has been between 70 and 95%, with SP of 87% [3, 5, 7]. Few studies have focused on nonthyroidal, nonsalivary Correspondence to: Dr. Negar Azarpira Transplant Research Center Department of Pathology, Namazi Hospital, Shiraz University of Medical Sciences Shiraz 7193711351 (Iran) E-Mail negarazarpira @ yahoo.com

Downloaded by: Stockholms Universitet 198.143.54.1 - 8/14/2015 9:36:02 AM

Key Words Aspiration · Neck mass · Cytology

1 (5.3)

1 (5.3)

2 (10.5) 3 (15.8)

1 (5.3)

granulomatous inflammation nonspecific acute inflammation 1 (5.3)

diffuse large B-cell lymphoma peripheral T-cell lymphoma metastasis nasopharyngeal carcinoma squamous cell carcinoma

4 (21)

4 (21)

lipoma

2 (10.5)

metastatic melanoma 1 (5.3) poorly differentiated carcinoma 1 (5.3) MPNST 1 (5.3)

1 (12.5)

epidermal inclusion cyst 5 (62.5)

metastatic squamous cell carcinoma 1 (12.5) 1 (12.5)

n (%)

solid masses (subgroup 2A)

Acta Cytologica 2015;59:68–76 DOI: 10.1159/000371412

69


FNA Cytological Diagnosis of Neck Masses

Granulomatous inflammation

Overall, 46 cases of nonthyroidal, nonsalivary gland neck masses with both FNA cytological and histopathological diagnoses were evaluated. According to the results, 32 cases were male and 14 were female, with a

Lymphoid masses (group 1)

Results

Table 2. FNA cytological diagnoses of all cases

In this retrospective study, all cases of neck mass with FNA cytological diagnosis from April 2009 to July 2013 were retrieved. All FNAs were done by pathologists working at Motahhari clinic and Khalili hospital, which are affiliated with Shiraz University of Medical Sciences. The samples were taken using 22-gauge disposable needles attached to a 10-ml syringe. Multiple slides were prepared. Some of them were air-dried and stained by the Wright method, while the others were alcohol-fixed and stained by Papanicolaou. Overall, 322 cases were found, among which only 46 were categorized as nonthyroidal, nonsalivary gland neck masses. All the cytological and histopathological slides were reviewed by 3 independent pathologists. The FNA results were categorized as follows: group 1 – lymphoid masses and group 2 – nonlymphoid masses. The second group was then divided into the following 2 subgroups: 2A – nonlymphoid neck solid masses and 2B – nonlymphoid neck cysts. Age, sex, cytological findings, and histopathological final diagnoses were recorded in a questionnaire. The values of SN, SP, positive predictive value (PPV), negative predictive value (NPV), and diagnostic ACC were calculated for each group and subgroup using the following formulas: SN = TP/TP + FN; SP = TN/TN + FP; PPV = TP/TP + FP; NPV = TN/TN + FN, and ACC = TP + TN/ TP + TN + FP + FN, where TP = true positive, TN = true negative, FP = false positive, and FN = false negative.

Nonlymphoid masses (group 2)

Materials and Methods

Hodgkin’s lymphoma

n (%)

gland neck masses [2, 9–14]. SN of 90% and SP of 80% have been reported for FNA diagnosis of head and neck lymphoma [10]. The present study aims to evaluate FNA cytology of nonthyroidal, nonsalivary gland neck masses and to compare the results with histological diagnosis achieved by open biopsy.

branchial cleft cyst thyroglossal duct cyst

0

metastatic squamous cell carcinoma 8 (42) metastatic papillary thyroid carcinoma 2 (10.5)

8

2 (10.5)

9

hemangioma

10

13

4 (21) lymphoma

6

Reactive lymph node

malignant

malignant (n = 0)

benign

benign (n = 8) n (%)

malignant

malignant (n = 9)

benign

n (%)

Benign malignant

benign (n = 10)

cystic masses (subgroup 2B)

malignant (n = 13)

solid masses (subgroup 2A)

n (%)

Nonlymphoid masses (group 2)

Benign (n = 6)

Lymphoid masses (group 1)

cystic masses (subgroup 2B)

n (%)

Table 1. FNA cytological diagnoses of all cases

roidal/nonsalivary gland neck masses Groups/ parameters

Lymphoid neck mass (group 1), %

Nonlymphoid solid neck mass (group 2A), %

Nonlymphoid cystic neck mass (group 2B), %

Total cases, %

SN SP PPV NPV ACC

92 100 100 83 94

69 100 100 60 78

– 100 – 87.5 87.5

79 100 100 73 86

Table 4. False-negative cases

No. Cytological diagnosis

Histopathological diagnosis

1

No malignant cell is seen suggestive of abscess

Poorly differentiated squamous cell carcinoma

2

Cystic lesion with inflammatory process

Metastatic squamous cell carcinoma

3

No malignant cell is seen suggestive of granuloma


4

Benign cyst


5

Benign nerve sheath tumor, most probably schwannoma

MPNST

6

No malignant cell is seen


male:female ratio of 2.2:1. In addition, the age of the patients ranged from 7 to 83 years, with a mean age of 48.1 ± 10 years. Of the 46 FNA cytological cases, 19 (41%) were from lymphoid tissue (group 1) and 27 (59%) from nonlymphoid tissue (group 2). In group 2 also, 19 cases (41%) had nonlymphoid solid neck masses and 8 (18%) had nonlymphoid cystic neck masses (table 1). Moreover, 23 cytological diagnoses (50%) were benign, while 23 (50%) were malignant. In histopathology, 29 cases (63%) were malignant and 17 (37%) were benign (tables 1, 2). FNA cytology of group 1 revealed 9 lymphomas (69%) and 4 metastatic carcinomas (31%). The diagnoses of lymphoma in cytology were subsequently confirmed with the histopathological findings. There were 4 Hodgkin lymphomas, 4 diffuse large B-cell lymphomas and 1 pe70


ripheral T-cell lymphoma that all were confirmed by immunohistochemistry study (table 1). Final histopathological diagnoses of metastasis indicated 3 cases of metastatic squamous cell carcinomas and 2 metastatic nasopharyngeal carcinomas (tables 1, 2). Cytological diagnoses of benign lymphoid lesions showed 4 reactive lymph nodes (66.6%) and 1 granulomatous inflammation (16.6%). There was 1 case (16.6%) labeled as benign cyst which was finally confirmed as metastatic squamous cell carcinoma in histopathology (1 false-negative case in cytological diagnosis; table 1). In group 2A, 9 (47%) of the 19 cases of nonlymphoid solid masses were diagnosed as positive for malignancy in cytology and 10 (53%) as benign lesions. Histopathological diagnoses showed 8 metastatic squamous cell carcinomas (42%), 2 metastatic papillary thyroid carcinomas (10.5%), 1 metastatic melanoma (5.3%), 1 poorly differentiated carcinoma (5.3%), 1 malignant peripheral nerve sheath tumor (MPNST) (5.3%), 2 hemangiomas (10.5%), 2 lipoma (10.5%), 1 granulomatous inflammation (5.3%), and 1 nonspecific acute inflammation (5.3%; tables 1, 2). Cytological diagnoses of all 8 cases of nonlymphoid cystic lesions were benign. Their final histopathological diagnoses showed 1 metastatic squamous cell carcinoma (12.5%), 1 branchial cleft cyst (12.5%), 1 thyroglossal duct cyst (12.5%), and 5 epidermal inclusion cysts (62.5%). The results of SN, SP, PPV, NPV, and ACC are summarized in table 3. In the present study, 6 of the 46 cases had different histopathological diagnoses from cytology. Case 1 was suggestive of abscess in cytology because many neutrophils were detected in a dirty background. FNA cytological diagnosis of case 2 was cystic lesion with inflammatory process because of the presence of many neutrophils, macrophages and degenerated cells in a dirty background. Case 3 was suggestive of granulomatous inflammation. There were aggregates of epithelioid histiocytes and some multinucleated giant cells as well. Case 4 was a cystic lymph node. It showed macrophages in a polymorphic lymphoid background. In case 6, no malignant cell was seen in cytological smears because of hypocellularity. Only few macrophages were present. The final histopathological diagnoses of cases 1, 2, 3, 4, and 6 were metastatic squamous cell carcinoma (table 4; fig. 1–8). Cytological diagnosis of case 5 was benign nerve sheath tumor – most probably schwannoma. Cytological smears showed grouped and isolated spindle cells with one blunt end. However, no obvious atypia or mitosis was seen. Ashraf/Raad/Azarpira/Khademi/ Shishegar/Gandomi/Hagpanah/Adibi


Table 3. Comparison of SN, SP, PPV, NPV, and ACC in nonthy-

Color version available online

a

b Color version available online

Fig. 1. a Cytology smear shows neutrophils and macrophages in a dirty background; case 2. Wright stain. ×200. b Section shows extensive necrosis in poorly differentiated squamous cell carcinoma; case 1. HE. ×100.

Fig. 2. a Cytology smear shows granuloma formation; case 3. Pap stain. ×100. b Seca

b

Histopathological diagnosis was MPNST, which was confirmed by immunohistochemistry study (table 4). In these 6 problem cases, there was agreement between 3 independent pathologists. However, one of them had good communication with clinicians and recommended biopsying or resecting the cystic lesions.

FNA is a simple and inexpensive method for the diagnosis of neck masses, but histology is the gold standard method for final diagnosis [3, 15–17]. In this study, the ACC of FNA cytology in nonthyroidal, nonsalivary



Discussion

71


tion shows granulomatous reaction in metastatic squamous cell carcinoma; case 3. HE. ×100.


a


Fig. 3. a Cytology smear shows group of spindle cells with no obvious atypia; case 5. Pap stain. ×200. b Section shows fascicles of spindle cells in MPNST; case 5. HE. ×200.

Fig. 4. a Cytology smear shows hypocellu-

a

gland neck masses was compared with histological final diagnosis. Up to now, few studies have evaluated the SN, SP and ACC of FNA for the diagnosis of thyroid, salivary gland, soft tissue, lymph node, and cysts (table 5) [3, 5]. Saatian et al. [3] evaluated the FNAs of 100 neck masses in two teaching hospitals in Tehran, Iran. SN, 72


b

SP, PPV, NPV, and ACC were 72, 87, 85, 75, and 79%, respectively. They concluded that FNA was a simple, safe and inexpensive diagnostic method for neck mass (table 5). Abdien et al. [5], in Saudi Arabia, evaluated 225 neck masses. SN, SP, PPV, NPV, and ACC for detecting maligAshraf/Raad/Azarpira/Khademi/ Shishegar/Gandomi/Hagpanah/Adibi


lar smear with few macrophages; case 6. Pap stain. ×400. b Section shows metastatic nasopharyngeal carcinoma diagnosed as metastatic carcinoma in cytology. HE. ×200.


Fig. 5. a Cytology smear shows papillary

a


structures diagnosed as metastatic papillary carcinoma in cytology. Wright stain. ×100. b Section shows metastatic papillary carcinoma to the lymph node. HE. ×100.

Fig. 6. a Cytology smear shows squamous

a

b

nancy were 95, 100, 100, 95, and 98%, respectively, in that study. They found that FNA was a good, simple and cost benefit method for the diagnosis of inflammatory neck lesions (table 5). Mahbod et al. [2] evaluated 55 cases of nonthyroidal neck masses in Iran. That study revealed SN, SP, PPV, and

ACC to be 81.2, 97.4, 92.8, and 92.7%, respectively. They believed that FNA was an acceptable test for the diagnosis of nonthyroidal neck masses. The SN of FNA in neck lymphoid malignancies was low (72%) in that study and, consequently, they suggested open surgical biopsy for such tissues (table 5).



73


epithelial cells with few inflammatory cells. Pap stain. ×200. b Section shows squamous epithelium with underlying inflammatory cells in the branchial cleft cyst. HE. ×100.


Fig. 7. a Cytology smear shows large ma-

lignant lymphocytes. Wright stain. ×400. b Section shows diffuse large B-cell lym-

a

b

a

b


phoma. HE. ×200.

According to our study results, we had an acceptable SN, SP, PPV, NPV, and ACC for diagnosing nonthyroidal, nonsalivary gland neck masses. Nonetheless, SN was obviously low followed by NPV in nonlymphoid solid masses (group 2A).

74


In our study, the major misdiagnosis was squamous cell carcinoma. The cases showed necrosis, cystic change, hypocellularity, and granulomatous inflammation. The secondary changes might have occurred in metastatic squamous cell carcinoma. These might have been caused by needle penetration into the necrotic areas. Metastasis Ashraf/Raad/Azarpira/Khademi/ Shishegar/Gandomi/Hagpanah/Adibi


Fig. 8. a Cytology smear shows aggregates of spindle cells with no atypia diagnosed as lipoma. Pap stain. ×100. b Section shows mature adipose tissue in lipoma. HE. ×100.

Table 5. Comparison between previous studies and our findings

First author [Ref], year

Country

Cases

Cases, SN, n %

SP, %

PPV, NPV, ACC, % % %

Saatian [3], 2011 Abdien [5], 2002 Mahbod [2], 2002 Our study Moatamed [16], 2009 Our study Hirchand [11], 2009 Our study

Iran, Tehran Saudi Arabia Iran, Tehran Iran, Shiraz USA Iran, Shiraz Nepal Iran, Shiraz

neck masses neck masses nonthyroidal neck masses nonthyroidal, nonsalivary gland neck masses nonsalivary gland neck cystic lesions cystic neck mass lymphoid masses lymphoid neck masses

100 225 55 46 92 8 72 19

87 100 97.4 100 100 100 95.7 100

85 100 92.8 100 100 – 91.6 100

72 95 81.2 79 75 – 88 92

75 95 – 73 93 87.5 93.7 83

89 98 92.7 86 94 87.5 93 94

can make cystic changes in the tumor or lymph node. If all smears are carefully screened for atypical cells, the atypical cell may be found. Granuloma formation is another pitfall in FNA diagnosis of squamous cell carcinoma. The well-differentiated squamous cell carcinoma may produce abundant keratin material with subsequent granulomatous and/or foreign body giant cell reaction. If the FNA is repeated, the malignant cells may be detected. Konar et al. [18] analyzed 2,512 lateral neck masses with FNA cytology in patients between 18 and 80 years old. Overall, 415 out of the 495 malignant cases had metastatic squamous cell carcinoma with secondary change. These false-negative cases had granulomatous inflammation, cystic changes and necrosis similar to our false-negative cases. Thus, they suggested careful examination of the cytological slides and repetition of FNA in suspicious cases (table 5). Cystic metastasis of squamous cell carcinoma may present in lymph nodes. Cysts can be formed by spontaneous keratin degradation and cellular debris in lymph nodes [19]. Cystic metastatic squamous cell carcinoma can also be misinterpreted as benign cystic lesions such as branchial cleft cyst. Inflammation in these lesions can make mildly reactive atypical cells and simulate squamous cell carcinoma. Also, a well-differentiated squamous cell carcinoma with abundant keratin production mimics an epidermal inclusion cyst [20]. Other metastatic tumors such as papillary thyroid carcinoma can make cystic or granulomatous changes [21, 22]. Another pitfall was benign nerve sheath tumor in FNA cytology, and final histopathological diagnosis was MPNST. This tumor can be misinterpreted as a benign lesion or other malignant tumor. In 1999, Jimenez-Heffernan et al. [23] reviewed the cytological smears of 10 patients with MPNST and compared them with histo-

pathological diagnosis. They found that MPNST could be very well differentiated and resemble benign nerve sheath tumors such as schwannoma or neurofibroma, or they might be very anaplastic and indistinguishable from other sarcomas. High cellularity and cellular dissociation may be helpful for the diagnosis of sarcoma in cytology. However, cellular and ancient schwannoma should be considered in differential diagnosis. Diagnostic ACC of FNA is also dependent on the location of the mass (superficial areas like the neck), type of the lesion (better in lymphoid masses) and expertise of both aspirator and cytopathologist. The use of FNA can help clinicians in rapid decision making to manage the patients or avoid unnecessary surgical plans.



Conclusion

Our results demonstrate that FNA procedure is a reliable method as the first step for the diagnosis of nonthyroidal, nonsalivary gland neck masses, especially for lymphoid diseases. To increase the diagnostic value of cytology interpretation, we recommend the following: (1) Repetition of FNA in cystic lesions or hypocellular smears (2) Taking good history, especially for metastasis (3) Careful examination of all FNA cytological smears

Acknowledgment

75


The authors are grateful for Ms. A. Keivanshekouh at the Research Improvement Center of Shiraz University of Medical Sciences for improving the use of English in the manuscript.

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