Role of Fine-Needle Aspiration Biopsy in the Assessment of Renal Enrico G. Cristallini, M.D., Cristina Paganelli, M.D., and Giovanni 6. Bolis, M.D.

Clinical and histological control of fine-needle aspiration biopsy (FNAB) diagnosis of 72 kidney masses observed between 1981 and 1988 confirmed 34 benign and 33 malignant lesions, but did not confirm four malignant and one benign lesions, giving a total diagnostic accuracy of 93.05%. The role of FNAB in selecting cases to be sent to surgery was investigated by comparing the incidence of useful surgery (for benign and primary malignant neoplasias) and the incidence of useless surgery (for nonneoplastic lesions and secondary malignant neoplasias) in nephrectomized patients who either had (group A, 27 patients) or didn’t have (group B, 198 patients) preoperative FNAB. The diyerences were highly signijicant (P < 0.001). Furthermore, patients operated for malignant neoplasias (20 in group A; I I 7 in group B) displayed highly signi3cant differences (P < 0.001) with respect to renal vein infiltration (1 in group A versus 22 in group B) and localregional lymph node metastases (I in group A versus 15 in group B). In conclusion, FNAB is a reliable method for selecting cases for surgery and for aiding in the diagnosis of malignant neoplasias. Diagn Cytopathol 1991;7:32-35. Key Words: Fine-needle aspiration biopsy; Renal masses

Because of its efficiency, low invasiveness and cost, echoor computerized tomography (CT)-guided fine-needle aspiration biopsy (FNAB) is finding ever wider use in the evaluation of masses that arise in deep organs. The diagnosis of kidney lesions has also gained much from the application of FNAB, since it reduces the incidence of surgery for nonneoplastic and metastatic lesions and increases the incidence for benign and primary malignant neoplasias. *s3

Received September 12, 1989. Accepted April 24, 1990. From the Istituto di Anatomia e Istologia Patologica, Universita di Perugia, Ospedale Civile S. Maria, Terni, Italy. Presented in part at the “1” Congress0 Nazionale della Federazione Italiana della Societa di Anatomia Patologica e Citologia Diagnostica (FISAPEC),” Varese, Italy, May 1989. Address reprint requests to Enrico Giuseppe Cristallini, M.D., Istituto di Anatomia e Istologia Patologica (R), Universita di Perugia, Ospedale S . Maria, 05100 Terni, Italy.

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To assess the reliability of the method 8 yr after its introduction as a method for selecting cases to be sent to surgery, we re-examined FNAB diagnoses of kidney masses compared with the clinical or histological results and analyzed the distribution of lesions in nephrectomized patients who did or did not undergo preoperative FNAB.

Materials and Methods From 1981 to 1988, 99 patients underwent FNAB for kidney neoplasias identified at ultrasonography, CT, or angiography. Echo- or CT-guided FNAB was done on an outpatient basis by a radiologist who used a 9-15-cm-long, 2 1-22-gauge Chiba needle mounted on previously heparinized 20-ml disposable syringe. The aspirate was examined on a dark-base Petri dish. The larger fragments, selected with a lens and Pasteur pipette, were fixed in 10% formalin, dehydrated in acetone, and embedded in methacrylate. The residue material containing the smaller fragments was centrifuged and used for preparing smears. Minibiopsies were stained with hematoxylin-eosin (H&E), and smears were stained with Papanicolaou. The diagnosis formulated at FNAB was verified histologically on material from surgery or autopsy or clinically, by following variations in lesion size over time with sonogram or CT. In cases of metastases, verification was based on the histotype of the primary neoplasia. Cases operated after FNAB (27 of 99 patients; 15 female, 12 male; group A) were compared with those who did not undergo preoperative FNAB (198 patients; 96 female, 102 male; group B). The diagnoses formulated on the surgical fragments were classified as nonneoplastic or neoplastic benign lesions and primary or secondary malignant lesions. Useful surgeries (for benign and primary malignant neoplastic lesions) and useless surgeries (for nonneoplastic and metastatic lesions) were summed for each group. Age, size of neoplasia, presence or absence of infiltration in 0 1991 WILEY-LISS. INC.

FNAB AND RENAL MASSES

the renal vein, and local-regional lymph node metastasis at the time of surgery were taken into consideration for each patient. The chi-square and the Student t test were applied, as appropriate, to calculate the significanceof the differences between the two groups. Sensitivity, specificity, negative predictive value, and total diagnostic accuracy were calculated.

Results FNAB almost invariably allowed differentiation of nonneoplastic from neoplastic lesions. Nonneoplastic indicates that cytological examination of the aspirate sediment revealed erythrocytes, macrophages with or without hemosiderin, nonatypical epithelial cells, and, occasionally, the delicate laminations typical of echinococcosis (Fig. 1). Neoplastic refers to those aspirates that contained tissue fragments and blood. Differential diagnosis between epithelial and connective tissue neoplasias was generally easy. In the first group, clear-cell and granular-cell neoplasias could be distinguished from one another (Figs. 2 and 3). When differential diagnosis between benign and malignant epithelial lesions was not possible, the size of the lesion (greater than or less than 3 cm) was evaluated instead. Eosinophilic cells with abundant cytoplasm, small round nuclei, and no mitoses or necrosis were evidence of an oncocytoma, irrespective of size (Fig. 4). FNAB usually allowed differentiation of benign from malignant connective tissue neoplasias. Angiomyolipomas, in the former group, could be recognized on the basis of vessels with sclerohyalin walls surrounded by hyperplastic muscle cells and immersed in fibroadipose

Fig. 2. Papillary carcinoma of the mixed clear-cell (arrowhead) and granular-cell (arrow) cell (H&E, 200),

Fig. 3. Clear-cell carcinoma with a compact solid structure (H&E,

x 220).

Fig. 1. Wall of a hydatid cyst. Delicate laminations are seen in the outer nonnucleated layer (H&E, x 350).

Fig. 4. Oncocytoma: large cells with abundant eosinophilic granular cytoplasm and small round nuclei (H&E, X250).

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CRISTALLINI ET AL. Table I. Fine-Needle Aspiration Biopsy Diagnosis of Renal Masses Compared With Clinical or Histological Results FNAB diann0si.r Benign lesions Malignant lesions Total

Number of cases

Benign

38

33 (TN)

34 12

Clinical

Histological

Malignant

Benign

Malignant

-

1 (TN)

4 (FN)

-

12 (TP)

1 (FP)

21 (TP)

33

12

2

25

True-negatives (TN): 33 + I = 34. False-negatives (FN): 4. Truepositives (TP): 12 + 21 = 33. False-positive (FP): 1.

tissue with polymorphic nuclei in the adipocytes 5*6 (Fig. 5). Out of 99 aspirates from kidney neoplastic lesions, 7 (7.07%) were unsuitable for diagnosis, and in 20 cases (20.20%) the FNAB diagnosis could not be verified. Cytohistological examination of the remaining 72 cases revealed 30 simple cysts, 26 clear-cell carcinomas, 6 granular-cell carcinomas, 4 angiomyolipomas, 2 adenomas, 2 metastases, 1 oncocytoma, and 1 hydatid cyst. The diagnoses were formulated on the first pass in 65 cases (90.27%) and on the second in 7 (9.72%). No complications were observed. Thirty-three of the 38 lesions diagnosed as benign were verified by clinical follow-up, the other 5 histologically. Twenty-two of the 34 malignant lesions were verified histologically and 12 clinically. Thirty-four benign (truenegatives) and 33 malignant (true-positives) lesions were confirmed. Four malignant lesions were diagnosed as benign (false-negatives) and one benign lesion as malignant (false-positive) (Table I). Sensitivity was 89.18%, specificity was 97.14%, negative predictive value was 89.47%, and total diagnostic accuracy was 93.0570. Considering pathology distribution within the two groups of nephrectomized patients (Table 11), there were 2 1 useful surgical operations in group A (1 benign and 20 primary malignant neoplasias) and 128 in group B (11 benign and 117 primary malignant lesions). Six surgical operations proved useless in group A (all nonneoplastic lesions) and 70 in group B (65 nonneoplastic and 5 metastatic lesions). The differences were highly significant (P < 0.001).

Fig. 5. Angiomyolipoma, with thick-walled blood vessels, smooth muscle, and adipose tissue (H&E, X 150).

Patients with primary malignant neoplasias (20 in group A; 117 in group B) were further studied with respect to age, lesion diameter, absence or presence of infiltration in the renal vein, and local-regional lymph node metastasis at the time of operation (Table 111). Average age was lower in group A (60.1 yr) than in group B (62.2 yr) and so was average lesion diameter (57.8 versus 67.2 mm), but the differences were not significant. The renal vein was infiltrated in 1 group A and 22 group B cases. There was one case of local-regional lymph node metastasis in group A and 15 in group B; this difference was highly significant (P < 0.001).

Discussion Although increasing use of sophisticated radiodiagnostic techniques, such as ultrasonography and CT, reveals an ever greater number of renal masses, these techniques do not always make it possible to establish which lesions should be sent to surgery. Although FNAB has proved helpful in resolving this problem, its use is still limited. When FNAB is carried out and interpreted correctly, it can differentiate nonneoplastic from neoplastic benign lesions and primary from secondary malignant lesions. Diagnosis on the needle biopsy material of our 72 cases proved to be correct in 67 cases (34 true-negatives; 33 true-positives) and wrong in 5 (4 false-negatives; 1 false-



Table 11. Renal Pathology in 225 Nephrectomized Patients With (Group A) and Without (Group B) Preoperative FNAB Histological diagnosis of surgical fragment Benign

Group A B Total

Non neoplastic

Neoplastic

Number of patients

No.

%

No.

27 198 225

6 65 71

22.22 32.82 31.55

11 12

Useful surgical operations: group A: 1

34

Malignant

1

+ 20 = 21; group B: 11 + 117 =

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Primary

Secondary

%

No.

%

No.

3.70 5.55 5.33

20

14.01 59.09 60.88

-

-

117

5 5

2.52 2.22

131

%

FNAB AND RENAL MASSES Table 111. Characteristics of Patients With Primary Malignant Renal Neoplasias Submitted (Group A) and Not Submitted (Group B) to Preoperative FNAB A veruge

Group A B

Total

Renal vein infiltration

Lymph node metastases

Number of patients

age

A veruge diameter

(vr)

(mml

Absent

Present

20 117 137

60.1 62.2

57.8 67.2

-

-

19 95 114

22 23

positive). Total diagnostic accuracy was, therefore, 93.05%, which is within the limits reported in the literature9" and which confirms the reliability of the method. One of the four false-negatives, an aspirate containing rare eosinophilic cells interpreted as an oncocytoma at FNAB, proved to be a granular-cell carcinoma after histological examination. In the other three cases (highly vascularized clear-cell carcinomas over 10 cm in diameter), erythrocytes and macrophages full of hemosiderin were aspirated. In no case did the diagnostic error delay surgery, since the lesions had been correctly interpreted on the basis of the radiological and clinical workup. The false-positive diagnosed as a clear-cell carcinoma was shown to be an angiomyolipoma on histological examination of the surgical fragment. Cytological examination of the liquid aspirate sediment from kidney cysts enabled us to identify a hydatid cyst. Using the same procedure, others have diagnosed 2%-3% of the carcinomas that arise on the kidney to be cysts. Aspiration of neoplasias located in the superior pole of the kidney and infiltrating the adrenal gland helps identify the site of origin when radiodiagnostic techniques do not provide an answer. FNAB is particularly helpful in investigating renal masses in patients with extrarenal primary malignant neoplasias. l3-I5 In fact, if diagnosis of metastasis makes surgery useless, diagnosis of a second primary malignant neoplasia calls for immediate surgery. In our series of 20 patients with extrarenal malignant neoplasias, FNAB of the renal mass revealed three (15%) second primary malignant neoplasias. By selecting renal cases to be sent to surgery, FNAB reduces the number of surgical operations for nonneoplastic and secondary malignant lesions (useless operations) and increases those for benign neoplastic and primary malignant lesions (useful operations). The differences between useful (21 group A; 128 group B) and useless (6 group A; 70 group B) operations were both highly significant (P < 0.001). FNAB made early diagnosis possible in patients with malignant neoplasias, at least as far as renal vein infiltration and lymph node metastases were concerned; the be-

'*

1

A bten t

Present

19 102 121

15 16

1

tween-group differences were highly significant (P < 0.001). In conclusion, the present findings suggest that, because of its simplicity, diagnostic accuracy, and low costbenefit ratio, FNAB should be included in the diagnostic protocol of all renal masses.

References 1. Frable WJ. Thin-needle aspiration biopsy. Philadelphia: Saunders, 1983:7-19. 2. Nosher JL, Amorosa JK, Leiman S, Plafker J. Fine needle aspiration of the kidney and adrenal gland. J Urol 1982;128:895-9. 3. Nguyen GK. Percutaneous fine-needleaspiration biopsy cytology of the kidney and adrenal. Pathol Annu 1987;22:163-91. 4. Van Krieken JHJM, Oosterwijk E, Lycklama A, Nijeholt AAB, Ruiter DJ. Renal oncocytoma: a report of two cases with immunohistochemical evaluation. Hum Pathol 1988;19:46W. 5. Glenth@jA, Partoft S. Ultrasound-guided percutaneous aspiration of renal angiomyolipoma: report of two cases diagnosed by cytology. Acta Cytol 1984;28:265-8. 6. Nguyen GK. Aspiration biopsy cytology of renal angiomyolipoma. Acta Cytol 1984;28:2614. 7. Kline TS. Handbook of fine needle aspiration biopsy cytology (2nd ed). New York: Churchill Livingstone, 1988:43343. 8. Pilotti S, Rilke F, Alasio L, Garbagnati F. The role of fine needle aspiration in the assessment of renal masses. Acta Cytol 1988; 32:l-10. 9. Dekmezian RH, Charnsangavej C, Rava P, Katz RL. Fine needle aspiration of kidney tumors in 105 patients: a cytologic and histologic correlation. Acta Cytol 1985;29:931. 10. Murphy WM, Zambroni BR, Emerson LD, Moinuddin S, Lee LH: Aspiration biopsy of the kidney: simultaneous collection of cytologic and histologic specimens. Cancer 1985;56:200-5. 1 1 . Plowden KM, Erozan YS, Frost JK. Cellular atypias associated with benign lesions of the kidney as seen in fine needle aspirates. Acta Cytol 1984;28:648-9. 12. Ambrose SS, Lewis EL, OBrien D P 111, Walton KN, Ross JR. Unsuspected renal tumors associated with renal cysts. J Urol 1977; 117:70&7. 13. Cristallini EG, Padalino D, Bolis GB. Role of FNAB in the followup of cancer patients. Appl Pathol 1989;7:219-24. 14. Friedman M, Shimaoka K, Fox S, Panahon AM. Second malignant tumors detected by needle aspiration cytology. Cancer 1983;52:699706. 15. Giardini R, Pilotti S, Alasio L, Rilke F. The role of aspiration cytology in staging and monitoring of malignant neoplasms. In: Luciani L, Piscioli F, eds. Aspiration cytology in the staging of urological cancer. Clinical, pathological and radiological basis. Berlin: Springer, 1988:75-6.

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Role of fine-needle aspiration biopsy in the assessment of renal masses.

Clinical and histological control of fine-needle aspiration biopsy (FNAB) diagnosis of 72 kidney masses observed between 1981 and 1988 confirmed 34 be...
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