Anatomic Pathology / PARENCHYMAL MARGINS IN NEPHRON-SPARING SURGERY
Potential Pitfalls in the Frozen Section Evaluation
of Parenchymal Margins in Nephron-Sparing Surgery
Teresa McHale, MD,1 S. Bruce Malkowicz, MD,2 John E. Tomaszewski, MD,1
and Elizabeth M. Genega, MD1
Key Words: Frozen section; Nephron-sparing surgery; Partial nephrectomy; Renal cell carcinoma; Kidney
DOI: 10.1092/N55X0T0EDH37J3UG
Abstract
With advances in radiographic imaging, there has
been an increase in the incidental detection of small
renal cell carcinomas, with a resultant increase in
partial nephrectomies for these tumors. Partial
nephrectomy often necessitates assessment of renal
parenchymal margins by frozen section. To determine
the most common problematic “lesions” encountered
on renal parenchymal margins, we evaluated all
diagnostically challenging frozen sections that had been
referred to a genitourinary pathologist.
Frozen sections with detached atypical cells and
crushed tubules were the most common lesions that
presented diagnostic uncertainty. We found that normal
constituents of renal parenchyma, namely tubules and
glomeruli, can be mistaken for neoplasia. Neoplastic
tubules of low-grade renal cell carcinomas may be
misinterpreted as thickly cut, crushed benign tubules,
and the significance of tubulopapillary “adenomas” in
frozen sections is unclear. The present report highlights
diagnostic difficulties that pathologists may encounter
on frozen sections of renal parenchymal margins.
Renal cell carcinomas account for the majority of
primary epithelial neoplasms of the kidney and 2% to 3% of
all malignant neoplasms.1-3 Approximately 12,000 patients
die of the disease each year.2,3 Radical nephrectomy is the
standard treatment for localized renal cell carcinoma, especially for patients with large tumors and a normal contralateral kidney. Partial nephrectomy (nephron-sparing surgery)
traditionally has been used for patients in whom radical
nephrectomy would substantially compromise renal function, including those with bilateral synchronous tumors, a
solitary functioning kidney, and/or significant comorbid
diseases that affect renal function.4-10 With advances in radiologic imaging, particularly ultrasound and computed
tomography, there has been an increase in the incidental
detection of small, low-stage tumors. At the same time,
interest has grown for the use of nephron-sparing surgery in
patients with small, localized, sporadic tumors who have a
normal contralateral kidney.5,6,8-15
The emerging survival data from several studies indicates that patient prognosis is not compromised for those
who have had these partial resections. 4,8,10,15,16 Several
investigators have compared outcomes in patients undergoing radical nephrectomy with those undergoing partial
nephrectomy and have found no significant difference in
cancer-specific or overall survival.6,7,9,13,14,17 Moreover,
nephron-sparing surgery may actually be preferable for
some patients, as there is a suggestion of a lower long-term
risk for the development of proteinuria and chronic renal
insufficiency with partial resections.9,10,18 As laparoscopic
technology advances, there is a growing effort to incorporate partial nephrectomy as a procedure performed for
these patients.
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A major concern with performing nephron-sparing
surgery is the potential for local recurrence. This has been
reported in up to 10% of partial nephrectomies compared
with 3.3% of radical nephrectomies.5-10,16,19,20 The use of
nephron-sparing surgery often requires intraoperative assessment of renal parenchymal margins to ensure local control of
disease. Frozen sections of renal parenchyma occasionally
may be diagnostically challenging, and pathologists should
be aware of the potential diagnostic pitfalls of frozen renal
tissue. We are unaware of any study in the pathology literature that has addressed this issue. At our institution, we
frequently examine frozen renal parenchyma from kidneys
harboring neoplasms, as well as from potential transplant
kidneys. The purpose of this study was to highlight issues
that can arise at the time of intraoperative frozen section on
frozen renal tissue.
Materials and Methods
Renal specimens on which frozen sections had been
performed at our institution during a 6-month period (March
to September 2001) were retrieved from the surgical
pathology files. The pathology reports and frozen section
and permanent slides on these cases were reviewed (T.M.
and E.M.G.). Partial nephrectomy specimens performed for
renal cell carcinoma and biopsy specimens from transplant
kidneys with mass lesions, which were referred to a genitourinary pathologist (E.M.G. or J.E.T.) at the time of frozen
section, were selected for this study. Cases of urothelial
carcinoma of the kidney and ureter and biopsy specimens
from potential donor transplant kidneys for the evaluation of
nonneoplastic disease were excluded from the study.
Results
Intraoperative frozen sections were performed on 22
renal specimens; 21 nephrectomies were performed for renal
cell carcinoma (19 nephron-sparing surgeries and 2 radical
nephrectomies), and an excision was performed of a renal
hilar mass from a potential donor transplant kidney.
Nephron-sparing surgery was attempted in all 21 cases of
renal cell carcinoma but subsequently was converted to
radical nephrectomy in 2 cases. Sixty-two frozen sections
were performed on the 22 cases. Nine of the 62 frozen
sections were brought to the attention of a genitourinary
pathologist at the time of frozen section.
In the kidneys with renal cell carcinomas, the tumor size
ranged from 1.1 to 3.5 cm (mean, 2.3 cm), and the frozen
sections represented biopsies of parenchymal margins adjacent to the tumor (“tumor bed”). The biopsy specimens
submitted for frozen section ranged from 0.1 to 2.5 cm, with
the majority of the biopsy specimens less than 0.2 cm. ❚Table
1❚ outlines the 9 “lesions” referred to a genitourinary pathologist at frozen section, the questions posed by the referring
pathologist, the genitourinary pathologist’s interpretation,
and the final diagnosis.
Within this series, there were cases with both nonneoplastic and neoplastic “detached atypical cells.” Case 1
❚Image 1❚ shows small clusters of cells with abundant, finely
granular eosinophilic cytoplasm and bland nuclei with fine
chromatin and smooth contours. While the differential diagnosis included benign tubular epithelial cells, benign histiocytes, or cells of a low-grade oncocytic cortical neoplasm,
the cells were interpreted to represent histiocytes. In comparison, the detached atypical cells seen in case 2 ❚Image 2❚
have hyperchromatic nuclei, scant cytoplasm, and an
❚Table 1❚
Diagnostically Challenging Renal Frozen Sections
Case
No.
1
2
3
4
“Lesion” on
Frozen Section
Question From
Referring Pathologist
Histiocytes vs tumor
RCC
RCC
Adenoma
5
6
7
8
Detached atypical cells
Detached atypical cells
Detached atypical cells
Tubulopapillary lesion and
crushed tubules
Crushed tubules
Crushed tubules
Atypical cyst
Fatty hilar mass, donor kidney
9
Crushed vascular tissue
RCC
Benign tubules vs RCC
Benign tubules vs RCC
Atypical cyst vs RCC
Fat necrosis vs benign fat
GU Pathologist’s
Diagnosis
Histiocytes
Suggestive of RCC
Few atypical cells†
Low-grade papillary renal
neoplasm‡ and separate RCC
RCC
Atypical tubules
Atypical cyst
Favor adipose tissue–predominant
angiomyolipoma
Glomerulus
Final Diagnosis*
No tumor seen
Renal cortical neoplasm
No tumor seen
Renal cortical neoplasms
RCC
No tumor seen
Atypical cyst§
Adipose tissue–predominant
angiomyolipoma ||
No tumor seen
GU, genitourinary; RCC, renal cell carcinoma.
* Final diagnosis based on assessment of both the original frozen section and the permanent section.
† Additional tissue requested, but not received from the surgeon.
‡ Additional tissue requested; surgeon proceeded to radical nephrectomy.
§ Atypical cyst in patient with von Hippel-Lindau disease with 4 concurrent renal cell carcinomas removed at the time of this surgery.
|| Diagnosis of angiomyolipoma confirmed on permanent section (H&E and immunohistochemical analysis).
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© American Society for Clinical Pathology
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❚Image 1❚ (Case 1) Frozen section contains cells with abundant eosinophilic cytoplasm and bland nuclei, compatible
with histiocytes (arrows), admixed with fibrin (H&E, ×40).
❚Image 2❚ (Case 2) Detached cluster of atypical cells with
irregular hyperchromatic nuclei (arrow), highly suggestive of
tumor, present on the frozen section (H&E, ×40).
increased nuclear/cytoplasmic ratio and were favored to
represent tumor cells; this impression was confirmed on the
permanent section.
Several cases in this study contained “crushed tubules.”
The frozen section from case 4 revealed a low grade tubulopapillary lesion, favored to represent a so-called tubulopapillary adenoma, and a second subtle lesion composed
of ill-formed and haphazardly arranged tubules, many devoid
of lumens, within a sclerotic stroma ❚Image 3A❚. The cells
forming the tubules have eosinophilic cytoplasm, and in
comparison with the adjacent renal parenchyma with benign
tubules ❚Image 3B❚ , the “lesional” tubules have distinct
nuclear pleomorphism ❚Image 3C❚. This lesion was interpreted to be a renal cell carcinoma at frozen section, which
was confirmed with the permanent section. In case 6, a few
tubular structures composed of cells with overlapping,
focally irregular nuclei were present ❚Image 4❚. Although the
cytologic features were insufficient for a diagnosis of carcinoma, morphologically the tubules were mildly atypical and,
therefore, were diagnosed as such on frozen section. No
residual lesional cells were present on the permanent section,
and the final additional margins were free of tumor.
One frozen section was performed on a cyst from a
patient with von Hippel-Lindau disease (case 7). The cyst
was lined by cells with nuclear atypia and granular
eosinophilic cytoplasm ❚Image 5❚. In the absence of cells with
clear cytoplasm, a diagnosis of “atypical cyst” was made.
The renal hilar mass identified in a donor transplant
kidney (case 8) consisted of a lesion composed of adipose
tissue within which there were small clusters of epithelioid
cells with irregular nuclei and granular eosinophilic cytoplasm ❚Image 6A❚. The lesion was favored to represent an
adipose tissue–predominant angiomyolipoma, which was
confirmed with the permanent sections ❚Image 6B❚ and
❚Image 6C❚.
© American Society for Clinical Pathology
Discussion
Traditionally, the standard treatment for unilateral renal
cell carcinoma in patients with a normal contralateral kidney
has been radical nephrectomy. Partial resections have been
limited to patients in whom more extensive surgery would
compromise renal function.4-10 The indication for nephronsparing surgery may be crucial for cases in which radical
nephrectomy would render the patient anephric, namely,
patients with tumor in a solitary kidney or bilateral synchronous tumors. Patients with a renal mass and a contralateral
kidney in which renal function is affected by nonneoplastic
renal disease and systemic diseases also may be candidates
for nephron-sparing surgery to preserve functioning renal
parenchyma. Hereditary forms of renal cell carcinoma,
including von Hippel-Lindau disease, are another indication
for nephron-sparing surgery, in view of the occurrence of
multicentric and bilateral tumors in these patients.
As a consequence of the rising incidence of small, lowstage, sporadic renal cell carcinomas, largely owing to
increased detection because of refinements in radiographic
techniques, interest has grown for elective nephron-sparing
surgery for these incidentally detected tumors.5,6,8-15 In the
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A
B
❚Image 3❚ (Case 4) A, Discrete lesion (lower right) composed
of irregular tubular structures in a sclerotic stroma in the
frozen parenchymal margin (H&E, ×5). B, The tubular epithelial cells of the adjacent benign tubules (A, top and lower left)
have nuclei with smooth nuclear membranes and finely granular chromatin (H&E, ×40). C, In comparison, the neoplastic
tubules are composed of cells with moderately pleomorphic
nuclei that have coarser chromatin and irregular nuclear
contours (H&E, ×40).
C
light of survival data, which do not demonstrate a worse
overall outcome for patients who undergo partial nephrectomy rather than radical nephrectomy, these partial resections are being advocated for patients with a unifocal, small
(usually <4 cm) renal mass and a normal contralateral
kidney.4,7,9,13,14,16,17 Both tumor stage and tumor size have
been shown to correlate with outcome in patients who have
undergone a partial resection.8,10,14,16 Recurrence rates and
outcomes are reported to be more favorable for patients with
small (4 cm or less vs >4 cm), low-stage (pT1 or less vs
>pT1) tumors.8,10,13-17,21
One of the principal concerns in performing nephronsparing surgery for renal cell carcinoma is the risk of local
tumor recurrence, reported in up to 10% of patients.5-10,16,20
The local recurrence may be due to incomplete resection of
the primary tumor, undetected multifocal disease, or the
occurrence of a new tumor.5,7,10,22 To prevent incomplete
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resection, excision of the tumor with an adjacent rim of
normal renal parenchyma usually is performed,5,20,22 and
some suggest the margin only needs to be 1 mm.23 The
amount of renal tissue given as the surgical margin may be
small, but, provided it is free of tumor, its size is of no significance with follow-up of approximately 4 years.22 This may
be due in part to the “additional margin” generally attained
with the use of laser coagulation or electrocautery to the
surgical bed after excision of the tumor. While a wealth of
literature exists concerning the clinical aspects of nephronsparing surgery, little attention has been given to the pathologic examination of renal parenchymal margins. At our
institution, examination of these margins by frozen section is
performed to assess for completeness of excision. Surgical
margins often consist of minute fragments of renal
parenchyma, and such small biopsy specimens, with crush
and freeze artifact, may present diagnostic dilemmas. In the
© American Society for Clinical Pathology
Anatomic Pathology / ORIGINAL ARTICLE
present study, we found several instances in which difficulties arose in the evaluation of frozen nonneoplastic and
neoplastic renal tissue.
Normal constituents of renal parenchyma can mimic
neoplasia on frozen section. Benign renal tubules, if crushed
or cut thickly and longitudinally, with no visible lumen, can
be mistaken for neoplastic tubules, as can tubules within
chronically damaged kidneys, which may demonstrate
regenerative reactive epithelial atypia. Complicating the
issue further is the fact that frankly dysplastic epithelium
may line renal tubules, which has been documented to occur
in “normal” kidneys that contain renal cell carcinoma.24
Conversely, neoplastic tubules may be interpreted erroneously as tangentially and thickly cut benign renal tubules.
Evaluation of the architecture and arrangement and growth
pattern of the tubules is necessary, as well as the assessment
of the nuclear/cytoplasmic ratio, nuclear membrane contour,
and quality of the nuclear chromatin for the differentiation of
benign from malignant cells and tubules ❚Table 2❚.
Another potential problem is the presence of a so-called
renal cortical adenoma on a frozen section. These lesions
often have a tubulopapillary growth pattern, are cytologically
low grade, and often are less than 1 cm in greatest dimension. At the time of frozen section, a lesion with such an
appearance may represent a cortical “adenoma,” a satellite
lesion from the main tumor, or tissue from the periphery of a
papillary renal cell carcinoma. Therefore, we believe it is
prudent at the time of frozen section, and after a discussion
with the surgeon, to make a diagnosis of “low grade tubulopapillary neoplasm.” Any cortical lesion, regardless of size,
that contains tumor cells with clear cytoplasm, we consider
to be a carcinoma.
A
❚Image 4❚ (Case 6) Frozen section with a few tubules
(arrow) without visible lumens. The cells have moderately
abundant cytoplasm and overlapping nuclei with fine chromatin and focally irregular nuclear contours (H&E, ×40).
We occasionally are asked to evaluate renal cysts at
frozen section, most often from potential donor transplant
kidneys, and less commonly from patients with hereditary
disorders. Renal cysts may have an epithelial lining
composed of cytologically benign, atypical, or frankly
malignant cells, and the cysts can occur in patients with or
without solid parenchymal neoplasms and with or without
hereditary disorders.25-28 Although no definitive criteria have
been established for classifying cysts as atypical or frankly
B
❚Image 5❚ (Case 7) A, Frozen section of renal cyst in a patient with von Hippel-Lindau disease (H&E, ×10). B, The cyst is lined by
mildly hyperplastic epithelium composed of cells (arrows) with slightly angulated nuclei and eosinophilic cytoplasm (H&E, ×40).
© American Society for Clinical Pathology
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A
B
❚Image 6❚ (Case 8) A, Frozen section of renal hilar mass
shows clusters of large epithelioid cells (arrows) with granular eosinophilic, focally vacuolated cytoplasm and irregular
nuclei within fat, suggestive of an adipose tissue–predominant angiomyolipoma (H&E, ×20). B, A similar appearance is
seen on the permanent section (H&E, ×10). C, An immunohistochemical stain (HMB-45, 1:50 dilution, DAKO, Carpinteria, CA) highlights the epithelioid cells, which supports the
diagnosis (HMB-45, ×10).
C
❚Table 2❚
Comparison of Histologic Features of Neoplastic Tubules and Benign Renal Tubules in Frozen Sections
Features
Cytologic
Increased nuclear/cytoplasmic ratio
Nuclear contours
Chromatin clumping
Hyperchromasia
Nucleoli
Cytoplasm
Architectural
Tubular architecture
Tubular lumens visible
Solid architecture
Tubulopapillary architecture
Stroma
*
Neoplastic Tubules
Benign Renal Tubules
Yes, in general
Irregular
Yes
Yes
Variable (none to prominent)
Variable (clear, granular, and eosinophilic;
often densely granular)
No
Smooth, round
No
No
Usually inconspicuous
Homogeneous and finely granular; eosinophilic
Yes
Yes or no
Yes
Yes
Sclerotic
Yes
Yes or no
No*
No
Often appears edematous, occasionally fibrotic
May appear to have solid growth if tubules are cut tangentially or tissue is crushed.
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malignant,29,30 we generally regard renal cysts lined by clear
cells, even focally and with low-grade cytology (at most
grade 1 renal cell carcinoma), as cystic (conventional) renal
cell carcinomas. Cysts lined by cells with nuclear atypia and
granular, eosinophilic cytoplasm (not clear cytoplasm),
usually are diagnosed as “atypical cyst.”
Unusual renal and perirenal lesions occasionally may be
encountered on a frozen section, as seen by the identification
of a renal hilar angiomyolipoma in a donor transplant kidney.
While diagnostic questions are unlikely to arise with a
classic angiomyolipoma, certain variants of this tumor may
present diagnostic challenges: the adipose tissue–predominant variant may be misinterpreted as fat necrosis, lipoma, or
liposarcoma, and the epithelioid variant may be misinterpreted as renal cell carcinoma.
The incidence of partial nephrectomies seems to be
increasing. This reports highlights diagnostic questions
that may arise with frozen renal tissue. We found the
most common problematic lesions in frozen sections of
renal parenchymal margins to be crushed tubules and
detached atypical cells. Careful evaluation of the arrangement and growth pattern of the tubules and the cytologic
features of the cells is required to assist in the determination of the presence of malignancy. At times, however,
the features of neoplasia may be subtle. Given the minute
fragments of renal parenchyma often received for frozen
section evaluation, definitive diagnoses cannot always be
made, and in such cases, additional tissue should be
requested from the surgeon.
From the Departments of 1Pathology and 2Urology, Hospital of
the University of Pennsylvania, University of Pennsylvania
Medical Center, Philadelphia.
Address reprint requests to Dr Genega: Dept of Pathology,
Beth Israel Deaconess Medical Center, 330 Brookline Ave,
Boston, MA 02215.
Acknowledgment: We thank Navneet Narula, MD, for critical
review of the manuscript.
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