Bilateral benign renal oncocytomas and the role of renal biopsy: single institution review
Leone et al. BMC Urology
Bilateral benign renal oncocytomas and the role of renal biopsy: single institution review
Andrew R. Leone 0
Laura C. Kidd 0
Gregory J. Diorio
Wade J. Sexton
Philippe E. Spiess
0 Equal contributors Department of Genitourinary Oncology, H. Lee Moffitt Cancer Center and Research Institute , 12902 Magnolia Drive Office 12538, Tampa, FL 33612 , USA
Background: The goal was to assess the natural history and management of patients with pathologically proven bilateral (synchronous) RO after undergoing initial partial nephrectomy (PN). Methods: All patients underwent either robotic/laparoscopic or open PN by two experienced genitourinary oncologists from 2005-2013. Final pathology was determined by surgical excision, CT-guided percutaneous core biopsy (CT-biopsy) or fine needle aspiration (FNA). Patient demographics, tumor characteristics (pathologic data, location, size) type of surgery, pre/post estimated glomerular filtration rate (eGFR) and surgical complications were recorded. Results: Twelve patients were identified with bilateral RO. Median age at the time of surgery was 68 years (46-77) (Table 1). The median size of the largest tumor(s) resected was 2.75 cm (1.5-5.5 cm) and second largest tumor(s) was 1.75 cm (1.0-4.0 cm). Four patients underwent bilateral staged PN and one patient underwent simultaneous bilateral PN (horseshoe kidney). Two patients underwent RFA at the time of biopsy of the contralateral mass after PN. Five patients underwent CT-bx/FNA (5/5) of the contralateral mass followed by active surveillance. Mean follow up was 34 months. There was no significant change in median creatinine pre- and post-operatively. One patient was lost to follow up and one patient died of unknown causes 5 years post-operatively. eGFR decreased an average of 16.96% post-operatively, including a single patient whose eGFR increased by 7.8% after surgery and a single patient whose eGFR did not change (Table 2). Conclusions: Patients with bilateral renal masses and pathologically proven RO can be safely managed with active surveillance after biopsy confirmation of the contralateral mass.
Bilateral; Biopsy; Oncocytoma; Renal cell carcinoma; Synchronous
Renal oncocytoma (RO) is the second most common
benign renal neoplasm which arises from the intercalated
collecting duct cells in the kidney [1, 2]. It has an
estimated incidence of 3 to 7% of all primary renal masses
[3, 4] and comprises 10 to 15% of enhancing small renal
masses (≤4 cm in diameter) . It commonly presents in
men in the seventh decade of life and is often diagnosed
incidentally . RO can be unilateral or bilateral (4 to
14% of cases), solitary or multifocal (2 to 12% of cases)
and can exist concurrently with malignant components,
specifically renal cell carcinoma (RCC) , frequently
chromophobe RCC (chRCC) . Oncocytosis has been
used to describe numerous discrete oncocytic nodules,
usually with the presence of a larger primary nodule .
In clinical practice, RO often represents a diagnostic
challenge, due to its similarity in appearance to renal cell
carcinoma on both pathology and imaging, 
specifically chromophobe RCC. RO and chromophobe RCC
share a common cellular origin from intercalated cells
. Recent research has attempted to distinguish the
two tumors. The radiologic finding of “segmental
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Table 1 Demographic and outcomes data
Mean BMI (kg/m2)
Median largest tumor size (cm)
Median next largest tumor (cm)
Mean Pre-operative Creatinine (mg/dL)
Post-operative Creatinine (mg/dL) at 1 month
Median follow-up after PN (months)
Alive at follow-up
aExcludes one patient lost to follow-up
bCKD defined as eGFR <60 mL/min/1.73 m2
enhancement inversion” on computerized tomography
(CT) has shown acceptable specificity, but tends to be
reliable in a size-dependent matter . Also, this finding
has shown low sensitivity, ranging from 15 to 21% in
magnetic resonance imaging (MRI) and CT respectively,
and only fair inter-observer agreement . One recent
study showed a high sensitivity (receiver-operating
characteristic area under the curve 0.817, p < 0.001) of
predicting RO versus chRCC with the combined presence
of a central stellate scar and higher Hounsfield Units
(HUs) on multiphase CT . Despite these and other
studies, there is an inability to clinically accurately
Table 2 Follow-up Characteristics
distinguish between RCC and RO based on imaging
alone. Thus, enhancing suspicious small renal masses
(SRMs) are treated as probable malignancy and managed
via surgical excision (partial or radical nephrectomy
(RN)), ablation, or surveillance [10, 11]. Recently, the
role of renal mass biopsy (RMB) has experienced
resurgence in popularity in managing patients with SRMs. In
an effort to avoid the morbidity associated with
treatment modality, and possibly avoid overtreatment in
patients with bilateral renal masses, some have even
advocated for all patients with SRM to undergo RMB
The efficacy and practical role of biopsy in the
diagnosis of renal oncocytoma has been a focus of study in
recent years. There have been variable data to both
support and refute the use of a core or FNA prior to
deciding upon management. Depending on the adequacy
of the tissue obtained, pathology can result as either a
specific subtype of RCC, RO, or a mix of both, called
hybrid oncocytic/chromophobe tumors (HOCT). When
pathologists cannot discriminate between chRCC and
oncocytoma, the designation of “oncocytic neoplasm” is
used . Again, this contributes to a clinical dilemma
in how to manage these patients.
Despite the risk of concurrent malignancy, however,
there is a shift toward more conservative management
of SRMs. This study sought to investigate the use of
renal biopsy following unilateral partial nephrectomy in
the setting of primary bilateral synchronous renal
oncocytomas. This subset has been previously observed in a
case series of three patients in 2010 . Our cohort of
patients represents the largest presenting with bilateral
renal oncocytomas. We propose that an approach
involving partial nephrectomy proven diagnosis of
* range provided to ensure no identifying information
** follow-up period from first partial nephrectomy
† eGFR calculated using CKD-EPI equation, definitions of CKD per KDIGO guidelines
oncocytoma with bilateral masses undergo renal mass
biopsy. In the case of confirmation of oncocytoma or
oncocytic neoplasm, patients can be safely followed on
active surveillance protocols.
After institutional review board approval MCC 15666,
we searched our nephrectomy database between 2005
and 2013 for all patients with bilateral oncocytoma.
Twelve patients were identified who had also undergone
either a robotic/laparoscopic or open partial
nephrectomy by two surgeons (PES, WJS) at Moffitt Cancer
Center in Tampa, Florida. Further record provided the
final pathology, which was determined by surgical
specimen and correlated with CT-guided percutaneous core
biopsy or fine needle aspirate. Size of biopsy needle, as
well as biopsy technique was variable and performed at
the discretion of the radiologist. Additional patient
information was gathered retrospectively, including: age,
gender, BMI, largest and next largest tumor sizes, number
of tumors per patient, pre-operative creatinine, the
presence of absence of pre-operative chronic kidney disease
(CKD), post-operative creatinine at one month, percent
of patients surviving to follow-up, median follow-up
time and percent undergoing radiofrequency ablation
(RFA). Management decisions were based on surgeon
discretion, based on factors such as linear growth rate
kinetics, size of the contralateral tumor, patient
comorbidities and patient preference.
Patient demographic data was listed and pathological
characteristics were reported based on phrasing used in
the patients’ charts. Renal function pre- and
postoperatively was also recorded. Estimated GFR (eGFR)
was calculated via the CKD-EPI equation with CKD
classifications per KDIGO practice guidelines .
Follow-up was determined on an individual basis at the
discretion of the two surgeons listed above. Patients
were generally followed in clinic with labs and imaging
every three to six months for two years, with increasing
intervals after that. All statistics were performed using
IBM SPSS software version 22.
Of the 583 patients in our database from 2005 to 2013,
twelve were found who were diagnosed with
synchronous bilateral renal oncocytoma and had undergone
unilateral partial nephrectomy. Nine of these patients had
also undergone subsequent CT-guided biopsy or FNA of
the contralateral kidney. Table 1 summarizes patient
demographics. The patient median age at time of surgery
was 68 years (46–77). The median size of the largest
tumor(s) resected was 2.75 cm (1.5–5.5 cm). Median size
of the second largest tumor(s) was 1.75 cm (1.0–4.0 cm).
Four patients underwent bilateral staged PN and one
patient underwent simultaneous bilateral partial
nephrectomy for horseshoe kidney. Two patients underwent
radiofrequency ablation at the time of biopsy of the
contralateral mass following PN. Five patients
underwent CT-guided biopsy (n = 5) and FNA (n = 5) of the
contralateral mass after PN, followed by active
surveillance with routine imaging. There were no reported
complications secondary to FNA or core biopsy
collection. No patients required repeat intervention for
suspected malignancy at a mean follow-up time of
34 months. There was no significant change in median
creatinine pre- and post-operatively (0.95 mg/dL and
1.01 mg/dL, respectively). Two patients (16.7%)
strated CKD (defined as eGFR <60 mL/min/1.73 m )
pre-operatively, which doubled after the surgeries to four
patients with CKD (33.3%). One patient was lost to
follow up and one patient died of unknown causes five
years after PN. Of the five followed by active
surveillance, three showed no growth at one year via CT scan
and two had minimal growth, 3 mm and 1 mm.
Estimated GFR was calculated via the CKD-EPI
equation and definitions of CKD were per KDIGO 
guidelines. Pre-operative and post-operative CKD
category, creatinine (mg/dL) and eGFR are all listed in
Table 2, as well as percent change in eGFR after surgery
at follow-up. Three of 12 patients (25%) were at stage
G1, 7 of 12 (58.3%) at stage G2 and 2 patients (16.7%)
were at G3a prior to surgery. After surgery, one of the
12 patients (8.3%) was at stage G1, 7 of 12 (58.3%) were
at G2, 2 of 12 (16.7%) were at G3a, likewise for G3b, with
no patients falling into G4 and G5 ranges. eGFR decreased
an average of 16.96%, including a single patient whose
eGFR increased by 7.8% after surgery and a single patient
whose eGFR did not change post-operatively.
Table 3 details the procedure performed (PN vs. RN,
FNA vs. core biopsy) and laterality, surgical pathology
and sizes of tumors, as well as biopsy pathology. Two
patients who underwent bilateral PN, also had either
FNA or core biopsy performed. In one of the two cases,
initial right FNA showed “oncocytic neoplasm, favor
oncocytoma”, while right PN surgical pathology
confirmed oncocytoma. In the second case, left core biopsy
showed “renal neoplasm with oncocytic features”,
confirmed as oncocytoma after left PN, as well as right FNA
demonstrative of “cytologic change consistent with
oncocytoma” and right PN surgical pathology affirmed
the diagnosis of oncocytoma.
Despite the relative rarity and benign nature of renal
oncocytoma ad compared to other renal tumors, the
possibility of co-existence with RCC warrants further
evaluation when suspected on incidental imaging.
Although scarce, there have been few cases of development
Table 3 Pathological Characteristics
Patient # of Tumors Tumor Sizes
1.6, 1.5, 1.5, 0.7 PN
1.5, 1.0, 1.0, 0.4 PN
Core bx + AS “oncocytoma”
Core bx + PN “oncocytoma”
“renal neoplasm with
oncocytic features” (biopsy)
“renal oncocytic neoplasm” 1
Core bx + AS “renal oncocytic neoplasm” 1
# of Tumors Tumor Sizes Management Pathology
Core bx + RFA “renal oncocytoma”
Core bx + AS “oncocytic neoplasm
PN partial nephrectomy; *RN radical nephrectomy (patient with horseshoe kidney); bx biopsy; FNA fine needle aspiration; RFA radiofrequency ablation; AS
of contralateral RCC in patients with RO, with
chromophobe carrying the best prognosis . In the case of renal
oncocytosis, besides hybrid tumors, chRCC has been
shown to be both the most common malignant dominant
tumor type (26%; 6 of 23 specimens) as well as secondary
tumor type (70%; 16 of 53 specimens) found on histology.
Childs et al. investigated metachronous renal tumors
following PN of primary RO, showing that these newly
arising tumors were more likely to be benign compared
to patients presenting with a newly diagnosed SRM; of
12 patients with either surgical or biopsy pathology, 8
were RO versus 4 RCC (of various types). They also
determined that the risk of metachronous RCC after PN
of renal oncocytoma was similar to that of the general
population, and utilized a less aggressive surveillance
approach with ultrasound (US) versus CT .
Other studies have confirmed the benign nature of
oncocytoma by showing no evidence of metastasis in
patients both undergoing active surveillance and/or
nephrectomy. Bhatt et al. published 36 patients with RO, 34
of whom underwent nephrectomy, none of whom
developed metastases at a median follow-up time of
84 months after surgery . Similar results were
obtained in a cohort of 20 patients with oncocytosis,
who showed no metastases at a median follow-up of
35 months, although CKD was a major morbidity, with
50% affected prior to surgery and 25% developing CKD
after nephrectomy . One consideration in that case is
the presence of multiple oncocytic nodules which have
been shown to intersperse between the nephrons and
affect nearby tubules in oncocytosis . Familial
syndromes can also play a role in the clinical and pathologic
presentation of oncocytoma, which is associated with
the autosomal dominant Birt-Hogg-Dubé (BHD)
syndrome. The most common tumor type found in these
patients is a hybrid mixed histology, containing features
of both oncocytoma and RCC,  often termed
“oncocytic neoplasms” by pathologists .
Recent investigation has also elucidated more about the
growth rates of renal oncocytoma. These rates have been
cited at 0.14 to 0.20 cm per year [5, 18], compared to
small renal masses in general, at 0.28 cm per year,,
according to a meta-analysis , and 0.38 cm/yr for chRCC .
Renal mass biopsy has shown to have promising utility.
Diagnostic yield on first biopsy has been shown to be 80.6
to 93% [13, 19, 20] with overall improvement in yield with
a subsequent biopsy [13, 19]. Core biopsy sensitivity and
specificity are 99.1 and 99.7%, respectively, while FNA is
93.2 and 89.8%, respectively . In addition, complications
have not been found to be a major morbidity in RMB, with
studies quoting complication rates between 8.5 and 10.4%,
most of which were minor and self-limited [13, 20]. Both
the high rate of diagnostic accuracy of RMB, as well as the
low rate of complications, argues in favor of biopsy and
subsequent implementation of an active surveillance
A single-institution study of 15 patients diagnosed
with renal oncocytoma via CT-guided biopsy was
followed to better elucidate the course of RO with
watchful waiting. Mean follow-up time was 30 months
and showed that 6 of the 15 underwent surgery (2 partial
and 4 total nephrectomies) for rapid growth (0.5 cm/yr.),
tumor burden or patient preference. All surgical
pathologies were confirmed RO except for a single case of
oncocytoma associated with chRCC (T2 Fuhrman grade 3).
Nine of the 15 patients underwent biannual ultrasound
imaging and were asymptomatic at a mean follow-up time
of 49.7 months. Those who underwent surgery were
younger and had a significantly higher tumor growth velocity
than the non-operative patients (2.4 ± 2.1 mm/yr versus
0.7 ± 0.5 mm/yr., P = 0.008) .
This possibility of harboring malignant histology was
demonstrated in a study of 20 patients with oncocytosis.
After either partial or radical nephrectomies, 13 patients
had dominant tumor hybrid histology, followed by 6
chRCC, 3 pure oncocytoma and 1 with clear cell RCC.
Multiple secondary nodules were examined and were
also varied in histology, including hybrid, chRCC, pure
RO, conventional RCC and clear cell papillary RCC .
One essential consideration in patients diagnosed with
SRMs is that of preserving renal function. In our single
institution review, 2 of 12 patients had baseline CKD
with 2 more developing it after surgery (bilateral PN and
left PN). Lane et al. showed that medically-induced CKD
(versus surgically-induced CKD) was associated with
greater rate of progressive decline in renal function,
allcause mortality and non-renal cancer mortality, with
non-renal mortality and GFR stability being similar in
the surgically-induced CKD and non-CKD cohorts.
Another study of 1928 patients showed male gender (odds
ratio (OR) 3.55), older age at diagnosis of SMR (OR
1.04), hypertension (OR 0.46), serum calcium (OR 2.06)
and lower serum albumin (OR 0.23) to be significantly
correlated with pre-operative CKD. Additionally, radical
nephrectomy, as compared to partial nephrectomy, was
shown to have the strongest association with
postoperative CKD (OR 11.89). Hence, the authors of that
paper suggested consideration of elderly men with
hypertension as candidates for PN versus radial
nephrectomy to avoid development of CKD .
Although the latter study only addressed RCC
patients, these are certainly still factors to be considered in
the setting of patients with bilateral RO. Taken together,
they suggest the importance of careful screening of
patients for risk factors pre-operatively, which may compel
intervention instead of surveillance.
In summary, renal mass biopsy followed by active
surveillance has been considered safe [5, 23], reliable,
costeffective, with no change in survival overall. Use of renal
mass biopsy has increased and should also be applied to
the unique subset of patients suspected of having
bilateral renal oncocytoma. Biopsy plus active surveillance is
also of benefit because it does not preclude the patient
from future urologic interventions, such as partial
nephrectomy or ablation .
Limitations of this study include its retrospective
nature and one patient lost to follow-up. We also had a
small sample size, due to the rarity of bilateral
synchronous oncocytoma. Our median time to follow-up was
34 months, which could perhaps not be long enough to
capture development of new tumors or other
complications in the disease course after partial nephrectomy.
Also, we recommend the use of confirmatory biopsy in
diagnosing the contralateral tumor, but not every patient
in our cohort underwent biopsy and/or FNA (only 9 out
of 12). Another limitation is the fact that all patients in
our cohort underwent partial nephrectomy, denying us
the ability to observe these masses free of intervention.
From our single institution experience we believe that
patients with unilateral renal oncocytoma with
contralateral mass who have undergone unilateral partial
nephrectomy of the RO should undergo confirmatory biopsy
of the contralateral mass and can be safely managed
with active surveillance imaging protocols. Future
prospective multi-institutional trials are needed to
determine optimal management of bilateral renal masses in
the setting of prior unilateral oncocytoma.
AS: Active surveillance; chRCC: Chromophobe type, renal cell carcinoma;
FNA: Fine needle aspiration; RCC: Renal cell carcinoma; RMB: Renal mass
biopsy; RO: Renal Oncocytoma; SRM: Small renal mass
Availability of data and materials
Data is saved on HIPAA protected database in de-identified format and can
be shared if requested as it is DE identified.
AL: acquisition of data, analysis and interpretation of data, drafting
manuscript, critical revision of the manuscript and statistical analysis. Co-first
author. LK: acquisition of data, analysis and interpretation of data, drafting
manuscript, critical revision of the manuscript and statistical analysis. Co-first
author. GD analysis and interpretation of data, drafting manuscript, critical
revision of the manuscript and statistical analysis. KZ analysis and
interpretation of data, drafting manuscript, critical revision of the
manuscript and statistical analysis. PS analysis and interpretation of data,
drafting manuscript, critical revision of the manuscript and statistical
analysis. WS drafting manuscript, critical revision of the manuscript and
statistical analysis. PS acquisition of data, analysis and interpretation of
data, drafting manuscript, critical revision of the manuscript and statistical
analysis. All authors read and approved the final manuscript.
Co-authors Dr. Kamran Zargar-Shoshtari and Dr. Pranav Sharma are Associate
Editors and Dr. Philippe Spiess is a Section Editor for this journal. The authors
have nothing to disclose.
Ethics approval and consent to participate
IRB approval from USF IRB was obtained Renal Cancer: A Retrospective
Review of the Patients Diagnosed and Treated at H. Lee Moffitt Cancer
Center and Research Institute (MCC #15666). A waiver of consent was
obtained as part of the IRB acceptance and therefore patients included in
this study were not consented.
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