Introduction
Renal lesions can be classified as
malignant, benign, or inflammatory. Inflammatory renal lesions may mimic
malignant renal lesions on imaging and include infection, inflammation, or
trauma induced lesions (1). Of the
non-inflammatory cases, benign masses compose approximately 13% of newly
diagnosed lesions such as oncocytomas and angiomyolipomas; the rest renal cell
carcinoma (2). Renal cell carcinoma
(RCC) accounts for 3.8% of all cases of adult malignant neoplasms. It typically
presents in the sixth and seventh decades of life. RCC of clear cell histology is the most
common, followed by papillary and chromophobe subtypes (2). Overall, the incidence
of RCC has increased in the last three decades with an estimated 63,920 cases
and 13,860 deaths (3). The advent of
improved imaging techniques such as computer tomography (CT) and magnetic
resonance imaging (MRI) has partially driven this rising incidence, as
clinicians can now detect pre-symptomatic renal tumors incidentally (3, 4).
Accordingly, small renal masses (SRM) that are less than or equal to 4 cm are
being detected more frequently. In the prior decade, the average renal tumor
size decreased from 6.7 cm to 5.9 cm (5).
In part, imaging can assist in
differentiating renal masses of unknown malignant potential. For instance, benign lesions like angiomyolipomas
can be identified by the presence of macroscopic fat. CT or MRI scan with intravenous contrast
administration can help distinguish those renal masses that need further
evaluation. For a renal mass to be
considered malignant, it should enhance with administration of contrast.
However, 10-20% of small, solid CT-enhancing renal masses are found to be
benign after surgical removal (6). In
particular, differentiating a benign renal cyst and a cystic RCC by imaging is
difficult.
In terms of the size distribution of
RCC, 35% of tumors are < 4 cm, 33% are between 4 and 7 cm, and 32% are >
7 cm (5). Larger masses are increasingly
correlated with malignancy and worse outcomes (7). The size of the renal mass,
tumor risk profile, and clinical symptoms are all significant prognostic
factors. However, pathologic stage is
the most important prognostic factor. Patient-related factors like
comorbidities and frailty are also influential in determining appropriate
management.
In
the management of a renal mass the most important predictors of
post-operative GFR besides pre-operative GFR are both residual
functioning parenchyma and ischemia time (8). Chronic kidney disease (CKD) in general is
defined as an estimated glomerular filtration rate (GFR) of less than 60
mL/min/1.73m2 for over 90 days (9).
The different stages of CKD are categorized as shown in Table 1. End stage renal disease (ESRD)
is defined as GFR less than 15 mL/min/1.732m2 and requires renal replacement
therapy such as hemodialysis. As we progress beyond the Halstedian era of
radical extirpative approaches in oncologic surgery and move into the era of
minimally invasive surgery, a series of questions arise in the management of
renal masses. One specific question that
we will address is whether sparing nephrons impacts mortality.
Table 1. Definitions of CKD stages based on GFR
Chronic Kidney Disease Stage
|
Estimated GFR (ml/min/ 1.73m2)
|
I
|
≥ 90
|
II
|
60 – 89
|
III
|
30 – 59
|
IV
|
15 – 29
|
Management Approaches
As stated above, localized SRMs have
increased in incidence and now are a fairly common clinical situation. Historically, radical nephrectomy represented
the gold standard for the treatment of all renal masses. The first documented radical nephrectomy was
completed for the treatment of renal cell carcinoma in 1963 (10). It still represents the standard of care in
non-localized cases and for renal masses of unknown malignant potential in 30%
of cases (11). However, practices have
changed dramatically in the last two decades.
It has been recognized that SRMs have broad heterogeneity in tumor
biology and several management strategies are now offered, including radical
nephrectomy (RN), partial nephrectomy (PN), thermal ablation (TA) as well as
active surveillance (AS). Moreover, for
treating SRMs, the risk of ensuing CKD and ESRD
requiring renal replacement therapy has largely favored nephron-sparing
surgery.
PN involves complete but localized
resection of the tumor, while maintaining the most amount of normal parenchyma
possible. For the surgical management of
SRMs of <4 cm, PN has become standard of care. Some even suggest its
application be expanded to masses up to 7 cm in size, given their 20-30% likelihood
of benign pathology (12). With regards to approach, both laparoscopic and robotic
PNs have been shown to have good outcomes with short recovery time, acceptable
ischemia time, and less morbidity than open PN (13, 14). Robotic technology is generally preferred
for PN, given the technical limitations of laparoscopic surgery, and the
literature does support its use for moderate to complex renal masses given the
decreased conversion rate to RN for robotic PN in comparison to laparoscopic PN
(15).
Thermal ablative treatments such as
renal cryoablation (CA) and radiofrequency ablation (RFA) have materialized as
alternative nephron-sparing therapies for patients with localized SRMs. Both
techniques can be initiated percutaneously or via laparoscopic exposure. Some
report reduced morbidity with this treatment but the long-term oncological
control has not been well established, with a greater incidence of local
recurrence reported for these techniques than for surgical approaches. RFA is reported to
have a likelihood of tumor recurrence of 12.9% and risk of metastasis of 2.5%,
even within a well-selected population (16). Meanwhile, a meta-analysis by
Kunkle and Uzzo looking at CA showed a likelihood of tumor recurrence of 5.2%
and risk of metastasis of 1% (16). These TA recurrences may be salvageable with
repeat ablation, although some need traditional surgery. In the latter case,
radical or partial nephrectomy may be impossible to perform secondary to the widespread fibrotic
reaction caused by the TA (17).
However, the same population that may
benefit from ablative treatment of SRMs, may benefit from inclusion into an
active surveillance with delayed intervention protocol (18). Bosniak et al
showed that renal tumors grow at slow and variable rates of up to 1.1 cm per
year with a median growth rate of 0.36 cm per year (19). A more recent study by Crispen and colleagues
that followed patients with a localized, enhancing renal mass revealed that
absolute growth rate following detection of the tumor was 0.039 cm/year (20).
In another study observing 209 patients with SRMs and limited life expectancy
for a mean of 28 months, local progression occurred in 12% and 2 patients
(1.1%) developed metastases (21). Besides the slow growth rate and limited
progression of most SRMs, the risk of competing causes of death and of
intervention may also favor AS in this population. A study by Hollingsworth et
al. evaluating patients’ survival 5 years after surgical treatment of RCC
showed that one third of the elderly may die from their comorbidities (22).
Therefore, elderly patients or patients of poor surgical risk with a small,
solid, well-defined renal lesion may be managed with active surveillance,
involving serial renal imaging biannually or annually, and delayed intervention
when necessary.
Renal function after TA techniques and on AS
Some literature endorses superior renal
function with TA over conventional surgery. A study by Woldu et al. comparing
renal parenchymal loss between CA, RFA, and PN showed that TA was associated
with less renal parenchymal loss (23).
In another retrospective comparison of patients with a
suspicious renal
mass of less than 5 cm, Lucas et al revealed that RFA has a freedom of
CKD of 95.2% in comparison to PN at 70.7% and RN at 39.9% (24). In a European study evaluating cryoablation,
renal function was relatively well conserved, as prior to treatment GFR was 66
mL/min and it was 60 mL/min post-CA (25). In addition, those with existing CKD
experienced no change in GFR.
Limited data exists on renal function
while on active surveillance. In a
recent analysis from the Delayed Intervention and Surveillance for Small Renal
Masses Registry (DISSRM), in a group of 64 patients on AS with a renal mass of
< 4 cm and a median baseline GFR of 70.3, 64% of patients experienced a
decline in GFR at a yearly rate of 1.82 mL/min/1.73m2. This GFR decline is higher than would be
expected from aging alone. Furthermore, 24% of patients in the study
experienced upstaging in their CKD classification (26). However, given the
multiple comorbidities and advanced age of many patients who present with a
SRM, AS remains an attractive alternative that warrants further investigation.
Renal Function after Extirpative Surgery
Most of the literature has focused on
renal function after radical and partial nephrectomy. A main concern with performing RN is
reduction of GFR and ultimately requiring dialysis. In a retrospective study of
290 patients with SRMs < 4 cm, McKiernan, et al. showed that 5-year freedom
from chronic renal insufficiency, which was defined as a creatinine of > 2
mg/mL, was 100% in the PN group and 84.6%% in the RN group (27). In another retrospective study, Huang and
colleagues revealed that 65% of RN patients, in comparison to 20% of the PN patients,
had grade III CKD (GFR < 60 ml/min/1.73m2) at 3-year follow-up (28).
Severe CKD was also more likely after RN than PN, with an incidence of 36%
versus 5% respectively. In other
studies, when the tumor mass and pre-operative GFR was taken into account the
loss of kidney function remained higher in RN than PN (29, 30).
Furthermore, a retrospective study by
Kaushik and colleagues evaluated patients undergoing RN or PN for a benign
renal mass, which eliminates the confounder of malignancy in the survival
equation. They demonstrated that overall
survival at ten years was 69% for RN and 80% for PN, with a decreased risk of
CKD in the PN group in comparison to RN group (31). This alludes to a possible superiority of NSS
over RN with regards to renal function.
Finally, one of the largest and most recent studies evaluating 2068
patients with a 5-year follow up period showed that renal function after RN led
to new onset CKD stage III in 36.1% of patients and new onset CKD stage IV in
3.4% of patients (32).
Ischemia is the major concern with PN,
as this may induce tissue necrosis and irreversible damage to the functioning
renal parenchyma. This is especially pronounced in cases where ischemia is more
than 40 minutes, although even in shorter intervals there is some evidence of
parenchyma atrophy (33). However,
whether reducing ischemia time leads to a reduction in nephron damage as
measured by GFR function is unclear. A recent meta-analysis by Liu et al.
revealed that there was a higher odds of GFR decline in patients who undergo
on-clamp partial nephrectomy in comparison to off-clamp partial nephrectomy
without ischemia (34). Yet, no study
thus far has prospectively looked at the post-operative renal function of
off-clamp versus on-clamp with ischemia.
Nevertheless, the largest randomized
control trial comparing RN and PN failed to show a survival benefit of
NSS. In the EORTC 30904 trial, Van
Poppel and colleagues demonstrated that 85.7% of patients undergoing RN
experience a reduction in their GFR to below 60 ml/min/ 1.73m2 in
comparison to only 64.7% of the group undergoing PN (35, 36). Despite this diminished impact on renal
function, the PN group did not experience improved overall mortality
outcomes. In
other words, the higher
incidence of de-novo CKD post-surgery in the RN cohort did not portend
greater
overall mortality. Since the European population has a lower level of
comorbidities in comparison to an American population, this study was
more accurately evaluating the impact of surgical CKD (CKD-S). Perhaps,
with regards to overall survival, CKD-S caused by nephrectomy might not
be as deleterious as medical CKD (CKD-M).
Defining surgical versus medical chronic kidney
disease
Traditionally, literature on CKD has
focused on medical CKD-M, which affects over 19 million Americans (37). This type of CKD stems from microscopic
damage at the level of nephrons, either from hypertension, diabetes, or other
medical causes. CKD-M increases the risk of death, mainly from adverse
cardiovascular events (38). In
addition, CKD has been associated with coagulopathies, anemia, left ventricular
hypertrophy, arterial calcification, and other pathophysiology (39-43). Most
importantly, CKD places patients at risk for ESRD and its accompanying high
rate of mortality, morbidity, and cost to the healthcare system (44).
Only the urological and transplant
literature distinguish surgical CKD-S from medical causes of renal
dysfunction. CKD-S as defined by Lane et al is when patients develop chronic
renal insufficiency after nephrectomy without an underlying medical cause for
their renal disease (45). Because
patients who present with a renal mass tend to be elderly with multiple
comorbidities, many develop a mixed picture of CKD-M and CKD-S after
extirpative renal surgery (46). This was
confirmed by the landmark study from Memorial Sloan Kettering Cancer Center
discussed above (45). Twenty-six percent
of 662 patients with a small solitary tumor had preexisting grade III CKD. Furthermore, in a retrospective study of 4180
patients undergoing nephrectomy of any type, Lane and colleagues showed that
the annual decline in GFR for patients with existing CKD-M who develop CKD-M/S
was 4.7% after surgery (45). On the
other hand, for those without pre-existing CKD who developed CKD-S, the decline
was only 0.7% in GFR. Post-operative GFR was not a significant predictor of
survival after 6.6-year median follow-up for patients with CKD-S but did
predict survival in those with CKD-M/S with worse survival for those with lower
post-operative GFR. This data was
supported by another study from the same group in which CKD-M/S and CKD-S
groups were compared to those with CKD-M who did not undergo surgery. Demirjian and colleagues showed that the
CKD-S group had better overall survival and less of a decline in renal function
(47). This validates that CKD-S is a
separate entity from CKD-M and mixed CKD-M/S. It follows that urological
experience with CKD-S may parallel that of the donor nephrectomy population
analyzed in the transplant literature.
The pathophysiology of surgical CKD and review of
the transplant literature
The hypothesized mechanism for renal
injury after renal transplant in the remaining donor’s kidney is renal
hyperfiltration possibly followed or preceded by renal hypertrophy. Animal models as well as research on human
renal tissue show that after nephron loss there is a concomitant increase in
the GFR of the remaining kidney (48, 49). It is hypothesized that given the
decline in the number of nephrons, the remaining kidney tissue hypertrophies leading
to increased renal volume due to the increase of renal plasma flow and increased
intraglomerular pressure (50).
Eventually the nephrons become unable to compensate with the increased
load leading to nephron exhaustion (51). Brenner and colleagues propose that
this increased hyperfiltration and the decrease in nephron number may explain
why some patients develop renal injury, hypertension, proteinuria and other
kidney related diseases (52).
However, since not all patients develop
this adverse pathology or a significant GFR decline after surgery, there must
be a further explanation. There may be a threshold below which a kidney can
tolerate further strain— that is a nephron reserve defined by the nephron
surface area and mass (53). Once this
reserve is overwhelmed, perhaps damage becomes unmanageable with ensuing kidney
function decline. The evidence for this theory largely stems from animal
studies, retrospective papers, and one prospective study. Brenner et al in a rat model showed that after
thermal renal ablation of a renal mass the remaining nephrons experience
hypertrophy on pathology (54). From this
experiment, it was hypothesized that the increase in GFR with concomitant low
nephron reserve leads to increased intraglomerular hypertension and eventually
albuminuria and kidney function decline in humans also (55). This increase in GFR measured by higher than
normal rates has been shown to occur in patients with unilateral renal
agenesis, congenitally reduced nephron numbers, and acquired reduction in renal
mass (56-58). Elsherbiny and colleagues
suggest that increased renal plasma flow may induce renal damage that
eventually leads to glomerulosclerosis, GFR decline, and hypertension (59). Their study looked at nephron size using
biopsies obtained from donor kidneys during transplantation and showed that
indeed some of these predicted structural characteristics of hyperfiltration
are seen in humans pre-operatively in patients with high GFR at time of their
biopsy. Moreover, larger glomerular
volume, increased mean profile tubular area, and lower glomerular density were
all associated with risk factors for CKD (59).
To be a kidney donor, stringent
criteria must be met including having a high baseline GFR and minimal to no
comorbidities. The transplant literature
has analyzed survival in these patients who have donated their kidney. This population may most accurately reflect
CKD-S. In a large cross-sectional study among older kidney donors,
Fehrman-Ekholm et al showed that 10% developed proteinuria and half of the male
donors developed hypertension (60). Both
of these results are higher than expected in the general non-donor
population. Overall, 72% of the group
had a decline in their average estimated GFR based on their age. Out of 402 donors who lived to follow up,
only 5 patients developed a GFR of less than 30 and 1 patient ultimately
required dialysis. Ibrahim and colleagues evaluated the incidence of ESRD after
unilateral donor nephrectomy and found that 14.5% of their cohort developed CKD
with a GFR of less than 60 ml/min/ 1.73m2 at most recent follow
up. They also noted a higher than
expected incidence of hypertension and albuminuria, but overall survival did
not differ between kidney donors and matched non-donors (61). This further suggests that surgically induced
reductions in GFR may not affect patient survival, unlike medically induced
declines. In addition, this data may
elucidate why the EORTC 30904 failed to show a survival benefit for
PN despite the increased CKD in the RN cohort.
Future directions
Other than renal biopsy, there is
currently no mechanism that predicts what the pathology of a renal mass will
be. Both advances in imaging and
development of biomarkers that can be correlated with histology are necessary
to help differentiate renal masses. This would prevent the surgical removal of
a substantial number of tumors that are actually benign or of low malignant
potential. It could also guide in selecting the appropriate management strategy
based on tumor risk profile along with patient characteristics. Improving our
assessment of kidney function beyond GFR would also assist in more aptly risk
stratifying patients.
Furthermore, research should be
dedicated to resolving the question of whether RN is superior to PN in terms of
overall survival in a more heterogeneous population. Ideally, another randomized controlled trial should be completed. Along these lines,
further evaluation of the alternative nephron-sparing techniques and their
oncological as well as renal functional impact is necessary. Studies with longer-term follow up are needed
for thermal ablation and active surveillance.
Finally, a better grasp of the pathophysiology
of surgically induced chronic kidney disease is warranted. Further understanding of the mixed state of
medically and surgically induced CKD in the aging population is also necessary. While surgically induced CKD seems to be a
separate entity with different mortality rates, the literature currently makes
little or no distinction.
Conclusions
In patients with small renal masses, a
solitary kidney, multiple comorbidities, or those with multiple tumors,
nephron-sparing surgery, mainly partial nephrectomy, is considered standard of
care. Thermal ablative treatments have
materialized as alternative nephron-sparing therapies for patients with
localized small renal masses. These therapies have been associated with higher
recurrence rates and have unknown long-term oncological outcomes. Therefore, of
the nephron-sparing treatments, we would argue that partial nephrectomy
optimizes oncological control while protecting renal function.
Nonetheless, a large randomized
controlled trial comparing radical and partial nephrectomy failed to show a
survival benefit of nephron sparing surgery.
This finding as well as data from the kidney donor population indicates
that surgically induced renal dysfunction may not warrant as much concern or
vigilance as medically induced renal disease. Further investigation and
randomized trials are warranted to help elucidate the benefits of PN in
comparison to RN as well to explore the pathophysiology and impact of medically
versus surgically induced chronic kidney disease.
Acknowledgments
Danny Lascano was funded by a National
Institutes of Health- National Institute of Diabetes and Digestive and Kidney
diseases (NIH-NIDDK) T35 grant. (Grant: 5T35DK93430-3).
Conflicts of interest
The authors declare that they have no
competing interests.
References
1. Das CJ, Ahmad Z, Sharma S, Gupta AK.
Multimodality imaging of renal inflammatory lesions. World J Radiol.
2014;6(11):865-73. Doi:
http://dx.doi.org/10.4329/wjr.v6.i11.865
2. Frank I, Blute ML, Cheville JC,
Lohse CM, Weaver AL, Zincke H. Solid renal tumors: an analysis of pathological
features related to tumor size. J Urol. 2003;170(6 Pt 1):2217-20. Doi: http://dx.doi.org/10.1097/01.ju.0000095475.12515.5e
3. SEER Cancer Statistics Review (CSR)
1975-2011.
4. Konnak JW, Grossman HB. Renal-Cell
Carcinoma as an Incidental Finding. J Urol. 1985;134(6):1094-6. [PMid:4057398]
5. Nguyen MM, Gill IS, Ellison LM. The
evolving presentation of renal carcinoma in the United States: trends from the
Surveillance, Epidemiology, and End Results program. J Urol. 2006;176(6 Pt
1):2397-400. Doi:
http://dx.doi.org/10.1016/j.juro.2006.07.144
6. Silver DA, Morash C, Brenner P,
Campbell S, Russo P. Pathologic findings at the time of nephrectomy for renal
mass. Ann Surg Oncol. 1997;4(7):570-4. Doi: http://dx.doi.org/10.1007/BF02305538
7. Yaycioglu O, Rutman MP,
Balasubramaniam M, Peters KM, Gonzalez JA. Clinical and pathologic tumor size
in renal cell carcinoma; difference, correlation, and analysis of the
influencing factors. Urology. 2002;60(1):33-8. Doi:
http://dx.doi.org/10.1016/S0090-4295(02)01668-0
8. Simmons MN, Fergany AF, Campbell SC.
Effect of Parenchymal Volume Preservation on Kidney Function After Partial
Nephrectomy. J Urol. 2011;186(2):405-10. doi: 10.1016/j.juro.2011.03.154. Epub
2011 Jun 15. Doi:
http://dx.doi.org/10.1016/j.juro.2011.03.154
9. Levey AS, Eckardt KU, Tsukamoto Y,
Levin A, Coresh J, Rossert J, De Zeeuw D, Hostetter TH, Lameire N, Eknoyan G.
Definition and classification of chronic kidney disease: a position statement
from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int.
2005;67(6):2089-100. Doi:
http://dx.doi.org/10.1111/j.1523-1755.2005.00365.x
10. Robson CJ. Radical Nephrectomy for
Renal Cell Carcinoma. J Urol. 1963 Jan;89:37-42. [PMid:13974490]
11. Russo P. Oncological and renal
medical importance of kidney-sparing surgery. Nat Rev Urol. 2013;10(5):292-9.
doi: 10.1038/nrurol.2013.34. Doi:
http://dx.doi.org/10.1038/nrurol.2013.34
12. Russo P, Goetzl M, Simmons R, Katz
J, Motzer R, Reuter V. Partial nephrectomy: the rationale for expanding the
indications. Ann Surg Oncol. 2002;9(7):680-7. Doi: http://dx.doi.org/10.1007/BF02574485
13. Gill IS et al. Comparison of 1,800
laparoscopic and open partial nephrectomies for single renal tumors. J Urol.
2007;178(1):41-6. Doi: http://dx.doi.org/10.1016/j.juro.2007.03.038
14. Benway BM, Bhayani SB, Rogers CG,
Dulabon LM, Patel MN, Lipkin M, Wang AJ, Stifelman MD. Robot assisted partial
nephrectomy versus laparoscopic partial nephrectomy for renal tumors: a
multi-institutional analysis of perioperative outcomes. J Urol.
2009;182(3):866-72. doi: 10.1016/j.juro.2009.05.037. Doi:
http://dx.doi.org/10.1016/j.juro.2009.05.037
15. Long JA, Yakoubi R, Lee B,
Guillotreau J, Autorino R, Laydner H, Eyraud R, Stein RJ, Kaouk JH, Haber GP.
Robotic versus laparoscopic partial nephrectomy for complex tumors: comparison
of perioperative outcomes. Eur Urol. 2012;61(6):1257-62. doi:
10.1016/j.eururo.2012.03.012. Doi:
http://dx.doi.org/10.1016/j.eururo.2012.03.012
16. Kunkle DA, Uzzo RG. Cryoablation or
radiofrequency ablation of the small renal mass : a meta-analysis. Cancer. 2008
Nov 15;113(10):2671-80. Doi:
http://dx.doi.org/10.1002/cncr.23896
17. Nguyen CT, Lane BR, Kaouk JH,
Hegarty N, Gill IS, Novick AC, Campbell SC. Surgical salvage of renal cell
carcinoma recurrence after thermal ablative therapy. J Urol. 2008
;180(1):104-9. doi: 10.1016/j.juro.2008.03.046. Doi: http://dx.doi.org/10.1016/j.juro.2008.03.046 18. Bhan SN, Pautler SE, Shayegan B,
Voss MD, Goeree RA, You JJ. Active surveillance, radiofrequency ablation, or
cryoablation for the nonsurgical management of a small renal mass: a
cost-utility analysis. Ann Surg Oncol. 2013;20(11):3675-84. doi:
10.1245/s10434-013-3028-0. Doi: http://dx.doi.org/10.1245/s10434-013-3028-0
19. Bosniak MA, Krinsky GA, Waisman J.
Management of small incidental renal parenchymal tumours by watchful waiting in
selected patients based on observation of tumour growth rates. J Urol, suppl.
1996;155:584A abstract.
20. Crispen PL, Soljic A, Stewart G,
Kutikov A, Davenport D, Uzzo RG. Enhancing Renal Tumors in Patients with Prior
Normal Abdominal Imaging: Further Insight into the Natural History of Renal
Cell Carcinoma. J Urol. 2012;188(4):1089-93. doi: 10.1016/j.juro.2012.06.019. Doi:
http://dx.doi.org/10.1016/j.juro.2012.06.019
21. Jewett MA et al. Active
surveillance of small renal masses: progression patterns of early stage kidney
cancer. Eur Urol. 2011 Dec;60(6):1258-65. Doi: http://dx.doi.org/10.1016/j.eururo.2011.05.049
22. Hollingsworth JM, Miller DC,
Daignault S, Hollenbeck BK. Five-year survival after surgical treatment for
kidney cancer - A population-based competing risk analysis. Cancer.
2007;109(9):1763-8. Doi:
http://dx.doi.org/10.1002/cncr.22600
23. Woldu SL et al. Comparison of Renal
Parenchymal Volume Preservation Between Partial Nephrectomy, Cryoablation, and
Radiofrequency Ablation. J Endourol. 2015. [Epub ahead of print]. Doi: http://dx.doi.org/10.1089/end.2014.0866
24. Lucas, S. M., Stern, J. M., Adibi,
M. et al.: Renal function outcomes in patients treated for renal masses smaller
than 4 cm by ablative and extirpative techniques. J Urol, 179: 75, 2008 Doi: http://dx.doi.org/10.1016/j.juro.2007.08.156
25. Aron M, Kamoi K, Remer E, Berger A,
Desai M, Gill I. Laparoscopic Renal Cryoablation: 8-Year, Single Surgeon
Outcomes. J Urol. 2010;183(3):889-95. Doi: http://dx.doi.org/10.1016/j.juro.2009.11.041
26. Castaneda CV, Danzig MR,
Finkelstein JB, RoyChoudhury A, Wagner AA, Chang P, Pierorazio PM, Allaf ME,
McKiernan JM. The natural history of renal functional decline in patients
undergoing surveillance in the DISSRM registry. Urol Oncol. 2015 Jan 16. pii:
S1078-1439(14)00437-2. Doi: http://dx.doi.org/10.1016/j.urolonc.2014.11.016
27. McKiernan J1, Simmons R, Katz J,
Russo P. Natural history of chronic renal insufficiency after partial and
radical nephrectomy. Urology. 2002;59(6):816-20. Doi: http://dx.doi.org/10.1016/S0090-4295(02)01501-7
28. Huang WC, Levey AS, Serio AM,
Snyder M, Vickers AJ, Raj GV, Scardino PT, Russo P. Chronic kidney disease
after nephrectomy in patients with renal cortical tumours: A retrospective
cohort study. Lancet Oncol. 2006;7(9):735-40. Doi: http://dx.doi.org/10.1016/S1470-2045(06)70803-8
29. Donin NM, Suh LK, Barlow L, Hruby
GW, Newhouse J, McKiernan J. Tumour diameter and decreased preoperative
estimated glomerular filtration rate are independently correlated in patients
with renal cell carcinoma. BJU Int. 2012;109(3):379-83. Doi:
http://dx.doi.org/10.1111/j.1464-410X.2011.10331.x
30. Ohno Y, Nakashima J, Ohori M,
Hashimoto T, Iseki R, Hatano T, Tachibana M. Impact of Tumor Size on Renal
Function and Prediction of Renal Insufficiency After Radical Nephrectomy in
Patients With Renal Cell Carcinoma. J Urol. 2011 Oct;186(4):1242-6. Doi:
http://dx.doi.org/10.1016/j.juro.2011.05.087
31. Laguna MP. Re: Overall Survival and
Development of Stage IV Chronic Kidney Disease in Patients Undergoing Partial
and Radical Nephrectomy for Benign Renal Tumors Editorial Comment. J Urol.
2014;191(6):1729-30.Doi: http://dx.doi.org/10.1016/j.juro.2014.03.051
32. Chung JS et al. Trends in renal
function after radical nephrectomy: a multicentre analysis. BJU Int. 2014;113(3):408-15. Doi: http://dx.doi.org/10.1111/bju.12277
33. Simmons MN1, Lieser GC, Fergany AF,
Kaouk J, Campbell SC. Association Between Warm Ischemia Time and Renal
Parenchymal Atrophy After Partial Nephrectomy. J Urol. 2013;189(5):1638-42. Doi: http://dx.doi.org/10.1016/j.juro.2012.11.042
34. Liu W, Li Y, Chen M, Gu L, Tong S,
Lei Y, Qi L. Off-clamp versus complete hilar control partial nephrectomy for
renal cell carcinoma: a systematic review and meta-analysis. J Endourol.
2014;28(5):567-76.. Doi: http://dx.doi.org/10.1089/end.2013.0562
35. Van Poppel H et al. A Prospective,
Randomised EORTC Intergroup Phase 3 Study Comparing the Oncologic Outcome of
Elective Nephron-Sparing Surgery and Radical Nephrectomy for Low-Stage Renal
Cell Carcinoma. Eur Urol. 2011;59(4):543-52. Doi: http://dx.doi.org/10.1016/j.eururo.2010.12.013
36. Scosyrev E, Messing EM, Sylvester
R, Campbell S, Van Poppel H. Renal function after nephron-sparing surgery
versus radical nephrectomy: results from EORTC randomized trial 30904. Eur
Urol. 2014;65(2):372-7. Doi: http://dx.doi.org/10.1016/j.eururo.2013.06.044
37. Coresh J, Astor BC, Greene T,
Eknoyan G, Levey AS. Prevalence of chronic kidney disease and decreased kidney
function in the adult US population: Third National Health and Nutrition
Examination Survey. Am J Kidney Dis. 2003;41(1):1-12. Doi: http://dx.doi.org/10.1053/ajkd.2003.50007
38. Go AS, Chertow GM, Fan D, McCulloch
CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular
events, and hospitalization. N Engl J Med. 2004;351(13):1296-305. Doi: http://dx.doi.org/10.1056/NEJMoa041031
39. Muntner P, Hamm LL, Kusek JW, Chen
J, Whelton PK, He J. The prevalence of nontraditional risk factors for coronary
heart disease in patients with chronic kidney disease. Ann Intern Med.
2004;140(1):9-17. Doi: http://dx.doi.org/10.7326/0003-4819-140-1-200401060-00006
40. Shlipak MG, Fried LF, Crump C,
Bleyer AJ, Manolio TA, Tracy RP, Furberg CD, Psaty BM. Elevations of
inflammatory and procoagulant biomarkers in elderly persons with renal insufficiency.
Circulation. 2003 Jan 7;107(1):87-92. Doi: http://dx.doi.org/10.1161/01.CIR.0000042700.48769.59
41. Hsu CY, McCulloch CE, Curhan GC.
Epidemiology of anemia associated with chronic renal insufficiency among adults
in the United States: Results from the Third National Health and Nutrition
Examination Survey. J Am Soc Nephrol. 2002 Feb;13(2):504-10. [PMid:11805181]
42. Raggi P1, Boulay A, Chasan-Taber S,
Amin N, Dillon M, Burke SK, Chertow GM. Cardiac calcification in adult
Hemodialysis patients - A link between end-stage renal disease and
cardiovascular disease? J Am Coll Cardiol. 2002;39(4):695-701. Doi: http://dx.doi.org/10.1016/S0735-1097(01)01781-8
43. Levin A et al. Left ventricular
mass index increase in early renal disease: Impact of decline in hemoglobin. Am
J Kidney Dis. 1999;34(1):125-34. Doi:
http://dx.doi.org/10.1016/S0272-6386(99)70118-6
44. Foley RN, Parfrey PS, Sarnak MJ.
Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J
Kidney Dis. 1998;32(5 Suppl 3):S112-9. Doi: http://dx.doi.org/10.1053/ajkd.1998.v32.pm9820470
45. Lane BR, Campbell SC, Demirjian S,
Fergany AF. Surgically induced chronic kidney disease may be associated with a
lower risk of progression and mortality than medical chronic kidney disease. J
Urol. 2013;189(5):1649-55. doi: 10.1016/j.juro.2012.11.121. Doi: http://dx.doi.org/10.1016/j.juro.2012.11.121
46. Russo P, Huang W. The Medical and
Oncological Rationale for Partial Nephrectomy for the Treatment of T1 Renal
Cortical Tumors. Urol Clin North Am. 2008;35(4):635-43. Doi: http://dx.doi.org/10.1016/j.ucl.2008.07.008
47. Demirjian S, Lane BR, Derweesh IH,
Takagi T, Fergany A, Campbell SC. Chronic kidney disease due to surgical
removal of nephrons: relative rates of progression and survival. J Urol.
2014;192(4):1057-62. Doi:http://dx.doi.org/10.1016/j.juro.2014.04.016
48. Finn WF. Compensatory renal
hypertrophy in Sprague-Dawley rats: glomerular ultrafiltration dynamics. Ren
Physiol. 1982;5(5):222-34. [PMid:7134623]
49. Hostetter TH. Progression of renal
disease and renal hypertrophy. Annu Rev Physiol. 1995;57:263-78. Doi: http://dx.doi.org/10.1146/annurev.ph.57.030195.001403
50. Jeon HG, Lee SR, Joo DJ, Oh YT, Kim
MS, Kim YS, Yang SC, Han WK. Predictors of kidney volume change and delayed
kidney function recovery after donor nephrectomy. J Urol. 2010;184(3):1057-63. Doi: http://dx.doi.org/10.1016/j.juro.2010.04.079
51. Terasaki PI, Koyama H, Cecka JM,
Gjertson DW. The hyperfiltration hypothesis in human renal transplantation.
Transplantation. 1994;57(10):1450-4.
Doi: http://dx.doi.org/10.1097/00007890-199405000-00008
52. Brenner BM, Garcia DL, Anderson S.
Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens.
1988;1(4 Pt 1):335-47. Doi:http://dx.doi.org/10.1093/ajh/1.4.335
53. Luyckx VA, Brenner BM. The Clinical
Importance of Nephron Mass. J Am Soc Nephrol. 2010;21(6):898-910. Doi: http://dx.doi.org/10.1681/ASN.2009121248
54. Hostetter TH, Olson JL, Rennke HG,
Venkatachalam MA, Brenner BM. Hyperfiltration in remnant nephrons: a
potentially adverse response to renal ablation. Am J Physiol. 1981
Jul;241(1):F85-93.
[PMid:7246778]
55. Palatini P. Glomerular
hyperfiltration: a marker of early renal damage in pre-diabetes and
pre-hypertension. Nephrol Dial Transplant. 2012;27(5):1708-14. Doi:
http://dx.doi.org/10.1093/ndt/gfs037
56. Rugiu C et al. Clinical-Features of
Patients with Solitary Kidneys. Nephron. 1986;43(1):10-5. Doi: http://dx.doi.org/10.1159/000183710
57. Brenner BM, Chertow GM. Congenital
Oligonephropathy and the Etiology of Adult Hypertension and Progressive Renal
Injury. Am J Kidney Dis. 1994;23(2):171-5. Doi:
http://dx.doi.org/10.1016/S0272-6386(12)80967-X
58. Solomon LR, Mallick NP, Lawler W.
Progressive Renal-Failure in a Remnant Kidney. Br Med J (Clin Res Ed).
1985;291(6509):1610-1. Doi:
http://dx.doi.org/10.1136/bmj.291.6509.1610
59. Elsherbiny, H. E., Alexander, M.
P., Kremers, W. K. et al.: Nephron Hypertrophy and Glomerulosclerosis and Their
Association with Kidney Function and Risk Factors among Living Kidney Donors.
Clinical Journal of the American Society of Nephrology, 9: 1892, 2014. Doi: http://dx.doi.org/10.2215/CJN.02560314
60. Fehrman-Ekholm I, Duner F, Brink B,
Tyden G, Elinder CG. No evidence of accelerated loss of kidney function in
living kidney donors: Results from a cross-sectional follow-up. Transplantation.
2001;72(3):444-9. Doi: http://dx.doi.org/10.1097/00007890-200108150-00015
61. Ibrahim HN, Foley R, Tan L, Rogers
T, Bailey RF, Guo H, Gross CR, Matas AJ. Long-Term Consequences of Kidney
Donation. N Engl J Med. 2009;360(5):459-69. doi: 10.1056/NEJMoa0804883. Doi:
http://dx.doi.org/10.1056/NEJMoa0804883
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