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G e n i t o u r i n a r y I m a g i n g • R ev i ew

Ng et al.
Diagnosis and Staging of Renal Cell Carcinoma

Genitourinary Imaging
Review

Renal Cell Carcinoma: Diagnosis,


Staging, and Surveillance
Chaan S. Ng1 OBJECTIVE. This educational review focuses on the staging and radiologic evaluation of
Christopher G. Wood2 renal cell carcinoma. It includes discussion of the epidemiology, pathology, and therapeutic
Paul M. Silverman1 options of renal cell carcinoma and the implications for radiologic follow-up.
Nizar M. Tannir 3 CONCLUSION. The incidence of renal cell carinoma has been increasing. Imaging
Pheroze Tamboli 4 plays a central role in its detection, staging, and treatment evaluation and follow-up.
Carl M. Sandler 1

R
American Journal of Roentgenology 2008.191:1220-1232.

enal cell carcinoma (RCC), the laparoscopic and nephron-sparing approach-


Ng CS, Wood CG, Silverman PM, Tannir NM, eighth most common malignan- es. MDCT has been a major advance, provid-
Tamboli P, Sandler CM cy affecting adults, accounts for ing angiographic and 3D imaging essential
between 3% and 4% of new can- for presurgical planning.
cer cases in the United States. It is the sev- This article focuses on the epidemiology,
enth most common cancer in men and the pathology, staging, radiologic evaluation,
ninth most common in women [1]. We now and therapeutic options of RCC and the im-
know that RCC actually represents a family plications for radiologic follow-up.
of related disorders with distinct cytogenetic
and immunohistochemical properties that Epidemiology
Keywords: imaging, renal cell carcinoma, staging have differing prognoses, imaging character- There were an estimated 51,190 new cases
istics, and potential morbidities. of, and 12,890 deaths from, renal cancer in
DOI:10.2214/AJR.07.3568
The classic clinical presentation of flank 2007 in the United States, accounting for
Received December 20, 2007; accepted after revision pain, hematuria, and a palpable flank mass is 2.3% of all cancer deaths in the United States
April 10, 2008. comparatively uncommon (5–10% of cases). [1]. The incidence has steadily increased
However, clinical symptomatology may be during the past 50 years in the United States
C. G. Wood is a consultant for Pfizer, Inc.; Antigenics, quite nonspecific—for example, anorexia, tired­ and has occurred in 9.1/100,000 population
Inc.; Bristol-Myers Squibb; Ethicon, Inc.; and Bayer
Healthcare.
­ness, weight loss, or fever of unknown origin in 1997, with a mortality rate of 3.5/100,000
[2]. Other presentations include varicocele for- [5–7]. Reported worldwide incidence rates
1
Department of Radiology, Box 368, The University of mation (from tumor thrombus in the left renal range from 0.6/100,000 to 14.7/100,000 [8].
Texas M. D. Anderson Cancer Center, 1515 Holcombe vein or the inferior vena cava [IVC]) and dis- Most tumors present in the fifth to seventh
Blvd., Houston, TX 77030-4009. Address correspon-
seminated malignancy. RCC may also present decade of life, with a median age at diagnosis
dence to C. S. Ng (cng@mdanderson.org).
with a variety of paraneoplastic syndromes, of 66 years and median age at death of 70
2 such as polycythemia secondary to excessive years. The incidence is two to three times
Department of Urology, The University of Texas M. D.
Anderson Cancer Center, Houston, TX. secretion of erythropoietin, hypercalcemia higher in men and is slightly more common
3
secondary to factors regulating calcium, and in blacks than in whites [5]. The incidence of
Department of Medical Oncology, The University of
Texas M. D. Anderson Cancer Center, Houston, TX.
hepatic dysfunction (Stauffer syndrome). Inci- renal tumors at autopsy is approximately 2%
dentally detected tumors in asymptomatic indi- [9]. The tumors are usually solitary but may
4
Department of Pathology, The University of Texas M. D. viduals have been steadily increasing with the be multifocal (6–25%), with bilateral RCC
Anderson Cancer Center, Houston, TX. dissemination of imaging techniques, including occurring sometime in the course of life in
CME
CT, MR, and sonography, accounting for ap- 4% of patients [10].
The article is available for CME credit. proximately 60% of renal tumors in the 1990s, Certain genetic conditions are associated
See www.arrs.org for more information. compared with approximately 10% in the early with an increased incidence of RCC, including
1970s [3, 4]. von Hippel-Lindau disease, hereditary papillary
AJR 2008; 191:1220–1232
Besides identifying these incidental le- renal cancer, and, possibly, tuberous sclerosis
0361–803X/08/1914–1220 sions, diagnostic imaging plays an increasing [11]. RCC occurs in von Hippel-Lindau disease
role in this disease, particularly in the con- in 35–40% of patients, occurs at a younger age,
© American Roentgen Ray Society text of newer surgical approaches such as and is frequently bilateral (75%) or multifocal

1220 AJR:191, October 2008


Diagnosis and Staging of Renal Cell Carcinoma

(87%) [12]. RCC is also more common in ac- in the absence of metastases exceeding 50%; atic cases. Although data are not available,
quired cystic renal disease. Long-term dialy- in the presence of distant metastases, the this may very well increase in the new era in
sis carries a three- to sixfold increased risk 5-year survival rate decreases to 10% (with a which tumors are being detected incidentally
compared with the normal population. He- 10-year survival rate of < 5%). at an earlier stage and smaller size. Evidence
reditary papillary RCC is an autosomal dom- The possible factors that have contributed suggests, although not conclusively, that
inant form of the disease that is associated to improved survival include advances in re- asymp­tomatic tumors are smaller and of
with multifocal papillary renal tumors. The nal imaging and surgical techniques, stage lower grade and earlier stage [3, 7].
disease has a 5:1 male predominance. Other migration to smaller and lower-stage disease
suggested risk factors include cigarette as a result of earlier diagnosis in asymptom- Pathology
smoking; obesity; diuretic use; exposure to atic individuals, and the introduction of im- RCC (hypernephroma or Grawitz’s tumor)
petroleum products, chlorinated solvents, munotherapy for advanced disease. Tumor is the most common tumor to affect the adult
cadmium, lead, asbestos, and ionizing radia- size has been found to be an independent kidney, accounting for 80–90% of primary
tion; high-protein diets; hypertension; kid- predictor of outcome, with larger tumors malignant renal neoplasms in adults.
ney transplantation; and HIV infection [5, having a poorer survival; for example, 5- and On gross pathology, tumors most often ap-
10, 13–15]. 10-year disease-free survivals after surgery pear encapsulated. Tumors may be solid, cys-
for T1, T2, T3a, T3b, and T3c tumors are ap- tic, or mixed, including or engulfing fat and
Survival Statistics proximately 95% and 91%, 80% and 70%, calcification [17]. As many as 10% of tumors
Despite the increasing incidence of the 66% and 53%, 52% and 43%, and 43% and have some cystic component [18], and such
disease in recent decades, survival has 42%, respectively [16]. tumors may be more aggressive [19].
steadily improved, with a current overall Regarding the potential contribution from Histologic subtypes according to the Heidel-
5-year survival of approximately 62% [7]. incidentally detected tumors, the overall berg classification [20] include clear cell (“con-
American Journal of Roentgenology 2008.191:1220-1232.

Prognosis is influenced by the extent of dis- 5-year survival rate is approximately 85% for ventional”) adenocarcinoma (80%), papillary
ease at diagnosis, with a 5-year survival rate such cases, compared with 53% in symptom- (15%), chromophobe (5%), collecting duct
(1%), and unclassified (4%) [21, 22]. Each of
these subtypes has differing cytogenetic and
immunohistochemical profiles as well as dif-
fering prognoses. Histopathologic grading of
the nuclei of the tumor is made by dividing
them into the four-tier Fuhrman nuclear clas-
sification [23], with grade I being the best-dif-
ferentiated and grade IV the most anaplastic.
Clear cell carcinoma displays large uniform
cells with abundant clear cytoplasm rich in gly-
cogen and lipid (Fig. 1A). Clear cell carcinoma
is typically highly vascular. Papillary tumors are
subdivided into type I tumors (Fig. 1B), which
A B occur sporadically and metastasize somewhat
later, and type II (Fig. 1C), which are more likely
inherited, may be multiple, and often present
with a higher Fuhrman grade and poorer prog-
nosis. Collecting duct tumors, which arise from
the medullary collecting duct, often occur in
younger patients and are associated with a poor
overall prognosis. Renal medullary carcinoma is
a rare subtype, closely related to collecting duct
carcinoma and having a poor prognosis, which
occurs in young patients with sickle cell anemia
or sickle trait. Chromophobe tumors and onco-
cytomas, both of which arise from collecting
C D duct epithelium, may be confused on histologic
Fig. 1—Histopathologic slides of renal cell carcinoma (RCC). (H and E) examination but have differing immunohis-
A, Conventional clear cell RCC. Tumor shows large uniform cells with abundant cytoplasm that is rich in tochemical profiles (Fig. 1D). Chromophobe
glycogen.
B, Papillary RCC type I. Tumor papillae are lined by short cuboidal cells with basophilic cytoplasm. Nuclei are
tumors have the best overall prognosis, and on-
small with few inconspicuous nucleoli. Collection of foamy histiocytes is present in middle of lower half of cocytomas are benign.
image. The tumor can extend directly into the
C, Papillary RCC type II. Tumor shows papillae lined by columnar to pseudostratified cells that have striking perinephric fat, ipsilateral adrenal gland, or
eosinophilic cytoplasm.
D, Chromophobe RCC. Note sheet of tumor cells with focal necrosis (upper left corner). Tumor cells have adjacent musculature, and, less frequently,
abundant pale flocculent cytoplasm, prominent cell membranes, perinuclear halos, and wrinkled nuclei. the liver, spleen, pancreas, and colon. Rarely,

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Ng et al.

A B C
American Journal of Roentgenology 2008.191:1220-1232.

D E F
Fig. 2—Schematic diagrams of TNM staging of renal cell carcinoma. (© 2008 The University of Texas M. D. Anderson Cancer Center)
A, Stage T1 tumor < 7 cm.
B, Stage T2 tumor > 7 cm.
C and D, Stage T3a tumors involving perinephric fat (C) and adjacent adrenal gland (D).
E, Stage T3b tumor involving renal vein or inferior vena cava (IVC) inferior to diaphragm.
F, Stage T3c tumor involves IVC superior to diaphragm.

the tumor may invade the renal collecting sion of the 2002 TNM staging of the Ameri- year survival rates by TNM stage are shown
system. RCC has a propensity for extending, can Joint Committee on Cancer (AJCC) and in Table 3. The prognosis is noticeably ad-
as tumor thrombus, into the tributaries of the the International Union Against Cancer versely affected by spread of the tumor be-
renal veins and subsequently to the main re- (UICC) is presented in Tables 1 and 2 [24]. yond the renal fascia and into the retroperi-
nal vein, the IVC, the hepatic veins, and po- In light of the increasing trend for the dis- toneum (TNM T3a and higher). The natural
tentially the right atrium. Hematogenous covery of very small tumors as incidental history of the disease, however, is often un-
metastases are more common and occur ear- findings on imaging studies performed for predictable, and there are wide ranges in
lier than lymphatic dissemination, the former other purposes, revisions to this 1997 version survival. There are reports, albeit rare (<
most commonly to the lungs and bone, but have been proposed, including subclassifica- 1:600), of stabilization or even spontaneous
essentially to any organ, including the subcu- tion of T1 into T1a < 2.5 cm; T1b, 2.5–4.0 remissions in the face of metastatic disease
taneous tissues and skeletal muscle. cm; and T1c, 5.0–7.0 cm tumors. The Robson [10, 26].
classification [25] is an alternative staging Crotty et al. [27] reported that 86% of chro-
Staging system no longer used but still referred to in mophobe tumors in their series were Robson
Staging systems are designed to reflect the some of the older literature. stage I at presentation. Beck et al. [28] reported
modes of spread (Fig. 2) and are used to strat- Prognosis is generally reflected in stag- that chromophobe and papillary histology were
ify treatment options and to assess prognoses ing severity, with lower-stage disease being associated with an improved disease-free sur-
and survival characteristics. The current ver- associated with longer survival rates. Five- vival at 5 years compared with patients with

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Diagnosis and Staging of Renal Cell Carcinoma

TABLE 1:  TNM Staging of Renal Cell Carcinoma Twenty-five to 33% of patients have overt
Stage Description metastases at presentation [2, 13, 31]. The
more common sites of metastases as reported
TX Primary tumor cannot be assessed
in stage IV disease (TNM T4 or N1+ M1 dis-
T0 No evidence of primary tumor ease) are the lung (69%), bone (43%), liver
T1 Tumor < 7 cm in greatest dimension, limited to kidney (34%), lymph nodes (22%), adrenal gland
  T1a Tumor < 4 cm in greatest dimension, limited to kidney (19%), brain (7%), and thyroid, skin, and blad-
der (< 1% each) [32]. Rarer sites include skel-
  T1b Tumor > 4 cm but < 7 cm in greatest dimension, limited to kidney
etal muscle, bowel, gallbladder, pancreas, and
T2 Tumor ≥ 7 cm in greatest dimension, limited to kidney orbits [10, 13, 33]. Large tumors tend to be as-
T3 Tumor extends into major veins or invades adrenal gland or perinephric tissues, but not beyond sociated with more advanced dissemination.
Gerota’s fascia
  T3a Tumor invades adrenal gland or perinephric tissues but not beyond Gerota’s fascia Radiologic Evaluation
  T3b Tumor grossly extends into renal vein(s) or vena cava below diaphragm
The goals of radiologic imaging are to
detect and stage the primary tumor. In most
  T3c Tumor grossly extends into vena cava above diaphragm institutions, CT is the main imaging tech-
T4 Tumor invades beyond Gerota’s fascia nique for the evaluation of the intra-
NX Regional lymph nodes cannot be assessed abdominal component of renal tumors. In
some specific instances, such as allergy to
N0 No regional lymph node metastasis
iodinated contrast medium, MRI and sono-
N1 Metastasis in a single regional lymph node graphy can provide complementary infor-
American Journal of Roentgenology 2008.191:1220-1232.

N2 Metastasis in more than one regional lymph node mation. The risks of nephrogenic systemic
MX Distant metastasis cannot be assessed fibrosis (NSF) in patients with significantly
impaired renal function, which is consid-
M0 No distant metastasis
ered to be associated with some gadolini-
M1 Distant metastasis um-based MRI contrast agents, should be
Note—Adapted from current version of American Joint Committee on Cancer (2002) [24]. considered carefully when staging with
MRI is deemed advisable [34].
It is generally considered that a risk-adapt-
clear cell RCC. When controlled for size and that should be included in staging, including ed approach is used for workup of other pos-
stage of tumor, however, chromophobe, but not recognition of RCC tumor variants, sarcomatoid sible sites of metastases. Chest CT should be
papillary, carcinoma offered a significantly im- histology, histopathologic grade, molecular performed if the primary tumor is large or
proved survival. The times from nephrectomy proliferation markers (silver-staining nucleolar locally aggressive because metastases are
to metastasis and from metastasis to death were organizer regions, proliferating cell nuclear more common in these patients [35]. Chest
twice those for patients with chromophobe his- antigen, and Ki-67 antigen), performance sta- radiography without CT should be reserved
tology when compared with those with clear tus, weight loss, hypercalcemia, and erythro- for patients with a low risk of metastatic dis-
cell or papillary subtypes. cyte sedimentation rate [7, 10, 29, 30]. How- ease or for those in long-term follow-up [36,
It has been suggested that there are other ever, current staging does not incorporate 37]. Brain MRI and nuclear medicine bone
potentially important determinants of survival these factors. scanning are generally justified only if there

TABLE 2:  TNM Stage Groupings TABLE 3:  Survival by TNM Stage
Stage T N M Disease Extent TNM Stage 5-Year Survival Rate (%)
Grouping Stage Stage Stage
All organ-confined T1–T2 N0 M0 70–90
I T1 N0 M0
≤ 4 cm T1a N0 M0 90–100
II T2 N0 M0
> 4 but < 7 cm T1b N0 M0 80–90
III T1 N1 M0
≥ 7 cm T2 N0 M0 70–80
T2 N1 M0
Invasion of perinephric fat T3a N0 M0 60–80
T3 N0 M0
Adrenal involvement T3a N0 M0 0–30
T3 N1 M0
Venous involvement T3b–T3c N0 M0 40–65
IV T4 N0 M0
Locally advanced T4 N0 M0 0–20
T4 N1 M0
Lymphatic involvement Any T, N+, M0 0–20
Any T N2 M0
Systemic metastases Any T, any N, M1 0–10
Any T Any N M1
Note—Adapted from current version of American Joint Committee on Cancer (2002) [24].
Note—Adapted from current version of American
Joint Committee on Cancer (2002) [24].

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Ng et al.

A B C

Fig. 3—CT reformations of bilateral renal tumors in


60-year-old woman. Large arrows indicate primary
renal tumor.
A, CT scan shows solid left renal mass (large arrow)
and complex cystic right renal mass (small arrow).
B, Coronal multiplanar reformation (MPR) during
arterial phase shows one left and two right renal
arteries (small arrows).
C, Coronal maximum intensity projection during
arterial phase shows bilateral tumors (large arrows)
American Journal of Roentgenology 2008.191:1220-1232.

and renal arteries (small arrows).


D, Volume-rendered image during arterial phase also
shows renal arteries (small arrows).
E, Coronal MPR during delayed phase shows inferior
vena cava (large thin arrows) and left renal vein
(arrowheads), renal collecting system, aorta, and
renal arteries (small thin arrows).
D E

are symptoms and signs to suggest disease at enable assessment of contrast enhancement, nous supply to the kidney but has limited ad-
these sites or if the tumor is large and locally and assist in characterizing the lesion. IV ditional usefulness for lesion detection and
aggressive, although even the latter is debat- contrast-enhanced images targeted on the characterization when a nephrographic phase
ed [31]. Technetium-99m-methylene diphos- kidneys are obtained in the arterial, late arte- is used. The combination of excretory and
phonate (MDP) bone scanning, however, rial (corticomedullary and portal venous), nephrographic phases has been shown to im-
may be limited in detecting the typical osteo­ nephrographic, and excretory phases at prove lesion detection and staging [42, 43].
lytic bone metastases from RCC. The value 15–30, 45–60, 80–90, and 180 seconds, re- Several investigators have shown that clear
of pelvic CT in staging is also limited [38]. spectively, after commencement of the IV cell RCC enhances to a greater extent and is
infusion. Imaging of the liver and the re- more heterogeneous in appearance than other
CT Evaluation maining abdominal structures is performed histologic subtypes (Figs. 4A and 4B). Kim et
Suggested protocols for preoperative eval- in the portal venous phase. Excretory phase al. [44] showed that an increase in attenuation
uation and follow-up using MDCT are pre- images from the kidneys through the bladder of 84 HU in the corticomedullary phase dif-
sented in the text that follows. In addition to are generally obtained to complete the evalu- ferentiates clear cell RCC from non–clear cell
assessing tumor stage, preoperative evalua- ation of the entire urinary tract when re- tumors with a sensitivity of 74% and a speci-
tion focuses on delineating the tumor with quested by the referring clinician. ficity of 100%. Herts et al. [45] showed that
particular attention to the relationship of the Multiplanar reformatted and 3D volume- papillary tumors were more homogeneous
tumor to adjacent structures, including vas- rendered presentations of the renal phase im- and had a much lower tumor-to-parenchyma
cular relationships. In comparison, follow-up ages are helpful in allowing visualization of enhancement ratio than was present in non-
evaluation is directed toward surveillance for the relationships of structures, particularly for papillary subtypes, particularly with tumors
residual or recurrent disease. In general, surgeons [39–41]. Such reformations are best smaller than 3 cm in diameter (Figs. 4C and
100–150 mL of iodinated IV contrast medi- obtained with the thinnest possible images 4D). Chromophobe tumors also are less hyper­­
um is used at a flow rate of 2–3 mL/s. and some degree of reconstruction interval vascular than clear cell tumors and tend to
overlap (typically, < 1.5-mm interval and have a more peripheral pattern of enhancement;
Preoperative Evaluation 10–50% overlap) and are transferred to a however, their appearance is not sufficiently
For an MDCT protocol, unenhanced im- workstation for creating multiplanar reformat- characteristic to allow them to be reliably dif-
ages of the liver and kidneys are obtained ted images, 3D volume rendering, and maxi- ferentiated from papillary lesions (Figs. 4E
with 5-mm collimation in 5-mm increments. mum-intensity-projection (MIP) images (Figs. and 4F). Oncocytomas cannot be reliably dif-
Unenhanced images of the kidneys allow de- 3A–3D). The late arterial phase provides a ferentiated from RCC by imaging and thus are
tection of calcification or fat in the kidney, useful angiographic image of arterial and ve- also considered to be surgical lesions. The

1224 AJR:191, October 2008


Diagnosis and Staging of Renal Cell Carcinoma

Fig. 4—CT appearances of various cell types of renal


cell carcinoma (RCC).
A and B, Conventional clear cell RCC in 59-year-
old woman. CT scans of TNM stage T1a tumor in
corticomedullary and nephrogenic phases show
typical hypervascularity of tumor (arrow, A) and
subsequent washout (arrow, B).
C and D, Papillary RCC in 48-year-old man. CT scans
of TNM stage T1a tumor in corticomedullary (C) and
nephrogenic (D) phases show typical hypovascularity
of tumor (arrow).
E and F, Chromophobe RCC in 61-year-old man. CT
scans of TNM stage T2 tumor in corticomedullary (E)
and nephrogenic (F) phases show hypovascularity of
A B tumor (arrow).
G, Medullary RCC (large arrow) and adjacent
paraaortic adenopathy (small arrows) in 36-year-old
man. CT shows TNM stage T1b N1 tumor.

MRI Evaluation
MRI is generally only used when optimal
CT cannot be performed, as in the case of a
severe allergy to iodinated contrast medium
or pregnancy. MRI has similar reported
American Journal of Roentgenology 2008.191:1220-1232.

overall staging accuracies to those of CT


[46]. Its multiplanar capability, however, is
C D particularly useful for delineating the supe-
rior extent of tumor in the IVC [2, 14, 17].
We use coronal and axial conventional T1-
weighted (TR/TE, 600/60) and axial dual-echo
fast spin-echo T2-weighted (6,000/first­-echo
TE, 136; second-echo TE, 68) fat-suppressed
images of the abdomen. Images are supple-
mented by dynamic contrast-enhanced 3D fast
spoiled gradient-recalled echo sequences
(FSPGR) to further delineate the primary tumor
and liver lesions and to evaluate any vascular
thrombus identified. In particular, tumor, rather
than bland, thrombus is indicated by the pres-
E F
ence of enhancing vessels in the thrombus.
be suggested when an aggressive tumor in a Multiple dynamic acquisitions can be used to
young patient with sickle cell disease or trait obtain arterial, nephrogenic, and pyelographic-
is encountered. like images [47–50]. MDCT with 3D reforma-
tions and MRI have similar overall staging ac-
Follow-Up Evaluation curacies for RCC [51].
For an MDCT protocol, unenhanced im-
ages of the liver and kidneys are obtained Sonographic Evaluation
with 5-mm collimation in 5-mm increments. Sonography can be useful for assessing
Unenhanced images of the liver assist in the the presence and extent of venous thrombus.
detection of hypervascular metastases (which It can also be helpful in distinguishing cysts
are typical of renal metastases) that might from hypovascular solid tumors seen on CT
G otherwise be obscured on contrast-enhanced (e.g., papillary RCC). Sonography can reveal
images. IV contrast-enhanced images of the the septations better because of complex in-
well-known prominent central scar that can abdomen and pelvis are obtained 70–80 sec- terfaces to the ultrasound beam. Sonography
be used to suggest the diagnosis of oncocyto- onds after the beginning of the IV infusion, has reported accuracies for T staging of
ma may also be present in necrotic clear cell acquired at 5-mm slice thickness, and recon- 77–85% [52, 53] and for detection of venous
tumors. Medullary RCC tumors are located structed at 2.5-mm intervals. Late arterial thrombus of 87% [54]. However, it has limi-
centrally in the kidney and show variable, phase images can assist in identifying hyper- tations in visualizing the retroperitoneum
typically limited, contrast enhancement (Fig. vascular liver metastases. Delayed excretory and perinephric tissues [54, 55], although
4G). They cannot be reliably distinguished phase images are obtained at approximately some proponents argue otherwise [53]. Intra-
from other RCCs or urothelial tumors but may 180 seconds. operative sonography has been effectively

AJR:191, October 2008 1225


Ng et al.

preoperative CT or MR angiograms to be
valuable, particularly when partial nephrec-
tomy or laparoscopic approaches are planned.
Three-dimensional and multiplanar refor-
matted images, as well as angiographic dis-
plays, aid appreciation of the relationships of
the tumor to the collecting system, adjacent
normal parenchyma, and vascular supply
[10, 37, 38, 57].

PET
The efficacy of PET in renal malignancy
Fig. 5—Tumor involvement of perinephric fat in Fig. 6—Metastases to regional lymph node (TNM remains under investigation. It shows some po-
72-year-old woman. CT scan shows tumor with stage N2) in 81-year-old woman. CT scan shows
associated perinephric nodularity (arrow). TNM enlarged left paraaortic node (small arrows) and tential in staging, the detection of unsuspected
stage T3a disease was confirmed on resection adjacent stage T1b papillary renal cell carcinoma metastases, follow-up, and the evaluation of
specimen. (large arrow). indeterminate renal masses [7, 58–61].

used in patients undergoing nephron-sparing considered in selected cases—for example, Recommendations for Preoperative Imaging
surgery to identify multifocal lesions and in- when an abscess or metastatic disease from a Patients must be adequately staged in or-
trarenal tumor anatomy [56, 57]. known primary tumor is suspected, espe- der to plan appropriate management options.
cially from lymphoma or melanoma [10, 17]. Abdominal CT and MRI are the mainstay of
American Journal of Roentgenology 2008.191:1220-1232.

Percutaneous Biopsy Percutaneous biopsy is also generally per- staging the primary tumor and of evaluating
Preoperative percutaneous biopsy of the formed in patients who will undergo ablative the possibility of locoregional nodal or ab-
renal lesion is generally not undertaken be- or thermal therapy to determine the underly- dominal visceral metastases, such as to the
cause the results usually do not affect what ing histologic subtype of the tumor. adrenal glands, liver, pancreas, and contra­
therapy will be recommended except in pa- lateral kidney. Delineation of vascular anato-
tients with multiple tumors or occasionally Angiography my and evaluation of venous thrombosis,
in patients with an underlying predisposing Approximately 20% of patients have mul- best provided by a multiphasic evaluation as
condition. Percutaneous biopsies may be tiple renal arteries, and many surgeons find discussed previously, are helpful when sur-
gery is being contemplated. CT or MRI can
be used, depending on local preferences and
patient factors.
Controversies exist as to whether, and how
best, to evaluate for the possibility of intra­
thoracic metastases. A stage-directed strat­egy
is probably reasonable: For small primary
tumors (T1), in which the risk of metastatic
disease is small, simple chest radiography is
probably satisfactory. For stage T2 or higher
primary tumors, chest CT should probably
be performed. Screening for bone or brain
A metastases is probably re­quired only when
there are suggestive symptoms.

B
Fig. 7—Venous involvement of renal vein and inferior
vena cava (IVC).
A, CT scan in 45-year-old woman shows enhancing
tumor thrombus in expanded left renal vein (large
arrows) (TNM stage T3b) and IVC (small arrow).
B, Thrombus in left renal vein extends to origin of
renal vein at IVC on coronal contrast-enhanced
MR image (arrows) (TNM stage T3b) in 68-year-old
woman. Arrowheads indicate left renal tumor.
C, Thrombus in expanded right renal vein extends
to supradiaphragmatic IVC on coronal contrast-
enhanced MR image (arrows) (TNM stage T3c) in
82-year-old woman. Note aorta and renal artery
origins are also visible (arrowheads).
D, “Salt-and-pepper” appearance of vascularized
tumor thrombus (arrows) in expanded IVC on CT scan
in 61-year-old woman.
C D

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Diagnosis and Staging of Renal Cell Carcinoma

A B C
American Journal of Roentgenology 2008.191:1220-1232.

D E F

Fig. 8—Metastatic disease (TNM stage M1). Note


hypervascular nature of most metastases.
A, Pulmonary metastases in 76-year-old man. CT
scan shows typical well-defined “cannonball”
nodules (arrows).
B, Mediastinal and hilar nodal metastases (arrows) in
68-year-old man are seen on CT scan.
C, Conventional radiograph shows typical lytic
appearance of metastases (arrows) in 58-year-old
woman.
D, CT scan shows lytic lesion in left iliac bone and
associated hypervascular soft-tissue metastasis
(arrows) in same patient as in C.
E, Hypervascular liver metastases (arrows) are seen
G H on CT scan in 72-year-old man. Note that these must
be differentiated from hemangiomas.
F, Metastases to left adrenal gland (arrows) in
Therapeutic Options and Implications Lindau disease in whom future surgeries may 76-year-old woman.
for Radiologic Follow-Up be required). G, Metastases to skeletal muscle (arrows) in 64-year-
Surgical resection is the only effective old man.
H, Metastases to pancreas (arrows) in 76-year-old
means of cure for clinically localized renal Radical Nephrectomy man.
tumors [10, 62]. Classically, this involves total Total nephrectomies are typically undertak-
nephrectomy, but more recently, partial or en via a retroperitoneal posterolateral approach
“nephron-sparing” nephrectomy has been [10]. It is “radical” when it classically includes and 95%, respectively [63] (Fig. 5). Surgical
shown to be equally effective in selected excision of the perirenal fat, including the ipsi- management is not directly affected by the pres-
groups. The indications for partial nephrecto- lateral adrenal gland, and a lymph node dissec- ence of perinephric extension of disease be-
my include a tumor < 4 cm, peripheral loca- tion. The dissection involves the region from the cause a radical nephrectomy includes en bloc
tion, absence of the contralateral kidney, bilat- diaphragmatic crus to the aortic bifurcation of removal of all the contents of Gerota’s fascia.
eral renal tumors, and renal insufficiency. the ipsilateral—and possibly the contralateral— Ipsilateral adrenalectomy is included in
Another consideration is whether there is a aspects of the IVC or the aorta [7]. The sensitiv- the classic radical nephrectomy. However,
risk of future impairment of renal function ity, specificity, and accuracy for the detection of ipsilateral adrenal metastases occur in only
from another condition or a risk of bilateral perinephric extension of disease by high-resolu- 1–10% of patients. It occurs especially in
renal tumors (e.g., patients with von Hippel- tion CT have been reported to be 96%, 93%, large left-sided upper pole tumors, usually

AJR:191, October 2008 1227


Ng et al.

by direct extension (i.e., T3a tumors) [64]. [70]—which may be more common in necrotic tumors because of the shorter renal vein on
One of the roles of imaging is to assist in tumors or tumors that involve the renal vein. the right [53, 76].
allowing adrenal-sparing nephrectomies in Conversely, small nodes may contain micro- Identification of thrombus in the venous
order to reduce the risk of future adrenal in- metastases—that is, false-negative metastases system, especially the IVC, is particularly im-
sufficiency [7]. (4% in the series by Studer et al.). portant because it affects surgical manage-
Surgery, although substantially more chal- It is reported that 3–22.5% of patients who ment, typically necessitating an anterior ab-
lenging, is not necessarily excluded in the pres- undergo radical nephrectomy without clini- dominal approach. Furthermore, if thrombus
ence of contiguous organ invasion, which typi- cally evident metastases have regional nodal extends into the heart, a combined thoracic
cally involves the liver, diaphragm, psoas involvement at surgery [67, 71]. In pathologic and intracardiac approach with cardiac by-
muscles, pancreas, and bowel (Robson stage series, the prevalence of metastatic nodes in pass may be required.
IVA, or TNM T4 disease). Both CT and MRI cases of occult RCC diagnosed only at autop- Current CT techniques have reported sensi-
may have difficulty in distinguishing abutment sy is reported at 14% [72]. tivities and specificities for detecting renal vein
of tumor from invasion of adjacent organs. Accurate determination of nodal staging thrombus of 85% and 98%, respectively [78].
requires tissue; some surgeons therefore ad- Color Doppler sonography has reported sensi-
Partial (Nephron-Sparing) Nephrectomy vocate routine retroperitoneal nodal dissec- tivities and specificities for detecting thrombus
Partial nephrectomy is a relatively new tion. However, the clinical value of this is in the renal veins of 75% and 96%, respective-
technique. When evaluating this possibility, controversial, in particular as to whether it ly, with 100% accuracy for detection of throm-
the relationship of the tumor to the rest of the affects survival, and surgeons vary in their bus in the IVC [54]. MRI has similar reported
kidney and, in particular, to the arterial sup- approach [10, 26, 57, 67, 73]. sensitivity and specificity for detecting throm-
ply to the tumor and the remainder of the bus in the renal vein of 86–94% and 75–100%,
kidney, is important. Nephron-sparing sur- Venous Involvement respectively, as well as 100% accuracy for de-
American Journal of Roentgenology 2008.191:1220-1232.

gery has been shown to be equally as effica- Extension of tumor into the renal veins has tecting IVC thrombus [79, 80]. MRI, with its
cious as total nephrectomy, with reported been reported to occur in 20–35% of patients, multiplanar capability, is probably the best
local recurrence rates of < 2% [10] and 5-year and into the IVC, in 4–10% [74–76], the latter technique for identifying the superior extent of
survival rates of 87–90%, which are compa- being infrahepatic (50%), intrahepatic (40%), IVC involvement [49, 81].
rable to those from radical nephrectomy [57]. or intraatrial (10%) [77] (Figs. 7A–7C). IVC Fortunately, prognosis is not adversely af-
However, in the case of a solitary kidney, a thrombus is more common from right-sided fected by tumor in the venous system or by its
risk of developing proteinuria, focal segmen-
tal glomerulosclerosis, and progressive renal
failure exists if more than 50% of the renal
mass is removed [57].
Both total and partial nephrectomies can
be undertaken laparoscopically. Some sur-
geons supplement the laparoscopic approach
with direct “hand assistance” in the operative
field. Laparoscopic approaches reduce peri-
operative morbidity and length of the hospital
stay. However, operation times are generally
longer, and morcellation of the sample leads A B
to difficulties in pathologic staging and intro-
duces the risk of tumor seeding [10]. Cryoab-
lation and radiofrequency ablation, which
may be undertaken laparoscopically or percu-
taneously, are promising techniques for treat-
ing small tumors [30, 57, 65].

Nodal Status and Dissection


The presence of nodal metastases is an ad-
verse prognostic factor [66, 67]. Using a cutoff
of 1 cm for short-axis nodal size, sensitivity and
specificity have been reported to be 83% and C D
88% [68] and overall accuracies have been re-
Fig. 9—Local recurrence after nephrectomy as seen on CT.
ported to be 83–89% [68, 69] (Fig. 6). Howev- A, Postsurgical appearances in left nephrectomy bed (lower arrow) in 52-year-old man resolved at follow-up.
er, radiologic assessment of nodal status, in Note associated surgical vascular clips (upper arrow).
common with other tumors, has its limitations. B, Local tumor recurrence is seen in left nephrectomy bed (arrows) in same patient as in A.
Enlarged (> 1 cm) nodes are not necessarily C, Pitfall of unopacified small bowel is seen in left nephrectomy bed of 58-year-old man, which could be
misinterpreted as adenopathy (large arrow) and local tumor recurrence (small arrow) without careful tracing of
metastatic but may be reactive—that is, false- bowel.
positive (58% in one series by Studer et al. D, Follow-up CT scan in same patient as in C shows gas in bowel loops (large and small arrows).

1228 AJR:191, October 2008


Diagnosis and Staging of Renal Cell Carcinoma

TABLE 4: Stage-Specific Postoperative Imaging Surveillance After Radical


Nephrectomy for Localized Renal Cell Carcinoma
Stage Chest Radiography Abdominal CT
T1 Yearly
T2 Every 3 and 6 months, then every 6 months for 3 years, then annually 2 and 5 years
T3 3 and 6 months, then every 6 months for 3 years, then annually 2 and 5 years
Note—Adapted from Levy et al. [95].

A B
American Journal of Roentgenology 2008.191:1220-1232.

Fig. 11—CT appearances after partial nephrectomy in 55-year-old man.


A, CT scan obtained 6 weeks after left partial nephrectomy shows low-density lesion (arrow) at surgical site
that could be confused with mass lesion.
B, Six months after partial nephrectomy, note resolution of postoperative changes (arrow). Also note previous
right nephrectomy.

relief—for example, severe pain or hematuria; in factor (VEGF) and platelet-derived growth fac-
a small number of cases (≈ 0.3%), regression of tor (PDGF). Four targeted agents are presently
metastases has been reported after resection of in clinical use for metastatic RCC: sunitinib,
the primary tumor. Cytoreductive nephrectomy sorafenib, temsirolimus, and bevacizumab.
has been shown to offer a survival benefit in se- Sunitinib (Sutent, Pfizer), a multi­­tyrosine kinase
Fig. 10—Metastatic bone disease in same 58-year- lected patients with metastatic disease [83]. Pre- inhibitor (MKI), has shown an objective re-
old woman as in Figures 8C and 8D. Bone scintigram operative embolization can provide symptomatic sponse rate (ORR) of 31% and a median pro-
shows uptake in left iliac bone, right rib, and right
femur (arrows). relief and reduce intraoperative bleeding in large gression-free survival of 11 months for sunitinib-
tumors. Also, resection is sometimes performed treated patients [86, 87]. It is considered the
level in the IVC, provided the tumor is free- to obtain material needed in immunotherapy. standard-of-care treatment for patients with ad-
floating and can be successfully removed Radiation therapy is sometimes used for pallia- vanced, good- and intermediate-risk, conven-
(5-year survival rates of 50–69% in the ab- tion—for example, pain from bone metastases. tional clear cell RCC. Sorafenib (Nexavar, Bayer
sence of metastatic disease). However, prog- HealthCare), another MKI, is considered sec-
nosis is severely impaired if tumor invades Immunotherapy and Targeted Therapies ond-line therapy after cytokine failure [88].
the wall of the IVC (5-year survival rate, The mainstay of systemic therapy for meta- Temsirolimus (Torisel, Wyeth), an inhibitor of
25%), although this can improve if the in- static RCC has historically been immunother- mammalian target of rapamycin (mTOR), is
volved IVC can be resected completely apy (or cytokine therapy) with interleukin-2 considered the standard of care for patients with
(5-year survival rate, 57%) [2, 66, 82]. Un- (IL-2) and interferon-α (IFN-α). High-dose poor-risk metastatic RCC, irrespective of histol-
fortunately, current imaging techniques have IL-2 has consistently produced a 15–20% re- ogy [89, 90]. Bevacizumab (Avastin, Genen-
some limitations in distinguishing bland sponse rate, 6–8% complete remission rate, tech), a humanized antibody to VEGF, has
thrombus from tumor thrombus and in dis- and approximately 5% cure rate [84, 85]; shown promise in patients with good- and inter-
tinguishing invasive from noninvasive tumor however, it is a fairly toxic regimen. IFN-α mediate-risk metastatic RCC [91] but has not yet
with respect to the vessel wall [2]. Intra- has provided modest survival benefit, has a been approved for metastatic RCC by the U.S.
vascular tissue that enhances after IV con- more favorable toxicity profile, and is more Food and Drug Administration (FDA).
trast administration or that contains neovas- easily administered than IL-2. As a result,
cularization (the thread-and-streak sign) is IFN-α has been adopted as the control arm in Postoperative Surveillance and
good evidence of tumor thrombus rather than many clinical trials of novel agents. Recurrent Disease
bland thrombus (Fig. 7D). Novel therapies for metastatic RCC have tar- Local recurrence in the nephrectomy bed
geted the consequences of von Hippel-Lindau occurs in approximately 20–40% of patients,
Metastatic Disease and Palliation (VHL) gene inactivation and the resulting up- typically in the first 5 years after nephrectomy
In the context of metastatic disease, a nephre- regulation of hypoxia-inducible factor (HIF) [17, 36]; the risks are highest when the resection
ctomy may still be indicated for sympto­matic target genes, notably vascular endothelial growth margins are incomplete. Isolated recurrences

AJR:191, October 2008 1229


Ng et al.

in the nephrectomy bed are uncommon (1.8%) technique is required; for example, unopacified More specialized follow-up may be re-
[92], and resection is typically difficult [10] but small-bowel loops, which inevitably occupy quired for patients with end-stage renal dis-
in selected patients may improve survival. the nephrectomy bed, can mimic local recur- ease, acquired cystic disease of the kidney,
Chae et al. [93] analyzed the patterns of re- rence (Fig. 9). Sonography has not been found or von Hippel-Lindau disease [10]. One of
currence in 194 patients with RCC who had to be reliable in assessing the nephrectomy bed. the features of RCC is that it can have an un-
undergone complete resection. Tumor recur- During the surveillance period, it is recom- predictable time course, with recurrence-free
rence was found in 21% of the patients within a mended that evaluation of potential intratho- intervals of up to 30 years; prolonged periods
mean time of 17 months. Tumor recurrence oc- racic disease be undertaken by chest radiogra- of follow-up may therefore be needed [53].
curred within 2 years in 83% of the patients. phy, with chest CT, bone scanning (Fig. 10),
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A B C
Fig. 12—Local recurrence after cryoablation as seen on CT of 61-year-old man.
A, Scan before ablation shows hypervascular tumor (arrow) adjacent to cyst.
B, Scan 2 months after ablation shows low-density lesion with minimal marginal enhancement, typical of postablation changes (arrow).
C, Local recurrence (arrow) is seen 18 months after ablation.

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F O R YO U R I N F O R M AT I O N
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1232 AJR:191, October 2008


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