evaluation of an inflammation-based prognostic score in patients with metastatic renal cancer

Evaluation of an Inflammation-based Prognostic Scorein Patients With Metastatic Renal Cancer

Sara Ramsey, MD1

Gavin W. A. Lamb, MD1

Michael Aitchison, MD1

John Graham, MD2

Donald C. McMillan, MD3

1 Department of Urology, Gartnavel GeneralHospital, Glasgow, United Kingdom.

2 Beatson Oncology Center, Glasgow, United King-dom.

3 University Department of Surgery, Royal Infirm-ary, Glasgow, United Kingdom.

BACKGROUND. Recently, it was shown that an inflammation-based prognostic

score, the Glasgow Prognostic Score (GPS), provides additional prognostic infor-

mation in patients with advanced cancer. The objective of the current study was to

examine the value of the GPS compared with established scoring systems in pre-

dicting cancer-specific survival in patients with metastatic renal cancer.

METHODS. One hundred nineteen patients who underwent immunotherapy for

metastatic renal cancer were recruited. The Memorial Sloan-Kettering Cancer Cen-

ter (MSKCC) score and the Metastatic Renal Carcinoma Comprehensive Prognostic

System (MRCCPS) score were calculated as described previously. Patients who had

both an elevated C-reactive protein level (>10 mg/L) and hypoalbuminemia (<35

g/L) were allocated a GPS of 2. Patients who had only 1 of those 2 biochemical

abnormalities were allocated a GPS of 1. Patients who had neither abnormality

were allocated a GPS of 0.

RESULTS. On multivariate analysis of significant individual factors, only calcium

(hazard ratio [HR], 3.21; 95% confidence interval [95% CI], 1.51–6.83; P ¼ .002),

white cell count (HR, 1.66; 95% CI, 1.17–2.35; P ¼ .004), albumin (HR, 2.63; 95% CI,

1.38–5.03; P ¼ .003), and C-reactive protein (HR, 2.85; 95% CI; 1.49–5.45; P ¼ .002)

were associated independently with cancer-specific survival. On multivariate anal-

ysis of the different scoring systems, the MSKCC (HR, 1.88; 95% CI, 1.22–2.88;

P ¼ .004), the MRCCPS (HR, 1.42; 95% CI, 0.97–2.09; P ¼ .071), and the GPS (HR,

2.35; 95% CI, 1.51–3.67; P < .001) were associated independently with cancer-spe-

cific survival.

CONCLUSIONS. An inflammation-based prognostic score (GPS) predicted survival

independent of established scoring systems in patients with metastatic renal

cancer. Cancer 2007;109:205–12. � 2006 American Cancer Society.

KEYWORDS: metastatic renal cancer, prognostic score, performance status,calcium, C-reactive protein, albumin, cancer-specific survival.

R enal cell cancer, although it is the 12th most common cause of

cancer deaths, is among the most lethal urologic cancers. Each

year in the United Kingdom, there are approximately 3500 new cases.

Approximately 30% of patients present with metastases, and an addi-

tional 40% of patients develop metastases after undergoing poten-

tially curative resection.1

The traditional mainstay of treatment in metastatic disease is

immunotherapy, although the development of new targeted agents,

such as sorafenib, sunitinib, and temsirolimus, may alter our first-

line therapy for these patients. It has been demonstrated in 4 rando-

mized, placebo-controlled trials that interferon-based immunother-

apy provides a consistent survival advantage, although this is

measured in months and is a toxic treatment with considerable side

effects.2–5 Although a number of trials have reported improved time

Address for reprints: Sara Ramsey, MD, Depart-ment of Urology, Gartnavel General Hospital, Glas-gow G12 0YN, United Kingdom; Fax: 0141-211-1045; E-mail: [email protected]

Received September 7, 2006; revision receivedOctober 12, 2006; accepted October 18, 2006.

ª 2006 American Cancer SocietyDOI 10.1002/cncr.22400Published online 5 December 2006 in Wiley InterScience (www.interscience.wiley.com).

205

to disease progression with the new targeted agents,

only 2 randomized trials have reported improved

overall survival with sunitinib6 and temsirolimus.7

In addition to immunotherapy, there is evidence

to support cytoreductive nephrectomy or metaste-

ctomy in specific circumstances.8 However, these are

major surgical procedures, and postoperative comp-

lications may render a patient unfit for subsequent

immunotherapy.

There is continuing interest in improving the

selection of patients with a good prognosis for more

active treatment and the selection of patients with a

poor prognosis for less active and less toxic treatment,

because this will improve overall patient outcomes.

Currently, the Eastern Cooperative Oncology Group

(ECOG) performance status is used widely as a prog-

nostic tool in patients with metastatic disease. How-

ever, the assessment of performance status is sub-

jective and has significant interobserver variability.9

Therefore, there is a need for tumor- or host-based

factors which predict cancer-specific survival better

and allow the better selection and stratification of

patients for treatment. For these factors to be use-

ful clinically, they should be available routinely,

well standardized, and validated in different patient

cohorts.

There is increasing evidence that the presence of

a systemic inflammatory response, as evidenced by

an elevated circulating C-reactive protein concentra-

tion or hypoalbuminemia, is an independent pro-

gnostic factor in patients with advanced cancer.10,11

With reference to renal cancer, an elevated C-reactive

protein level has been associated with poorer cancer-

specific survival in patients with advanced disease.12–14

Therefore, it is noteworthy that the combination

of hypoalbuminemia and an elevated C-reactive pro-

tein, measured by the Glasgow Prognostic Score

(GPS), has been shown to provide additional prognos-

tic information in patients with advanced cancer.15–19

A number of prognostic scoring systems are in use

to stratify patients with metastatic renal cancer into

risk groups.12,20 However, those systems incorporate a

variety of different biochemical, histologic, and radi-

ologic features; and it is not known how these scoring

systems compare. Therefore, the objective of the

current study was to examine the value of the

GPS, compared with established scoring systems, for

predicting cancer-specific survival in patients with

metastatic renal cancer

MATERIALS AND METHODSPatients with metastatic renal cancer who, on the

basis of clinical findings and computed tomography

scans of the chest, abdomen, and pelvis, were diag-

nosed with metastatic disease between 2001 and 2005

in the West of Scotland and were referred to

the specialist renal cancer unit, were included in

the study. The outpatient treatment regimes were

either subcutaneous a-interferon given at a dose of 10

million units 3 times weekly on a 12-weekly basis or a

modified Atzpodien regime of subcutaneous a-inter-feron and subcutaneous interleukin-2 for 5 weeks

with an additional 3 weeks of 5-flourauracil given

intravenously. No patients in this study had received

systemic therapy or radiotherapy prior to commence-

ment of immunotherapy.

Patients who underwent surgery were staged

pathologically according to the 1997 International

Union Against Cancer TNM classification of renal

tumours.21 Tumors were graded according to criteria

set out by Fuhrman and coworkers22 if biopsies or

surgery had been performed. Clinical stage and ECOG

performance status were recorded prior to treatment

initiation. Prior to commencement of treatment for

metastases, routine laboratory measurements of lac-

tate dehydrogenase, hemoglobin, calcium, differential

white cell count, albumin, and C-reactive protein

were obtained. The Research Ethics Committee of

North Glasgow National Health Service Trust approved

the study.

The Memorial Sloan-Kettering Cancer Center

(MSKCC) scores were derived as described pre-

viously20 (Table 1). In this system, abnormal hemo-

globin and calcium levels, a lactate dehydrogenase

level 3 times greater than the upper limit of normal, a

Karnofsky performance status <80%, and the absence

of prior nephrectomy are considered risk factors.

Patients are classified as favorable risk if they have no

risk factors, intermediate risk if they have 1 or 2 risk

factors, and poor risk if they have �3 risk factors.

The Metastatic Renal Carcinoma Comprehensive

Prognostic System (MRCCPS) scores also were derived

as described previously12 (Table 1). Briefly, 6 pretreat-

ment variables are used to categorize patients into

low-, intermediate-, and high-risk groups. Neutrophil

count is given the greatest weight, and the remaining

factors, which are assigned 1 point each, are a C-

reactive protein level >10 mg/L, a lactate dehydro-

genase level >220 U/L, the presence of bone meta-

stases, and the onset of metastatic disease <3 years

after diagnosis. Patients with 0 or 1 points are classi-

fied as low risk, patients with 2 or 3 points are classi-

fied as intermediate risk, and patients with �4 pointes

are classified as high risk.

The GPS was constructed as described pre-

viously15,16 (Table 1). Briefly, patients with both an

elevated C-reactive protein (>10 mg/L) and hypoal-

206 CANCER January 15, 2007 / Volume 109 / Number 2

buminemia (<35 g/L) were allocated a score of 2.

Patients in whom only 1 of these biochemical

abnormalities was present were allocated a score of 1.

Patients in whom neither of these abnormalities was

present were allocated a score of 0.

StatisticsComparisons between groups of patients were carried

out using contingency table (chi-square) analysis, as

appropriate. Grouping of the laboratory variables lac-

tate dehydrogenase, hemoglobin, calcium, white cell

count, neutrophil count, lymphocyte count, albumin,

and C-reactive protein was carried out by using stand-

ard thresholds.7–9,17 Survival (cancer-specific) analysis

of the group variables was performed using a Cox pro-

portional-hazards model. Deaths up to the end of July

2006 were included in the analysis. Multivariate sur-

vival analysis, including all covariates that were signif-

icant on univariate analysis, was performed using a

stepwise, backward procedure to derive a final model

of the variables that had a significant independent

relation with survival. To remove a variable from the

model, the corresponding P value had to be >.10.

Analyses were performed using SPSS software (SPSS

Inc., Chicago, IL).

RESULTSThe characteristics of patients with metastatic renal

cancer (n ¼ 119) are shown in Table 2. The majority

were men, were aged >60 years, and had undergone

prior surgical treatment. The majority of patients had

an ECOG performance status of 0 and had lactate de-

hydrogenase, calcium, white cell count, neutrophil

count, percentage lymphocytes, and albumin mea-

surements in the normal range. In contrast, the

majority of patients had an elevated C-reactive pro-

tein concentration; and of, the 18 patients who had

hypoalbuminemia, 15 patients (83%) had an elevated

C-reactive protein concentration.

The minimum follow-up of patients was 5

months, the median follow-up of all patients was

10 months, and the median follow-up of the survivors

was 15 months. During this period, 78 patients died

of their cancer, and the median survival was 8 months.

On univariate survival analysis of individual variables,

lactate dehydrogenase (P < .10), hemoglobin (P < .01),

calcium (P < .001), white cell count (P < .01), neutro-

phil count (P < .05), albumin (P < .01), and C-reactive

protein were associated significantly with cancer-

specific survival (Table 2). On multivariate analysis of

these significant factors, only calcium (hazard ratio

[HR], 3.21; 95% confidence interval [95% CI], 1.51–

6.83; P ¼ .002), white cell count (HR, 1.66; 95% CI,

1.17–2.35; P ¼ .004), albumin (HR, 2.63; 95% CI, 1.38–

5.03; P ¼ .003), and C-reactive protein (HR, 2.85; 95%

CI, 1.49–5.45; P ¼ .002) were associated independently

with cancer-specific survival.

On univariate survival analysis of the scoring sys-

tems, the MSKCC (P < .001) (Fig. 1), the MRCCPS

(P < .01) (Table 2), and the GPS (P < .001) (Fig. 3)

were associated significantly with cancer-specific sur-

vival (Figs. 1–3). On multivariate analysis of these

scoring systems, the MSKCC (HR, 1.88; 95% CI, 1.22–

2.88; P ¼ .004), the MRCCPS (HR, 1.42; 95% CI, 0.97–

2.09; P ¼ .071), and the GPS (HR, 2.35; 95% CI, 1.51–

3.67; P < .001) were associated independently with

cancer-specific survival. Using cancer-specific mortal-

ity as an endpoint, the area under the receiver opera-

tor curve was 0.687 (95% CI, 0.587–0.786; P ¼ .001) for

the MSKCC scoring system, 0.638 (95% CI, 0.530–

0.746; P ¼ .014) for the MRCCPS scoring system, and

0.710 (95% CI, 0.611–0.808; P < .001) for the GPS scor-

ing system.

The relation between clinicopathologic character-

istics and an inflammation-based prognostic score

TABLE 1Prognostic Scoring Systems in Patients With Metastatic Renal Cancer

MSKCC system Score MRCCPS system Score GPS system Score

No prior nephrectomy 1 Disease-free interval (�3 y) 1

KPS (<80) 1 Metastatic sites (�3) 1

Hemoglobin (<13 g/dL [men]/<11.5 g/dL [women]) 1 Bone metastases (present) 1

Lactate dehydrogenase (>300 U/L) 1 Lactate dehydrogenase (�220 U/L) 1

Corrected calcium (>10 mg/dL) 1 C-reactive protein (�11 mg/L) 1 C-reactive protein (>10 mg/L) 1

Neutrophil count (�6500 � 109) 2 Albumin <35 g/L) 1

Total score

Low risk 0 0–1 0

Intermediate risk 1–2 2–3 1

High risk 3–5 �4 2

MSKCC indicates Memorial Sloan-Kettering Cancer Center; MRCCPS, Metastatic Renal Carcinoma Comprehensive Prognostic System; GPS, Glasgow Prognostic Score; KPS, Karnofsky performance score.

Inflammation-based Prognostic Score/Ramsey et al. 207

TABLE 2Clinicopathologic Characteristics and Cancer-Specific Survival in Patients Undergoing Treatmentfor Metastatic Renal Cancer: Univariate Analysis

Characteristic Patients (N 5 119) HR (95% CI) P

Age group 1.46 (0.93–2.30) .102

�60 y 56

>60 y 63

Sex 1.34 (0.84–2.15) .216

Men 85

Women 35

ECOG PS 1.07 (0.62–1.86) .812

0 92

�1 26

Lactate dehydrogenase 1.89 (0.90–3.96) .094

<300 U/L 108

�300 U/L 9

Hemoglobin 2.04 (1.28–3.23) .003

�13 g/dL (men)/�11.5 g/dL (women) 56

<13 g/dL (men)/<11.5 g/dL (women) 63

Calcium 3.67 (2.01–6.69) <.001

�2.5 mmol/L 100

>2.5 mmol/L 19

Prior surgical treatment 0.85 (0.62–1.17) .328

Curative 50

Cytoreductive 48

None 21

Disease-free interval 0.72 (0.38–1.37) .315

�3 y 99

>3 y 20

Immunotherapy 0.96 (0.52–1.79) .910

Interferon 100

Interferon, interleukin, and 5-FU 19

No. of metastatic sites 0.83 (0.53–1.29) .402

1 61

�2 58

White cell count 1.56 (1.13–2.15) .007

<8.5 � 109/L 86

8.5–11 � 109/L 22

>11 � 109/L 11

Neutrophil count 1.87 (1.13–3.11) .015

<6.5 � 109/L 92

�6.5 � 109/L 27

Lymphocyte percentage

20–40% 58 1.30 (0.93–1.81) .122

12–19.9% 46

0–11.9% 15

Albumin 2.52 (1.38–4.61) .003

�35 g/L 103

<35 g/L 16

C-reactive protein 3.75 (2.02–6.97) <.001

�10 mg/L 35

>10 mg/L 84

MSKCC 2.44 (1.60–3.70) <.001

Low risk 31

Intermediate risk 72

High risk 13

MRCCPS 1.70 (1.21–2.39) .002

Low risk 27


High risk 29

GPS 3.03 (2.01–4.56) <.001

Low risk 33


High risk 14

HR indicates hazard ratio; 95% CI, 95% confidence interval; ECOG PS, Eastern Cooperative Oncology Group performance status; 5-FU, 5-fluouracil; MSKCC,

Memorial Sloan-Kettering Cancer Center; MRCCPS, Metastatic Renal Carcinoma Comprehensive Prognostic System; GPS, Glasgow Prognostic Score.

(GPS) in patients with metastatic renal cancer is illu-

strated in Table 3. An increasing GPS was associated

with a lower hemoglobin level (P < .001), a higher cal-

cium level (P � .001), a higher neutrophil count

(P < .10), a lower percentage lymphocytes (P < .01),

and a greater risk of poor survival, as estimated by the

MSKCC and the MRCCPS scoring systems. The me-

dian survival in these patients was 28 months,

11 months, and 3 months for patients who had GPS

scores of 0, 1, and 2, respectively (Fig. 3).

On multivariate analysis of the GPS, hemoglobin,

calcium, neutrophil count, and lymphocyte percent-

age, the GPS (HR, 2.93; 95% CI, 1.88–4.55; P < .001),

the calcium level (HR, 2.72; 95% CI, 1.47–5.02;

P ¼ .001), and the neutrophil count (HR, 1.66; 95% CI,

1.00–2.77; P ¼ .051) were associated independently

with cancer-specific survival. When the calcium level

was combined with the GPS to form a new score

(from 0 to 3), the new score predicted cancer-specific

survival (HR, 2.86; 95% CI, 2.04–4.00; P < .001). Using

cancer-specific mortality as an endpoint, the area

under the receiver operator curve for the new com-

bined score was 0.703 (95% CI, 0.603–0.804; P < .001).

DISCUSSIONIn the current study, we have shown that the presence

of a systemic inflammatory response, as evidenced by

an elevated C-reactive protein concentration and

FIGURE 1. Relation between Memorial Sloan-Kettering Cancer Centerscores (low/intermediate/high risk from top to bottom) and cancer-specific

survival in patients with metastatic renal cancer.

FIGURE 3. Relation between the Glasgow Prognostic Score (0/1/2 from top tobottom) and cancer-specific survival in patients with metastatic renal cancer.

FIGURE 2. Relation between Metastatic Renal Carcinoma Compre-

hensive Prognostic System scores (low risk/intermediate risk/high risk from

top to bottom) and cancer-specific survival in patients with metastatic renal

cancer.


TABLE 3Correlations Between Clinicopathologic Characteristics and an Inflammation-Based Prognostic Score (GlasgowPrognostic Score) in Patients With Metastatic Renal Cancer

Characteristic GPS 0 (N 5 33) GPS 1 (N 5 72) GPS 2 (N 5 14) P

Age .074

�60 y 10 39 7

>60 y 23 33 7

Sex .892

Men 23 51 10

Women 10 21 4

ECOG PS .990

0 23 60 9

�1 9 12 5

Lactate dehydrogenase .165

<300 U/L 31 66 11

�300 U/L 2 4 3

Hemoglobin <.001

�13 g/dL (men)/�11.5 g/dL (women) 25 28 3

<13 g/dL (men)/<11.5 g/dL (women) 8 44 11

Calcium /001

�2.5 mmol/L 30 15 9

>2.5 mmol/L 0 14 5

Prior surgical treatment .738

Curative 12 31 7

Cytoreductive 14 32 2

None 7 9 5

Disease-free interval .632

�3 y 29 58 12

>3 y 4 14 2

Immunotherapy .989

Interferon 26 64 10

Interferon, interleukin, and 5-FU 7 8 4

No. of metastatic sites .938

1 18 35 8

�2 15 37 6

White cell count .162

<8.5 � 109/L 27 50 9

8.5–11 � 109/L 4 15 3

>11 � 109/L 2 7 2

Neutrophil count .057

<6.5 � 109/L 30 52 10

�6.5 � 109/L 3 20 4

Lymphocyte percentage .009

20–40% 20 31 6

12–19.9% 12 30 4

0–11.9% 0 11 4

MSKCC score <.001

Favorable risk 15 15 1

Intermediate risk 16 49 7

Poor risk 1 6 6

MRCCPS score <.001

Low risk 16 10 1

Intermediate risk 14 38 9

High risk 3 22 4

Median survival (range), mos 28.3 (18.8–37.8) 10.7 (9.1–12.4) 3.4 (2.2–4.6) <.001

GPS indicates Glasgow Prognostic Score; ECOG PS, Eastern Cooperative Oncology Group performance status; 5-FU, 5-fluouracil; MSKCC, Memorial Sloan-

Kettering Cancer Center; MRCCPS, Metastatic Renal Carcinoma Comprehensive Prognostic System.


hypoalbuminemia, predicts cancer-specific survival

independent of other established prognostic factors,

such as performance status, calcium, lactate dehydro-

genase, and neutrophil counts, in patients with meta-

static renal cancer. Moreover, we have shown that the

GPS compares favorably with the MSKCC scoring sys-

tem and is superior to the MRCCPS scoring system.

At the time of diagnosis, there are well established

prognostic factors on which to base the prediction of

likely survival in cancer patients. In contrast, predict-

ing the survival of patients with advanced disease is

more problematic. Consequently, clinicians often

overestimate survival.23,24 The results of the current

study suggest that the GPS may be useful in the

assessment of survival in patients with metastatic re-

nal cancer. It is simple to use and is based on

routinely available, well standardized measurements.

Therefore, it is possible that this simply derived,

inflammation-based score will be a useful tool in the

prediction of survival and possible stratification, at di-

agnosis, of patients with metastatic renal cancer.

The mechanisms by which a systemic inflamma-

tory response may influence survival in these cancer

patients are not clear. However, it is possible that the

presence of a systemic inflammatory response and

the associated nutritional decline25,26 may influence

tolerance and compliance with active treatment.13,16

It also may reflect the proinflammatory cytokine

activity, in particular, interleukin-6,27,28 which not

only stimulates renal tumor growth but can produce

profound catabolic effects on host metabolism.25,29 In

this way, the presence and magnitude of a chronic,

systemic inflammatory response, as reflected by the

GPS, may produce progressive nutritional and func-

tional decline, ultimately resulting in reduced sur-

vival. Indeed, this concept is consistent with the

observation in the current study that almost all

patients with hypoalbuminemia had an elevated

C-reactive protein concentration.

Because of the high toxicities and low response

rates of immunotherapy, there has been considerable

interest in the use of new targeted agents, such as sor-

afenib and sunitinib, in patients with metastatic renal

cancer. The reported reduced side-effect profile and

the potential for simple outpatient administration are

more appealing to patients and oncologists alike.

Early reports of increased progression-free survival

and, more recently, of increased overall survival6,7

may lead to the adoption of these drugs as first-line

treatment. It remains to be established whether the

GPS predicts which patients will benefit from these

new agents.

In summary, the prognosis remains poor for pa-

tients who are diagnosed with metastatic renal cancer,

even if they receive active treatment. The presence of

a systemic inflammatory response (an elevated GPS)

appears to be a useful indicator of outcome among

these patients, independent of established scoring

systems. Moreover, the GPS has the advantage of

being simple to measure, routinely available, and well

standardized.

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evaluation of an inflammation-based prognostic score in patients with metastatic renal cancer

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