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ORIGINAL
Value of the CRP–albumin ratio in patients with resectablepancreatic cancer
Yusuke Arakawa, Katsuki Miyazaki, Masato Yoshikawa, Shinichiro Yamada, Yu Saito, Tetsuya Ikemoto, Satoru Imura,
Yuji Morine, and Mitsuo Shimada
Department of Digestive Surgery and Transplantation, Institute of Health Biosciences, Tokushima University, Tokushima, Japan

Abstract : Background : The C-reactive protein (CRP)–albumin ratio (CAR) was reported as a prognostic factor ofresectable hepatocellular carcinoma. The aim of this study was to analyse the significance of CAR in resectablepancreatic cancer. Patients and Methods : 163 patients with curative resection for pancreatic cancer were enrolled in this retrospective study. Cases of non-curative resection were excluded. The CAR was calculated withthe preoperative plasma CRP and albumin values, with a cut-off value of 0.06, as calculated in a previous report.
Results : Patients in the low CAR group had significantly better overall survival (OS) and disease-free survival(DFS) compared with the high CAR group (P < 0.05). On multivariate analysis, for high CAR, CA19-9 > 300 U / ml
and receipt of adjuvant chemotherapy were independent risk factors for OS and DFS. High CAR was significantly associated with advanced T stage. Conclusion : The CAR might be a prognostic factor for patients with resectable pancreatic cancer. J. Med. Invest. 68 : 244-248, August, 2021
Keywords : Pancreas cancer, C-reactive protein, albumin

INTRODUCTION

PATIENTS AND METHODS

The prognosis of patients with pancreatic ductal adenocarcinoma (PDAC) is extremely poor. Despite the development ofsurgical techniques and perioperative chemotherapy, the 5-year
survival rate is 8% in the United States (1). PDAC is also thefifth most common cause of cancer death in Japan (2). The
frequency of postoperative recurrence remains high in patientswith PDAC (3) ; therefore, a novel prognostic marker to predictrecurrence is required.
Nowadays, tumour-related pathological factors have been
identified as predictive markers in patients with PDAC, including tumour stage, lymph node metastasis, vascular andlymphatic invasion and perineural invasion. Several predictive
markers based on preoperative systemic inflammation and nutritional status such as the neutrophil–lymphocyte ratio (NLR),
platelet–lymphocyte ratio (PLR), modified Glasgow prognostic
score (mGPS), and prognostic index (PNI) were reported in lungcancer (4), hepatocellular carcinoma (5), melanoma (6), renal cell
carcinoma (7), gastric cancer (8), intrahepatic cholangiocarcinoma (9) and colorectal cancer (10). These factors has been reported as useful biomarker to predict the prognosis in PDAC (11, 12).
C-reactive protein (CRP) to albumin ratio is based on two
acute inflammatory protein (13). The CRP–albumin ratio (CAR)
was reported as a prognostic factor of resectable hepatocellular
carcinoma, colorectal cancer, oesophageal cancer, gastric cancer,
renal cancer, and pancreatic cancer (14-18).
The aim of this study was to analyse and validate the significance of the CAR in resectable pancreatic cancer at our hospital.

One hundred sixty-three patients who underwent curative
surgical resection for PDAC during 2004 to 2018 at the Universityof Tokushima Hospital were enrolled in this retrospective study.
Fourteen patients were excluded because of non-curative resection. All the patients had PDAC proven histologically. Finally,
149 patients were analysed in this study. Laboratory data including serum CRP and albumin were collected within 1 month
before surgery. Patients were followed up monthly for tumourmarkers including CEA and CA19-9 and underwent computed
tomography every 4–6 months. When recurrence was suspected,
precise diagnostic imaging studies including positron emission
tomography were performed. After confirmation of recurrent
pancreatic cancer, systemic chemotherapy, radiation therapy,
or best supportive care were indicated. The clinicopathologicalcharacteristics of the patients are shown in Table 1. All patientssigned informed consent for this study, which was approved by
the clinical ethics committee at our institution (#3362).
The NLR, PNI, PLR, and mGPS were calculated with cutoff values of 3, 45, 150, and 1, respectively. The CAR was also
calculated. To determine the appropriate cutoff value of CAR,
receiver operation characteristic (ROC) curve analysis was
performed. The cutoff value of CAR was 0.06 and the AUC value
was 0.54223.

Received for publication February 1, 2021 ; accepted March 31, 2021.
Address correspondence and reprint requests to Yusuke Arakawa,
Institute of Health Bioscience, Tokushima University Graduate
School, Department of Surgery, 3-18-15 Kuramoto-cho, Tokushima,
770-8503, Japan and Fax : +81-88-631-9698.

Statistical analysis
Statistical comparisons for significance were made using chisquared test or Fisher’s exact test with one degree of freedom,
as appropriate. Cumulative patient survival and recurrence-freesurvival were determined using the Kaplan–Meier method witha log-rank test. Univariate and multivariate analyses were
performed using a Cox proportional hazard model. A P-value ofless than 0.05 was considered statistically significant. Statisticalanalysis was performed with JMP 14 software (SAS Institute,Cary, NC, USA).

The Journal of Medical Investigation Vol. 68 2021

The Journal of Medical Investigation Vol. 68 August 2021

245

Table 1. Clinicopathological characteristics of patients with surgical resection for pancreas ductal adenocarcinoma
Parameters
Age, years

70 (63-76)

female / male

77 (51.7) / 72 (48.3)

Body mass index kg / m2

22.1 (19.7-24.2)

Fibrinogen, g / ml

439 (367-510)

C reactive protein, mg / L

0.09 (0.05-0.27)

Serum albumin, g / dl

3.9 (3.7-4.2)

WBC, 109 / L

5450 (4400-6600)
9

Neutrophils, 10 / L

3650 (2600-4495)

Lymphocytes, 109 / L

1290 (1040-1715)

CEA ng / ml

2.3 (1.4-3.9)

CA19-9 U / ml

126 (27.5-670)

Type of resection (DP / PD / TP)

40 / 56 / 4

PV resection (n, %)22 (14.7)

Neoadjuvant chemotherapy (n, %)16 (10.7)

Postoperative chemotherapy (n, %)89 (59.3)

UICC stage (n, %)ⅠA

20 (15.4)

ⅠB

16 (16)ⅡA

47 (31.5)

ⅡB

43 (28.9)

Ⅲ

23 (15.4)

Resection margin R0

115 (76.7)

Tumor size ≥ 2cm

113 (75.6)

Lymph node metastasis (n)52 (35.1)

Lymphatic invasion (ly)100 (68.0)

Vascular invasion (v)114 (77.6)

Perineural invasion (ne)119 (81.5)

Anterior serosal invasion (s)34 (29.6)

Retroperitoneal invasion (rp)45 (38.1)

Microscopic portal vein invasion (pv)

23 (22.3)

Microscopic arterial invasion (a)6 (5.7)

Plexus invasion (pl)11 (12.5)

Data are expressed as median (IQR) or n(%)

Figure 1. Kaplan–Meier curves of overall survival and diseasefree survival according to CAR. (A) Overall survival. (B) Disease-freesurvival.

RESULTS

Comparison of prognostic factors for overall survival (OS) in patients with surgical resection for PDAC
The OS rate was significantly worse in patients with a high
CAR compared with those with a low CAR (Figure 1A). The
prognostic factors for OS in patients with surgical resection for
PDAC is shown in Table 2. In the univariate analysis, sevenfactors were independent prognostic factors for OS including
CAR (HR 2.826, 95% CI 1.720–4.645, P < 0.001), PNI (HR2.250, 95% CI 1.384–3.645, P = 0.0007), PLR (HR 1.643, 95%
CI 1.022–2.684, P = 0.0045), CA19-9 (HR 2.085, 95% CI 1.314–
3.311, P = 0.0013), adjuvant chemotherapy (HR 2.208, 95% CI
1.396–3.491, P = 0.0022), T3+4 (HR 2.873, 95% CI 1.700–5.114,
P < 0.001), and lymph node metastasis (HR 1.846, 95% CI 1.143–
2.945, P = 0.0095). In the multivariate analysis of these sevenfactors, three factors were independent prognostic factors for OS
including CAR (HR 2.668, 95% CI 1.523–4.672), CA19-9 (HR2.011, 95% CI 1.213–3.334), and adjuvant chemotherapy (HR2.231, CI 1.379–3.609).

Comparison of prognostic factors for disease-free survival (DFS) in
patients with surgical resection for PDAC
The DFS rate was significantly worse in patients with a high
CAR compared with those with a low CAR (Figure 1B). The
prognostic factors for DFS with surgical resection for PDAC
are shown in Table 3. In the univariate analysis, five factors
were independent prognostic factors for DFS including CAR(HR 2.826, 95% CI 1.720–4.645, P < 0.001), PNI (HR 1.542,
95% CI 1.008–2.340, P = 0.0308), CA19-9 (HR 1.864, 95% CI
1.239–2.797, P = 0.0031), adjuvant chemotherapy (HR 1.884,
95% CI 1.257–2.824, P = 0.0020), and T(3+4) (HR 1.890, 95% CI
1.232–2.966, P = 0.0032). In the multivariate analysis of these
five factors, three factors were independent prognostic factors for
DFS including CAR (HR 1.990, 95% CI 1.198–3.307, P = 0.0103),
CA19-9 (HR 1.864, 95% CI 1.239–2.797, P = 0.0083), and adjuvant chemotherapy (HR 1.884, 95% CI 1.257–2.824, P = 0.0032).

Y. Arakawa, et al. CRP–albumin ratio and pancreatic cancer

246

Clinicopathological features according to the CAR
Clinicopathological factors were compared between the highCAR and low CAR groups in Table 4. The high CAR group wascorrelated with higher CRP, lower serum albumin, higher serum
fibrinogen, low LCR, high NLR, low PNI and high mGPS. In thetumour-related factors, the high CAR group was significantly
associated with T (3+4). Also, the high CAR group showed an
association with portal vein resection and adjuvant chemotherapy but this was not significant. The other factors showed nosignificant difference between these two groups.

Table 2. OS related variables
Univariate
Factorp-value

Multivariate
HR (95% CI)

p-valueHR (95% CI)

0.00062.668 (1.523-4.672)

CAR< 0.06 / ≥ 0.06

< 0.001

2.826 (1.720-4.645)

LCR< 15090 / ≥ 15090

0.05051.593 (0.390-1.007)

NLR< 3 / ≥3

0.941

1.021 (0.603-1.672)

PNI< 45 / ≥ 45

0.00072.250 (1.384-3.645)

0.35711.282 (0.755-2.175)

PLR< 150 / ≥ 150

0.00451.643 (1.022-2.684)

0.6254

1.139 (0.675-1.923)

0.00682.011 (1.213-3.334)mGPS

0 / 1,2

0.67992.270 (0.806-5.190)

GenderFemale / male

0.70231.315 (0.829-2.087)< 70 / ≥ 70

0.15581.391 (0.874-2.201)

Age
BMI kg / m< 25 / ≥ 25

0.5203

1.216 (0.639-2.143)

CEA ng / ml

< 5/ ≥ 5

0.58781.203 (0.578-2.248)

CA19-9 U / ml

< 300 / ≥ 300

0.00132.085 (1.314-3.311)

Resection type

PD / DP / TP

0.44741.190 (0.726-1.951)

PV resection

No / yes

0.47311.310 (0.575-2.600)

NAC(-)

No / yes

0.92231.039 (0.433-2.116)

AC(-)

No / yes

0.00222.208 (1.396-3.491)

0.00112.231 (1.379-3.609)

T(3+4)

No / yes< 0.001

2.873 (1.700-5.114)

0.08701.539 (0.906-3.166)

N(+)

No / yes

0.00951.846 (1.143-2.945)

0.0987

1.693 (0.906-3.166)

2

Table 3. DFS related variables
Univariate
Factorp-value

Multivariate
HR (95% CI)

p-valueHR (95% CI)

0.01031.990 (1.198-3.307)

0.6387

1.113 (0.708-1.735)

0.00831.802 (1.166-2.776)

CAR<0.06 / ≥ 0.06

< 0.001

2.826 (1.720-4.645)

LCR<15090 / ≥ 15090

0.00301.843 (0.357-0.822)

NLR< 3/ ≥ 3

0.3812

1.176 (0.759-1.792)

PNI< 45 / ≥ 45

0.03081.542 (1.008-2.340)

PLR< 150 / ≥ 150

0.22351.270 (0.840-1.928)

mGPS (0 / 1+2)

0 / 1,20.05291.956 (0.662-4.642)

Gender (F / M)

Female / male

0.91961.040 (0.698-1.553)

Age > 70

< 70 / ≥ 70

0.4904

1.176 (0.780-1.759)

BMI > 25 kg / m< 25 / ≥ 25

0.37001.295 (0.729-2.158)

CEA > 5 ng / ml

< 5/ ≥ 5

0.1032

1.604 (0.886-2.713)

CA19-9 > 300 U / ml

< 300 / ≥ 300

0.00311.864 (1.239-2.797)

PD / DP / TP

PD / DP / TP

0.44151.322 (0.850-2.058)

PV resection

No / yes

0.19371.466 (0.809-2.478)

NAC(-)

No / yes

0.41351.306 (0.709-2.405)

AC(-)

No / yes

0.00201.884 (1.257-2.824)

0.0032

1.884 (1.245-2.851)

T(3+4)

No / yes

0.00321.890 (1.232-2.966)

0.0646

1.548 (0.974-2.514)

N(+)

No / yes

0.05611.494 (0.979-2.252)

2

The Journal of Medical Investigation Vol. 68 August 2021
Table 4. CAR related variables
FactorCAR High(n = 38)

CAR Low(n = 111)

p-valueAge ≥ 70

18 (47.7)

53 (47.6)

0.9678

Male gender

21 (55.3)

51 (45.6)

0.3211

BMI ≥ 25 kg / m2

7 (18.4)

15 (13.5)

0.4706

CEA ≥ 5 ng / ml

8 (21.1)

14 (12.7)

0.2777

CA19-9 ≥ 300 U / ml

12 (31.6)

45 (40.5)

0.3223

CRP ≥ 1 mg / dl

14 (36.8)0 (0)< 0.001

Alb ≥ 3.5 g / dl

20 (52.6)

101 (91.0)< 0.001

Fibrinogen ≥ 400

36 (94.7)

60 (54.1)< 0.001

DP / PD / TP

8 / 28 / 2

38 / 70 / 3

0.2585

PV resection

9 (23.7)

14 (12.6)

0.1161NAC

6 (15.8)

10 (9.1)

0.2686AC

18 (47.4)

71 (64.0)

0.0737T(3+4)

32 (84.2)

64 (62.2)

0.0087N(+)

15 (40.5)

36 (33.3)

0.4296

LCR < 15090

35 (100)

36 (33.3)< 0.001

NLR ≥ 321 (60)33 (30.6)

0.0018

PNI < 45

10 (28.6)

77 (71.3)< 0.001

PLR < 150

13 (37.1)

50 (46.3)

0.3432mGPS 1,2

11 (28.9)0 (0)< 0.001n (%)

DISCUSSION
In this study, OS and DFS were significantly worse in patientswith resectable PDAC and a high CAR of > 0.06. The CAR
was an independent prognostic factor for OS and DFS in themultivariate analysis. To the best of our knowledge, no study
has compared other prognostic markers such as lymphocyte to
CRP ratio (LCR), NLR, PNI, PLR, and mGPS in patients withresectable PDAC.
In our study, the higher value of CAR was correlated withother prognostic markers which calculated with CRP and serum
albumin and it was statistically superior to the other prognostic
markers. The higher value of CAR was also correlated with higher T factor which reflected in local advancement of the pancreaticcancer.
The precise mechanism of the relation between the CAR andprognosis in patients with resectable PDAC has not been fully
elucidated yet. Several possible mechanism has been reported inbasic research articles. Mantovani A et al. reported that the migration, invasion, and metastasis of cancer cells could contributeto the inflammation through the activation of several chemokines such as CXCR4 and its ligand CXCL12 (19) ; as a result, the
CRP reflects a cancer-specific inflammatory response to tumour
necrosis or local tissue damage and indicates a favourable environment for the establishment and growth of distant metastasis.
Yang J et al. also reported that CRP binding activated Fcγ receptors and stimulated the PI3K / AKT, ERK, and NFκB pathways
and inhibited caspase cascade activation induced. CRP also enhanced myeloma cell secretion of IL-6 and IL-6-protected myeloma cells resulting from chemotherapy drug-induced apoptosis.
Therefore CRP could be one of the candidate of new therapeutic
approach for cancer in basic research (20).
On the other hand, serum albumin level is low in patients withPDAC especially in the perioperative period because of malnutrition247

and cachexia. Improvement of perioperative immune-nutritional
status reduced post-operative inflammation (21, 22). Poor nutritional state in pancreatic surgery has been reported to be
associated with worse postoperative survival (11). Therefore,
the CAR calculated with two critical factors could represent the
inflammation and nutritional status of PDAC patients.
Recently, CAR was also reported as one of the poor prognostic
marker not only in solid cancer but also hematologic cancer suchas malignant lymphoma (23). Moreover, Araki T et al. reported
that evaluation of CAR could predict therapeutic response to
immune check point inhibitor such as nivolumab (24).
There were several limitations to this study. This study was
retrospective and the sample size was relatively small. Further
studies using a larger sample size and a prospective approach orpropensity score matching are required.
In conclusion, the preoperative CAR is a poor prognostic factor
in patients with resectable PDAC. CAR can be simply calculatedusing preoperative serum CRP and albumin and reflects local
inflammation caused by invasion of PDAC.

COMPETING INTERESTS
The authors declare that they have no competing interests

ACKNOWLEDGEMENTS
We thank H. Nikki March, PhD, from Edanz Group (https://
en-author-services.edanzgroup.com/ac) for editing a draft of thismanuscript.

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