Clinical significance of peripheral blood inflammatory cells and fibrinogen in prostate cancer and prognosis

doi:10.21203/rs.3.rs-4672214/v1

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Clinical significance of peripheral blood inflammatory cells and fibrinogen in prostate cancer and prognosis

https://doi.org/10.21203/rs.3.rs-4672214/v1

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Objective: To explore the relationship between peripheral blood inflammatory cells and fibrinogen and the clinicopathological characteristics of the prostate, and to assess their clinical value in evaluating prostate cancer.

Methods: A retrospective analysis was conducted on the clinicopathological data of 429 patients who underwent prostate biopsies at the Second Hospital of Tianjin Medical University between June 2020 and December 2022. The levels of neutrophils, lymphocytes, monocytes, platelets, and plasma fibrinogen in peripheral blood before surgery in patients with prostate cancer and benign prostatic hyperplasia were analyzed. Further comparisons were made between the levels of inflammatory cells and fibrinogen in peripheral blood in patients with prostate cancer at different stages, different Gleason scores, and with or without bone metastases.

Results: The levels of inflammatory cells and fibrinogen in preoperative prostate cancer patients showed statistically significant differences compared to those with benign prostatic hyperplasia (P<0.05). Specifically, fibrinogen levels were significantly elevated in patients with stage 4 prostate cancer (4.13±1.40 g/L), Gleason scores of 9-10 (5.12±1.20 g/L), and bone metastases (4.11±1.48 g/L) (P<0.001). Fibrinogen levels exhibited a positive correlation with prostate pathology results, cancer stage, Gleason score, presence of bone metastases, and PSA levels (P<0.001).

Conclusions: The levels of preoperative peripheral inflammatory cells and fibrinogen are closely linked to prostate pathology outcomes. Moreover, the level of fibrinogen demonstrates potential as a prognostic indicator for disease progression and prognosis in prostate cancer patients.

Prostate cancer

Neutrophils

Lymphocytes

Fibrinogen

Disease progression

In recent years, the advent of “liquid biopsy” has redirected focus towards serological testing, aiming to identify non-invasive markers crucial for prostate cancer (PCa) diagnosis. While prostate-specific antigen (PSA) is a recognized diagnostic marker for prostate cancer, its diagnostic efficacy is limited. Studies have revealed that 54% of patients are diagnosed with prostate cancer at an advanced stage involving distant metastases, resulting in a low 5-year survival rate of only 30%^[1]. Thus, the identification of predictive markers for the onset and progression of prostate cancer holds significant clinical and research value for guiding clinical decision-making in the management and follow-up treatment of prostate cancer patients.

Research has identified inflammation as a potential risk factor associated with cancer, including its role in prostate cancer onset and progression^[2–5]. The ratios of neutrophil to lymphocyte (NLR) and platelet to lymphocyte (PLR) in peripheral blood have prognostic significance across various malignancies, and the lymphocyte to monocyte ratio (LMR) aids in distinguishing prostate cancer from benign prostatic hyperplasia (BPH).Furthermore, during tumor development, alterations in coagulation function are observed in patients. For instance, there is a significant elevation in fibrinogen (FIB) and platelets (PLT) levels in patients with malignant tumors, which are closely associated with tumor occurrence and progression^[6–7].

This study aims to investigate the relationship between preoperative levels of peripheral blood inflammatory cells and plasma fibrinogen and the pathological characteristics of prostate cancer, with a focus on their potential implications in disease progression.

Patient Population

A total of 429 patients treated at the Second Hospital of Tianjin Medical University between June 2020 and December 2022 underwent ultrasound-guided transperineal prostate biopsy. The patients were aged 45 to 97 years, with an average age of (74.61 ± 8.05) years.Prior to the prostate biopsy, all patients underwent routine blood tests, coagulation assessments, and PSA screenings. Additionally, patients had complete clinical pathological data with no history of prior use of 5α reductase inhibitors, prostate surgery, primary malignant tumors, anticoagulation therapy, hematologic diseases, severe cardiovascular or cerebrovascular conditions, autoimmune disorders, liver diseases, history of radiotherapy, chemotherapy, or endocrine treatments. All patients underwent prostate biopsy and subsequent histopathologic examinations. The study adhered to the ethical guidelines outlined in the Declaration of Helsinki (revised in 2013) and was approved by the Ethics Review Committee of the Second Hospital of Tianjin Medical University.

Detection Method

Venous blood samples were collected from patients on the morning of the second day after admission. The blood samples were divided into three test tubes for different analyses. PSA levels were measured using chemiluminescence immunoassay from the first test tube, fibrinogen levels were determined using the FIB detection kit by automatic coagulation analyzer from the second test tube, and NLR, PLR, and LMR were calculated from the third test tube using a Beckman Coulter LH750 blood cell analyzer. Prior to prostate biopsy, patients underwent a clean enema, and during the procedure, patients were positioned lithotomically, and the perineal skin was disinfected and anesthetized with 2% lidocaine. Prostate tissue was targeted and systematically biopsied, with samples placed in formalin solution for histopathological diagnosis by two senior pathologists in the Department of Pathology.

Statistical Analysis

Statistical analysis was performed using SPSS 25.0 software. Measurement data were assessed for normality, and normally distributed data were represented as (± s) and analyzed using a t-test for two independent samples. Non-normally distributed data were represented as M (Q25, Q75) and analyzed using the nonparametric Mann-Whitney U test. Enumeration data were expressed as rates (%), with inter-group rate comparisons conducted using the chi-square test and Fisher’s exact test. Pearson correlation analysis was employed, with a significance level set at P < 0.05.

1. General Clinical Data and Blood Marker Levels of the Two Groups

A total of 429 patients were analyzed between June 2020 and December 2022, with 322 (75.06%) diagnosed with PCa and 107 (24.94%) with BPH. Among PCa patients, 63 (19.57%) had bone metastases while 259 (80.43%) did not. The distribution of T2, T3, and T4 stages were 211 (65.63%), 53 (16.46%), and 58 (18.01%) patients, respectively. Significant differences were observed between the PCa and BPH groups in various markers: PSA (P<0.001), fibrinogen (P<0.001), lymphocyte (P<0.001), monocyte (P = 0.043), neutrophil (P<0.001), platelet (P<0.001), NLR (P<0.001), PLR (P<0.001), and LMR (P<0.001). Notably, the LMR was lower in the PCa group compared to the BPH group. No statistically significant difference was found in hemoglobin levels between the two groups (P = 0.203). (Table 1)

Table 1

Comparison of blood markers between benign prostatic hyperplasia and prostate cancer
	BPH(n = 107)	Pca(n = 322)	t	p value
PSA,ng/ml	13.12 ± 15.57	42.11 ± 70.97	4.19	<0.001
Fibrinogen,g/L	3.07 ± 0.88	3.44 ± 1.25	2.823	<0.001
Lymphocyte,109/L	1.87 ± 0.42	1.72 ± 0.62	1.084	<0.001
Monocyte,109/L	0.35 ± 0.17	0.48 ± 0.20	5.746	0.043
Neutrophi,109/L	3.83 ± 1.09	4.59 ± 1.99	3.752	<0.001
Platelet,109/L	203.99 ± 39.80	222.70 ± 56.83	3.157	<0.001
NLR	2.20 ± 0.99	3.11 ± 2.37	2.168	<0.001
PLR	115.88 ± 39.92	146.43 ± 71.60	1.655	<0.001
LMR	7.04 ± 4.31	4.23 ± 2.66	5.816	<0.001
Hemoglobin,g/L	144.05 ± 14.88	144.52 ± 16.47	0.263	0.203

2. Relationship Between Blood Markers in Patients with PCa with or without Bone Metastases

Of the 259 patients with bone metastases, the majority (74.13%) were in T2 stage, while 37 (14.29%) and 30 (11.58%) were in T3 and T4 stages, respectively. Analysis revealed that patients with bone metastases had higher levels of PSA (P<0.001), fibrinogen (P<0.001), monocytes (P<0.001), neutrophils (P = 0.002), NLR (P<0.001), and PLR (P<0.001) compared to those without bone metastases. Additionally, hemoglobin levels were lower in patients with bone metastases (P = 0.002). There were no significant differences in lymphocyte (P = 0.9), platelet (P = 0.598), and LMR (P = 0.423) between the two groups. (Table 2)

Table 2

Comparison of blood markers between patients with or without bone metastases for prostate cancer
	Non-bone metastases(n = 259)	Bone metastases(n = 63)	t	p value
PSA,ng/ml	31.70 ± 32.45	84.93 ± 139.20	5.585	<0.001
Fibrinogen,g/L	3.28 ± 1.13	4.11 ± 1.48	4.91	<0.001
Lymphocyte,109/L	1.78 ± 0.60	1.51 ± 0.63	3.18	0.9
Monocyte,109/L	0.44 ± 0.18	0.61 ± 0.24	6.174	<0.001
Neutrophi,109/L	4.38 ± 1.66	5.47 ± 2.83	4.016	0.002
Platelet,109/L	218.85 ± 55.41	238.52 ± 60.23	2.484	0.598
NLR	2.80 ± 1.77	4.40 ± 3.73	5.012	<0.001
PLR	136.58 ± 60.02	186.91 ± 97.35	5.203	<0.001
LMR	4.57 ± 2.76	2.86 ± 1.55	4.719	0.423
Hemoglobin,g/L	145.68 ± 14.65	139.76 ± 21.96	2.579	0.002
Stage(%)
T2	192(91.00)	19(9.00)		<0.001
T3	37(69.81)	16(30.19)
T4	30(51.72)	28(48.28)
Gleason(%)				<0.001
≤7	114(44.01)	3(4.76)
8	108(41.70)	37(58.73)
≥9	37(14.29)	23(36.51)

3. Relationship Between Blood Markers in Different Clinical Phases in Patients with PCa

Among patients with different stages (T2, T3, T4), significant variations were observed. Patients in T4 stage exhibited higher levels of PSA (P<0.001), fibrinogen (P<0.001), monocytes (P<0.001), and platelets (P = 0.045) but lower levels of LMR (P<0.001). No significant differences were found in lymphocyte (P = 0.272), neutrophil (P = 0.359), NLR (P = 0.445), PLR (P = 0.168), and hemoglobin (P = 0.468) levels across the three groups. (Table 3)

Table 3

Comparison of blood markers in prostate cancer patients with different clinical stages
	T2(n = 211)	T3(n = 53)	T4(n = 58)	p value
PSA,ng/ml	31.50 ± 36.43	49.36 ± 41.55	74.09 ± 142.81	<0.001
Fibrinogen,g/L	3.23 ± 1.16	3.55 ± 1.12	4.13 ± 1.40	<0.001
Lymphocyte,109/L	1.75 ± 0.63	1.74 ± 0.68	1.61 ± 0.47	0.272
Monocyte,109/L	0.44 ± 0.18	0.46 ± 0.18	0.61 ± 0.25	<0.001
Neutrophi,109/L	4.48 ± 1.87	4.72 ± 2.67	4.88 ± 1.67	0.359
Platelet,109/L	216.99 ± 57.12	233.34 ± 56.81	233.78 ± 53.58	0.045
NLR	2.99 ± 2.10	3.40 ± 3.69	3.28 ± 1.65	0.445
PLR	141.01 ± 72.78	158.56 ± 86.07	155.04 ± 47.67	0.168
LMR	4.57 ± 2.91	4.17 ± 2.19	3.09 ± 1.53	<0.001
Hemoglobin,g/L	145.18 ± 15.86	144.43 ± 17.40	142.17 ± 17.81	0.468
Bone metastases(%)				<0.001
Yes	19(9.00)	16(30.19)	28(48.28)
No	192(91.00)	37(69.81)	30(51.72)
Gleason(%)				<0.001
≤7	103(48.82)	11(20.75)	3(5.17)
8	84(39.81)	31(58.50)	30(51.72)
≥9	24(11.37)	11(20.75)	25(43.11)

4. Relationship of Blood Markers Between Different Gleason Scores in PCa Patients

Patients with Gleason scores ≤ 7, 8, and ≥ 9 were analyzed for markers’ variations. Patients with Gleason scores ≥ 9 exhibited significantly higher levels of PSA, fibrinogen, monocytes, neutrophils, platelets, NLR, and PLR but lower levels of LMR and hemoglobin. No statistically significant difference was found in lymphocyte levels among the groups. (Table 4)

Table 4

Comparison of blood markers in prostate cancer patients with different Gleason scores
	Gleason 6 and 7(n = 117)	Gleason 8(n = 145)	Gleason 9 and 10(n = 60)	p value
PSA,ng/ml	18.71 ± 20.72	51.95 ± 97.77	64.00 ± 37.67	<0.001
Fibrinogen,g/L	2.86 ± 0.65	3.21 ± 1.02	5.12 ± 1.20	<0.001
Lymphocyte,109/L	1.83 ± 0.66	1.66 ± 0.61	1.67 ± 0.50	0.065
Monocyte,109/L	0.38 ± 0.11	0.44 ± 0.17	0.77 ± 0.16	<0.001
Neutrophi,109/L	4.06 ± 1.65	4.45 ± 2.17	5.96 ± 1.46	<0.001
Platelet,109/L	205.09 ± 47.84	216.14 ± 56.78	272.90 ± 43.80	<0.001
NLR	2.55 ± 1.72	3.18 ± 2.77	4.06 ± 2.08	<0.001
PLR	126.59 ± 61.23	147.87 ± 72.64	181.63 ± 74.80	<0.001
LMR	5.13 ± 2.01	4.31 ± 3.15	2.31 ± 0.93	<0.001
Hemoglobin,g/L	148.29 ± 13.25	142.03 ± 18.01	14.18 ± 17.12	0.007
Stage(%)				<0.001
T2	103(88.03)	84(57.93)	24(40.00)
T3	11(9.41)	31(21.38)	11(18.33)
T4	3(2.56)	30(20.69)	25(41.67)
Bone metastases(%)				<0.001
Yes	3(2.56)	37(25.52)	23(38.33)
No	114(97.44)	108(74.48)	37(61.67)

5. Relationship Between Fibrinogen and Prostate Pathology and Grade

Among the blood markers studied, only fibrinogen showed a significant difference in levels between benign and malignant prostate conditions and across different grades of prostate cancer. Fibrinogen levels were higher in prostate cancer patients, particularly those with bone metastases, advanced clinical stages, and elevated Gleason scores. Correlation analysis indicated a positive association between plasma fibrinogen levels and pathology, clinical stage, bone metastasis, PSA, and Gleason score. The correlation coefficients (γ) were 0.135, 0.273, 0.265, 0.208, 0.545 (P < 0.001) respectively. Other blood markers did not effectively predict the degree of benign or malignant prostate or grade. (Table 5)

Table 5

Relationship between Fibrinogen and prostate pathology and grade
	Pathology		Clinical stage		Bone metastases		PSA		Gleason
	γ	p value	γ	p value	γ	p value	γ	p value	γ	p value
FIB	0.135	<0.001	0.273	<0.001	0.265	<0.001	0.208	<0.001	0.545	<0.001

Current studies suggest that the occurrence and development of tumors are linked to the inflammatory response and coagulation function of the body system^[8]. However, limited research has explored the correlation between inflammatory indicators, coagulation markers, and prostate pathology alongside the Gleason score^[9-10]. This study aims to investigate the relationship between inflammatory markers and coagulation markers and their impact on the diagnostic value and clinicopathological features of PCa biopsies by analyzing the blood markers of patients undergoing prostate biopsies. The objective is to offer a more comprehensive non-invasive clinical reference index for the diagnosis and treatment of PCa.

Neutrophils play a role in regulating tumor cell proliferation and metastasis through cytokines and chemokines within the microenvironment, with elevated levels serving as a predictor of poor prognosis in patients with malignant tumors^[11-12]. Monocytes, crucial immune cells, promote tumor proliferation and metastasis^[12]. Lymphocytes primarily function in the destruction and apoptosis of tumor cells, with decreased levels indicating reduced immunity to tumors^[13]. Neutrophil-to-Lymphocyte Ratio (NLR) is a widely used representative biomarker of systemic inflammation in the body. NLR can be calculated from a simple and cost-effective peripheral blood sample.Studies suggest that NLR and Lymphocyte-to-Monocyte Ratio (LMR) can holistically reflect the inflammation and immune status of cancer patients, holding prognostic value for various cancers like breast, gastric, and lung cancers, though consensus on their diagnostic utility for prostate cancer remains elusive^[14-20]. This study’s findings revealed significantly higher levels of neutrophils, monocytes, and NLR in the PCa group compared to the BPH group, while lymphocytes and LMR were lower, with statistically significant differences noted. Fibrinogen (FIB) is a key protein in the human coagulation process. FIB forms a protective fibrin barrier around tumor cells, providing a stable structural framework for the extracellular matrix and enhancing their resistance to endogenous immune mechanisms. This supports the role of cytokines such as vascular endothelial growth factor and fibroblast growth factor in the action on tumor cells, ultimately promoting tumor proliferation and angiogenesis^[21]. It has been reported that the lack of fibrinogen significantly reduces the spontaneous metastatic potential of invasive tumor cell lines^[22].Previous studies have shown that plasma FIB levels are independent prognostic factors for overall survival, cancer-specific survival, and progression-free survival in patients diagnosed with PCa^[23]. These findings collectively suggest a correlation between plasma FIB levels and the prognosis of PCa patients. However, the association between plasma FIB levels and clinical pathological features of PCa remains poorly understood.Our correlation analysis results demonstrate a positive association between preoperative FIB levels in prostate disease patients and features such as prostate pathology, cancer stage, Gleason score, bone metastasis, and PSA level, hinting at the possible involvement of FIB in prostate cancer development. Utilizing preoperative blood routine and plasma FIB could thus be a feasible, convenient, and economical approach to assess disease progression and prognosis in prostate cancer patients.

Numerous studies have highlighted alterations in the coagulation system of patients with tumors, with elevated peripheral fibrinogen levels correlating with poor prognostic features across various malignancies including upper tract urothelial carcinoma, colorectal, esophageal, gastric, ovarian, and liver cancers^[7,24-25]. The exact mechanism behind increased plasma FIB in tumor patients remains uncertain, but it is speculated that cancer cells can trigger platelet activation through the release of active substances once they enter the bloodstream^[26]. The relationship between peripheral blood FIB levels and prostate cancer has been minimally explored both domestically and internationally. Existing research mainly involves comparing FIB levels between healthy individuals or those with benign lesions and prostate cancer patients, revealing higher plasma FIB levels in tumor cases with a strong association with prostate cancer, suggesting a significant clinical role in its diagnosis^[23,27]. This study conducted an analysis of FIB levels among varying prostate pathologies and cancer grades, demonstrating higher FIB levels in patients with prostate cancer, advanced tumor stages, higher Gleason scores, and bone metastases, with statistically significant differences observed.

Nevertheless, this study has certain limitations, and the qualitative results obtained are constrained by the limited number of cases. To enhance the clinical relevance of this study, further case collection is imperative to determine meaningful cut-off values and evaluate sensitivity and specificity, aiming to establish a foundation for clinical diagnosis.

In summary, the levels of blood inflammatory cells and fibrinogen serve as valuable adjuncts in the pathological diagnosis of prostate conditions. Particularly, fibrinogen levels exhibit a high predictive capability in grading prostate cancer. Although the exact mechanism of this association remains unclear, our findings provide compelling evidence for further investigation.Our findings will aid clinical practitioners in accurately diagnosing prostate cancer, reducing unnecessary invasive surgeries, and alleviating economic burdens on patients.

Reporting Checklist: The authors have adhered to the STROBE reporting checklist.

Conflict of interest: All authors have disclosed their conflicts of interest following the ICMJE uniform disclosure form. They affirm no competing interests.

Ethics statement: The authors take responsibility for all aspects of this study, ensuring any concerns regarding accuracy or integrity are duly addressed. This study received approval from the Ethical Review Board of the Second Hospital of Tianjin Medical University and was carried out in compliance with the principles set forth in the Declaration of Helsinki (2013 revision). Informed consent was obtained from all participants involved in the study.

Funding

This article received support from the Talent Incubation Project of Tianjin Medical University Second Hospital (2023ZDSYS06), the 2022 Youth Fund Project of Tianjin Medical University Second Hospital (2022ydey18), the Central Guiding Local Science and Technology Development Funds for Technological Innovation Base Construction (22ZYJDSY00010), and the Clinical Research Project of the Scientific Research Fund of Tianjin Medical University Second Hospital (2019LC02).Natural Science Foundation of Tianjin (No. 21JCQNJC01790).Scientific and Technological Research Program of Tianjin Health Commission (No.TJWJ202021QN033).

Author Contribution

(I) Conception and design: W Zhang, Z Liu, Y Wang; (II) Administrative support: Z Liu, Y Wang; (III) Provision of study materials or patients: W Zhang, Y Ma, Z Liu, Y Wang; (IV) Collection and assembly of data: W Zhang, Y Ma, H Huang, Y Liu, Z Liu, Y Wang; (V) Data analysis and interpretation: W Zhang, Y Ma, H Huang, Y Liu, Z Liu, Y Wang; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Acknowledgments

We express our gratitude to the researchers and study participants for their invaluable contributions.

Data Availability

Data is provided within the manuscript or supplementary information files

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Clinical significance of peripheral blood inflammatory cells and fibrinogen in prostate cancer and prognosis

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Abstract

Introduction

Patients and Methods

Patient Population

Detection Method

Statistical Analysis

Results

1. General Clinical Data and Blood Marker Levels of the Two Groups

2. Relationship Between Blood Markers in Patients with PCa with or without Bone Metastases

3. Relationship Between Blood Markers in Different Clinical Phases in Patients with PCa

4. Relationship of Blood Markers Between Different Gleason Scores in PCa Patients

Discussion

Conclusions

Declarations

Funding

Author Contribution

Acknowledgments

Data Availability

References

Additional Declarations

Supplementary Files

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