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Abstract

Objective

Sinonasal squamous cell carcinoma usually presents at an advanced stage at the time of diagnosis, and there is still a lack of indicators to predict the prognosis of sinonasal squamous cell carcinoma patients. We aim to investigate whether the peripheral blood ratios may be good options for predicting the progression in patients with sinonasal squamous cell carcinoma.

Methods

We performed a retrospective analysis of 198 patients with sinonasal squamous cell carcinoma between January 2010 and December 2022. The systemic inflammatory response index, platelet/lymphocyte ratio, neutrophil/lymphocyte ratio, and lymphocyte/monocyte ratio were calculated. We examined the predictive value for the prognosis of sinonasal squamous cell carcinoma patients.

Results

The systemic inflammatory response index (1.21 vs. 0.79, P < 0.001), lymphocyte/monocyte ratio (3.51 vs. 5.01, P < 0.001), neutrophil/lymphocyte ratio (2.83 vs. 2.02, P < 0.001), and platelet/lymphocyte ratio (136.70 vs. 113.84, P = 0.0042) values were significantly different between T4 stage and T1-3 stage. Univariate analysis showed that using appropriate threshold values, systemic inflammatory response index (0.5), platelet/lymphocyte ratio (127.4), lymphocyte/monocyte ratio (4.9), and neutrophil/lymphocyte ratio (2.6) predicted overall survival, progression-free survival, and distant metastasis-free survival. Multivariate Cox regression showed that high lymphocyte/monocyte ratio was associated with poor prognosis.

Conclusions

The values of neutrophil/lymphocyte ratio, systemic inflammatory response index, lymphocyte/monocyte ratio, and platelet/lymphocyte ratio can be used as parameters for the prognosis of sinonasal squamous cell carcinoma. In sinonasal squamous cell carcinoma patients, lymphocyte/monocyte ratio is a sensitive factor in predicting overall survival and distant metastasis-free survival.

Keywords

Sinonasal squamous cell carcinoma neutrophil/lymphocyte ratio systemic inflammatory response index monocyte/lymphocyte ratio platelet/lymphocyte ratio

Introduction

Sinonasal squamous cell carcinoma (SNSCC) is the most common histological subtype of all sinonasal tumors, accounting for 50%–80% of cases.¹ It is a rare head and neck tumor, accounting for only about 3% of head and neck malignancies.² Early specific symptoms of the disease are relatively absent, given the anatomy of the nasal cavity and paranasal sinuses, patients usually present at an advanced stage by the time of diagnosis.³

Furthermore, despite the improvement in the treatment of SNSCC, the five-year overall survival (OS) rate has not significantly improved over the past 50 years. Still, it lingers at 30%–50%, with local recurrence being the leading cause of death.⁴ Moreover, locally advanced SNSCC is highly invasive to surrounding tissues.⁵ Due to the rare pattern of occurrence of SNSCC, those factors considered predictive of SNSCC prognosis have only been tested in a limited number of patients.⁶ There is still a lack of specific prognostic markers to stratify patients by risk level, which could guide more aggressive treatment regimens and more frequent clinical follow-ups for high-risk patients to improve the prognosis of SNSCC patients.

Cancer-related inflammation is the seventh most important feature of cancer and is thought to contribute to the development of tumors.⁷ It plays a crucial role in cancer occurrence, progression, and response to treatment by coordinating the tumor microenvironment and thereby influencing the proliferation and migration of tumor cells.⁸ This inflammatory response is caused by inflammatory cells and inflammatory factors that travel into the peripheral blood and cause changes in neutrophils, lymphocytes, monocytes, and platelets in the peripheral blood.⁹ In recent years, many prognostic indicators such as the systemic inflammatory response index (SIRI), platelet/lymphocyte ratio (PLR), neutrophil/lymphocyte ratio (NLR), and lymphocyte/monocyte ratio (LMR) have been formulated. They are considered independent prognostic markers for various cancers.^10–12 With further investigation of these indicators, some are also regarded as helpful in diagnosing early stage tumors.¹³

Turri-Zanoni et al.¹⁴ suggested that high pretreatment NLR and PLR were associated with poor prognosis in SNSCC. A high level of NLR was also suggested to be significantly associated with poorer OS rates in the predictive model of SNSCC by Brkic et al.¹⁵ All the above studies investigated the value of NLR in small samples of SNSCC. No studies have compared multiple hematocrit ratios on the prognosis of SNSCC. This article explores this question in a single-center retrospective study and aims to discover the predictive value of the prognosis in SNSCC. This study is available as a preprint on webside.¹⁶

Materials and methods

Patient selection

Patients histopathologically diagnosed with SNSCC and treated at the Eye, Ear, Nose, and Throat Hospital, Fudan University, China, from January 2010 to December 2022, were analyzed and staged according to the eighth edition of TNM – American Joint Committee on Cancer.¹⁷ Individuals having a second primary or metastatic tumor were disqualified. The study did not include those who had autoimmune illnesses or had recently had steroid therapy. Individuals with acute or chronic inflammatory diseases (such as hepatitis B/C virus, gastritis, or nephritis) were also excluded. Exclusion criteria also included having a history of using antipsychotic medications, having a hematological illness, or having received treatment for one within the year before starting therapy. The patients in this study were selected consecutively from our institutional database based on the eligibility criteria. Eventually, a total of 198 patients were enrolled in this study. As a retrospective study, informed consent was not required. Ethical approval was obtained from the Research Ethics Committee of Eye & ENT Hospital, Fudan University, on 21 January 2021 (2021015). All patient data have been fully de-identified. All the study procedures were performed in accordance with the Declaration of Helsinki (1975, as revised in 2024).

Data collection

We collect absolute numbers of neutrophils (N), monocytes (M), platelets (P), and lymphocytes (L) at initial diagnosis. SIRI is defined as (N × M)/L, NLR as N/L, LMR as L/M, and PLR as P/L. Each patient recruited in the study must have comprehensive clinics, hematological examination, imaging findings, and follow-up information, and blood must be drawn from them within a week before the commencement of medication. All patients were followed up every 3 months for the first 2 years for time to disease progression and death, and every 6 months after that until death.

OS was defined as the period from the start of treatment to death from any cause. Progression-free survival (PFS) was defined as the period from the start of treatment to the first incidence of progression, relapse after response, or death from any cause. The period from the start of treatment to distant metastases or death from any cause was defined as distant-metastasis-free survival (DMFS).

Statistical analysis

Statistical analyses were performed using R software (version 3.5.0, Bell Laboratories), X-tile (Yale, USA), and MedCalc. Continuous variables were presented as mean ± SD. The Wilcoxon test was used to assess the statistical significance of the inflammatory factor levels between different groups. The receiver operating characteristic (ROC) curve was plotted to evaluate the inflammatory factor for diagnosis. Kaplan-Meier analysis was used to determine OS, PFS, and DMFS. Cox proportional hazards regression analysis calculated the hazard ratio (HR), confidence intervals (CIs), and P-values. A time-dependent ROC curve was plotted to evaluate the inflammatory factor for prognosis. Two-tailed P < 0.05 was statistically significant for the tests.

The study has been reported in accordance with the relevant Equator Network guidelines.¹⁸

Results

Patient characteristics

Table 1 summarizes the basic characteristics of patients with SNSCC. The median age at presentation was 57 (21–84). There were 59 females and 139 males. Thirty-five patients (35/198, 17. 7%) had a clinically positive lymph node. Most patients (153/198, 77.3%) were in stage IV. The most involved site was the nasal cavity (118/198, 59. 6%), followed by the maxillary sinus (68/198, 34.3%) and ethmoid sinus (12/198, 6.1%). 64.1% (127/198) and 20.2% (40/198) had evidence of orbital invasion and brain invasion. A total of 147 patients (147/198, 74.2%) received IMRT/VMAT, and 51 (51/200, 25.8%) received 3D-CRT. According to the timing of RT, post-operation chemoradiotherapy (S + CRT), pre-operation chemoradiotherapy (CRT + S), and definitive chemoradiotherapy (CRT) were administered in 130 (130/198, 65.7%), 42(42/198, 21.2%), and 26 (26/198, 13.1%) cases.

Table 1.

The clinicopathological features of patients.

Characteristics	Number of cases	Percentage
Age
<60	111	56. 1%
≥ 60	87	43.9%
Sex
Female	59	29.8%
Male	139	70.2%
Tumor site
Nasal cavity	118	59. 6%
Maxillary sinus	68	34.3%
Ethmoid sinus	12	6.1%
T stage
T1-3	46	23. 2%
T4	152	76.8%
N status
N-negative	163	82.3%
N-positive	35	17. 7%
Clinical stage
Stage I and II	10	5.0%
Stage III	35	17. 7%
Stage IV	153	77.3%
Orbit invasion
No	71	35. 9%
Yes	127	64.1%
Brain invasion
No	158	79. 8%
Yes	40	20.2%
RT technique
3D-CRT	51	25. 8%
IMRT	134	67. 7%
VMAT	13	6.5%
Treatment mode
CRT + S	42	21.2%
S + CRT	130	65. 7%
CRT	26	13.1%
Surgery type
Endoscopic S	134	80.2%
Open S	34	19.8%

RT: radiotherapy; 3D-CRT: three-dimensional conformal radiotherapy; IMRT: intensity modulated radiotherapy; VMAT: volumetric modulated arc radiotherapy; CRT: chemoradiotherapy; S: surgery.

The median values for SIRI, LMR, NLR, and PLR were 1.059 (range, 0.035–10.244), 3.665 (range, 0.611–13.48), 2.673 (range, 0.139–12.647), and 130.898 (range, 3.303–361.176) in SNSCC patients. Further analysis revealed that patients with SNSCC who were more locally aggressive (T4) compared to those who were less locally aggressive (T1-3) had different SIRI (1.21 vs. 0.79, P < 0.001), LMR (3.51 vs. 5.01, P < 0.001), NLR (2.83 vs. 2.02, P < 0.001), and PLR (136.70 vs. 113.84, P = 0.0042) values (Figure 1). There was no significant difference in levels of SIRI (1.21 vs. 0.79, P = 0.44), LMR (3.51 vs. 5.01, P = 0.94), NLR (2.83 vs. 2.02, P = 0.94), and PLR (136.70 vs. 113.84, P = 0.84) values between the lymph node-positive group and the lymph node-negative group.

Figure 1.

Differences in four peripheral blood indicators between SNSCC patients with more locally aggressive (T4) and less aggressive (T1-3). SNSCC: sinonasal squamous cell carcinoma.

Serum levels of cut-off to determine the prognosis

Using X-tile, we employed OS as an endpoint in SNSCC patients to establish the ideal SIRI, NLR, PLR, and LMR cut-off values. Patients were classified into two groups based on the SIRI cut-off value of 0.5. There was a significant difference in five-year OS (49.0% vs. 79.4%, P = 0.0064) (Figure 2A1) and DMFS (48.5% vs. 77.6%, P = 0.021) between the different levels of SIRI (Figure 2C1). Still, there was no statistically significant difference in five-year PFS (47.7% vs. 68.5%, P = 0.066) (Figure 2B1). Patients were separated into groups based on the best NLR cut-off value of 2.6. There were statistically significant differences in five-year OS (42.2% vs. 65.8%, P = 0.003) (Figure 2A2), PFS (40.2% vs. 63.0%, P = 0.013) (Figure 2B2) between the high and low levels of NLR, and DMFS (41.0% vs. 65.4%, P = 0.0048) (Figure 2C2) between the two groups. The patients were allocated to two categories using a PLR cut-off value of 127.4. Five-year OS (47.0% vs. 62.0%, P = 0.016) and DMFS (46.6% vs. 60.9%, P = 0.031) of the two levels of PLR differed statistically (Figure 2A3 and C3). Patients with values of LMR < 4.9 had better five-year OS (80.5% vs. 41.8%, P < 0.001) (Figure 2A4), PFS (75.7% vs. 41.0%, P = 0.0018) (Figure 2B4), DMFS (81.2% vs. 40.7%, P < 0.001) (Figure 2C4) than those with LMR ≥ 4.9.

Figure 2.

Comparison of the differences in OS (A1, A2, and A3), PFS (B1, B2, and B3), and DMFS (C1, C2, and C3) rates between the two groups of patients differentiated by the best cut-off values of each of the four peripheral blood indices. OS: overall survival; PFS: progression-free survival; DMFS: distant metastasis-free survival.

Multivariate analysis of serum levels for prognosis

In multivariate Cox regression, LMR was identified as an independent predictor factor for OS (P = 0.033) and DMFS (P = 0.017) in SNSCC patients (Table 2). We plotted ROC curves to compare the predictive value of several blood ratios for the prognosis of SNSCC patients. We found that although several blood ratios predicted both OS and DMFS in patients. The area under the curve (AUC) indicated the predictive ability. LMR (AUC = 0.723) had a higher predictive value for OS than SIRI (AUC = 0.678), NLR (AUC = 0.639), PLR (AUC = 0.612) (Figure 3A); similarly, LMR (AUC = 0.715) was also more predictive of DMFS in patients than SIRI (AUC = 0.649), NLR (AUC = 0.636), and PLR (AUC = 0.596) (Figure 3B).

Figure 3.

Comparison of the predictive values of LMR (OS: AUC = 0.723; DMFS: AUC = 0.715), NLR (OS: AUC = 0.639; DMFS: AUC = 0.636), SIRI (OS: AUC = 0.678; DMFS: AUC = 0.649), and PLR (OS: AUC = 0.612; DMFS: AUC = 0.596) for OS (A) and DMFS (B) in patients with SNSCC: LMR had a higher predictive power. LMR: lymphocyte/monocyte ratio; OS: overall survival; AUC: area under curve; DMFS: distant metastasis-free survival; NLR: neutrophil/lymphocyte ratio; SIRI: systemic inflammatory response index; PLR: platelet/lymphocyte ratio; SNSCC: sinonasal squamous cell carcinoma.

Table 2.

Multivariate Cox regression analysis for OS and DMFS in patients.

Variables	OS		DMFS
Variables	HR (95% CI)	P value	HR (95% CI)	P value
Age group (years)
< 60	Reference		Reference
≥ 60	1.12 (0.71–1.8)	0.630	1.01 (0.64–1.6)	0.951
Sex
Female	Reference		Reference
Male	0.62 (0.37–1.0)	0.062	0.66 (0.40–1.1)	0.098
T stage
T1-3	Reference		Reference
T4	1.46 (0.77–2.8)	0.247	1.28 (0.68–2.4)	0.443
SIRI
≥ 0.5	Reference		Reference
< 0.5	0.53 (0.22–1.3)	0.161	0.69 (0.30–1.6)	0.397
PLR
≥ 127.4	Reference		Reference
< 127.4	0.81 (0.48–1.4)	0.413	0.85 (0.51–1.4)	0.527
NLR
≥ 2.6	Reference		Reference
< 2.6	0.88 (0.51–1.5)	0.631	0.87 (0.51–1.5)	0.599
LMR
≥ 4.9	Reference		Reference
< 4.9	2.27 (1.07–4.8)	0.033	2.52 (1.18–5.4)	0.017

OS: overall survival; DMFS: distant metastasis-free survival; HR: hazard ratio; CI: confidence intervals; LMR: monocyte/lymphocyte ratio; NLR: neutrophil/lymphocyte ratio; SIRI: systemic inflammatory response index; PLR: platelet/lymphocyte ratio.

Discussion

The detection of the peripheral blood ratio is convenient, affordable, and repeatable. It reflects tumor-related inflammation in various tumors and is related to tumor prognosis.^9,19 Among several blood ratios (NLR, SIRI, LMR, and PLR), absolute neutrophil count, lymphocyte count, monocyte count, and platelet count in peripheral blood are included. Neutrophils can release angiogenesis factors and cell chemotactic factors, play a role in tumor angiogenesis,²⁰ and contribute to the formation of the immune microenvironment.²¹ Lymphocytes are a protective prognostic factor for cancer. The decrease of lymphocytes can lead to increased secretion of lymphocyte-related immune factors in peripheral blood circulation, thus inhibiting tumor cell proliferation and metastasis.²² It has been shown that monocytes can differentiate into macrophages and circulating monocytes in tumors, among which macrophages may affect tumor angiogenesis and promote tumor growth, invasion, and migration.²³ Like neutrophils, platelets also contribute to the formation of a tumor microenvironment by releasing platelet-derived epidermal growth factors and cytochemokines that promote cancer-related inflammation.²⁴

X-tile is a bioinformatics tool that identifies the most statistically significant cutoff-point by calculating log-rank χ² values across all divisions and selecting the threshold that yields the highest χ² and lowest P-value, reflecting the most robust prognostic stratification. Our study utilized X-tile software to determine the optimal cut-off value for SIRI, NLR, PLR, and LMR levels based on their association with OS, PFS, and DMFS. In some earlier reports, the cut-off values for NLR and PLR in SNSCC were similar to our results.^14,25

Tumor-related inflammation plays a vital role in the occurrence and development of tumors. Wu et al. demonstrated that chronic rhinosinusitis was associated with a greater risk of developing paranasal sinus malignancy.²⁶ NLR is the ratio of absolute neutrophil count to absolute lymphocyte count (L), and a high NLR value can be caused by an increase in neutrophil count or a decrease in lymphocyte count. An increase in neutrophil count indicates a stronger tumor-related inflammatory response. In comparison, the low lymphocyte count value indicates that the tumor-related toxic immune response was not strong in the early stage of the tumor. Several previous studies have used NLR as a prognostic factor for various tumors,^27,28 and studies on SNSCC have also shown that high NLR indicates a poor prognosis of tumors.^14,15 The peripheral blood ratio is more stable than a single blood cell count since it incorporates the absolute values of several blood cell counts. It can better reflect the balance of tumor-related inflammation and patients’ immunity. The poor five-year OS, PFS, and DMFS were seen in our research for SNSCC patients with greater SIRI, NLR, and lower LMR. Higher PLR values in patients were associated with worse five-year OS and DMFS but not PFS. The predictive value of LMR was higher than that of the other three blood ratios, and they all had predictive values for five-year OS and DMFS. In multivariate analysis, LMR was also considered an independent prognostic factor for five-year OS and DMFS in SNSCC patients. LMR, which measures the ratio of lymphocytes to monocytes, shows that a decline in lymphocytes indicates a poorer immune response to the tumor.

In contrast, monocyte elevation indicates increased components promoting tumor growth and invasion.²⁹ In other words, a low LMR value implies that the body is in an immune balance that promotes tumor growth. There hasn’t been any research that compares the predictive usefulness of four blood ratios in SNSCC or one that uses LMR to forecast patients’ prognoses for the disease. Our investigation only filled this gap.

Calculating multiple hematological ratios of conventional blood parameters and comparing them with thresholds may provide clues to the prognosis of SNSCC patients. Higher SIRI and NLR values or lower LMR values may indicate a poorer prognosis for SNSCC patients. For these patients, it is recommended to adopt a more intensive treatment regimen to achieve better treatment outcomes.

Limitation

Our research had limitations due to the single-center retrospective investigation. Firstly, patient characteristics were necessarily biased since our analysis used retrospective data from a single location. Second, the patients in the research received various treatments owing to the long follow-up period and the absence of unambiguous and consistent recommendations for the optimum treatment modality for SNSCC, which might affect the statistical outcomes. Lastly, individuals with acute and chronic inflammation were not included, and the changes in blood ratio in these patients were not further investigated. Notwithstanding these drawbacks, we offer comprehensive research on SNSCC patients, from which we were able to extract hematological indicators indicative of prognosis and diagnosis. Prospective studies with more centers are also expected to validate and refine our results.

Conclusion

SNSCC is a rare disease arising from the nasal cavity or the paranasal sinuses. Because of its rarity, few studies have focused on the prognostic factors. Peripheral blood ratios are data that can be calculated through simple routine blood tests, and their predictive value in SNSCC has not yet been reported. Our study investigated the feasibility of peripheral blood ratios (including SIRI, LMR, NLR, and PLR) in predicting long-term survival in SNSCC. In conclusion, NLR, SIRI, LMR, and PLR values can be used as prognostic parameters in SNSCC. In SNSCC patients, LMR was a sensitive predictor of OS and DMFS.

Footnotes

Acknowledgements

We sincerely thank all the patients and investigators involved in this study.

ORCID iDs

Tian Wang

Li Wang

Ethical consideration

This study is a retrospective study and complies with the guidelines for human studies. We used the actual and real clinical data to do the analysis. This paper did not involve clinical trials. The Institutional Ethics Committee of the Eye & ENT Hospital of Fudan University approved this study on 21 January 2021 (2021015). As a retrospective study, informed consent was not required.

Authors’ contributions

Tian Wang: study concept and design; acquisition of data; analysis and interpretation of data; writing–initial draft. Qi Zhang: study concept and design, editing draft, technical support. Li Wang and Jie Wang: acquisition of data. Keqing Zhao: manuscript revision and study supervision. Xinmao Song: study concept and design; acquisition of data; analysis and interpretation of data; editing draft; statistical analysis; and study supervision.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data availability statement

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

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Prognostic impact of peripheral blood ratio in sinonasal squamous cell carcinoma

Abstract

Objective

Methods

Results

Conclusions

Keywords

Introduction

Materials and methods

Patient selection

Data collection

Statistical analysis

Results

Patient characteristics

Serum levels of cut-off to determine the prognosis

Multivariate analysis of serum levels for prognosis

Discussion

Limitation

Conclusion

Footnotes

Acknowledgements

ORCID iDs

Ethical consideration

Authors’ contributions

Funding

Declaration of conflicting interests

Data availability statement

References