The relationship between neutrophil-lymphocyte ratio and postoperative length of stay in carotid body tumor resection: a retrospective cohort study

doi:10.21203/rs.3.rs-1600711/v1

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The relationship between neutrophil-lymphocyte ratio and postoperative length of stay in carotid body tumor resection: a retrospective cohort study

https://doi.org/10.21203/rs.3.rs-1600711/v1

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Background

Neutrophil-lymphocyte ratio (NLR) is a significant indicator of inflammation, which is associated with adverse outcomes of various surgeries. The objective of this study was to investigate the relationship between NLR and postoperative length of stay(PLOS) in carotid body tumor(CBT) resection.

Methods

This retrospective observational study was performed of 231 patients undergoing CBT resection between November 2008 to December 2020. Univariate and multivariate analyses using logistic regression models were conducted to confirm NLR as the independent factor affecting PLOS in CBTs. Smooth curve fitting and stratified analysis were conducted to calculate effect index of NLR to PLOS.

Results

Medium PLOS group was larger than the other two groups(31.2% vs. 44.6% vs. 24.2%). The PLOS in patients with a low NLR was significantly smaller than that in patients with a high NLR(2.37 ± 2.41 vs. 2.67 ± 2.76 vs. 4.35 ± 5.91, p < 0.01). After adjusted other factors influenced PLOS, each additional 1 of NLR, the PLOS increased by increase 0.12days (0.12,(0.06, 0.18), p < 0.01). After adjusting all other variables, the associations of NLR and PLOS in Shamblin II had statistical significance(0.19 (0.09, 0.29), p < 0.01).

Conclusions

NLR as an indicator of inflammation, was a routinely collected but overlooked biomarker shows the relationship between inflammation and PLOS in patients suffered from CBT. Patients with a higher NLR had a longer PLOS.

Carotid body tumor

Neutrophil-to-lymphocyte ratio

Postoperative length of stay

Shamblin classification

Carotid body tumor (CBT) is a kind of slow-growing benign and rare tumor of the neck region, originated from paraganglion cells of carotid body[1]. Large CBT has high risk leading to symptoms of neck nerve and carotid artery compression, which has long been a critical cause of stroke[2]. Surgical resection was considered as the radical treatment of CBT[3, 4], which be made at the earliest possible stage was agreed by many researchers, usually followed by nerve injury, artery injury, and wound complications, due to its characteristic of tight adhesion with carotid artery and nerves[5]. Ali et al reported arterial injury usually occurred with nerve injury in CBT resections[6].

Inflammation was believed common in repair[7], in which immunocytes made a better neuronal regeneration and functional recovery after injury, but it can also induce secondary damage and inhibit post-injury nerve repair[8]. As a rapidly accessible and inexpensive marker, neutrophil-to-lymphocyte ratio (NLR) was considered as an indicator of inflammation[9, 10], especially correlated with systemic inflammation in sepsis[11], chronic obstructive pulmonary disease[12], and abdominal operations[13]. Neutrophilia and lymphocytopenia were physiological responses to systemic inflammation, which resulted in NLR increasing[14, 15], as a potential marker of unfavorable prognosis of many tumor and cardiovascular diseases[16–18]. Its caused transient side effects may leaded to transient nerve damage or delayed healing, both of which may prolong postoperative length of stay(PLOS)[19].

Because COVID-19 spreading and economic crisis, hospitals are under bigger pressure to reduce costs of insurance while improving quality of treatment, making economic pressure become a new influence of the decision and effects of medicine[20]. As the incidence of CBT is closely related to chronic hypoxia stimulation, most patients come from plateau areas[21–23], in which part medical standards and income levels are not good enough to solve these problems as developed cities. It has become a new point that researching on how to reduce PLOS, one of the most obvious factors affecting the resource consumed[24], concerned to decrease economic burden of patients and government[25, 26].

NLR is a significant indicator of inflammation, but no evidence of its function in CBT has been shown, to the best of our knowledge. The objective of this study was to investigate the relationship between NLR and postoperative length of stay in CBT resection, thereby providing evidence for choosing appropriate time of operation.

Patients

This is a retrospective observational study conducted at Department of Vascular Surgery of Changhai Hospital (Shanghai, China). From November 2008 to December 2020, a total of 231 patients admitted of CBT undergoing resection were non-selectively and consecutively included. Excluded were patients with no record information, no preoperative CTA result to insure Shamblin classification, or untreated with surgical operation, shown in Fig. 1. The study protocol complied with the Declaration of Helsinki and was approved by the Changhai Hospital Ethics Committee. Written consent was obtained from all patients for study inclusion.

Definitions

For each patient, the data were retrospectively collected through the electronic database of the hospital electronic medical record system. PLOS was recorded as a continuous variable but in univariate analysis it was divided into short(1to 3days), medium(4 to 5days), and long(more than 6days)groups as a categorical variable to analyze. Peripheral venous blood was taken and sent to the laboratory for blood routine examination at the admission in vascular department. NLR was the quotient of the neutrophils and lymphocytes.

Operational information was recorded in anesthesia note and operation note. Surgical interventions were CBT resection with vascular reconstruction or not, decided according to conditions like tumorous size and stiffness, and adhesion to carotid artery, during operation. Some patients underwent preoperative embolization.

Statistical analyses

Continuous variables were presented as mean ± standard deviation. Categorical variables were expressed in frequency and a percentage. χ2 (categorical variables), Student T test (normal distribution), and Student T test (skewed distribution) were used to test for differences among different PLOS groups. Univariate and multivariate linear regression were employed. Three models were constructed in this study to analyze the relationship of NLR and PLOS. In Model I, no covariates were adjusted. In Model II, only sociodemographic data was adjusted, included gender, age, stature, weight, BMI, systolic pressure, diastolic pressure, pulse pressure, Hypertension, Diabetes, CHD, Cerebral infarction, Drank, Smoke. In Model III, Model II and other covariates that influenced PLOS shown in Table 1 were adjusted, included operation method, embolization, shamblin classification. To address for nonlinearity of NLR and PLOS, a smooth curve fitting (penalized spline method) was conducted. According to different Shamblin classification, the relationship between NLR and PLOS of different models was analyzed. All the analyses were performed with the statistical software packages R(http://www.R-project.org, The R Foundation) and EmpowerStats(http://www.empowerstats.com, X&Y Solutions, Inc, Boston, MA). P values less than 0.05(two-sided) were considered statistically significant.

Table 1

Patient characteristic of CBT
	PLOS			P-value
	Short PLOS (n = 72)	Medium PLOS (n = 103)	Long PLOS (n = 56)	P-value
Patient characteristics
Gender				0.12
Female	43 (59.72%)	65 (63.11%)	26 (46.43%)
Male	29 (40.28%)	38 (36.89%)	30 (53.57%)
Age(year)	47.03 ± 12.58	41.01 ± 12.82	41.84 ± 12.12	< 0.01
Stature(cm)	163.24 ± 8.11	164.11 ± 7.02	165.19 ± 7.70	0.40
Weight(kg)	63.24 ± 10.33	61.56 ± 11.65	63.37 ± 11.04	0.50
BMI(kg/m²)	23.46 ± 3.42	22.78 ± 3.36	22.76 ± 3.01	0.39
PP(mmHg)	48.01 ± 9.81	44.22 ± 8.94	42.68 ± 8.70	< 0.01
Drank				0.27
No	71 (98.61%)	98 (95.15%)	52 (92.86%)
Yes	1 (1.39%)	5 (4.85%)	4 (7.14%)
Smoke				0.95
No	66 (91.67%)	93 (90.29%)	51 (91.07%)
Yes	6 (8.33%)	10 (9.71%)	5 (8.93%)
Comorbidities
Hypertension	12	10	5	0.28
Diabetes mellitus	0	6	3	0.12
CHD	0	3	0	0.15
Cerebral Infarction	2	1	2	0.51
Tumor characteristics
Operation side				0.52
Left	38 (52.78%)	59 (57.28%)	35 (62.50%)
Right	33 (45.83%)	44 (42.72%)	21 (37.50%)
Both	1 (1.39%)	0 (0.00%)	0 (0.00%)
Operational Time(minute)	130.86 ± 108.03	150.58 ± 63.05	197.51 ± 80.35	< 0.01
Operation method				< 0.01
Resection with No vascular reconstruction	69 (95.83%)	92 (89.32%)	40 (71.43%)
Resection with vascular reconstruction	3 (4.17%)	11 (10.68%)	16 (28.58%)
Embolization				0.37
No	67 (93.06%)	100 (97.09%)	52 (92.86%)
Yes	5 (6.94%)	3 (2.91%)	4 (7.14%)
Shamblin classification				0.03
I	12 (16.67%)	15 (14.56%)	3 (5.36%)
II	30 (41.67%)	49 (47.57%)	18 (32.14%)
III	30 (41.67%)	39 (37.86%)	35 (62.50%)
Data are presented as n (%) or mean ± standard deviation (SD) unless stated otherwise. PLOS = Postoperative length of stay; BMI = Body Mass Index, PP = Pulse pressure; CHD = Coronary heart disease.

Patient characteristic

Demographics and characteristics of 231 participants were shown in Table 1 according to short, medium, and long PLOS groups. Medium PLOS had the largest part(31.2% vs. 44.6% vs. 24.2%). Short PLOS had a larger average age compared to other groups(47.03 ± 12.58years vs. 41.01 ± 12.82years vs. 41.84 ± 12.12years, p < 0.01) and bigger pulse pressure(48.01 ± 9.81mmHg vs.44.22 ± 8.94mmHg vs. 42.68 ± 8.70mmHg, p < 0.01). Longer PLOS groups had a longer operational time(130.86 ± 108.03minutes vs. 150.58 ± 63.05minutes vs. 197.51 ± 80.35minutes, p < 0.01). PLOS showed almost no difference in patients underwent resection with no vascular reconstruction(69 vs. 92 vs. 40) while in vascular reconstruction more patients had a long PLOS(3 vs. 11 vs. 16, p < 0.01).In short PLOS part, Shamblin II and III both had 30 patients and 12 of Shamblin I(16.67% vs. 41.67% vs. 41.67%). In medium part of PLOS, Shamblin II is more than Shamblin I and III(14.56% vs. 47.57% vs. 37.86%). In long PLOS part, the main body is Shamblin III(n = 35, 62.50%).

Laboratory data

In Table 2 of laboratory Data, longer PLOS parts had a bigger WBC(6.24 ± 1.52*109/L vs. 6.82 ± 2.26*109/L vs. 7.63 ± 2.84*109/L, p < 0.01),but a smaller LYM(30.52 ± 8.66% vs. 30.78 ± 10.66% vs. 26.71 ± 11.47%, p = 0.04). Our results demonstrated that the NLR of patients with a short PLOS was significantly smaller than that in patients with a long PLOS(2.37 ± 2.41 vs. 2.67 ± 2.76 vs. 4.35 ± 5.91, p < 0.01). Hb also had a statistically significant difference(138.03 ± 34.00g/L vs. 127.67 ± 18.59g/L vs. 129.55 ± 18.98g/L, p = 0.02).

Table 2

Laboratory Data
	Short PLOS (n = 72)	Medium PLOS (n = 103)	Long PLOS (n = 56)	P-value
WBC(10⁹/L)	6.24 ± 1.52	6.82 ± 2.26	7.63 ± 2.84	< 0.01
LYM (%)	30.52 ± 8.66	30.78 ± 10.66	26.71 ± 11.47	0.04
NEUT (%)	58.80 ± 11.54	59.77 ± 11.66	63.51 ± 15.82	0.10
RBC(10¹²/L)	4.50 ± 0.64	4.40 ± 0.56	4.43 ± 0.49	0.52
Hb(g/L)	138.03 ± 34.00	127.67 ± 18.59	129.55 ± 18.98	0.02
Platelet(10⁹/L)	238.24 ± 59.34	234.36 ± 72.08	240.21 ± 82.54	0.87
DD (mg/L)	0.33 ± 0.17	0.40 ± 0.53	0.33 ± 0.35	0.48
TT(s)	16.22 ± 2.11	16.40 ± 1.35	16.61 ± 1.49	0.44
Fib(g/L)	3.26 ± 0.73	3.67 ± 2.55	3.98 ± 1.48	0.11
FDP(ug/mL)	2.42 ± 1.31	2.21 ± 2.10	2.19 ± 1.99	0.73
TG(mmol/L)	1.60 ± 1.36	1.15 ± 0.68	1.85 ± 3.91	0.18
HDL(mmol/L)	1.23 ± 0.31	2.72 ± 12.71	1.23 ± 0.39	0.53
LDL(mmol/L)	2.59 ± 0.76	2.39 ± 0.80	2.44 ± 0.58	0.33
NLR	2.37 ± 2.41	2.67 ± 2.76	4.35 ± 5.91	< 0.01
Data are presented as mean ± standard deviation (SD) unless stated otherwise. WBC = LYM = Lymphocyte, NEUT = Neutrophilic granulocyte, RBC = Red blood cell, Hb = Hemoglobin, DD = D-dimer, TT = thrombin time, Fib = Fibrinogen, FDP = Fibrinogen degradation products, TG = Triglyceride, HDL = High density lipoprotein, LDL = Low density lipoprotein, NLR = Neutrophil-lymphocyte ratio.

Univariate analysis related to PLOS

By univariate linear regression(Table 3), we found that NLR(0.13(0.07, 0.19), p < 0.01), non-operational approaches compared to traditional operation(1.42(0.75, 2.09), p < 0.01), and Shamblin III compared to Shamblin I(0.98(0.26, 1.71), p < 0.01) were positively correlated with PLOS.

Table 3

Univariate analysis
	Statistics	PLOS	P-value
Patient characteristics
Gender
Female	134 (58.01%)	0
Male	97 (41.99%)	0.47 (0.00, 0.94)	0.05
Age(year)	43.09 ± 12.81	-0.02 (-0.03, 0.00)	0.08
BMI(kg/m²)	22.99 ± 3.30	-0.05 (-0.12, 0.01)	0.12
PP(mmHg)	45.03 ± 9.36	-0.04 (-0.06, -0.01)	< 0.01
Drank
No	221 (95.67%)	0
Yes	10 (4.33%)	0.73 (-0.41, 1.87)	0.21
Smoke
No	210 (90.91%)	0
Yes	21 (9.09%)	-0.19 (-1.00, 0.62)	0.65
Comorbidities
Hypertension
No	204 (88.31%)	0
Yes	27 (11.69%)	-0.39 (-1.11, 0.34)	0.30
Diabetes mellitus
No	222 (96.10%)	0
Yes	9 (3.90%)	0.53 (-0.68, 1.74)	0.39
CHD
No	228 (98.70%)	0
Yes	3 (1.30%)	0.40 (-1.66, 2.47)	0.70
Cerebrovascular disease
No	226 (97.84%)	0
Yes	5 (2.16%)	-0.21 (-1.81, 1.40)	0.80
Tumor characteristics
Operation side
Left	132 (57.14%)	0
Right	98 (42.42%)	-0.31 (-0.79, 0.16)	0.19
Both	1 (0.43%)	-1.74 (-5.29, 1.81)	0.34
Operation method
Resection with No vascular reconstruction	201 (87.01%)	0
Resection with Vascular reconstruction	30 (12.99%)	1.42 (0.75, 2.09)	< 0.01
Embolization
No	219 (94.81%)	0
Yes	12 (5.19%)	-0.02 (-1.07, 1.03)	0.97
Shamblin classification
I	30 (12.99%)	0
II	97 (41.99%)	0.54 (-0.19, 1.27)	0.15
III	104 (45.02%)	0.98 (0.26, 1.71)	< 0.01
NLR	2.98 ± 3.76	0.13 (0.07, 0.19)	< 0.01
Data are presented as n (%) or mean ± standard deviation (SD) unless stated otherwise. BMI = Body mass index, PP = Pulse pressure, CHD = Coronary artery disease, NLR = Neutrophil-lymphocyte ratio.

Multivariate analysis of NLR and PLOS

In this study, three models were constructed to analyze the independent effects of NLR on PLOS(univariate and multivariate linear regression) listed in Table 4. In Model I, the model-based effect size could be explained as the difference in NLR associated with PLOS(0.13(0.07, 0.19), p < 0.01). In Model II, the NLR was increased by 1, the PLOS increased by increase 0.11days(0.11(0.05, 0.17), p < 0.01). In Model III, the effect size was bigger than Model II, for each additional 1 of NLR, the PLOS increased 0.12days(0.12(0.06, 0.18), p < 0.01).

Table 4

Multivariate linear regression of relationship between NLR and PLOS.
	Model I			Model II			Model III
	β(95%CI)	p-value		β(95%CI)	p-value		β(95%CI)	p-value
NLR	0.13(0.07, 0.19)		< 0.01	0.11(0.05,0.17)		< 0.01	0.12(0.06, 0.18)		< 0.01
Model I: crude model; Model II: adjusted for gender, age, stature, weight, BMI, systolic pressure, diastolic pressure, pulse pressure, Hypertension, Diabetes, CHD, Cerebral infarction, Drank, Smoke; Model III: model II additionally adjusted for Operation method, Embolization, Shamblin classification.

Curve fitting of NLR and PLOS

In the present study, we analyzed the linear relationship between NLR and PLOS (Fig. 2). Smooth curve showed that the relationship between NLR and PLOS was almost linear after adjusting confounding factors. The effect value of the straight line was 0.12(0.06, 0.18, p < 0.01). For every 1 increased in NLR, PLOS increased by 0.12days.

Stratification analysis of Shamblin classification

Shamblin classification was used as the stratification variables to observe the trend of effect sizes in NLR and PLOS(Table 5), as a critical factor to predict surgical outcome.[27] After adjusting all other variables, the associations of NLR and PLOS in Shamblin II had statistical significance. The β value in Shamblin II was 0.20(0.09, 0.29), p < 0.01).

Table 5

Stratification analysis of associations between NLR and PLOS

	Model I		Model II		Model III
	β(95%CI)	p-value	β(95%CI)	p-value	β(95%CI)	p-value
Shamblin I	0.06(-0.03, 0.15)	0.21	0.03(-0.07, 0.13)	0.59
Shamblin II	0.20(0.10, 0.31)	<0.01	0.16(0.08, 0.24)	<0.01	0.20(0.09, 0.29)	<0.01
Shamblin III	0.15(0.05, 0.25)	<0.01	0.07(-0.04, 0.19)	0.19	0.09(-0.02, 0.19)	0.12
Model I: crude model; Model II: adjusted for gender, age, stature, weight, BMI, systolic pressure, diastolic pressure, pulse pressure, Hypertension, Diabetes, CHD, Cerebrovascular disease, Drank, Smoke; Model III: model II additionally adjusted for Operation method, Embolization.

Our finding demonstrated that NLR correlated well with PLOS increase in Shamblin II CBTs. The link between NLR and inflammation which may influence transient nerve injury[28, 29] and wound healing[30, 31] was documented previously[14]. Nasibeh et al. suggested that “An increased NLR is independently associated with higher odds of nonhealing in patients with diabetic foot ulcer” with a sample of 120 diabetic foot ulcers.[9] Similar findings were also reported in the study of Gökhun et al.[32]. Yoko Maruyama et al. thought that patients with a NLR < 3.5 tended to exhibit wound healing failure.[33] Their conclusions were consistent with our findings that higher NLR was associated with longer PLOS. The reason of this phenomenon may be that NLR is an indicator of inflammation which affects healing and nerve injury[34, 35]. This study, to our best knowledge, is the first time to observe the independent association between NLR and PLOS of patients undergoing CBTs resection, as the largest of CBT single-center research.

In this study, we also found trend of the effect sizes on the different Shamblin classification were not consistent. In previous research, it was reported higher Shamblin classification as a risk of complications[36]. Based on this reason, NLR and PLOS were analyzed by stratification of Shamblin classification. In Shamblin I and III, it showed almost no difference, while in Shamblin II the trend of NLR and PLOS was much stronger with statistical significance. This might be caused by the reason that (1)Shamblin I CBT had comparatively small size with relatively light adhesion with vessels and nerves, affected by inflammation rarely, which made PLOS shorter; (2)Shamblin III had larger volume and tighter adhesion with nerves and carotid, and therefore more severe damage to surrounding tissues. Its complications were more likely to cover the role of preoperative inflammation; (3)In Shamblin II, CBT resection was unavoidable to pull the nerve during operation, causing relatively easily transient nerve injury, thus prolonging PLOS. Patients with potential inflammatory response may be more prone to edema after nerve traction, leading to transient nerve injury.

The results of this study also found the stronger association with PLOS were detected in pulse pressure, operation method, and Shamblin classification. In contrast, it was also found that preoperative embolization cannot effectively reduce PLOS, which did not mean embolization uselessly because the preparing of embolization also needs times, even though some research showed no significant difference in attenuating the complication risk[37, 38].

Our findings contributed to the growing literature linking NLR and PLOS by analyzing their statistical relationship. This finding had potentially important clinical implications and, if supported by larger validation trials, the early application of NLR will be beneficial to timing of resection, patient classification management, and relief of medical resource shortage. Further studies are needed to confirm whether NLR can help predict the PLOS in CBTs and define the relationship between inflammation and PLOS in CBTs to reduce medical costs and improve clinical efficiency.

Limitations: Although it demonstrates a significant relationship between the NLR and PLOS, it has several limitations: (1)In this study, our research subjects are Patients undergoing CBT resection. Therefore, there is a certain deficiency in the universality and extrapolation of research. (2)The sample size of this research is relatively small, even it is the largest single-center research to our best known, may making some results losing statistical significance. (3)PLOS is determined by many factors, while NLR is a marker of inflammation. Prediction of PLOS by NLR has momentous clinical value. Furthermore, other confounding factors have been ruled out as much as possible during calculation to make the result credible.

As an indicator of inflammation, NLR was a routinely collected but overlooked biomarker shows the relationship between inflammation and PLOS in patients suffered from CBT. Patients with a higher NLR had a longer PLOS. In Shamblin II CBTs, NLR had a stronger association with PLOS than other Shamblin classifications.

Ethics approval and consent to participate

The study protocol complied with the Declaration of Helsinki and was approved by the Changhai Hospital Ethics Committee. Informed consent was obtained from all patients for study inclusion. The participants were aware of the study purpose, risks and benefits.

Consent for publication

The author agrees that the paper will be published in BMC Cardiovasc Disord. This paper had no intellectual property disputes, no multiple submissions, no published in the journal. This paper will not be published worldwide, in any way, or permitted to be used by third parties without the written permission of BMC Cardiovasc Disord.

Availability of data and material

Data was provided in supplementary material.

Competing interests

None of the authors have any conflict of interest to declare.

Funding

National Natural Science Foundation of China (NSFC): 82000464, 81770482

Authors' contributions

Drs. Yu Li and Dihao Wen have contributed equally to this study.

Prof. Zhiqing Zhao and Xiaolong Wei performed operation, Shiying Wang, Chauhan Wang and Yaru Li collected data, Yu Li and Dihao Wen analyzed data and wrote paper under guidance of Jian Zhou and Yudong Sun.

Acknowledgements

We would like to acknowledge Xiatian Zhu for her assistance in acquisition of subjects and data, preparation of manuscript and Xinglin Chen in analysis and interpretation of data.

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No competing interests reported.

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The relationship between neutrophil-lymphocyte ratio and postoperative length of stay in carotid body tumor resection: a retrospective cohort study

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