Identification of the prognostic factors of patients with diabetic foot ulcer treated with tibial cortex transverse transport surgery

doi:10.21203/rs.3.rs-2573590/v1

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Identification of the prognostic factors of patients with diabetic foot ulcer treated with tibial cortex transverse transport surgery

https://doi.org/10.21203/rs.3.rs-2573590/v1

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Objectives: The aim of this study was to establish a clinical prediction model to predict the prognosis of diabetic foot ulcer (DFU) patients treated with tibial cortex transverse transport surgery (TTT).

Methods: This was a single-center, retrospective study. The clinical data and inspection results were collected by following up on DFU patients hospitalized at the First Affiliated Hospital of Guangxi Medical University and treated with TTT surgery. 202 patients’ clinical data were collected finally and they were divided into two groups according to Wagner’s grading classification. The indicators related to the severity of DFU and with the time of wound healing after surgery were confirmed through logistic regression and Lasso regression analysis. In addition, a clinical prediction model was established. Finally, the intersection of the two sets of indicators yielded the indicators related to wound severity and the postoperative healing time.

Results: 202 patients were separated into Wagner 2/3 group(n=135,mean age 62.40±9.68 years) and Wagner 4 group(n=67, mean age 61.12±9.07 years).After the student’s t-test, Lasso regression, and Logistic regression analysis, three factors were identified to describe the severity of the DFU between the two groups: platelet-to-lymphocyte ratio (PLR) (OR: 0.992, 95% CI: 0.987-0.998), monocyte-to-neutrophil ratio (MNR) (OR: 0.000, 95% CI: 0.000-0.050), Hemoglobin (HGB) (OR: 0.965, 95% CI: 0.938-0.992). Univariate COX regression analysis determined 12 factors (PLR, MNR, ect) related to the healing time after the operation.

Conclusions: PLR and MNR were factors related to DFU severity and prognosis after TTT surgery.

Diabetic foot ulcer

TTT surgery

platelet-to-lymphocyte ratio

monocyte-to-neutrophil ratio

prognostic analysis

Diabetic foot ulcer (DFU) is a severe late complication of diabetes and a public health problem(1). Presently, the global morbidity of DFU is about 6.3%(2). Moreover, patients with DFU have a higher amputation rate and mortality. Around 1 out of 4 diabetic patients develop DFU in their lifetime(3). Many factors contribute to the occurrence and development of DFU, including infection.

The occurrence mechanism of DFU is not completely clear. However, the role of the inflammatory response cannot be ignored in DFU. The platelet-to-lymphocyte ratio (PLR) and monocyte–to-neutrophil ratio (MNR) are novel systemic inflammatory response markers that reflect the inflammatory conditions. Several studies have investigated these markers because they are easily determined from the peripheral blood.

The tibial cortex transverse transport (TTT) surgery is a novel and significantly effective surgery to treat DFU(4).This surgery accelerates DFU healing by enhancing angiogenesis and immunomodulation(5). The immune system of a person affects the inflammatory state of the body. However, the correlation between DFU after TTT surgery and PLR and MNR is not reported. This study evaluated the relationship between PLR and MNR and the severity of DFU. The relationship between PLR and MNR and the prognosis of DFU after TTT surgery was also evaluated.

TTT surgery

The surgical procedure was performed as described in a previous study(4).

Baseline characteristics

A retrospective study was conducted on DFU patients who underwent TTT surgery. The baseline characteristics of the DFU patients were provided by the Computer Centre of the First Affiliated Hospital of Guangxi Medical University. The Ethics Committee of The First Affiliated Hospital of Guangxi Medical University approved this study (Approval Number:2022-E316-01) .

The patients included in the study were diagnosed with diabetes based on the American Diabetes Association (ADA) criteria(6). They were at least 18 years old and had one or more non-healing ulcers below the ankle for six months or more. All patients had undergone TTT surgery. They were excluded if they suffered from a severe pulmonary, urinary tract or systemic infection, or if they suffered from severe dysfunction of the heart, lung, kidney, brain or other organs. The participants were also excluded if they used anticoagulation, antiplatelet, antibiotics and other drugs affecting examination results in the previous month. In addition, patients were excluded if their clinical data were incomplete or they had amputation surgery or TTT surgery two times.

After the above screening, 202 DFU patients were included in the study during July 2016 to July 2021. These patients were separated into two groups according to the Wagner grading stage(7). The results of the first examination after hospitalization such as age, sex, and inspection results are presented in Table 1. The process of research was presented in Fig. 1. All the patients were followed up for at least one year. The standard of wound healing is that the wound is completely re-epithelialized without infection, exudation, etc.

Table 1

Baseline of patients based on Wagner grade
Factors	Wagner 2/3	Wagner 4	Overall	P-value
	(n = 135)	(n = 67)	(n = 202)
Sex
Female(n)	34	11	45	0.159
Male(n)	101	56	157
Age(years)	62.40 ± 9.68	61.12 ± 9.07	61.98 ± 9.48	0.367
BMI(kg/m²)	24.03 ± 3.15	24.80 ± 2.99	24.28 ± 3.11	0.099
WBC(×10⁹/L)	9.42 ± 3.34	15.20 ± 7.10	11.33 ± 5.61	༜0.001
PLT(×10⁹/L)	390.55 ± 150.47	380.64 ± 123.24	387.26 ± 141.79	0.641
NEUT(×10⁹/L)	6.43 ± 3.01	12.66 ± 6.77	8.49 ± 5.46	༜0.001
LY(×10⁹/L)	1.91 ± 0.64	1.34 ± 0.53	1.72 ± 0.69	༜0.001
MO(×10⁹/L)	0.75 ± 0.29	1.00 ± 0.50	0.83 ± 0.39	༜0.001
PLR	229.86 ± 125.96	318.94 ± 132.08	259.41 ± 134.44	༜0.001
MLR	0.43 ± 0.21	0.84 ± 0.44	0.56 ± 0.36	༜0.001
MNR	0.13 ± 0.06	0.08 ± 0.03	0.12 ± 0.06	༜0.001
NLR	3.74 ± 2.27	11.13 ± 7.09	6.19 ± 5.67	༜0.001
HGB(g/L)	104.8 ± 20.51	94.93 ± 25.95	101.04 ± 22.81	0.007
CR(µmoI/L)	100.84 ± 101.73	181.62 ± 247.46	127.63 ± 168.70	0.001
UA(µmol/L)	327.27 ± 109.08	311.44 ± 157.08	322.02 ± 126.84	0.405
CCR(ml/min)	70.77 ± 27.92	63.93 ± 31.12	68.50 ± 30.20	0.130
ALB(g/L)	33.81 ± 5.83	30.53 ± 6.21	32.72 ± 6.16	༜0.001
ESR(mm/h)	70..2 ± 30.38	89.63 ± 34.16	76.52 ± 32.92	༜0.001
TC(mmol/L)	4.27 ± 1.33	4.50 ± 2.27	4.34 ± 1.70	0.372
TG(mmol/L)	1.53 ± 0,93	1.68 ± 1.03	1.58 ± 0.97	0.291
HDL(mmol/L)	0.90 ± 0.31	0.89 ± 0.46	0.90 ± 0.36	0.831
LDL(mmol/L)	2.62 ± 1.04	2.75 ± 1.60	2.66 ± 1.25	0.505
Continuous variables are presented as mean ± standard deviation, and categorical variables are presented as number.BMI, body mass index; WBC, white blood cell; PLT, platelet; NEUT, neutrophil; LY, lymphocyte; MO, monocyte; PLR, platelet-lymphocyte ratio; MLR, monocyte-lymphocyte ratio; MNR, monocyte-netrophil ratio; NLR, neutrophil-lymphocyte ratio; HGB, hemoglobin; CR, creatinine; UA, uric acid; CCR, endogenous creatinine clearance rate; ALB, albumin; ESR, erythrocyte sedimentation rate; TC, total cholesterol; TG, triglyceride; HDL, high density lipoprotein; LDL, low density lipoprotein.

Statistical analysis

A student's t-test compared the means of the continuous variables between two groups, and a one-way ANOVA test compared three or more groups. Logistic regression analysis screened the correlation between the variables. The "Lars" package of the R software performed the LASSO regression analysis and visualization. The "pROC" package computed the receiver operating characteristic curve (ROC) curves to assess the accuracy of the factors and nomogram(8). Univariate Cox regression analysis screened the prognostic factors. The "survival" package performed predictive analysis. Without any other description, statistical significance was defined as a two-sided probability value less than 0.05. The SPSS.26 version and R.4.1.0 version were used separately.

PLR、MNR and HGB are associated with the severity of DFU

Significant differences were identified in 12 factors between the two groups (Table 1). Also, the ROC curves indicated good accuracy (Figs. 2a and 2b). After the LASSO (7 factors, LY, PLR, MLR, MNR, NLR, HGB, CR) (Fig. 2c and 2d) and logistics regression analysis (3 factors, PLR, MNR and HGB), three factors (PLR、MNR and HGB ) (Table 2) were identified in association with the severity of DFU. Next, a nomogram was established (Fig. 2e) based on these factors to describe DFU severity. The ROC curve was also accurate (Fig. 2f).

Table 2

Logistic regression analysis based on 12 factors
Factors	P	OR	95%CI low	95%CI up
WBC	0.587	0.539	0.058	5.002
NEUT	0.647	1.716	0.170	17.334
LY	0.982	0.970	0.065	14.459
MO	0.656	4.264	0.007	2512.031
PLR	0.008	0.992	0.987	0.998
MLR	0.197	106.101	0.089	126327.146
MNR	0.033	0.000	0.000	0.050
NLR	0.616	1.147	0.671	1.961
HGB	0.012	0.965	0.938	0.992
CR	0.621	1.001	0.998	1.003
ALB	0.935	0.996	0.916	1.084
ESR	0.755	0.997	0.981	1.014

Nomogram for prognosis related factors of DFU patients

Univariate Cox regression analysis idetified 12 factors related to wound healing in DFU patients after TTT surgery. Among them, seven factors (WBC, NEUT, MO, PLR, MLR, NLR and ESR) negatively affected the recovery of DFU, while five factors (age, LY, MNR, UA, ALB) predict a better prognosis of DFU (Fig. 3a) and the calibration curves also presented a good prediction (Fig. 3b). The prediction nomogram was established from these 12 factors (Fig. 3c), and it predicted well.

Prognostic analysis

Patients were separated into three groups based on the Wagner grading (Fig. 4a). Patients with the Wagner grade 4 had a lower healing rate and took longer time to heal. However, patients with Wagner grades 2 and 3 displayed a higher healing rate and a shorter healing time (P < 0.01). The high-PLR group showed a lower healing rate and healing time, but the MNR group presented an opposite trend (P < 0.01) (Figs. 4b and 4c). The PLR increased, and the MNR decreased as the Wagner grade increased (P < 0.05) (Figs. 5a and 5b). Correlation analysis showed that PLR was negatively related to MNR (R=-0.44, P < 0.01) (Figs. 5c and 5d).

Diabetes is a major chronic disease. The number of people with diabetes is growing continuously: it reached 450 million in 2015 (9, 10). DFU, is a significant complications of diabetes, affecting about 25% of people with diabetes(2, 11). DFU is mainly associated with peripheral neuropathy and lower extremity arterial disease(12).However, the mechanism of DFU is unclear. Diabetes causes systemic effects on patient's immune function and alters the state of inflammation. DFU is prone to co-infection, causing further gangrene, osteomyelitis, and the development of severe DFU. Patients with DFU have a higher mortality and amputation rate than the general diabetic population.

Treatment of DFU, especially severe DFU, is a worldwide challenge. Conventional surgical treatment, include debridement and revascularization. They help avoid amputation in some patients and heal the ulcer. However the rate of recurrence remains high(11). TTT surgery is effective for treating severe and recalcitrant DFU. TTT surgery showed a higher rate of wound healing and limb salvage and a lower recurrence rate. It also enhanced angiogenesis and immunomodulation in the patients(13) .

Our study identified two indices, PLR and MNR, in correlation with the Wagner grading of DFU, which also predicted the prognosis of DFU patients treated with TTT surgery. PLR is an inflammatory index associated with the diagnosis and prognosis of diabetes(13–16). In the present study, PLR showed a positive correlation with the severity of DFU, as indicated by the Wagner DFU grade. These findings were consistent with previous results. At the same time, PLR was associated with the prognosis of wound healing in DFU patients treated with TTT surgery. A higher PLR predicted a longer time to heal after TTT surgery. This correlation has not been reported earlier. Therefore, PLR can be a simple clinical index to speculate the time for wound healing after TTT surgery.

Diabetes creates a chronic inflammatory state in the patients. Hence, the severity of diabetes and the risk of its complications can be observed by detecting the inflammation indicators(17–19). One of the main causes of DFU is linked to peripheral arterial disease (PAD)(20, 21).Patients with DFU and PAD have increased rates of unhealed wounds, amputations, and even mortality(22, 23). PAD also predicts the risk of DFU amputation(24). Previous studies have reported the association between increased PLR and critical limb ischemia (CLI) and PAD(25).Chronic inflammation over a long period impairs immune function and reduces the number of lymphocytes. This state also elevates the platelets and inflammatory factors, damaging the vascular endothelium and causing atherosclerosis, the pathological basis for the further formation of PAD(26).

Monocyte-to-neutrophil ratio (MNR), a ratio of peripheral blood cells, is a new indicator reflecting inflammation level. Related studies have demonstrated that MNR represents a combination of thrombosis and inflammation (27).The current study showed that monocytes and neutrophils negatively affect healing in DFU patients treated with TTT surgery, while the opposite is true for MNR. However, these two results are not contradictory. Monocytes are the primary cells of innate immunity and play a central role in initiating and resolving inflammatory responses to pathogens. Several studies have shown that monocytes are functionally impaired in diabetic patients, with reduced anti-inflammatory capacity and immune differentiation(28, 29). Monocytes maintain a balance between pro-inflammatory and anti-inflammatory responses. Inflammatory development is stronger in the early stages of wound healing when the M1 phenotype dominates monocytes. In the later stages of wound healing, the state of inflammation decreases, and the M2 phenotype predominates. DFU is a persistent non-healing wound, in a state of chronic inflammation, with a predominant M1 phenotype of the mononuclear cells. Wounds have been in the early stages of healing for a long time, with increased numbers of mononuclear cells and delayed healing. Elevated white blood cell counts in patients with impaired glucose tolerance increase the neutrophils(30, 31). The neutrophil elevation is more pronounced in DFU patients with co-infection, suggesting a significant inflammatory response. The MNR increases when inflammation is reducing during wound healing. The observation is consistent with the present finding. This study also observed reduced MNR in patients with high Wagner grades. The possible reason could be the greater severity of the wound infections and higher levels of inflammation in these patients. Therefore, detecting of these inflammatory indicators can provide us with some strategies for the early prediction of wound healing after TTT surgery.

This study has some limitations. First, there may be some information bias because it is a retrospective study. In addition, the study analyzed a limited number of influencing factors. It did not examine all indicators associated with DFU severity and healing after receiving TTT surgery for DFU. Further, the developed nomogram model was not sufficient to use the criterion map in clinical practice, although the ROC curve showed good accuracy. Follow-up studies are needed to refine the diagnostic model. Therefore, a multicenter and more extensive cohort study is required. In the future, the model can be updated for better accuracy and reasonable prediction to help guide the treatment of DFU.

The present study performed a comprehensive summary of the risk factors associated with the severity of DFU and its prognosis.PLR and MNR are critical predictors of DFU severity and prognosis after TTT surgery. High PLR and/or low MNR indicate severe DFU and poor prognosis after TTT surgery, while low PLR and/or high MNR indicate good prognosis after TTT surgery. The results of this study can guide risk stratification and preoperative prevention for DFU patients. The can also enable a better prognosis for patients treated with TTT surgery.

DFU	diabetic foot ulcer
TTT	tibial cortex transverse transport
BMI(kg/m2)	body mass index
WBC(×109/L)	white blood cell
PLT(×109/L)	platelet
NEUT(×109/L)	neutrophil
LY(×109/L)	lymphocyte
MO(×109/L)	monocyte
PLR	platelet-lymphocyte ratio
MLR	monocyte-lymphocyte ratio
MNR	monocyte-netrophil ratio
NLR	neutrophil-lymphocyte ratio
HGB(g/L)	hemoglobin
CR(μmoI/L)	creatinine
UA(μmol/L)	uric acid
CCR(ml/min)	endogenous creatinine clearance rate
ALB(g/L)	albumin
ESR(mm/h)	erythrocyte sedimentation rate
TC(mmol/L)	total cholesterol
TG(mmol/L)	triglyceride
HDL(mmol/L)	High density lipoprotein
LDL(mmol/L)	low density lipoprotein
ADA	American Diabetes Association
ROC	receiver operating characteristic curve
PAD	peripheral arterial disease
CLI	critical limb ischemia

Acknowledgement

Author Contributions

All authors participated in data acquisition. Jinmin Zhao and Qikai Hua contributed to visualization, supervision, project administration and funding acquisition. Sijie Yang contributed to original drafting review and editing. Kaixiang Pan contributed to methodology. Wencong Qin contributed to the software. Hongjie Su contributed to the investigation. Kaibing Liu contributed to the formal analysis. Jun Hou contributed to the data curation. All authors contributed to the article and approved the submitted version.

Funding

This work was supported by National Natural Science Foundation of China（82260448）， the Science and Technology Plan Project of Guangxi Province (2021AB11027)，Science and Technology Plan Project Contract of Qingxiu District, Nanning City, Guangxi Provice (2020053), and Clinical Research Climbing Plan Peak Project Contract of the First Affiliated Hospital of Guangxi Medical University (YYZS2020010)

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Ethics approval and consent to participate

This study was approved by the First Affiliated Hospital of Guangxi Medical University Institution Review Board (IRB No. 2022-E316-01). Informed consent was obtained from all subjects and/or their legal guardian(s). All procedures were undertaken in accordance with the Helsinki Declaration and all methods were carried out in accordance with relevant guidelines and regulations in the declaration.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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No competing interests reported.

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Identification of the prognostic factors of patients with diabetic foot ulcer treated with tibial cortex transverse transport surgery

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Version 1

Abstract

Figures

Introduction

Material And Methods

TTT surgery

Baseline characteristics

Statistical analysis

Results

PLR、MNR and HGB are associated with the severity of DFU

Nomogram for prognosis related factors of DFU patients

Prognostic analysis

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

Status:

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