D-dimer-based prediction model for flap loss in iliac bone transplantation

doi:10.21203/rs.3.rs-4282177/v1

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D-dimer-based prediction model for flap loss in iliac bone transplantation

https://doi.org/10.21203/rs.3.rs-4282177/v1

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published 17 Aug, 2024

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Background:

In recent years, the utilization of autogenous vascularized iliac crest flap for repairing jaw defects has seen a significant rise. However, the visual monitoring of iliac bone grafts presents challenges, frequently leading to delayed detection of flap necrosis. Consequently, there's a pressing need to devise effective indicators for monitoring postoperative complications in iliac crest flaps.

Methods:

A retrospective review was conducted on 160 patients who underwent vascularized iliac bone transplantation surgery in the Department of Oral and Maxillofacial Surgery, School and Hospital of Stomatology, Wuhan University, China, between January 2020 and December 2022.

Results

On the first day following surgery, patients who experienced thrombosis exhibited a substantial increase in plasma D-dimer levels, reaching 3.75 mg/L, a Fig. 13.84 times higher than the baseline. This difference was statistically significant (P < 0.05) compared to patients without postoperative complications. Furthermore, the nomogram we have developed and validated effectively predicts venous thrombosis, assigning individual risk scores to patients. This predictive tool was assessed in both training and validation cohorts, achieving areas under the curve (AUC) of 0.630 and 0.600, with the 95% confidence intervals of 0.452–0.807 and 0.243–0.957, respectively.

Conclusions:

Our study illustrates that postoperative plasma D-dimer levels can serve as a highly sensitive biomarker for monitoring thrombosis-induced flap loss. Moreover, we have developed a novel prediction model that integrates multiple factors, thereby enhancing the accuracy of early identification of patients at risk of thrombosis-associated flap loss. This advancement contributes to improving the overall management and outcomes of such procedures.

Iliac crest flap

Bone transplantation

Jaw reconstruction

Flap loss

D-dimer

Prediction model

Jaw defects, stemming from a variety of origins such as malignant tumors, large benign lesions, infections like osteomyelitis, or congenital abnormalities, notably disrupt both the aesthetic harmony and functional capacities of those affected. With advancements in microsurgery, the reconstruction of jaw defects frequently involves the use of autogenous vascularized fibula and iliac flaps. Notably, the vascularized iliac crest flap is particularly favored for several reasons. Firstly, its donor site along the iliac crest is conveniently concealed, thereby minimizing visible scarring. Secondly, its abundant blood supply fortifies the flap with robust anti-infection properties. Thirdly, the iliac flap’s intrinsic contour closely mimics the mandible’s shape, allowing for a more aesthetically pleasing restoration. Most crucially, the iliac crest flap provides a dependable bone source with ample height, which is essential for the successful reconstruction of jaw defects and the placement of dental implants. These attributes contribute to the widespread preference for vascularized iliac flaps in jaw repair procedures.[1–3]

Nonetheless, a recent meta-analysis indicated that roughly 7% of patients undergoing mandibular reconstruction with vascularized iliac crest flaps experience flap failure.[4] While this percentage might seem small, flap loss can inflict significant consequences, from compromised function and aesthetics to financial strain. It becomes paramount, therefore, to recognize and reduce the risks associated with the surgical process to maximize patient outcomes. Research pinpoints venous thrombosis as the main culprit behind the failure of the vascularized iliac crest flap.[5] In consequence, early and accurate identification of thrombosis within a transplanted iliac crest flap is vital. Such detection can pave the way for prompt surgical intervention to excise the thrombotic blockage or amplify antithrombotic therapy, thereby bolstering the prospects for successful flap survival. Contrary to soft tissue free flaps, such as the anterolateral thigh perforator flap, which can be visually inspected and palpated for signs of compromise, monitoring the vascularized iliac flap is uniquely challenging because it is typically enveloped by skin or mucosa at the recipient site. Thus, it is crucial to establish alternative means for the early detection and monitoring of potential complications with the iliac crest flap.[6]

The fibrinolytic marker D-dimer emerges as a critical indicator, pointing to active intravascular clot degradation. In the incipient stage of venous thrombosis, a surge in coagulation culminates in the prolific creation of fibrinogen which, when acted upon by the body’s regulatory mechanisms in clot resolution, generates fibrin degradation products, including D-dimer. Consequently, elevated D-dimer concentrations can intimate the presence of thrombosis.[7–9] Our current research indicates that D-dimer levels, particularly noteworthy changes observed within the first day following surgery, could provide a viable biomarker for ensuing flap loss. Significant elevations in D-dimer were noted in patients who encountered flap failure when benchmarked against patients without complications. Although D-dimer assays are indeed sensitive, their lack of specificity—attributable to diverse influencing variables such as age, malignancy, and trauma—necessitates a more discriminating predictive model.[8–10] We have thus developed a model consolidating multifarious factors, which considerably augments the predictive precision, equipping clinicians with a structured multiparametric scoring system to gauge flap failure risks in patients exhibiting raised postoperative D-dimer levels.

In summation, the study pioneers the implementation of postoperative plasma D-dimer levels as a prognosticator for iliac graft viability. Additionally, by formulating a novel multiplexed model for predicting graft failure, the study offers considerable enrichment to prediction capabilities, thereby facilitating potential early interventions to rescue flaps at risk.

This retrospective study was approved by the Review Board of the Ethics Committee of the School and Hospital of Stomatology, Wuhan University (NO. 2023-B42). The need for informed consent was waived due to the retrospective nature of the study. The flow diagram illustrating the case search and selection criteria is depicted in Figure S1. Medical records were reviewed for patients who underwent vascularized iliac bone transplantation surgery in the Department of Oral and Maxillofacial Surgery, School and Hospital of Stomatology, Wuhan University, China, between January 2020 and December 2022. The collected data consisted of demographic information, recipient site, pathological diagnosis, baseline plasma D-dimer levels prior to surgery, and plasma D-dimer levels within 5 days after the operation. Additionally, postoperative complications and their corresponding management were recorded and analyzed.

Statistical Analyses

Statistically significant differences were analyzed using two-sided unpaired Student’s t-tests, 1-way analysis of variance (ANOVA), using GraphPad Prism 9.3.1 (GraphPad Software). Correlations were determined by Pearson’s r coefficient. P < 0.05 was considered statistically significant.

Patient summary

A retrospective review of data from 160 patients was carried out, with patient characteristics detailed in Supplementary Table S1. Postoperatively, complications arose in 16 patients, comprising 7 instances of flap loss, and 9 successful flap preservations subsequent to titanium plate removal, with one patient experiencing postoperative bleeding, as noted in Table 1. Those who suffered flap loss exhibited an average age of 42.14 ± 10.51 years, predominantly female (5 out of 7 cases), and primarily diagnosed with benign lesions (4 out of 7 cases). Contrastingly, patients facing titanium plate rejection had an older average age of 52.00 ± 16.57 years, mostly male (7 out of 9 cases), with squamous cell carcinoma (SCC) being the prevalent pathological type (6 out of 9 cases). Such outcomes may be linked to additional radiotherapy typically required for SCC patients post-surgery, potentially impairing vascular and osseous cells. Occasionally, hypersensitivity to the titanium plate may lead to fistula formation, necessitating plate removal. The demographics of patients who encountered complications are summarized in Table 1.

Table 1

Demographics of patients who experienced complications.
Variable	FL (n = 7)	TR (n = 9)	p Value
Age (years)	42.14 ± 10.51	54.33 ± 17.01	0.119
Gender			0.072
Males	2	7
Females	5	2
benign or malignant			0.182
Benign lesions	4	2
Malignant tumours	3	7
Pathological diagnosis
Ameloblastoma	1	1
Odontogenic cyst (OC)	1	1
Squamous cell carcinoma	1	6
Adenoid cystic carcinoma	0	1
Mucoepidermoid carcinoma	1	0
Malignant transformation of OC	1	0
Others	2	0
Abbreviations: FL, flap loss; TR, titanium plate rejection.

Table 1 Demographics of patients who experienced complications.

Baseline level of D-dimer in patients who receive vascularized iliac crest flap

Upon reviewing the preoperative plasma D-dimer levels in 160 patients undergoing vascularized iliac crest flap procedures for the maxilla (Figure 1A) and mandible (Figure 1B), the analysis revealed no substantial correlation with variables such as patient age (Figure 1C), gender (Figure 1D), systemic diseases (including hypertension and diabetes) (Figure 1E), or pathological classifications (Figure 1F). This suggests that these demographic and health-related factors do not markedly influence the foundational plasma D-dimer levels in these patients.

Postoperative alterations of D-dimer levels and their influencing factors in patients without complications

An analysis of the plasma D-dimer levels in a cohort of 143 patients, who manifested no post-surgical complications, uncovered a distinct pattern of fluctuation in these levels. It was noted that following the surgery, D-dimer concentrations ascended on the first and second days, peaking on the latter. A marginal decline was then noted on the third day, with levels rebounding on the fourth, stabilizing at a plateau congruent with first-day measurements. The levelling of D-dimer persisted thereafter. Quantitatively, post-surgical D-dimer levels surged to approximately 4.8 times the preoperative baseline on day one, 7.17 times on day two, and settled back to 3.18 times on day three. The highest elevation was recorded on the second day post-operation (Figure 2A).

Patients diagnosed with squamous cell carcinoma exhibited a pronounced increment in plasma D-dimer levels, peaking two days post-surgery. Subsequent to a decline that aligned them with the non-complicated cohort on the third day, their levels witnessed further reduction by the fourth day. A resurgence to levels seen in the untroubled group characterized the fifth day. Initial escalation in D-dimer for SCC individuals reached about 7.81 times and 15.53 times above baseline on the first and second days, respectively (Figure 2B). In contrast, those with ameloblastoma presented a moderate rise in D-dimer levels post-surgery, achieving equivalence with the non-complicated group on day one. A gradual downward trajectory ensued through days two and three, with a fourth-day upturn, before a fifth-day fall-off to levels matching those without complications. The D-dimer levels in ameloblastoma patients were about 3.45 to 4.66 baseline multiples from the first to the third day, surging to roughly 8.31 times the baseline on day four (Figure 2B). The variability in post-surgical plasma D-dimer dynamics between ameloblastoma and SCC patients suggests a close link of these fluctuations with the pathological nature of the lesions.

Individual analysis of factors potentially linked to the escalated post-surgical plasma D-dimer levels revealed a significant correspondence with lesion pathology, with SCC showing notably greater increases compared to ameloblastoma, a difference proven statistically momentous (P < 0.05, Figures 2C and D). However, distinctions in D-dimer surges were not significantly related to either gender or systemic disease presence (Figures 2E-H). A substantial association was established between the rise in D-dimer concentrations and both patient age (P ≤ 0.001, Figures 2I, J) and the duration of the operation (P < 0.01, Figures 2K, L).

Postoperative alterations in D-dimer levels and their influencing factors in patients with complications

The study examined plasma D-dimer level changes within the first three days following surgery among different patient cohorts: those with an uneventful recovery, those who suffered thrombosis culminating in flap loss (Figure 3A, left side), and those who experienced a rejection of the titanium plate (Figure 3A, right side). Preoperative baseline D-dimer readings were relatively consistent across the groups and indicated minor variations, with the uneventful postoperative group showing levels at 0.47 mg/L, the thrombosis group at 0.27 mg/L, and the titanium plate rejection group at 0.40 mg/L (Figure 3A). Additionally, there were no statistically relevant age differences among the patient cohorts (Figure 3B). The data revealed that on the first postoperative day, patients afflicted with thrombosis that led to flap loss experienced a pronounced elevation in plasma D-dimer levels, markedly higher than those seen in patients who had a smooth postoperative course. These heightened levels subsided on the second and third days, eventually aligning with the levels observed in the complication-free group by the third day. Conversely, patients who rejected titanium plates demonstrated D-dimer levels and trajectories over the three-day post-surgery period that mirrored those observed in patients who had uneventful recoveries (Figures 3C and E).

A meticulous analysis was conducted focusing on the first postoperative day's plasma D-dimer levels among the three patient categories. The measurements from those patients who suffered titanium plate rejection (1.81 mg/L, 4.52 times above baseline) were found to be comparable to those of the patients with an uneventful postoperative trajectory (2.29 mg/L, 3.96 times above baseline). In stark contrast, the thrombosis group, which faced complications resulting in flap loss, displayed significantly elevated D-dimer values (3.75 mg/L, 13.84 times above baseline). These differences reached a level of statistical significance (P < 0.05, Figures 3D, F). The outcome of this analysis robustly suggests that plasma D-dimer levels, particularly those recorded on the initial day following surgery, can be significantly varied between patients who encounter thrombotic complications leading to flap loss and those with no postoperative issues. This insight underscores the promising utility of first-day post-surgical plasma D-dimer levels as an early biomarker for the detection of iliac graft thrombosis.

Predicting complications of vascularized iliac bone transplantation through a multifactor prediction model

While it is established that post-surgery thrombosis patients tend to exhibit elevated plasma D-dimer levels, it is imperative to recognize that such changes could also stem from a range of factors, including age, the nature of the pathology, and the duration of the surgery. To refine complication risk predictions, a composite predictive model was crafted. This incorporates a multivariate logistic regression analysis to scrutinize patient factors correlated with flap loss. The model factors in a variety of independent predictors for risk, such as surgical time, age, pathology type, the absolute and relative value of D-dimer, and gender. According to this model, the surgical time corresponds with a 0.90-fold rise in thrombosis risk (OR = 0.90, 95% CI: 0.22–1. 37, p = 0.016); age associates with a 0.01-fold increase in risk of thrombosis (OR = 0.01, 95% CI: -0.08–0.05, p = 0.667); the pathological type contributes a 0.30-fold increase (OR = 0.30, 95% CI: -0.15–0.75 p = 0.175); gender has a 2.79-fold increased risk of thrombosis (OR = 2.79, 95% CI: 0.84–5.33, p = 0.011); the absolute D-dimer value predicts a 0.15-fold increase in thrombosis risk (OR = 0.15, 95% CI: -0.18–0.45, p = 0. 289); and the relative D-dimer value shows a -0.02-fold increased risk of thrombosis (OR = -0.02, 95% CI: -0.13–0.07, p = 0.693, Figure 4A). A comprehensive model encapsulating various independent risk factors was formulated, yielding a nomogram for clinical use. This nomogram, with precise graphical utility, allows for the assessment of individual thrombosis risk in a straightforward manner. Practitioners can establish the score for each variable by drawing a perpendicular line from the respective risk factor value to the score axis, then tallying these to ascertain the total risk score. The probability of vein thrombosis is easily interpreted by aligning this cumulative score on the total points scale (Figure 4B). The performance of the nomogram was rigorously evaluated with two distinct sets of patient data—the training and the validation cohorts—reaching a diagnostic reliability represented by areas under the ROC curve (AUC=0.630, 0.600, 95% confidence interval: 0.452-0.807, 0.243-0.957), respectively (Figure 4C). This risk-scoring system reveals that individuals undergoing lengthier surgical procedures, those who are older in age, of the female sex, with certain pathological conditions such as squamous cell carcinoma (SCC), and those registering higher absolute D-dimer figures tend to accumulate a greater risk score. This in turn indicates a higher propensity for a rise in postoperative plasma D-dimer levels, thereby suggesting a correspondingly increased likelihood of thrombotic events. Such a tool is instrumental in identifying patients at greater risk and implementing preventive strategies accordingly.

D-dimer, a notable fibrinogen degradation byproduct, becomes elevated in the body’s cascade response to venous thrombosis. This condition prompts an enzymatic breakdown of blood clots and fibrinogen degradation, predominantly mediated by plasmin. Enhanced plasmin activity results in the cleavage of fibrinogen, giving rise to a spectrum of fibrin degradation products. As the breakdown persists, these larger molecules yield progressively smaller elements, including D-dimer, formed through the re-polymerization of fibrinogen monomers. The presence of D-dimer, detectable within two hours following thrombus formation,[7] is a critical biomarker for timely clinical intervention. The utilization of the D-dimer assay is now common in diagnosing venous thromboembolism, attesting to its high sensitivity in reflecting acute thrombosis and fibrinolytic activation. Our findings revealed that, following surgery, patients who suffered from flap loss demonstrated a rapid and significant elevation in plasma D-dimer levels on the first day. This is attributed to the acute sensitivity of D-dimer as an indicator for thrombus formation.

However, the assay’s sensitivity is countered by its limited specificity due to possible D-dimer elevation from other conditions—such as malignancies, aging, hospitalization, inflammatory states, pregnancy, and surgical trauma.[9, 10] The data strongly supports the notion that surgical trauma can precipitate a rise in D-dimer concentrations. Our investigation centered on 143 individuals with uneventful iliac flap procedures, revealing a range of augmentations in plasma D-dimer levels post-surgery. Notably, by the 5^th day post-surgery, these levels had plateaued. This stabilization suggests that the sustained physiological stress prompted by the surgery may engage both the coagulation and fibrinolysis mechanisms.[11] Consequently, we have established a positive correlation between postoperative D-dimer levels and the operation time. Additionally, various independent risk factors previously documented, including age, cancer, and gender exacerbate postoperative D-dimer elevation. With advancing age, there is a discernible escalation of pro-thrombotic factors that engender a hypercoagulable state.[10, 12] This phenomenon is augmented by the greater incidence of comorbid conditions in the elderly demographic, many of which are linked to increased plasma D-dimer concentrations.[13] Consequently, in older patients who experience surgical trauma, idiosyncrasies in microcirculation and clotting functions are likely to yield enhanced D-dimer levels throughout the healing period. The intricate relationship between oncology and coagulation is underscored by the ability of cancer cells to secrete a plethora of coagulation factors, which in turn amplify thrombin generation and precipitate a hypercoagulable milieu in patients with cancer. Such a state is conducive to the onset of venous thromboembolism, as reflected in escalated plasma D-dimer levels.[14, 15] Furthermore, studies suggest that women typically exhibit higher concentrations of both coagulation factors and D-dimer than men, hinting at a potentially heightened susceptibility to hypercoagulability. Consequently, female surgical patients may encounter an augmented risk for venous thrombosis, influenced by elevated coagulation factor levels.[16] Therefore, while the D-dimer assay is an invaluable tool in detecting thrombotic phenomena, its interpretation requires careful consideration of the patient’s full clinical picture and corroborative diagnostics to ensure precise diagnosis and appropriate therapeutic strategies.

In light of the myriad of independent risk factors that may elevate post-surgical plasma D-dimer levels, it is imperative to establish a multidimensional analytical model to unravel their respective impacts thoroughly. Our objective was to devise and corroborate a predictive nomogram tailored to forecast venous thrombosis episodes and allocate a personalized risk score for each patient. Through diligent clinical scrutiny, we selected five pivotal predictors to incorporate into the nomogram, thus enabling intricate risk differentiation. Our findings reveal that the nomogram affords a commendable accuracy in prognosis, as reflected by the areas under the receiver operating characteristic (ROC) curves in both training and validation stages. This model serves as a robust instrument for furnishing dependable risk estimates that can significantly inform clinical dialogues, therapeutic choices, and monitoring tactics. Crucially, our model leverages data that are effortlessly accessible within standard clinical procedures, markedly increasing its utility and relevance in real-world settings.

There are several limitations in this study that need to be considered. Additionally, it relied on a retrospective analysis, which inherently introduces potential biases. Secondly, the modest sample size, and its collection exclusively from individuals of a single country and ethnicity, could affect the predictive precision of our model and may limit its wide applicability across different populations. Moving forward, it would be beneficial to conduct prospective, multicenter clinical trials to substantiate and hone the clinical utility of our proposed predictive approach. Despite these limitations, our study contributes meaningful insights and lays groundwork for subsequent research endeavors dedicated to evaluating risk of flap loss in patients, through the monitoring of post-surgical plasma D-dimer concentrations following jaw defect reconstruction with iliac crest flaps.

In summary, our study stands at the forefront of introducing postoperative plasma D-dimer levels as a novel prognostic indicator for the possibility of iliac graft failure. Furthermore, we have successfully developed a novel prediction model that incorporates multiple factors to refine the prediction of patients prone to iliac graft failure. This avant-garde methodology is designed to bolster patient prognosis and finetune the handling of procedures involving iliac grafts, ultimately paving the way for enhanced surgical success rates and patient care. Our findings invite further research and validation to substantiate the clinical utility and broaden the application spectrum of our model.

Ethics approval and consent to participate

Consent for publication

Not applicable.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Competing interests

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

Funding

This work was supported by the National Natural Science Foundation of China (81801842).

Authors' contributions

Z.-L. Yu and J. Jia contributed to conception and design, data acquisition and analysis, drafted and critically revised the manuscript; Y. Zhou contributed to data acquisition; Z.-Y. Wu drafted the manuscript. S.-R Ma revised the manuscript. All authors gave final approval and agreed to be accountable for all aspects of the work.

Acknowledgments

Not applicable.

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No competing interests reported.

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Editorial decision: Revision requested
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You are reading this latest preprint version

D-dimer-based prediction model for flap loss in iliac bone transplantation

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Abstract

Background:

Methods:

Results

Conclusions:

Figures

Introduction

Patients and methods

Statistical Analyses

Results

Patient summary

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

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