Abstract
Background
To investigate the relationship between computerized tomography (CT) findings and the Ocular Trauma Score (OTS) in patients with open globe injury (OGI).
Methods
This study included 123 individuals with OGI, examining injury characteristics, clinical symptoms, and CT scans for scleral irregularity, reduced globe volume, dislocated crystalline lens, aberrant vitreous density, chorioretinal thickening, and foreign body/air presence. The prognostic value of CT imaging in OGI was evaluated by assessing its relationship with OTS findings.
Results
The most common OTS category was stage 3, found in 71 eyes (57.7%). The prevalent CT findings included severe scleral irregularity or globe collapse (34.1%), dislocated crystalline lens (33.3%), and abnormal vitreous density (26.8%). Multivariate analysis revealed that severe scleral irregularity or globe collapse (Odds Ratio [OR] = 1.36, p = 0.006) and abnormal vitreous density (OR = 1.7, p < 0.001) were significantly associated with more advanced OTS stages (I or II), indicating more severe ocular trauma. The presence of three CT findings was associated with a higher likelihood of falling into OTS stages I or II (OR = 6.82, p = 0.001). Conversely, the absence of CT findings was associated with a decreased probability of having more severe OTS stages (OR = 0.05, p < 0.001).
Conclusions
The study concludes that imaging findings are valuable for correlating with the severity of open globe injuries, highlighting the importance of CT in assessing ocular trauma.
Keywords: Computerized tomography, Ocular trauma score, Open Globe injury
Introduction
Open-globe injuries are a frequent and mostly avoidable reason for one-sided vision impairment and blindness [1]. These injuries not only affect the physical and mental well-being of patients but also lead to significant socio-economic impacts on their families and society at large [2]. Therefore, achieving a good prognosis in OGI cases is of utmost importance. Various studies have investigated predictive factors and outcomes related to severe ocular traumas to assess the prognosis of OGIs [3, 4, 5]. Age, initial visual acuity (VA), mechanism of injury, characteristics of the wound, and associated ocular lesions are factors that can predict visual outcomes after OGIs [3, 6].
The Ocular Trauma Score (OTS) serves as a predictive tool for estimating final VA in open globe injuries, aiding in the prediction of visual outcomes [7]. Introduced in 2002 and based on the Birmingham Eye Trauma Terminology System, OTS is utilized for assessing both open and closed globe injuries [8]. It evaluates several factors: initial VA, globe rupture, endophthalmitis, perforating injury, retinal detachment, and afferent pupillary insufficiency, assigning a numerical value to each. The cumulative score indicates the expected visual prognosis, with higher scores correlating with more favorable visual outcomes. OTS categorizes injuries into five stages, from 1 (the least favorable prognosis) to 5 (the most favorable prognosis). This scoring system aids clinicians in making informed treatment decisions and provides patients and their families with realistic expectations regarding visual recovery.
In scenarios involving acute trauma, challenges such as periorbital soft-tissue swelling and additional lesions complicate the examination of the eye, while factors like non-responsive behavior, altered consciousness, or sedation can obstruct patient cooperation. This underscores the importance of orbital imaging in the diagnostic and treatment planning process for open-globe injuries. As the predominant and initial imaging technique, computerized tomography (CT) scans offer a comprehensive view of the eye, orbit, and adjacent anatomical structures, delineating the extent and severity of ocular trauma [9]. These scans are pivotal in identifying intraocular foreign bodies (IOFB), evaluating the integrity of the globe, and spotting orbital fractures. Given that elements of the Ocular Trauma Score (OTS), such as initial VA, hinge on subjective patient input and can influence the accuracy of scoring and predictions, objective assessments like CT scans gain significance in determining the course of treatment and prognosis [5, 10]. The early post-trauma period may limit or preclude the evaluation of various clinical indicators necessary for OTS assessment. Moreover, certain conditions accounted for in the OTS, such as endophthalmitis, might only manifest days after the trauma occurs. In contrast, the acquisition of a CT scan does not rely on patient compliance, ensuring objective data collection. Identifying a correlation between CT scan outcomes and OTS could expedite and solidify the forecasting of visual prognosis. To the best of our knowledge, this correlation was assessed in two recent studies, one of which evaluated 34 pediatric trauma patients and concluded that the number of CT findings might assist in predicting pediatric OTS and estimating visual prognosis in pediatric OGI patients [10].
The other study, on the other hand, indicated a correlation between OTS and the type and number of CT findings in OGI cases in a cohort of both pediatric and adult cases [11]. This particular cohort, consisting of 182 patients, predominantly featured severe ocular traumas categorized primarily within OTS stages I or II. Yet, the association between CT findings and the OTS score might differ in moderate or milder ocular trauma cases. Therefore, in our study, we aimed to assess the correlation between orbital CT imaging findings and OTS scores in a cohort from a tertiary center, distinctively differing in composition from cohorts in prior studies.
Methods and materials
Patient selection
In this retrospective study, we analyzed the records of patients who presented with ocular injuries at Dokuz Eylul University Hospital and were subsequently diagnosed with open globe injuries (OGI) following examination or surgical intervention during the period from January 2013 to January 2023. Exclusion criteria included the absence of orbital CT scans or the presence of inadequate CT imagery, a history of prior ocular surgeries, and incomplete examination records. Orbital CT scans were ordered as part of the standard emergency workup in patients presenting with signs of ocular trauma, primarily by emergency physicians, to assist in assessing globe integrity when clinical examination was limited or inconclusive due to pain, periorbital swelling, or lack of patient cooperation. Informed consent forms were obtained from all patients. This study was approved by the institutional review board and ethics committee of the hospital and followed the tenets of the Declaration of Helsinki.
Data collection
Patient files were reviewed for demographic information, ocular trauma types, and the history of previous ocular surgeries. VA measurements had been recorded based on Snellen chart scores, in addition to counting finger (CF), hand movement (HM), light perception (LP), and no light perception (NLP). NLP was confirmed using the light source of an indirect ophthalmoscope when the fellow eye was completely occluded. Data pertinent to the OTS calculation—such as globe rupture, endophthalmitis, perforating injury, retinal detachment, and afferent pupillary defect—were also extracted [7]. For clarity, globe rupture in the OTS framework is a specific variable distinguished from other OGI subtypes, such as penetrating or perforating injuries, and is assigned a negative score due to its association with poor visual prognosis.
Injury zones were classified according to the Ocular Trauma Classification Group: zone 1 as the cornea (with or without involvement of the corneoscleral limbus), zone 2 as the sclera within 5 mm posterior to the limbus, and zone 3 as the sclera beyond zone 2 [12]. CT imaging was performed utilizing a multidetector CT scanner (Philips CT 5000 Ingenuity) with specifications of 80 kV, 20–665 mA, and a gantry rotation time of 0.4 s. The orientation of the segment was adjusted to be parallel with the optic nerve’s path in the infraorbitomeatal view. Non-contrast axial and coronal images were acquired with a slice thickness of 2 mm and a slice spacing of 1.5 mm. Ocular and orbital CT findings were jointly reviewed by a radiologist and an ophthalmologist, reaching a consensus on the categorization of CT findings into severe scleral irregularity (indicative of decreased globe volume or collapse), dislocated crystalline lens, abnormal vitreous cavity density, chorioretinal layer thickening, and the presence of IOFB or air (Fig. 1).
Fig. 1.
Classification of computerized tomography findings: (A) Scleral irregularity in the right eye. (B) Dislocated crystalline lens in the right eye. (C) Abnormal vitreous density in the left eye. (D) Thickening of choroid-retinal layer in the left eye. (E) Intraocular foreign body in the left eye
Statistical Analysis. Statistical analyses were performed using SPSS V 25.0 (IBM SPSS Statistics for Windows, Armonk, NY). Continuous data were described using mean ± standard deviation (SD), and categorical variables were represented as percentages. The Chi-square test determined the association between the number of CT findings and OTS categories. The Fisher exact test was used to assess the variability in CT findings across OTS stages. The relationships between diverse CT outcomes and OTS stages were analyzed with binary mixed model logistic regression. The association between the quantity of CT observations and OTS categorizations was examined via Chi-square test, expressing the strength of association as odds ratios (ORs). A P-value less than 0.05 was considered statistically significant.
Results
A total of 123 eyes from 123 patients (100 males and 23 females) with OGI were included in this study. Mean age of the patients was 38.6 ± 21 years (3–89 years). The injuries were predominantly sharp in nature, accounting for 84 cases (68.3%), while blunt injuries were observed in 39 cases (31.7%). The most common VA level at presentation was HM (30.9%), followed by LP (23.6%) and CF (18.6%). The most common OTS stages were stage III (57.7%) and stage II (22%). The mean follow-up time was 16.33± 18.1 (2–96) months. The demographics and injury characteristics of the patients are shown in Table 1.
Table 1.
Demographical characteristics of the study eyes with open Globe injury
| Type of open globe injury | |
| Sharp injury | 84 (68.3) |
| Blunt injury | 39 (31.7) |
| Location of the injury | |
| Corneal | 69 (56.1%) |
| Corneoscleral | 20 (16.3%) |
| Scleral | 34 (27.6%) |
| Zone of involvement | |
| Zone I | 68 (55.3%) |
| Zone II | 40 (32.5%) |
| Zone III | 15 (12.2%) |
| Presence of concomitant findings | |
| IOFB | 31 (25.2%) |
| RD | 20 (16.3%) |
| Endophthalmitis | 7 (5.7%) |
| Globe rupture* | 1 (0.8%) |
| VA at presentation | |
| NLP | 12 (9.8%) |
| LP/HM | 67 (54.5%) |
| 1/200 − 19/200 | 23 (18.7%) |
| 20/200–20/50 | 13 (10.6%) |
| ≥ 20/40 | 8 (6.5%) |
| OTS Stage | |
| V (92 − 100) | 5 (4.1%) |
| IV (81 − 91) | 16 (13.0%) |
| III (66 − 80) | 71 (57.7%) |
| II (45 − 65) | 27 (22.0%) |
| I (0 − 44) | 4 (3.3%) |
IOFB, intraocular foreign body; HM, hand motion; LP, light perception; NLP, no light perception; OTS, ocular trauma score; RD, retinal detachment; VA, visual acuity. * Globe rupture is defined as a full-thickness break in the ocular wall caused by blunt trauma, as per the Birmingham Eye Trauma Terminology System (BETTS), and is a distinct subtype of open globe injury in the OTS framework
In the CT scans, severe scleral irregularity or globe collapse was the most common finding, identified in 42 eyes (34.1%), followed dislocated crystalline lens in 41 eyes (33.3%). A majority of the eyes exhibited either one (n = 41, 33.3%) or two (n = 30, 24.4%) CT findings, while 34 eyes (27.6%) showed no CT findings across any scans. The CT findings for the study eyes are detailed in Table 2.
Table 2.
Computerized tomography findings of the study eyes
| CT scan findings | Number of eyes (n,%) |
|---|---|
| Type | |
| Severe scleral irregularity/globe collapse | 42 (34.1%) |
| Dislocated crystalline lens | 41 (33.3%) |
| Abnormal vitreous density | 33 (26.8%) |
| Thickening of choroid-retinal layer | 10 (8.1%) |
| Intraocular foreign body or air | 31 (25.2%) |
| Number | |
| None | 34 (27.6%) |
| One CT finding | 41 (33.3%) |
| Two CT findings | 30 (24.4%) |
| Three CT findings | 16 (13.0%) |
| Four CT findings | 2 (1.6%) |
CT, computerized tomography
Abnormal vitreous density was the most common CT finding in stage I of OTS (p < 0.001), severe scleral irregularity/globe collapse was the most common CT finding in stage II of OTS (p < 0.001), and dislocated crystalline lens was the most common CT finding in stage III of OTS (p = 0.001). The types of CT findings in different OTS stages are given in Table 3.
Table 3.
The types of CT finding in different OTS stages
| OTS stage (OTS range) | |||||||
|---|---|---|---|---|---|---|---|
| I (0 − 44; n = 4) | II (45 − 65; n = 27) | III (66 − 80; n = 71) | IV (81 − 91; n = 16) | V (92 − 100; n = 5) | Global p value | ||
| CT Findings | Severe scleral irregularity or globe collapse | 2 (50%) | 18 (66.6%) | 22 (30.9%) | 0 | 0 | p < 0.001 |
| Dislocated crystalline lens | 1 (25%) | 15 (55.5%) | 25 (35.2%) | 0 | 0 | 0.001 | |
| Abnormal vitreous density | 3 (75%) | 15 (55.5%) | 14 (19.7%) | 1 (6.2%) | 0 | < 0.001 | |
| Thickening of choroid-retinal layer | 1 (25%) | 2 (7.4%) | 7 (9.8%) | 0 | 0 | 0.428 | |
| Intraocular foreign body/air | 0 | 7 (25.9%) | 17 (23.9%) | 6 (37.5%) | 1 (20%) | 0.685 | |
CT, computerized tomography; OTS, ocular trauma score
Univariate analysis revealed associations of abnormal vitreous density (OR = 7.10; p < 0.001), severe scleral irregularity/globe collapse (OR = 5.78; p < 0.001), and dislocated crystalline lens (OR = 2.85; p = 0.016) with advanced OTS stages (I and II). Multivariate analysis, however, indicated that only abnormal vitreous density (OR = 1.703; p < 0.001) and severe scleral irregularity/globe collapse (OR = 1.36; p = 0.006) were significantly associated with OTS stages I and II. The associations between OTS stages I or II and different CT findings are detailed in Table 4.
Table 4.
Association between OTS stage I or II and different types of CT findings
| CT finding | OR | 95% CI | p value |
|---|---|---|---|
| Univariate analysis | |||
| Severe scleral irregularity or globe collapse | 5.785 | 2.404–13.918 | < 0.001 |
| Dislocated crystalline lens | 2.858 | 1.232–6.627 | 0.016 |
| Abnormal vitreous density | 7.107 | 2.881–17.529 | < 0.001 |
| Thickening of choroid-retinal layer | 1.301 | 0.315–5.373 | 0.711 |
| Intraocular foreign body or air | 0.826 | 0.315–2.162 | 0.813 |
| Multivariate binomial logistic regression | |||
| Severe scleral irregularity or globe collapse | 1.361 | 1.464–10.398 | 0.006 |
| Dislocated crystalline lens | 0.514 | 0.620–4.508 | 0.309 |
| Abnormal vitreous density | 1.703 | 2.101–14.367 | < 0.001 |
CT, computerized tomography; CI, confidence interval; OR, odds ratio; OTS, ocular trauma score
Additionally, an increased number of CT findings correlated with more severe ocular trauma, with the presence of three CT findings raising the likelihood of being in OTS stages I or II by 6.8 times (p = 0.001), as shown in Table 5.
Table 5.
Association between the number of CT findings and OTS stage I or II
| Number of CT finding | OR | 95% CI | p value |
|---|---|---|---|
| No CT finding | 0.059 | 0.007–0.457 | < 0.001 |
| One CT finding | 0.621 | 0.250–1.545 | 0.380 |
| Two CT findings | 2.113 | 0.865–5.157 | 0.145 |
| Three CT findings | 6.825 | 2.229–20.896 | 0.001 |
| Four CT findings | 3.033 | 0.184–49.999 | 0.442 |
CT, computerized tomography; CI, confidence interval; OR, odds ratio; OTS, ocular trauma score
Discussion
Patients with trauma suggestive of OGI often have limited ability to cooperate with examinations due to pain, chemosis, or intraocular hemorrhage, making CT scans a crucial adjunct. The OTS remains the predominant instrument for providing prognostic insights to patients; however, integrating it with imaging findings can enhance the understanding of its correlation with clinical outcomes. Therefore, in this study, we aimed to investigate the relationship between CT scan findings and OTS in patients with OGI. We found that severe scleral irregularity, abnormal vitreous density on CT scans, and the occurrence of multiple CT findings are linked to more severe ocular trauma, as evidenced by advanced OTS stages. Thus, both the nature and quantity of CT findings can be instrumental in predicting the OTS stage, thereby offering insights into the visual prognosis for individuals with OGIs. In contrast to prior studies focusing predominantly on high-severity trauma, our study examined a broader clinical population with a higher proportion of moderate injuries, providing a more nuanced understanding of CT’s role across a wider range of trauma severity [10, 11].
Previous studies have shown CT imaging to possess a sensitivity of 75%, a specificity of 93%, and an overall positive predictive value of 95% for diagnosing OGIs [1, 5]. These studies highlight that CT findings can significantly improve a clinician’s diagnostic accuracy for OGI and provide valuable prognostic insights regarding visual outcomes [5, 10, 11].
The primary indicators of OGI on CT scans include scleral irregularity, asymmetry in anterior chamber depth, dislocated crystalline lens, vitreous hemorrhage, and alterations in chorioretinal integrity [13]. Scleral deformity plays a pivotal role in determining the presence of an open globe, with the extent of globe deformity often correlating with the OGI prognosis. In one study, 22 out of 25 eyes with moderate to severe globe deformity experienced poor visual outcomes, and 14 of these were enucleated. Conversely, no eyes without scleral deformity underwent enucleation [5]. In our study, severe scleral irregularity/globe collapse was the most common CT finding with a rate of 34.1% and was also the most common finding in eyes with stage 2 OTS. Univariate analysis revealed that scleral irregularity increased the likelihood of being classified as stage I or II OTS by 5.7 times, which multivariate analysis adjusted to a 1.3-fold increase. In the study by Ameli et al. [11], scleral irregularity was identified as the most common CT finding in OGI, raising the likelihood of severe trauma by 1.3 times according to univariate analysis. However, this factor did not maintain its significance in the multivariate analysis. The variance in outcomes between this study and ours may be attributed to differences in the distribution of cases with advanced trauma across the two studies. Globe decompression and scleral deformities, usually caused by the prolapse of vitreous or uveal tissue through a defect, are not directly referenced in OTS. However, they are associated with conditions like rupture and perforation, which are variables considered in OTS, potentially clarifying our findings.
Several prior studies have shown a notable correlation between lenticular involvement and visual outcome [14, 15, 16, 17]. Dislocated crystalline lens was found in 33.3% of eyes and ranked as the second most common finding in the CT scans in our study. It was the most prevalent finding in eyes with stage III OTS. Univariate analysis showed that a dislocated lens increased the odds of being classified within OTS stages I or II by 2.8 times, though it did not serve as a significant predictor in multivariate analysis. This finding aligns with existing literature, suggesting that the effect of dislocated crystalline lens may be encapsulated by other factors identified through multivariate analysis, such as scleral irregularity and abnormal vitreous density [14]. Consistent with our findings, a previous study also observed no significant association between dislocated crystalline lens and the presence of an advanced OTS stage in multivariate analysis in OGI patients [11].
Alterations in vitreous density, potentially signaling vitreous hemorrhage or inflammation, were identified as the third most common CT finding (26.8%) in our study, ranking as the second highest in eyes at OTS stage II. The prevalence of vitreous hemorrhage in ocular trauma varies significantly across studies, with rates ranging from 14.9% in OGI to 82% in cases of occult trauma [10, 11, 18]. A particular study focusing on pediatric OTS and CT correlations found a prevalence of 14.9%, attributing this lower rate to the intact, non-liquefied state of vitreous gel and the vitreous cortex’s strong adherence to the retina in the pediatric population [10]. In our study, abnormal vitreous density increased the odds of being in OTS stage I or II by 7.1 times according to univariate analysis and 1.7 times in multivariate analysis. Changes in vitreous humor density have been associated with poor visual outcomes [5, 19] While Han et al. [14] did not deem this finding significant in multivariate analysis, other studies underscore a link between vitreous density alterations and visual prognosis, corroborating our observations [4, 5, 19]. Although the individual effect sizes for predictors such as scleral irregularity and abnormal vitreous density were modest in multivariate analysis, they are clinically meaningful in the context of acute trauma care. These CT findings provide objective prognostic insight, particularly when clinical examination is limited. Additionally, the cumulative presence of multiple CT abnormalities further strengthens their predictive value and supports informed triage, surgical planning, and patient communication. In particular, our observation that the presence of three CT findings increases the likelihood of severe OTS staging by 6.8 times suggests a practical threshold that may guide emergency.
imaging decisions in time-sensitive or ambiguous cases. Variability in findings across studies may stem from differences in age groups, types of trauma, and severity levels.
In our study, IOFB or air were identified in 25.2% of cases, yet this finding showed no correlation with OTS scores. Conversely, earlier research indicated a strong association between the presence of an IOFB and lower OTS scores [11]. We posit that the discrepancy in findings may be due to a smaller proportion of cases with IOFB among our advanced trauma patients. Also, a predominance of blunt trauma-related open globe injuries over sharp trauma-related injuries was observed, which typically correlates with poorer OTS scores, in that study [4, 14].
However, aligning with our results, some studies have not found the presence of an IOFB to adversely impact visual outcomes in open globe injuries [4, 20]. Factors such as initial VA, injury zone, corneoscleral wound size larger than 4 mm, endophthalmitis, retinal detachment, vitreous hemorrhage, uveal prolapse, relative afferent pupillary defect, delay in primary repair, pars plana vitrectomy, and subsequent surgeries are better predictors of final visual outcomes in open-globe injuries with IOFB [21, 22, 23]. This suggests that the presence of an IOFB alone does not directly influence OTS scores, as multiple factors contribute to improving the visual prognosis.
In our study, thickening of the choroid-retina layer was noted in only 8.1% of cases, marking it as the least common CT finding. Potential causes for this include choroidal and retinal edema, choroidal and retinal detachment, or suprachoroidal hemorrhage. Contrary to findings from a previous study, we observed no correlation between chorioretinal thickening and OTS scores [11]. The limited number of cases with choroid-retina layer thickening in our study could account for this discrepancy. Additionally, the primary cause of trauma in the previous study was blunt trauma, which is more commonly associated with edema than tissue loss, as seen in OGI [24]. This distinction might explain the differing outcomes between that study and ours.
When evaluating CT findings collectively, our analysis revealed that the presence of three findings elevated the risk of falling into OTS stages 1 or 2 by roughly 6.8 times. Ameli et al. [11] reported that having two (OR = 2.46; p < 0.001) and three (OR = 2.92; p < 0.001) CT findings was linked to OTS stages I or II. Another study observed a significant difference in pediatric OTS scores between groups with two or three CT findings and those with one or fewer (P < 0.05), as well as between groups with one or fewer and those with four or more CT findings (P < 0.05) [10]. Thus, consistent with our findings, possessing more than one CT finding appears to correlate with a lower OTS score. Another study evaluated CT findings in OGI cases by scoring different segments (anterior segment, posterior segment, and abnormalities in globe contour and volume), finding that a higher score was associated with worse visual outcomes [25].
An additional observation was that the absence of CT findings significantly decreased the likelihood of being classified into OTS stages I or II. While CT cannot replace clinical examination, it serves as a valuable tool in complex and ambiguous cases. The presence or absence of CT findings can offer clinicians important insights into the potential visual prognosis. Although CT imaging is not required for all instances of ocular trauma, certain patient groups appear to benefit greatly from its application at an early phase. These include those with severe globe deformity, those with suspected IOFB, and those who cannot undergo complete clinical examination due to trauma-related reasons such as periorbital oedema, disoriented mental status, or sedation. By familiarizing themselves with these conditions, clinicians can expedite decisions for surgery and increase diagnostic precision by recognizing which patients need to undergo CT imaging before the procedure.
The limitations of this study are primarily its retrospective nature and confinement to a single center. The absence of randomization and the potential for selection bias in treatment allocation could have impacted the outcomes. However, after excluding individuals with incomplete data, this study was able to analyze 123 patients over a span of ten years. While our study did not analyze the exact time interval between trauma and CT acquisition due to retrospective data limitations, future prospective studies should investigate how the timing of imaging may influence the sensitivity and prognostic utility of specific CT findings. On the other hand, the study’s inclusivity of both adult and pediatric populations, as well as its comprehensive evaluation of a variety of OGI cases with a notable prevalence of moderate severity, sets this research apart from previous studies in the field, thereby underscoring its contributions [10, 11].
In conclusion, our study shows that both the nature and quantity of CT findings can be instrumental in predicting the OTS stage, thereby offering insights into the visual prognosis for individuals with OGIs. When enough clinical data is unavailable in an emergency, objective findings from CT can assist in predicting the degree of ocular injuries and possibly the long-term visual outcome. Multi-center studies with larger cohorts may further validate our results.
Acknowledgements
None.
Abbreviations
- OGI
Open globe injuries
- OTS
Ocular trauma score
- VA
Visual acuity
- CF
Counting finger
- HM
Hand movement
- LP
Light perception
- NLP
No light perception
- SD
Standard deviation
- ORs
Odds ratios
- IOFB
Intraocular foreign bodies
- CT
Computerized tomography
Author contributions
EK contributed to the conception and design of the study, data acquisition, and manuscript drafting. DÖ participated in data analysis, interpretation, and critical revision of the manuscript. CDE was involved in the acquisition and interpretation of data and provided substantial input in manuscript writing. MB contributed to statistical analysis and result interpretation. EAS assisted in data collection and manuscript revisions. ZA supervised the study, contributed to study design, and critically reviewed the final manuscript. All authors read and approved the final manuscript and agreed to be accountable for all aspects of the work.
Funding
The author declared that this study has received no financial support.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Ethics approval and consent to participate
This study was approved by the Dokuz Eylul University, School of Medicine Ethics Committee (Date: 10.01.2024, Decision No: 2024/02–17).
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
No datasets were generated or analysed during the current study.

