Risk of Conversion from Laparoscopic Appendectomy to Open Surgery: The Role of Clinical and Radiological Factors in Prediction

Abstract

Introduction:

Laparoscopic appendectomy is the most preferred surgical method in the treatment of acute appendicitis. In our study, we aim to determine the clinical and radiological factors affecting conversion from laparoscopic appendectomy to open surgery.

Materials and Methods:

All patients older than 18 years, who were operated on with the diagnosis of acute appendicitis in the General Surgery clinic of Prof. Dr. İlhan Varank Training and Research hospital between January 2020 and January 2022, were included in the study. The data consisting of clinical, laboratory, and radiological (computed tomography) findings of the patients were evaluated retrospectively. The patients were divided into two groups as those whose surgery was completed laparoscopically (Group 1) and those converted from laparoscopic appendectomy to open surgery (Group 2). The risk of conversion to open surgery was analyzed by binary logistic regression analysis as univariate and multivariate models.

Results:

Appendectomy was performed in 831 patients within the specified period. The surgery of 31 (3.73%) patients started laparoscopically; however, they were completed by converting to open surgery. Multivariable analysis showed that the risk of conversion to open surgery increased with leukocyte count, Alvarado score and with the presence of periappendiceal fluid and lymphadenopathy on CT.

Conclusion:

Our study shows that patients with high risk of returning to open surgery can be identified preoperatively with the risk analysis method in which clinical, laboratory, and radiological findings are evaluated together. We conclude that, starting the operation of these patients with the open technique from the beginning will prevent unnecessary expenditures and reduce morbidities.

Introduction

Acute appendicitis represents 7%–10% of all admissions to the emergency department due to acute abdomen and is the most common cause of acute abdomen.^1,2 Although its incidence is higher at younger ages, the risk of appendicitis is around 7%–8% during the lifetime of an individual.³ Surgery is the most commonly preferred treatment method for patients with acute appendicitis. The number of appendectomies performed in the United States is over 300,000 per year.⁴

Laparoscopic appendectomy, which first appeared in the literature by Kurt Karl Stephan Semm in 1983, has now become widespread throughout the world and is applied to ∼75% of appendicitis patients in the United States.^5,6 Laparoscopic appendectomy is reported to be superior to open appendectomy due to the advantages of less pain, better cosmetic results, lower surgical site infection, shorter hospitalization time, and early return to work.⁷

The World Society of Emergency Surgery (WSES) 2016 guideline reports that postoperative complication rates, including wound infection, ileus, and intra-abdominal abscess, are 11.1% for open appendectomies and 8.7% for laparoscopic appendectomies.⁸ However, when performed by inexperienced surgeons, laparoscopic appendectomy can prolong the operation time and increase the cost and the risk of complications.⁹ In surgeries that start laparoscopically, surgeons can sometimes convert to open surgery. The frequency of conversion to open surgery has been reported as 1%–10% in various studies.^10,11

When starting laparoscopically and then converting to open surgery, the cost associated with treatment as well as the risk of pulmonary and infectious complications increase significantly.^12,13

In this study, we aimed to examine the preoperative clinical and radiological factors affecting the conversion to open surgery during laparoscopic appendectomy.

Materials and Methods

Patient population and study design

This retrospective study was approved by local hospital board (date: March 9, 2022, No.: E-46059653-020) and written informed consent was obtained from all participants. In the study, we retrospectively evaluate the medical records of adult patients who were operated on with a preliminary diagnosis of appendicitis in our center between January 2020 and January 2022.

A total of 124 patients were selected randomly among patients who underwent laparoscopic appendectomy (the laparoscopic appendectomy group). As a result of the pathological evaluation, patients with lymphoid hyperplasia, fibrous obliteration, parasitic infections, and benign and malignant tumors, and 13 patients who did not have a preoperative computed tomography (CT) examination or had insufficient clinical-laboratory information were excluded in the study.

Clinical and laboratory data

While evaluating the clinical findings, we examined the patients' age, gender, presence of additional disease, history of previous abdominal surgery, time elapsed since the onset of symptoms, presence of high fever (>38°C), presence of nausea-vomiting complaints, presence of rebound in physical examination, and the Alvarado score.

While evaluating the laboratory findings, we recorded the leukocyte count, neutrophil percentage, and C-reactive protein (CRP) value in the blood tests of patients.

When evaluating the pathology results, we divided appendicitis patients into subgroups of acute appendicitis, phlegmonous appendicitis, suppurative appendicitis, and gangrenous-perforated appendicitis. Acute appendicitis is classified by the detection of neutrophils and leukocytes in the appendix mucosa, phlegmonous appendicitis by the progression of the inflammation in the appendix to the muscular and subserosal areas, suppurative appendicitis by the presence of pus in the lumen of the appendix, in addition to phlegmonous appendicitis, and gangrenous—perforated appendicitis with the presence of thrombosed veins and necrosis in the wall of the appendix.¹⁴

CT scanning and CT image analysis

Abdominal CT was performed on all patients using a 16-slice CT scanner (Optima 520 CT, General Electric [GE] company). CT images were acquired using standard clinical protocols, with or without intravenous contrast, in the supine position with full inspiration. The following parameters were used: tube voltage, 120 kV; automatic tube current modulation, 100–250 mAs; and slice thickness, 1.25 mm without gaps between slices. Images were reconstructed at a slice thickness of 5 mm. The reconstructed images were transmitted to the work station and image archiving and communication systems (PACS, Simplex PACS co.) for multiplane reconstruction postprocessing.

CT images were evaluated by two radiologists who were unaware of clinical, laboratory, and pathology results and the type of surgery performed. In case of conflict, a settlement is reached by compromise. In the CT scans of the cases, appendiceal double-wall diameter, single-wall thickness of the appendix, periappendiceal fat stranding, periappendicular fluid, mucosal hyperenhancement, intraluminal air in the appendix, appendicolith, presence of abscess, retrocecal location of the appendix on CT, and presence of lymphadenopathy were noted (Fig. 1).

FIG. 1.

The contrast-enhanced coronal (a) and axial (b) CT image shows a long, dilated retrocecal appendix with a thick enhancing wall and adjacent fat stranding and periappendiceal fluid in the subhepatic recess. No extraluminal air but intraluminal air is present.

Surgery

The type of surgery applied to the patient was evaluated as a laparoscopic surgery, open surgery, or surgery that started laparoscopically and converted into open surgery.

Statistical methodology

We evaluate conformity to normal distribution by Shapiro–Wilk test and Kolmogorov–Smirnov test. We use Pearson's chi-square test, Yates' corrected chi-square test, and Fisher's exact chi-square test to compare categorical data according to patient groups. We analyze multiple comparisons of the ratios with the Bonferroni-corrected Z test. We use an independent two-sample t-test to compare normally distributed quantitative data according to patient groups.

We employ Mann–Whitney U test to compare the non-normally distributed quantitative data according to patient groups. To analyze factors affecting the risk of conversion to open surgery, we use the binary logistic regression model. We present analysis results as mean ± standard deviation and median (minimum–maximum) for quantitative data, and frequency (percent) for categorical data. We analyze factors affecting the risk of conversion to open surgery using a binary logistic regression.

We present the results of our analyses as frequency (percentage) for categorical data. Finally, we use Yates correction to compare pathology results according to patient groups. We take the statistical significance level as P < .050. We use IBM SPSS V23 to analyze the data.

Results

Between January 2020 and January 2022, 831 patients underwent appendectomy in our center. Among them, 582 (70.00%) patients were operated laparoscopically from the start to end, whereas 198 (23.82%) patients underwent open surgery. For 31 patients (3.73%) the surgery started laparoscopically, but completed open. We exclude one patient among this latter group from the study because the pathology result indicated carcinoid tumor. Among the randomly selected patients, 109 were included in the final analysis: for 79 of these patients, surgery started and completed laparoscopically (Group 1); and for 30 patients, surgery started laparoscopically, but was completed as open surgery (Group 2).

Table 1 shows the distribution and comparison of the clinical features of the patients between our two groups. The presence of additional disease is statistically higher in Group 2 (P < .001). This difference is due to the difference between the rates of patients without additional disease and those with hypertension (HT). We find a statistically significant difference between the distribution of high fever and anorexia between the two groups (P = .038; P = .034). Since the number of patients with a history of previous abdominal surgery was only one in each group, which is not sufficiently big, statistical comparison is not meaningful.

Table 1.

Distribution and Comparison of Clinical Features of Patients

	Group 1 (Laparoscopic group)	Group 2 (Laparoscopic converted to open)	Total	Test ist	P
Gender
Female	23 (29.1)	9 (30)	32 (29.4)	0.000	1.000^a
Male	56 (70.9)	21 (70)	77 (70.6)	0.000	1.000^a
Comorbidities
No	69 (87.3)	15 (50)	84 (77.1)	15,106	<.001^a
Yes	10 (12.7)	15 (50)	25 (22.9)	15,106	<.001^a
Additional disease^b
No	69 (87.3)^c	15 (50)^d	84 (77.1)	59,189	<.001^e
HT	1 (1.3)^c	10 (33.3)^d	11 (10.1)
DM	10 (12.7)^c	6 (20)^c	16 (14.7)
IKH	0 (0)	5 (16.7)	5 (4.6)
Cardiac Arrhythmia	0 (0)	1 (3.3)	1 (0.9)
Fever
No	71 (89.9)	22 (73.3)	93 (85.3)	—	.038^f
Yes	8 (10.1)	8 (26.7)	16 (14.7)	—	.038^f
Nausea and/or vomiting
No	31 (39.2)	8 (26.7)	39 (35.8)	0.999	.318^a
Yes	48 (60.8)	22 (73.3)	70 (64.2)	0.999	.318^a
Anorexia
No	12 (15.2)	0 (0)	12 (11)	—	.034^f
Yes	67 (84.8)	30 (100)	97 (89)	—	.034^f
Rebound
No	8 (10.1)	3 (10)	11 (10.1)	—	1.000^f
Yes	71 (89.9)	27 (90)	98 (89.9)	—	1.000^f
Previous abdominal surgery
No	77 (98.7)	29 (96.7)	106 (98.1)	—	—
Yes	1 (1.3)	1 (3.3)	2 (1.9)	—	—

Chi-square test with Yates correction.

Multiple response, frequency (percentage), —-: No result.

c,d

There is no difference between groups with the same letter.

Pearson's chi-square test.

Fisher's exact test.

DM, diabetes mellitus; HT, hypertension; IKH, intracranial hemorrhage.

Table 2 shows the distribution and comparison of quantitative findings of the patients in the two groups. We find that the median age, median CRP, and Alvarado median values are significantly higher in Group 2. Likewise, we find that the median values for hospitalization time (days) are longer in Group 2 (P < .001). The average is 13.82.

Table 2.

Distribution and Comparison of Quantitative Findings of Patients

	Laparoscopic group		Laparoscopic converted to open		Total		Test ist	P
	Mean ± SD	Mean (min.–max.)	Mean ± SD	Mean (min.–max.)	Mean ± SD	Mean (min.–max.)	Test ist	P
Age	32.7 ± 12.54	29 (18–77)	46.73 ± 15.99	45 (21–77)	36.56 ± 14.89	32 (18–77)	566.5	<.001^a
Leukocyte count	145,37.97 ± 5093.24	14,010 (3880–27,400)	15,786.33 ± 4524.83	16,235 (5070–25,340)	14,881.56 ± 4954.46	14,320 (3880–27,400)	−1.177	.242^b
Neutrophil percent	77.39 ± 9.78	78.7 (55.5–93)	82.05 ± 6.14	82.95 (69.9–93.8)	78.67 ± 9.14	80.79 (55.5–93.8)	911.5	.064^a
CRP	39.1 ± 68.09	11,43 (0,01–379,83)	98,09 ± 118,58	44,88 (0,08–384,74)	55,33 ± 88,46	16,84 (0,01–384,74)	691,0	.001^a
Alvarado score	7.77 ± 1.21	8 (5–10)	8.67 ± 0.84	9 (7–10)	8.02 ± 1.19	8 (5–10)	695.5	.001^a
Time from symptom onset to surgery (days)	2.11 ± 1.24	2 (1–9)	2.93 ± 1.66	2 (1–9)	2.34 ± 1.41	2 (1–9)	736.5	.001^a
Hospitalization time (days)	2.76 ± 1.41	2 (1–10)	5.97 ± 3.67	5 (2–19)	3.64 ± 2.67	3 (1–19)	339.5	<.001^a
Appendix diameter/outer-outerwall	11.68 ± 1.98	11.3 (8–18)	13.82 ± 3.46	14 (7–24)	12.27 ± 2.64	12 (7–24)	−3.194	.003^b
Single Wall thickness (mm)	2.51 ± 0.92	2.5 (1–5)	3.17 ± 1.32	3 (1–8)	2.69 ± 1.07	2.55 (1–8)	781.5	.011^a

Mann–Whitney U test.

Independent two-sample t-test.

CRP, C-reactive protein; mm, millimeter; SD, standard deviation.

Table 3 shows the distribution and comparison of categorical findings of patients detected in CT in our groups. We find a statistically significant difference between the frequency of periappendiceal fat stranding, periappendiceal fluid (right iliac fossa fluid/phlegmon), mucosal hyperenhancement, extraluminal air, intraluminal air in appendix, abscess, and lymphadenopathy by patient groups. There was no statistically significant difference between other categorical variables between patient groups (P > .050).

Table 3.

Distribution and Comparison of Categorical Findings of Patients Detected in Computed Tomography

	Laparoscopic group	Laparoscopic converted to open	Total	Test ist	P
Periappendiceal fat stranding
No	18 (22.8)	1 (3.3)	19 (17.4)	4.444	.035^a
Yes	61 (77.2)	29 (96.7)	90 (82.6)	4.444	.035^a
Periappendiceal fluid (Right iliacfossa fluid/phlegmon)
No	64 (81)	8 (26.7)	72 (66.1)	26.268	<.001^a
Yes	15 (19)	22 (73.3)	37 (33.9)	26.268	<.001^a
Mucosal hyperenhancement
No	36 (46.8)	4 (15.4)	40 (38.8)	6.785	.009^a
Yes	41 (53.2)	22 (84.6)	63 (61.2)	6.785	.009^a
Extraluminal air
No	79 (100)	26 (86.7)	105 (96.3)	—	.005^b
Yes	0 (0)	4 (13.3)	4 (3.7)	—	.005^b
Intraluminal air in appendix
No	74 (93.7)	19 (63.3)	93 (85.3)	—	<.001^b
Yes	5 (6.3)	11 (36.7)	16 (14.7)	—	<.001^b
Appendicolith
No	61 (77.2)	24 (80)	85 (78)	0.003	.956^a
Yes	18 (22.8)	6 (20)	24 (22)	0.003	.956^a
Abscess
No	77 (97.5)	22 (73.3)	99 (90.8)	—-	<.001^b
Yes	2 (2.5)	8 (26.7)	10 (9.2)	—-	<.001^b
Retrocecal placement in CT
No	57 (72.2)	21 (70)	78 (71.6)	0.000	1.000^a
Yes	22 (27.8)	9 (30)	31 (28.4)	0.000	1.000^a
Lymphadenopathy
No	33 (41.8)	2 (6.9)	35 (32.4)	10.240	.001^a
Yes	46 (58.2)	27 (93.1)	73 (67.6)	10.240	.001^a

Chi-square test with Yates correction.

Fisher's exact test.

CT, computerized tomography.

We analyze the risk of conversion to open surgery by binary logistic regression analysis as univariate and multivariate models (Table 4). In univariate analysis, the risk of conversion to open surgery increases in the presence of advanced age, presence of additional disease, high fever, neutrophil percentage, high CRP and Alvarado scores, increased time from symptom onset to surgery, Phlegmenous + Suppurative + Gangrenous – Perforated appendicitis, increased appendix diameter, and abscess. In multivariate analysis, we found that risk of conversion to open surgery increased with increasing leukocyte count and Alvarado score and with the presence of periappendiceal fluid and lymphadenopathy on CT. Other variables are not statistically significant (P > .050).

Table 4.

Binary Logistic Regression Analysis of Risk Factors for Conversion to Open Surgery

	Univariate			Multivariate
	Beta	OR (%95 CI)	P	Beta	OR (%95 CI)	P
Gender (Reference: Male)	−0.043	0.958 (0.382–2.403)	.928	−0.598	0.55 (0.056–5.387)	.608
Age	0.065	1.067 (1.034–1.101)	<.001	0.036	1.037 (0.931–1.154)	.513
Comorbidities (Reference: No)	1.932	6.9 (2.601–18.306)	<.001	3.326	27.838 (0.596–1300.374)	.090
Fever (Reference: No)	1.172	3.227 (1.085–9.603)	.035	−0.957	0.384 (0.017–8.641)	.547
Leukocyte count	0.000	1 (1–1)	.241	0.000	1 (0.999–1)	.025
Neutrophil percent	0.063	1.065 (1.01–1.124)	.020	0.111	1.118 (0.927–1.347)	.243
CRP	0.007	1.007 (1.002–1.012)	.005	0.009	1.009 (0.993–1.024)	.272
Nausea and/or vomiting (Reference: No)	0.574	1.776 (0.703–4.486)	.224	−3,678	0,025 (0,001–0,993)	.050
Rebound (Reference: No)	0.014	1.014 (0.25–4.108)	.984	0.787	2.197 (0.02–239.295)	.742
Alvarado Score	0.781	2.183 (1.375–3.466)	.001	3.464	31.937 (1.812–562.877)	.018
Time from symptom onset to surgery (days)	0.390	1.477 (1.073–2.033)	.017	0,535	1,707 (0,662–4,402)	.268
Previous abdominl surgery (Reference No)	0.977	2.655 (0.161–43.861)	.495	0.696	2.006 (0.008–502.356)	.805
Patology result (Reference: Akut Appendicitis)	0.521	1.684 (0.71–3.994)	.237	0.262	1.299 (0.149–11.314)	.813
Appendix diameter/outer-outer wall	0.337	1.4 (1.151–1.704)	.001	0.486	1.626 (0.824–3.209)	.161
Single-wall thickness (mm)	0.596	1.814 (1.157–2.846)	.010	−0.676	0.509 (0.11–2.347)	.386
Periappendiceal fat stranding (Reference: No)	2.147	8.557 (1.089–67.25)	.041	−3.469	0.031 (0–3.946)	.160
Periappendiceal fluid (Right İliacFossaFluid/Phlegmon) (Reference: No)<	2.462	11.733 (4.38–31.431)	<.001	3.033	20.759 (1.333–323.278)	.030
Mucosal Hyperenhancement (Reference: No)	1.575	4.829 (1.521–15.337)	.008	—	—	—
Intraluminal air in Appendix (Reference: No)	−2.148	0.117 (0.036–0.376)	<.001	1.938	6.944 (0.399–120.982)	.184
Appendicolith (Reference: No)	−0.166	0.847 (0.3–2.391)	.754	0.739	2.094 (0.036–120.568)	.721
Abscess (Reference: No)	2.639	14 (2.77–70.765)	.001	1.379	3.973 (0.045–354.437)	.547
Retrocecal placement in CT (Reference: No)	0.105	1.11 (0.441–2.794)	.824	−0.284	0.753 (0.062–9.162)	.824
Lymphadenopathy (Reference: No)	2.307	10.043 (2.235–45.129)	.003	5.648	283.721 (2.384–33,770.392)	.021

—, no result; CI, confidence interval; CRP, C-reactive protein; CT, computerized tomography; mm, millimeter; OR, odds ratio.

When evaluating the relationship between the pathology result and the risk of conversion to open surgery, complicated appendicitis patients with phlegmenous, suppurative and perforated appendicitis were gathered under a single heading and compared with patients with acute appendicitis (Table 5). There is no statistically significant difference between the distribution of pathology results in our groups (P = .033).

Table 5.

Comparison of Pathology Results According to Patient Groups

	Laparoscopic group	Laparoscopic converted to open	Total	Test ist	P ^a
Pathology result
Acute appendicitis	39 (49.4)	11 (36.7)	50 (45.9)	1.413	.330
Phlegmenous + Suppurative + Gangrenous – Perforated appendicitis	40 (50.6)	19 (63.3)	59 (54.1)	1.413	.330

Yates correction.

Discussion

In this study, we study the clinical and radiological characteristics of two different groups of patients who underwent surgery after a preliminary diagnosis of appendicitis. One group consists of patients who underwent laparoscopic surgery. The second group consists of patients whose surgeries started laparoscopically, but then converted to open surgery.

With the increase in the worldwide application of laparoscopic surgery, the rate of laparoscopic appendectomy increased to 70.8% worldwide.⁶ In our study, this rate is also 70%, similar to the world data. While the rate of conversion to open surgery was around 10% in previous publications, recent publications report this to be around 5% due to increases in laparoscopic surgery experience.⁹ In our sample, this rate is below 5%. Pushpanathan et al. report, in their study on 120 patients, that the rate of conversion to open surgery is 27.5%, which is much higher than the literature. They attribute this high value to two reasons: first, the patients were operated on without routine radiological evaluations with CT or ultrasound before the surgery; and second, the risk of encountering complicated appendicitis patients was higher.¹⁰

In our study, we observe that, for patients whose surgery started laparoscopically but completed as open surgery, the clinical findings of higher fever, nausea, and high Alvarado score were common. Similarly, studies by Wagner et al. and Antonacci et al., in which patients' clinical variables were evaluated, show that the presence of high fever yields significant results for conversion to open surgery in univariate analyses.^9,12

Among the laboratory values, the most frequently studied variables in the literature are leukocyte count, neutrophil percentage, and CRP. In their study on 394 patients, Aydın et al. show that neutrophil percentage and CRP increase are risk factors for conversion to open surgery.¹⁵ In our study, in univariate analyses, we show that the risk of conversion to open surgery increases in cases where the percentage of neutrophils and CRP increase.

In the radiological evaluation, we find that the presence of periappendicular fluid and lymphadenopathy is significantly more common in the case group that was converted to open surgery. CT findings in acute appendicitis cases were previously described in the literature.^16–18 In a study that compares the complicated and uncomplicated appendicitis groups, Avanesov et al. find that the presence of periappendicular fluid on CT examination is more common for the complicated group.¹⁹

The presence of periappendicular fluid and lymphadenopathy in the right lower quadrant in acute appendicitis is among the findings that show inflammatory changes related to appendicitis and can be observed in different localizations depending on the location of the appendix.²⁰ It has been previously reported that periappendicular inflammatory changes and the presence of fluid are good predictors in the diagnosis of acute appendicitis.²¹ Accordingly, considering the signs of inflammation observed on CT in the treatment planning may be a guide for correct and adequate treatment.

When patients are evaluated in terms of gender and age, many studies in the literature report that male gender and advanced age are risk factors for conversion to open surgery. In their study on 104,865 pediatric appendicitis patients, Johnson et al. report that these variables were as significant as in adult patients.²² In our data, we did not find a significant effect of gender difference on conversion to open surgery; however, we find that the risk of conversion to open surgery increases with age in univariate analyses. It has been suggested that the increased risk of perforated appendicitis in elderly patients may be effective in the risk of conversion to open surgery as a result of decreased appendix diameter with increasing age, increased risk of ischemia due to angiosclerosis, decreased neurological abilities, decreased pain sensation, and decreased immune system activity.^12,13

Diabetes mellitus and obesity in patients were reported as risk factors for conversion to open surgery in a cohort study of 279,327 patients by Finnerty et al.¹³ In the study of Antonacci et al., including 434 patients, HT was found to be the most common, but the presence of additional disease was shown as a risk factor.¹² In our study, we show that the presence of HT is significantly higher in the group converted to open surgery, and the presence of additional disease is a risk factor in univariate analyses, but not in multivariate analyses.

When the time from the onset of symptoms to the surgery was evaluated, Wagner et al. find that the duration in the group of patients who converted to open surgery (laparoscopic surgery- 1.4 days versus reverting to open surgery- 2.1 days) is longer.⁹ We obtain similar results in our data, while the time to surgery and hospital stay are significantly longer in the group converted to open surgery in univariate analyses (we find no difference in multivariate analyses.).

Intra-abdominal adhesions due to a previous surgery are reported to create a risk factor since they may cause anatomical difficulties in imaging the appendix during surgery.¹³ In our study, a statistical evaluation was not possible due to the insufficient number of patients who previously had abdominal surgery.

Antonacci et al. report that the pathology result obtained postoperatively, showing the severity of appendiceal inflammation, is also effective in the risk of conversion to open surgery.¹² In our study, when we combine the patients who were converted to open surgery and laparoscopic appendectomies into a single group in terms of pathology results, we find no significant difference in terms of the risk of conversion to open surgery.

Conclusion

Knowing the risk factors for conversion from laparoscopic appendectomy to open surgery can guide the surgeon to start the surgery openly, thus avoiding unnecessary risk and cost increase. In the literature, there are studies reporting separate clinical, laboratory, and radiological findings, which cause an increased risk for conversion to open surgery. We find that collecting all these variables under one roof is more effective in evaluating the patient as a whole.

Footnotes

Authors' Contributions

Conceptualization: N.T. and C.D.; methodology: N.T., C.D., and B.N.K.; data curation: N.T., T.Y.K., and B.N.K.; writing—original draft preparation: N.T. and T.Y.K.; visualization and investigation: N.T., C.D., and E.Z.; supervision: C.D. and E.Z.; software and validation: N.T., C.D., and B.N.K.; writing—reviewing and editing: N.T. and E.Z.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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