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Clinical application of intraoperative somatic tissue oxygen saturation for detecting postoperative early kidney dysfunction patients undergoing living donor liver transplantation: A propensity score matching analysis

  • Jaesik Park,

    Roles Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Sangmin Jung,

    Roles Data curation, Investigation

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Sanghoon Na,

    Roles Data curation, Investigation

    Affiliation Department of Anesthesiology and Pain Medicine, Incheon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Ho Joong Choi,

    Roles Formal analysis, Investigation

    Affiliation Department of Surgery, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Jung-Woo Shim,

    Roles Investigation, Methodology

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Hyung Mook Lee,

    Roles Investigation, Methodology

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Sang Hyun Hong,

    Roles Formal analysis, Supervision

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

  • Min Suk Chae

    Roles Conceptualization, Formal analysis, Investigation, Methodology, Supervision, Visualization, Writing – original draft, Writing – review & editing

    shscms@gmail.com

    Affiliation Department of Anesthesiology and Pain Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

Abstract

Background

Somatic tissue oxygen saturation (SstO2) is associated with systemic hypoperfusion. Kidney dysfunction may lead to increased mortality and morbidity in patients who undergo living donor liver transplantation (LDLT). We investigated the clinical utility of SstO2 during LDLT for identifying postoperative kidney dysfunction.

Patients and methods

Data from 304 adults undergoing elective LDLT between January 2015 and February 2020 at Seoul St. Mary’s Hospital were retrospectively collected. Thirty-six patients were excluded based on the exclusion criteria. In total, 268 adults were analyzed, and 200 patients were 1:1 propensity score (PS)-matched.

Results

Patients with early kidney dysfunction had significantly lower intraoperative SstO2 values than those with normal kidney function. Low SstO2 (< 66%) 1 h after graft reperfusion was more highly predictive of early kidney dysfunction than the values measured in other intraoperative phases. A decline in the SstO2 was also related to kidney dysfunction.

Conclusions

Kidney dysfunction after LDLT is associated with patient morbidity and mortality. Our results may assist in the detection of early kidney dysfunction by providing a basis for analyzing SstO2 in patients undergoing LDLT. A low SstO2 (< 66%), particularly 1 h after graft reperfusion, was significantly associated with early kidney dysfunction after surgery. SstO2 monitoring may facilitate the identification of early kidney dysfunction and enable early management of patients.

Introduction

Living donor liver transplantation (LDLT) is a critical treatment for patients with end-stage liver disease (ESLD). Kidney dysfunction is one of the most common complications after liver transplantation (LT), affecting short- and/or long-term outcomes. Therefore, it is essential to identify intraoperative risk factors for the development of kidney dysfunction [1]. Many factors affect the development of kidney dysfunction after LT, such as the model for end-stage liver disease (MELD) score, age, sex, body mass index (BMI), chronic kidney disease, and diabetes mellitus (DM) [2]. Because of intraoperative hemodynamic fluctuations, renal tissue may be susceptible to hypoperfusion that subsequently leads to kidney functional impairment. Therefore, continuous monitoring of organ/tissue perfusion and saturation is valuable to avoid functional and structural injury [3].

Cerebral oximetry is a technique developed for detecting regional cerebral oxygen saturation using near-infrared (NIR) spectroscopy. NIR light contacts the hemoglobin beneath the sensor, which causes the light spectrum to change. This light returns to the detector of the oximeter and regional hemoglobin oxygen saturation (rSO2) [cerebral (SctO2) and somatic (SstO2) tissue oxygen saturations] can be determined [4]. Cerebral oximetry has been applied during major surgeries, such as cardiac surgery and carotid endarterectomy [5]. A lower rSO2 in patients undergoing cardiac surgery is associated with a higher risk of morbidities (such as necrotizing enterocolitis), high lactate levels, and low mixed venous oxygen saturation. These findings suggest that a lower rSO2 may be a clinical marker for poor systemic perfusion and saturation [6, 7]. In a previous report of adults undergoing cardiac surgery, the SstO2 value recorded from the thenar muscle of the hand was associated with the development of acute kidney injury (AKI). In that report, the SstO2 20 min after cardiopulmonary bypass had a cut-off value of ≤ 54.5% and acceptable area under the receiver operating characteristic curve (AUC) values of around 70% [8].

In patients undergoing LT, SstO2 monitoring may play a role in detecting early complications, such as graft rejection or abdominal compartment syndrome [911]. Multi-site applied NIR spectroscopic monitoring, including SctO2 and SstO2, is available to facilitate the detection of systemic/peripheral hypoperfusion [12, 13]. In a previous LT study [14], low arterial oxygen content was significantly associated with postoperative kidney dysfunction. Because low SstO2 is closely related to inadequate oxygen delivery [15], continuous and noninvasive SstO2 monitoring may be useful for assessing the risk of early kidney dysfunction during surgery.

The role of SstO2 in kidney function monitoring during LDLT surgery has still not been established; thus, we investigated the clinical utility of intraoperative SstO2 for identifying kidney dysfunction during the early postoperative period.

Patients and methods

Ethical considerations

The present study was approved by the Institutional Review Board and Ethics Committee of Seoul St. Mary’s Hospital (approval number: KC20RISI0176), Seoul, Republic of Korea on April 6, 2020, and the study was performed according to the principles of the Declaration of Helsinki. The requirement for informed consent was waived because of the retrospective nature of the study.

Study population

Data from 304 adults (aged > 19 years) undergoing elective LDLT between January 2015 and February 2020 at Seoul St. Mary’s Hospital were retrospectively collected from the electronic medical records system. Exclusion criteria included a preoperative history of kidney dysfunction (e.g., dialysis, chronic kidney disease [estimated glomerular filtration rate (eGFR) < 60 mL/min/1.73 m2], or hepatorenal syndrome), and missing laboratory data. Thirty-six patients were excluded based on the exclusion criteria, of which twelve (33.3%) were excluded because of missing data. In total, 268 adults were analyzed, and 200 were matched via 1:1 propensity score (PS) matching (S1 Fig).

Oximetry monitoring

All patients were monitored using the INVOS 5100c oximeter (Medtronic, Minneapolis, MN, USA) which consists of a light source and detectors. Based on the difference in NIR light absorption between oxygenated and unoxygenated hemoglobin, the oximeter system calculates hemoglobin saturation of the blood, in the brain or other tissues beneath the sensor, using the Beer-Lambert law [4, 16].

In the present study, a somatic sensor was placed on the forearm on the opposite side of the peripheral venous line (S2 Fig). The cerebral sensor was placed laterally on the skin of the patients’ forehead on the same side as the somatic sensor. Somatic (SstO2) and cerebral (SctO2) oximetry values were recorded five times after inducing anesthesia (immediately after anesthetic induction [T0], immediately after liver dissection [T1], at the time of inferior vena cava [IVC] partial clamping [T2], 5 min after graft reperfusion [T3], and 1 h after graft reperfusion [T4]).

Definition of early kidney dysfunction

Kidney function was evaluated based on the eGFR, calculated using the Modification of Diet in Renal Disease formula: eGFR = 175 × standardized serum creatinine-1.154 × age-0.203 × 1.212 (if black) × 0.742 (if female) [17]. The baseline eGFR was estimated the day before surgery, and serial eGFRs were measured on postoperative days (PODs) 1–7. Based on the eGFR [18], kidney function was classified as normal (eGFR ≥ 90 mL/min/1.73 m2), mild dysfunction (eGFR 89–60 mL/min/1.73 m2), or moderate dysfunction (eGFR 59–30 mL/min/1.73 m2). In our study, early kidney dysfunction was defined as the lowest eGFR < 60 mL/min/1.73 m2 during the first week after surgery.

Living donor liver transplantation

LT and general anesthesia were performed by expert surgeons and anesthesiologists, respectively. The surgical procedure and anesthetic management were described in detail in our previous study [19]. The surgical technique was identical for the entire study population [20]. The piggyback surgical technique was performed using the right liver lobe and the middle hepatic vein tributaries (segments 5 and 8) were connected to the middle hepatic vein of the recipient using prosthetic grafts. Vascular anastomoses (hepatic vein, portal vein, and hepatic artery) and bile duct reconstruction were performed. Cross-clamping of the inferior vena cava (IVC) was performed for the hepatic and portal vein reconstruction and hepatic vascular flow (portal venous flow and hepatic arterial resistive index) were evaluated with Doppler ultrasonography (Prosound SSD-5000; Hitachi Aloka Medical, Tokyo, Japan). Splenectomy, splenic artery ligation was performed as required.

Balanced anesthesia was applied with proper hemodynamic management (mean arterial pressure ≥ 65 mm Hg and central venous pressure ≤ 10 mm Hg) under hemodynamic monitoring. According to the transfusion guidelines, [21] packed red blood cells were transfused to reach a hematocrit ≥ 25%, and coagulation factors (fresh frozen plasma, single-donor platelets, and cryoprecipitate) were transfused based on laboratory findings or thromboelastography.

As calcineurin inhibitor was used as an immunosuppressant after surgery. The trough calcineurin inhibitor level was maintained between 7 and 10ng/mL for the first postopearative month. Other immunosuppressants (mycophenolate mofetil and prednisolone), which were administered according to our hospital’s LDLT protocol, were gradually adjusted and tapered after LDLT [20, 22].

Perioperative recipient and donor findings

The preoperative recipient findings included age, sex, BMI, comorbidities (hypertension and DM), ejection fraction, eGFR, MELD score, hepatic decompensation parameters (encephalopathy [West-Haven grade I–II] [23], ascites, and varix), and laboratory data (hematocrit, white blood cell [WBC] count, and percentages of neutrophils and lymphocytes). The intraoperative recipient findings included operation time, requirement for a norepinephrine infusion (≥ 0.05 μg/kg/min), averages of the hemodynamic parameters (systolic and diastolic blood pressure, heart rate, and central venous pressure), blood product requirements (packed red blood cells, fresh frozen plasma, single donor platelets, and cryoprecipitate transfusions), laboratory data (hemoglobin and lactate), hourly fluid infusion, and hourly urine output. The postoperative findings in recipients included the eGFR and kidney dysfunction (eGFR < 60 mL/min/1.73 m2). Donor findings included age, sex, BMI, graft-recipient weight ratio, total ischemic time, and donor graft fatty change.

Statistical analyses

We compared the levels of tissue oxygen saturation (SstO2 and SctO2) between the normal and kidney dysfunction groups using analysis of covariance (ANCOVA). Oxygen saturation at each stage was also compared using the Mann-Whitney U test and χ2 or Fisher’s exact test, as appropriate. The predictive accuracy of the models was evaluated based on the AUC. The optimal cut-off of the SstO2 for the prediction of early kidney dysfunction was determined using the AUC. In addition, 1:1 PS matching was used to correct any imbalance in confounders between the low and high SstO2 groups. After matching, we compared perioperative recipient and donor graft factors using the Mann-Whitney U test and χ2 or Fisher’s exact test, as appropriate. The association between low SstO2 1 h after graft reperfusion (< 66%) and postoperative early kidney dysfunction was evaluated by multivariate logistic regression analyses after adjusting for the PS and intraoperative factors, and odds ratios (ORs) with 95% confidence intervals (CIs) were calculated. Continuous data are presented as medians and interquartile range (IQR), and categorical data are presented as frequencies and proportions. A p-value < 0.05 was considered significant in all analyses. Statistical analyses were performed with SPSS for Windows (ver. 24.0; IBM Corp., Armonk, NY, USA), R software (ver. 2.10.1; R Foundation for Statistical Computing, Vienna, Austria), and MedCalc for Windows (ver. 11.0; MedCalc, Ostend, Belgium).

Results

Comparison of oxygen saturation between patients with and without early kidney dysfunction

Patients with early kidney dysfunction showed significantly lower intraoperative SstO2 than those without (ANCOVA, p < 0.001; Fig 1 and S1 Table). However, SctO2 did not differ between patients with and without kidney dysfunction (ANCOVA, p = 0.607).

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Fig 1. Comparison of oxygen saturation between patients with and without early kidney dysfunction at each stage.

The curve and shaded area represent median and IQR values of oxygen saturation, respectively. T0 = immediately after anesthetic induction; T1 = immediately after liver dissection; T2 = IVC partial clamping; T3 = 5 min after graft reperfusion; T4 = 1 h after graft reperfusion.

https://doi.org/10.1371/journal.pone.0262847.g001

Association of the area under the receiver operating characteristic curve with intraoperative SstO2 and change in SstO2 reflecting postoperative early kidney dysfunction in all patients

Regarding the SstO2 AUC values at different times (Fig 2(A)), that at T4 (1 h after graft reperfusion) was most significantly associated with early kidney dysfunction. A low SstO2 (< 66%) at T4 was significantly associated with early kidney dysfunction (AUC: 0.733, 95% CI: 0.675–0.785, sensitivity: 70.1%, specificity: 70.1%, p < 0.001 in the predictive model). Regarding the receiver operating characteristics curves of the change in SstO2 compared to saturation at T0, the difference in oxygen saturation between T0 and T1 was significantly associated with early kidney dysfunction (AUC: 0.708, 95% CI: 0.65–0.762, sensitivity: 70.1%, specificity: 67.2%, p < 0.001 in the predictive model; Fig 2(B)).

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Fig 2.

Comparison of the AUC values of SstO2 (A) and the AUC for the change in SstO2 compared to saturation at the time of anesthesia induction (B) for postoperative early kidney dysfunction, at each stage. T0 = immediately after anesthetic induction; T1 = immediately after liver dissection; T2 = IVC partial clamping; T3 = 5 min after graft reperfusion; T4 = 1 h after graft reperfusion.

https://doi.org/10.1371/journal.pone.0262847.g002

Comparison of pre-and intraoperative recipient and donor graft factors before and after PS matching

Significant differences were observed in the preoperative factors (MELD score, ascites, hematocrit, and WBC count) and donor-graft parameters (BMI, graft-to-recipient weight ratio, and total ischemic time; Table 1) between the high and low SstO2 groups. No significant differences were detected between the groups after PS matching.

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Table 1. Preoperative recipient and donor-graft findings for the high and low somatic tissue oxygen saturation (1 h after graft reperfusion) groups, before and after PS-matching.

https://doi.org/10.1371/journal.pone.0262847.t001

Correlation between low SstO2 1 h after graft reperfusion and early postoperative kidney dysfunction in PS-matched patients

A low SstO2 (< 66%) 1 h after graft reperfusion was significantly associated with the development of early kidney dysfunction in PS-matched patients (Table 2). After adjustment for the PS and intraoperative factors, a low SstO2 remained an independent predictor of early kidney dysfunction (p = 0.001).

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Table 2. Association between low somatic tissue oxygen saturation (< 66%) 1 h after graft reperfusion and postoperative early kidney dysfunction in PS-matched patients.

https://doi.org/10.1371/journal.pone.0262847.t002

Comparison of the incidence of postoperative early kidney dysfunction between PS-matched patients with high and low SstO2 1 h after graft reperfusion

Significantly more patients in the low SstO2 group (< 66%) suffered early kidney dysfunction (eGFR < 60 mL/min/1.73 m2) than in the high SstO2 group (≥ 66%) (p < 0.001; Table 3).

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Table 3. Comparison of the incidence of postoperative early kidney dysfunction between PS-matched patients with high and low somatic tissue oxygen saturation 1 h after graft reperfusion.

https://doi.org/10.1371/journal.pone.0262847.t003

Comparison of the proportions of kidney dysfunction between PS-matched patients with high and low SstO2 1 h after graft reperfusion

Significantly more patients suffered kidney dysfunction (eGFR < 60 mL/min/1.73 m2) during the first week in the low SstO2 group (< 66%) after surgery than in the high SstO2 group (≥ 66%) (Table 4).

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Table 4. Comparison of the proportions of kidney dysfunction between PS-matched patients with high and low somatic tissue oxygen saturation 1 h after graft reperfusion.

https://doi.org/10.1371/journal.pone.0262847.t004

Correlation between intraoperative somatic tissue oxygen saturation (%) and hourly urine output during liver transplantation

The somatic tissue oxygen saturation (%) at times T1–T4 was significantly associated with the hourly urine output (all p < 0.001, S2 Table).

Discussion

The main finding of this study was that intraoperative SstO2 may have clinical utility to identify patients at risk of a decrease in eGFR < 60 mL/min/1.73 m2 during the first week after LDLT. A low SstO2 (< 66%) 1 h after graft reperfusion had higher predictive accuracy for early kidney dysfunction than values measured in other intraoperative phases. The low SstO2 (< 66%) in PS-matched patients, adjusted for PS and intraoperative factors, was approximately four-fold more strongly associated with early postoperative kidney dysfunction. A decline in the SstO2 compared to that measured immediately after inducing anesthesia was also related to kidney dysfunction. Thus, SstO2 itself, and deterioration therein, could also be important for predicting kidney dysfunction.

Intraoperative SstO2 monitoring has been widely performed in pediatric patients, and is usually measured in the renal, splanchnic, or thoracic beds because of the anatomical features (i.e., thin skin and subcutaneous adipose tissue). Pediatric cohort studies suggest that SstO2 is closely associated with systemic oxygenation, transfusion of red blood cells, and circulatory indices. Patients with a lower SstO2 level require more extracorporeal membrane oxygenation, inspired nitrogen, and mechanical ventilation than those with a higher SstO2 level [13, 2426]. Pediatric renal SstO2 is an emerging and reliable non-invasive tool to identify early loss of kidney function. In cardiac surgery with cardiopulmonary bypass and an oximeter sensor at the level of the kidney (T10–L2) for renal oximetry, infants (aged < 1 year) with prolonged lower renal SstO2 values (i.e., oximetry < 65% and a relative decrease therein > 25%) during surgery and the first 48 h postoperatively showed more frequent AKI than those with higher values. Additionally, renal SstO2 may be better correlated with AKI compared to conventional laboratory markers (i.e., serum creatinine, urea and cystatin C, and urinary neutrophil gelatinase-associated lipocalin) [27].

Few studies have monitored SstO2 in the trunk beds of adults, including the renal beds, compared to the pediatric setting. One cardiac study reported that the intraoperative duration of renal SstO2 < 55% was associated with the postoperative occurrence of AKI [28]. However, because of the thicker skin and subcutaneous fatty tissues on the body trunk of adults than children, the SstO2 sensors are typically placed over skeletal muscles (i.e., the thenar eminence, forearm, or calf area) [29]. In a previous study of adults undergoing cardiac surgery, the SstO2 recorded from the thenar muscle of the hand was associated with the development of AKI. In that report, the SstO2 20 min after cardiopulmonary bypass had a cut-off value of ≤ 54.5% and acceptable AUC values of around 70% [8]. Intraoperative tissue oxygenation status may be a composite marker of the balance between oxygen supply and consumption, which is largely determined by hemodynamic perfusion, a venous-weighted mixture of venous and arterial hemoglobin-oxygen saturation, and anesthetic-suppressed or surgical stress-related elevation of the metabolic rate [30].

SstO2 is an emerging marker of early postoperative complications in patients undergoing LT; however, SstO2 measurement sites differ among LT studies [911]. In an intensive care unit study by Civantos et al., the oximetry sensor was placed on the dermatome overlying the liver allograft [9]. SstO2 was significantly associated with the cardiac index, hemoglobin, and APACHE II score. Shiba et al. reported that a reduction in SstO2 (monitored on the dermatome overlying the liver allograft) was associated with an increased risk of acute graft rejection [10]. Hu et al. reported that full drainage of ascites during LT led to an increased leg SstO2; however, IVC clamping and abdominal hypertension caused a significant reduction in the leg SstO2. Somatic leg desaturation was more strongly associated with postoperative complications than arm and cerebral desaturation [11]. In our study, the SstO2 was measured at the forearm, which is more easily adjusted than a trunk bed. A lower SstO2 (measured at the forearm 1 h after graft reperfusion) increased the likelihood of early postoperative kidney dysfunction. SstO2 measured at the forearm provides an estimate of hemoglobin oxygen saturation in the mixed arterial, capillary, and venous blood in the tissue bed being probed, and is largely determined by the balance between organ/peripheral tissue oxygen consumption/supply and perfusion [31]. LT patients require large resuscitation and inotrope infusion volumes for vascular homeostasis; thus, SstO2 measured at the forearm may represent organ/peripheral tissue microcirculation, which is closely related to cardiac and systemic resistive indices [32, 33]. Large vital sign fluctuations have been observed within 1 h after liver graft reperfusion, and vasopressors and volume loading are frequently used to restore hemodynamics. Peripheral vascular tone declines (which may contribute to systemic hypotension) because of a huge surge in the circulation of inflammatory mediators from the liver graft, which may lead to organ/tissue hypoperfusion and desaturation [34]. Therefore, the lowest SstO2 level measured at the forearm 1 h after graft reperfusion may be a clinical marker of the lowest level of renal perfusion.

Some limitations of this study should be discussed. First, because cerebral oximetry was developed for detecting hypoperfusion of the brain, there is no established reference value for detecting hypoperfusion of other organs. Although a low SstO2 has been associated with organ dysfunction in previous studies [9, 27, 33], further study is required to validate the level of SstO2 for other organs, particularly the kidneys. Second, the somatic oximeter sensor was placed on the forearm in this study, and not on the renal parenchymal surface. Therefore, although SstO2 may reflect tissue oxygen perfusion status, it does not directly reflect the renal perfusion or saturation conditions. Therefore, further studies are required to determine the predictive value of SstO2 according to monitoring site. Third, there are important differences between liver transplants from living and deceased donors. In previous studies, LT with grafts from deceased donors were more than twice as strongly associated with postoperative AKI [35]. Further studies are required to validate the predictive value of SstO2 for kidney dysfunction in LT from deceased donors.

Conclusion

Our results should increase the accuracy of detection of early kidney dysfunction by providing a basis for analyzing intraoperative SstO2 in patients undergoing LDLT. A low level of SstO2 during LDLT, particularly 1 h after graft reperfusion, was significantly associated with early kidney dysfunction after surgery. When a low SstO2 is detected, meticulous monitoring and efforts to improve the possible causes of compromised tissue perfusion (hypovolemia, hypotension, or shock) are likely important. SstO2 monitoring provided additional information that may facilitate early management of LT patients who are vulnerable to kidney dysfunction.

Supporting information

S2 Fig. A near-infrared spectroscopy probe, positioned on the left or right forearm.

https://doi.org/10.1371/journal.pone.0262847.s002

(TIF)

S1 Table.

Comparison of changes in the (A) somatic tissue and (B) cerebral oxygen saturation levels between patients with and without early kidney dysfunction.

https://doi.org/10.1371/journal.pone.0262847.s003

(DOC)

S2 Table. Correlation between the intraoperative somatic tissue oxygen saturation (%) and hourly urine output during liver transplantation.

https://doi.org/10.1371/journal.pone.0262847.s004

(DOC)

S1 Raw data. Data set on the association between low somatic tissue oxygen saturation (< 66%) 1 h after graft reperfusion and postoperative early kidney dysfunction in PS-matched patients.

https://doi.org/10.1371/journal.pone.0262847.s005

(XLSX)

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