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The Amount of Fluid Given During Surgery That Leaks Into the Interstitium Correlates With Infused Fluid Volume and Varies Widely Between Patients

Nishimura, Akiko DDS, PhD; Tabuchi, Yoko DDS; Kikuchi, Mutsumi DDS, PhD; Masuda, Rikuo DDS, PhD; Goto, Kinuko DDS, PhD; Iijima, Takehiko DDS, DMSc, PhD

doi: 10.1213/ANE.0000000000001505
Critical Care and Resuscitation: Original Clinical Research Report
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BACKGROUND: The revised Starling law suggests that intravenously infused fluid may leak into the interstitium and not remain in the intravascular space. This hypothesis is supported by clinical findings that postoperative weight gain is proportional to the amount of infused fluid. The distribution of intravenously administered fluid between the interstitium and intravascular space deserves evaluation, as postoperative weight gain because of intraoperative infusion is an important risk factor for postoperative adverse events. We quantitatively estimated fluid movement in patients undergoing orthognathic surgery by performing a volume kinetic study using hemoglobin concentration as a marker of dilution.

METHODS: Forty-one patients scheduled to undergo orthognathic surgery were enrolled in this study. The arterial hemoglobin concentration was measured at each procedural step. Acute normovolemic hemodilution was induced by withdrawing 400 mL of blood followed by the infusion of a known amount of hydroxyethyl starch, enabling the initial blood volume to be estimated. The dilution rate of the arterial hemoglobin concentration enabled the volume of fluid in the intravascular space to be quantified. The fluid volume that leaked into the interstitium was then calculated based on the change in the estimated intravascular plasma volume.

RESULTS: The blood volume estimated via this method was close to the value derived from a previously published formula. The mean volume of crystalloid infused as a maintenance fluid was 2062 ± 408 mL, ranging from 1220 to 3050 mL. None of the cases required blood product transfusion. The amount of infused fluid that remained intravascular varied widely from 2.0 to 35.7 mL/kg (mean, 12.0 ± 8.2 mL) after surgery, corresponding to 5.3% to 95.7% of the infused volume. The change in intravascular fluid volume during surgery was not strongly correlated with the infusion amount (Pearson correlation analysis: r = −0.05, P = .75, −0.44 < ρ ≤ 0.35, confidence intervals; Spearman correlation analysis: r = −0.14, P = .38, −0.51 < ρ ≤ 0.27). However, the amount of fluid that leaked into the interstitium during surgery did correlate with the infusion amount (Pearson correlation analysis: r = 0.42, P = .01, 0.03 < ρ ≤ 0.70; Spearman correlation analysis: r =0.45, P = .003, 0.07 < ρ ≤ 0.72).

CONCLUSIONS: We found that the increase in intravascular fluid volume caused by intravenous fluid administration was not correlated strongly with the volume of infused fluid. Instead, the amount of fluid leakage into the interstitial space depended on the infused fluid volume. This clinical result supports the revised Starling law, which suggests that intravascular fluid may often leak into the interstitium. More work is needed to better understand the factors governing leakage of infused fluid into the interstitial space.

From the Division of Anesthesiology, Department of Perioperative Medicine, Showa University School of Dentistry, Tokyo, Japan.

Accepted for publication June 9, 2016.

Funding: None.

The authors declare no conflicts of interest.

Reprints will not be available from the authors.

Address correspondence to Takehiko Iijima, DDS, DMSc, PhD, Division of Anesthesiology, Department of Perioperative Medicine, Showa University School of Dentistry, 2-1-1 Kitasenzoku, Ohta-Ku, Tokyo 145–8515, Japan. Address e-mail to iijima@dent.showa-u.ac.jp.

Postoperative weight gain is a major risk factor for postoperative complications.1,2 One reason for postoperative weight gain may be excessive fluid administration. Although basing fluid administration on an hourly rate (milliliter per kilogram per hour) is a common approach, it does not account for fluctuating physiologic needs and may not be optimal for all patients.3–7 Recently, a revision of the Starling law was proposed based on the argument that oncotic forces are often too weak to reverse the hydrostatically driven movement of fluid from the intravascular to extravascular space.8–11 According to this revision, leakage of fluid from the intravascular to extravascular space may occur in capillaries and even venules and may be exacerbated by high hydrostatic pressures. Absorption (defined as fluid movement from the extravascular to intravascular space) arising from oncotic forces rarely occurs.8 This concept suggests that infused fluid may accumulate in a dose-dependent fashion in the extravascular space.8,9

To clarify the distribution of intravenously infused fluid between the intravascular and interstitial spaces, we analyzed the change in hemoglobin concentration with perioperative hemodilution and fluid administration.12,13 We hypothesized that the amount of infused fluid would correlate with the change in intravascular fluid volume during surgery.

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METHODS

This study was approved by the Clinical Research Ethics Committee of the Showa University School of Dentistry (Approval number; 2011–037) and was registered at University hospital Medical Information Network Clinical Trial Registry (UMIN-CTR) (UMIN000013996). The ethics committee approved the study on October 14, 2011. Patients aged 20 years or older were recruited, and the follow-up extended from January 19 to July 29, 2012. Written informed consent was obtained from all subjects (n = 41).

Patients were anesthetized with either total intravenous anesthesia (TIVA) (propofol and remifentanil) or inhalational anesthesia (sevoflurane and remifentanil). After endotracheal intubation and monitor set-up, an arterial line was placed in a radial artery, and 400 mL of autologous blood was withdrawn from an antecubital vein and kept in a bag containing CPDA solution (citrate-phosphate-dextrose with adenine) at room temperature. The patients were then given 500 mL of hydroxyethyl starch intravenously (6% HES 70/0.55/4, saline hydroxyethyl starch (HES), 70 kd; Otsuka Pharmaceutical Factory, Japan. During surgery, acetated Ringer solution was infused for maintenance at a rate of 4 to 6 mL/kg/h and was administered on a supplementary basis as needed at the discretion of the anesthetist. After the surgery was complete, the withdrawn blood was reinfused to the patients.

The arterial hemoglobin concentration was measured at the following time points: before and after the withdrawal of blood, after HES infusion, after surgery, and after the reinfusion of the withdrawn blood. We assumed that the HES70 used in this study has an intravascular volume expanding effect equivalent to the infused volume (1.03 ± 0.21).14 Using these data along with the hemorrhage amount and the urine volume, we estimated the blood volume (BV) and the intravascular and extravascular fluid movement. The details of this procedure are described in the Appendix. To summarize in brief, a constant exchange of blood with plasma expander enabled us to estimate the BV, because the dilution rate of the hemoglobin concentration is inversely correlated with the BV. Once the initial BV has been obtained, the change in hemoglobin can then be converted to the change in BV if the total hemoglobin is constant or the loss of blood can be estimated. The bleeding amount was calculated carefully by weighing the gauze and calculating the volume of the suction amount minus the amount of irrigation saline. The average amount of bleeding in this study was estimated as 255 ± 169 mL.

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Basic Calculations

The amount of total hemoglobin in the circulation blood (HB) was derived by multiplying the BV and the initial hemoglobin concentration (Hb) as follows:

The total hemoglobin is constant during acute normovolemic hemodilution (ANH); therefore, the amount of hemoglobin after ANH was calculated based on the transition in the hemoglobin concentration as shown below. The hemoglobin content of the ANH bags (400 mL) was calculated as follows:

If the hemoglobin concentration after ANH was Hb, the following formula can be expressed:

BV can be calculated from Equations (1) and (2) as follows:

If the fluid (α mL) entering the intravascular space and the hemoglobin concentration become Hb, then the following formula can be expressed:

Thus, α can be expressed as follows:

Bleeding and urine output during surgery should also be considered. The details of these calculations are explained in the Appendix.

Finally, the following values were obtained. The retained intravascular fluid volume during surgery was defined as follows: (fluid volume, including plasma and remaining fluid, after surgery) − (plasma volume before surgery). This volume represents the amount of infused fluid given during the operation that remained in the intravascular space after surgery and corresponds to β in the Appendix. The fluid volume that leaked into the interstitium was defined as follows: (infused fluid volume) − (retained intravascular fluid volume: β). Also, the retained intravascular fluid volume after the reinfusion of autologous blood was defined as follows: (fluid volume, including plasma and remaining fluid, after the reinfusion of autologous blood) − (initial plasma volume). This volume corresponds to γ in the Appendix. The fluid volume that leaked into the interstitium was defined as follows: (infused fluid volume) − (retained intravascular fluid volume: γ).

The BV was also estimated with the Ogawa-Fujita formula (men: predicted BV = 0.168H3 + 0.050W + 0.444; women: predicted BV = 0.2502H3 + 0.0625W − 0.662; data obtained using the I131 dilution technique15) and the Iijima et al’s16 formula (men: predicted BV = 0.700H3 + 0.042W − 0.691; women: predicted BV = 0.075H3 + 0.038W + 2.002; data were obtained by the use of indocyanine green dilution and pulse dye densitometry). The values were then compared to validate the findings that were estimated using the volume kinetic (VK) study.

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Statistical Analysis

The values were represented as the mean ± standard deviation. The correlation coefficient between the fluid volume that leaked into the interstitium or the retained intravascular fluid volume and the infused fluid volume was computed using the Pearson and Spearman correlation coefficients (statistical software, SPSS version 17; SPSS Inc, Chicago, IL). A P value < .01 was considered statistically significant, and 99% of confidence interval for correlation coefficient was calculated for the reference of judgment of significance.

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RESULTS

General Condition of the Subjects in This Clinical Study

Table. De

Table. De

The average patient age was 27.3 ± 8.6 years. Thirty-eight of 41 patients were American Society of Anesthesiologists physical status 1, and 3 were American Society of Anesthesiologists physical status II. All the patients were undergoing orthognathic surgery to correct deformities of the maxilla and mandible. Because this surgery occasionally requires transfusion if a venous plexus or artery is damaged, ANH was applied prophylactically in all the patients. All patients had fasted since awakening from sleep and had been allowed to drink water until 2 hours before anesthetic induction. None of the patients were suspected of having preoperative dehydration. Crystalloid was infused for maintenance at a rate of 7.3 ± 1.8 mL/kg/h, and the duration of surgery varied widely from 1 hour, 45 minutes to 7 hours, 1 minute. Thus, the total volume of infused crystalloid ranged from 12.6 to 39.7 mL/kg. The intraoperative urine output was 2.6 ± 2.0 mL/kg/h, and the total urine volume was 692.0 ± 463.4 mL during the immediate postoperative period. None of the patients required the administration of supplemental colloid or homologous transfusion. None of the patients had any minor or major postoperative morbidity (Table).

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Estimation of BV for the Validation of Our VK Study

The BV was calculated based on the change in the hemoglobin concentration after a constant volume exchange of blood and HES. The mean value was 4079 ± 1240 mL. The estimated value with the Ogawa-Fujita formula15 was similar (4135 ± 626 mL). Using a formula proposed by us previously and based on the results of a multicenter trial16,17 that used a dye densitogram (DDG) analyzer, we found that BV was 4888 ± 786 mL.

We also calculated the fluid movement from the extravascular space to the intravascular space after blood withdrawal (α value in the Appendix). The fluid movement accompanying the acute withdrawal of blood was 232 ± 159 mL.

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Retained Intravascular Fluid Volume and Infused Amount of Crystalloid After Surgery and After the Reinfusion of Autologous Blood

The retained intravascular fluid volume varied widely, from 2.0 to 35.7 mL/kg (12.0 ± 8.2 mL) after surgery (β value in the Appendix). This volume represented between 5.3% and 95.7% (35.9% ± 24.7%) of the total infused fluid volume. The retained intravascular fluid volume was not correlated strongly with the infused fluid volume (Pearson correlation analysis: r = −0.05, P = .75, −0.44 < ρ ≤ 0.35; Spearman correlation analysis: r = −0.14, P = .38, −0.51 < ρ ≤ 0.27; not significant correlation; Figure 1).

Figure 1

Figure 1

Figure 2

Figure 2

After the reinfusion of autologous blood, the retained intravascular fluid volume fraction ranged from 7.3% to 113.3% (41.7% ± 24.5%) of the infused volume and again varied widely from 3.0 to 38.3 mL/kg (14.3 ± 8.4 mL). The retained intravascular fluid volume after reinfusion of autologous blood was also not strongly correlated with the infused fluid volume (Pearson correlation analysis: r = 0.13, P = .41, −0.28 < ρ ≤ 0.50; Spearman correlation analysis: r = 0.09, P = .56, −0.31 < ρ ≤ 0.47; not significant correlation; Figure 2).

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Leakage Into the Interstitium and Infused Amount of Crystalloid After Surgery

Figure 3

Figure 3

Figure 4

Figure 4

The volume of fluid that leaked into the interstitium did correlate with the infused fluid volume (Pearson correlation analysis: r = 0.42, P = .01, 0.03 < ρ ≤ 0.70; Spearman correlation analysis: r =0.45, P = .003, 0.07 < ρ ≤ 0.72; significant correlation; Figure 3). After the reinfusion of autologous blood, the volume of fluid that leaked into the interstitium decreased (Figure 4). The urine output was 383 ± 356 mL after surgery and 567 ± 424 mL after reinfusion. The infused volume was not strongly correlated with the leakage into the interstitium after blood reinfusion (Pearson correlation analysis: r = 0.25, P = .12, −0.16 < ρ ≤ 0.59; Spearman correlation analysis: r = 0.25, P = .11, −0.16 < ρ ≤ 0.59; not significant correlation; Figure 4).

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DISCUSSION

In this study, we analyzed the kinetics of infused fluid using the dilution rate of a biomarker in the bloodstream.18 This strategy has been described as a VK study and is used commonly to analyze and to simulate the distribution and elimination of infused fluids.19 The methodology has been applied widely to assess the distribution and elimination of fluids in various clinical settings.20–23 The present analysis used this model to quantify fluid movement in healthy patients undergoing jaw surgery. Because ANH was routine in our cases, we estimate the BV from the hemoglobin dilution rate.

Although VK studies are a well-established technique for exploring fluid shifts, we validated our estimate by comparing our results with the BV value estimated using a different formula. The value we estimated was similar to the value obtained in a former isotope study15 (4079 ± 1240 mL in our study versus 4135 ± 626 mL using the standard formula from the isotope study), which supports our method. Jacob et al24 previously estimated BV using the VK after ANH method and also found good agreement between the VK method and indocyanine green dilution and fluorescent red cells (−0.53% ± 7.84%). A shortcoming of the VK approach is that the BV or plasma value is estimated based on the hemoglobin level in the peripheral vessels, which may differ from the whole body hemoglobin level. The ratio between the whole body hematocrit level and the large vessel hematocrit level, called the F cell ratio, is assumed to be 0.8 to 1.0.25 Because our aim was to determine the relative change in intravascular fluid, we did not use the F-cell ratio to correct the value.

The fluid that “leaked” into the interstitium or “third” space after ANH (400 mL of blood withdrawn and 500 mL of HES infusion) was estimated based on the results of the VK study. This value varied substantially (232 ± 159 mL) but was consistent with our study protocol (at a hematocrit level of 40%, the volume of withdrawn plasma is approximately 240 mL, and if the volume of infused fluid [HES] is 500 mL, then 500 − 240 mL = 260 mL).

During the intraoperative period, we found that the infused fluid often moved from the intravascular to interstitial space. Our data showed that the retained intravascular volume was not strongly correlated with the infused volume. In several cases, only a few milligram per kilogram remained in the intravascular space (y = 0 corresponds to the absence of fluid; Figure 1). Our data are consistent with those of Rehm et al,26 who reported that the infused intraoperative crystalloid had little effect on the postoperative BV, and with other studies that found a minimal increase in BV despite a large positive balance of crystalloid in cardiovascular surgery patients.27,28

Previously, the Starling law, which describes an equilibrium between hydrostatic and oncotic forces, was considered responsible for governing the fractional distribution of infused fluid. Research on the glycocalyx as a protective barrier for fluid exchange, however, has suggested that this principle may not be uniformly correct.9 According to the revised Starling theory, outward movement of fluid is common, even in venules where hydrostatic pressure is low.9 In contrast, fluid reabsorption from the interstitium to the intravascular space, driven by the osmotic pressure difference between the plasma and the interstitium, occurs only transiently because the glycocalyx layer nullifies the difference between the extravascular and the intravascular osmotic pressures. Thus, return of interstitial fluid into the intravascular space occurs mostly because of lymph flow and not the osmotic pressure difference. Our clinical results agreed with this concept. Increases in infused fluid volume may have increased intravascular pressure, leading to more outward fluid movement from the intravascular to the interstitial compartment (“leakage into the interstitium”). Because the inward flow is driven by lymph accompanying protein movement, the volume of fluid retained intravascularly from the interstitial compartment back to the intravascular space would not necessarily be correlated with infused fluid volume (as we observed). The large variation in fluid absorption supports the hypothesis that fluid movement is driven not only by physiochemical forces but also by other forces such as the endocrine system.5 In other interpretations, absorption is dependent on intravascular hydrostatic pressure.

The distribution area of the infused crystalloid apparently consists of the extracellular space plus a small proportion of the intravascular space.29,30 Thus, the infused crystalloid may contribute to postoperative edema formation, particularly in the presence of anesthesia and/or surgical stress.31,32 Brandstrup1 has demonstrated that crystalloid accumulation is linked to postoperative complications, and several days are required for intraoperatively administered crystalloid to be completely excreted from the body. We demonstrated that large amounts of intraoperatively infused fluid may be distributed to the extracellular space, thus suggesting a cause of postoperative edema formation. However, the amount of fluid that leaked into the extracellular space decreased over time even after the reinfusion of homologous blood. Thus, our results should be applied to sustained postoperative edema formation with caution.

The concept of the “third space” provides a justification for the excess administration of fluids to support crystalloid-based BV maintenance. If the volume of the third space is determined by surgical stress and is self-limited, fluid administration would eventually expand the intravascular space. However, our observations that the fluid volume that leaked into the interstitium correlated with the infused volume suggest that the volume of the third space is unlimited and might increase with intraoperative infusion.3 In other words, the third space may be a product of fluid therapy, rather than an actual space determined by surgical stress.5,7,33

Current evidence does suggest that limiting perioperative fluid administration can improve outcomes. A 2014 trial administering crystalloid at the minimum maintenance fluid level found better outcomes among patients undergoing extensive urologic surgery.4 Clinical trials of a “zero-balance” fluid policy also have reported improved outcomes.3 Taken together, our data and those of previous trials suggest that minimizing crystalloid administration in surgical patients may not be detrimental.

Our study has limitations. We used HES to replace autologous blood removal, which may have influenced our results as HES may have a “plugging” effect on vascular permeability.34–36 Even so, we found that the amount of fluid that leaked into the interstitium was often greater than the amount of fluid that remained in the intravascular space. Our results also should be extrapolated to general surgical cases with caution. Intraoperative bleeding was limited in our patients, and cases with more blood loss may experience greater absorption to the intravascular space to maintain a minimum BV. In such cases, we predict that absorption would become predominant, rather than leakage into the interstitium. Further study of fluid replacement in bleeding patients is needed. Jacob et al30 showed that withdrawn BVs of >1000 mL cannot be restored using 3 times the amount of Ringer’s solution, and they estimated that only 17% ± 10% was retained intravascularly. This finding suggests that fluid replacement in bleeding patients may demonstrate the same “leakage” effect as in our study.

There were other limitations to this study. We had no formal control group within this case series of orthognathic surgery patients. Also, we could only estimate the blood loss by weighing sponges and measuring the amount of suction. Although the amount of bleeding could not be measured precisely, the impact of any error in the bleeding amount was thought to be very small in this study. The average bleeding amount corresponded to 17.5% ± 12.5% of the extravascular leakage fluid volume (leakage into the interstitium, urine output, and bleeding amount). Therefore, even if there was a 10% error in the estimated amount of bleeding, the error in the estimated amount of leakage fluid would be <2%.

In conclusion, we demonstrated that infused crystalloid was mostly leaked postoperatively in cases with minimal bleeding. This finding supports the concept behind the revised Starling law and a clinical practice of giving less intraoperative fluid. A greater understanding of the fundamental kinetics of infused fluids during surgery will help refine our understanding and optimal application of intraoperative fluid therapy.

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Appendix

ESTIMATION OF FLUID MOVEMENT

First formula, before the withdrawal of whole blood: The arterial hemoglobin concentration (Hb① [g/dL]) was expressed as [the total hemoglobin content (HB [g])]/[circulating blood volume (BV [mL])]. HB refers to the initial hemoglobin content in the whole blood.

Second formula, after the withdrawal of whole blood: The arterial hemoglobin concentration (Hb② [g/dL]) was expressed as [the total hemoglobin content (HB [g]) − the lost hemoglobin content because of withdrawal (−400 × Hb① [g])]/[circulating blood volume (BV [mL]) − 400 mL from withdrawal + α]. The parameter α was defined as the inflow to the intravascular space, including the infused HES.

Third formula, after HES infusion: The blood sample was collected immediately after the infusion of 500 mL of HES. The arterial hemoglobin concentration (Hb③ [g/dL]) was expressed as [the total hemoglobin content (HB [g]) − the lost hemoglobin content because of withdrawal (−400 × Hb① [g])]/[circulating blood volume (BV [mL]) − 400 mL from withdrawal + α + 500 mL of HES]. This procedure was considered to represent a 500-mL volume expansion.

Fourth formula, after surgery: The arterial hemoglobin concentration (Hb④ [g/dL]) was expressed as [the total hemoglobin content (HB [g]) − the lost hemoglobin content because of withdrawal (400×Hb① [g]) − the lost hemoglobin content during surgery (L × (Hb③ + Hb④)/2)]/[circulating blood volume (BV [mL]) − 400 mL from withdrawal + α + 500 mL of HES − L − U① + β]. The parameter L represents the amount of blood loss during surgery. The parameter U① represents the urine volume during surgery. The parameter β was defined as the inflow of fluid into the intravascular space (absorption) from the extravascular space and interstitial tissue. This flow included the infusion of fluid as well as fluid exchange between the intravascular and extravascular spaces. The β value corresponded to the retained intravascular fluid volume during surgery. The hemoglobin value of the hemorrhagic blood was estimated using the average of the values obtained after HES infusion and after surgery as follows: (Hb③+Hb④)/2.

Fifth formula, after reinfusion of autologous blood: The arterial hemoglobin concentration (Hb⑤ [g/dL]) was expressed as [the total hemoglobin content (HB [g]) − the lost hemoglobin content because of withdrawal (400 × Hb① [g]) − the lost hemoglobin content during surgery (L × (Hb③ + Hb④)/2) + the hemoglobin contained in the stored autologous blood (400 × Hb① [g])]/[circulating blood volume (BV [mL]) − 400 mL from withdrawal + α + 500 mL of HES − L − U② + γ + 400 mL of homologous blood]. The parameter U② was defined as the total urine volume after the reinfusion of autologous blood. The parameter γ was defined as the final volume of absorption after the reinfusion of the autologous blood.

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STATISTICAL POWER ANALYSIS

We performed a power analysis using G*Power software, version 3.1.4 (free software written by Franz Faul, Kiel University, Germany). Our results showed that r = 0.416 (between the infused volume and the leakage into the interstitium) and r = 0.016 (between the retained intravascular volume and the infused volume). From these data, the estimated total sample size was 31 patients to achieve a power of 0.8 for a correlation analysis between the infused volume and the leakage into the interstitium, and the total sample size was 24,144 patients to achieve a power of 0.8 for a correlation analysis between the retained intravascular volume and the infused volume. Therefore, a positive correlation observed for the 41 enrolled patients can be considered valid for the former correlation, whereas a negative correlation cannot be denied for the latter correlation until 24,144 patients have been enrolled. Because we used all enrolled 41 cases for statistical analysis instead of 31, we set significance level to <0.01 to avoid spurious judgment of significance.

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DISCLOSURES

Name: Akiko Nishimura, DDS, PhD.

Contribution: This author helped design the study, conduct the study, analyze the data, and write the manuscript.

Name: Yoko Tabuchi, DDS.

Contribution: This author helped conduct the study and analyze the data.

Name: Mutsumi Kikuchi, DDS, PhD.

Contribution: This author helped conduct the study and analyze the data.

Name: Rikuo Masuda, DDS, PhD.

Contribution: This author helped analyze the data.

Name: Kinuko Goto, DDS, PhD.

Contribution: This author helped analyze the data.

Name: Takehiko Iijima, DDS, DMSc, PhD.

Contribution: This author helped design the study, conduct the study, and write the manuscript.

This manuscript was handled by: Avery Tung, MD, FCCM.

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