Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran, Jean-Luc Fellahi
{"title":"牙龈毛细血管再充盈时间:评估组织灌注的新方法","authors":"Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran, Jean-Luc Fellahi","doi":"10.1186/s13054-025-05555-9","DOIUrl":null,"url":null,"abstract":"<p>Acute circulatory is a life-threatening condition, marked by inadequate tissue perfusion and oxygen delivery, leading to cellular dysfunction. Capillary refill time (CRT) is a widely used bedside marker of tissue perfusion but has limitations due to its sensitivity to temperature, pigmentation, and peripheral vascular disease [1, 2]. In veterinary medicine, gingival capillary refill time (GRT) is used to assess circulatory status via mucosal microcirculation, but its relevance in humans is unexplored [3]. GRT may provide a more robust alternative by directly assessing mucosal microcirculation and mitigating CRT limitations.</p><p>We conducted an ancillary analysis of the PeachCART cohort (NCT02248025) [4] to evaluate the feasibility, reproducibility, and clinical relevance of GRT in critically ill patients receiving fluid resuscitation for acute circulatory failure. We hypothesized that GRT would be feasible, correlate with CRT, and be a reliable predictor of perfusion-based fluid responsiveness.</p><p>The protocol was approved by the institutional review board; Oral and written information was given to all patients or relatives. Signed consent was waived by the ethics committee. GRT and CRT were recorded using an iPhone 6™ (8 MP camera). GRT involved applying calibrated pressure to the gingival mucosa with a 2 mL air-filled syringe compressed to 1 mL for 7 s. Four videos were taken per step by a single investigator and analyzed by two blinded readers. CRT was measured on chest skin using a 10 mL syringe compressed to 7 mL, as previously described. Volume expansion consisted of 500 mL lactated Ringer over 20 min, without changes in sedation or vasoactive drugs. Patients were monitored with PiCCO™ and thermodilution was performed before and after volume expansion. Metabolic and hemodynamic parameters, general patient characteristics, and Fitzpatrick skin phototype were also recorded. Primary outcomes were GRT feasibility and reproducibility; secondary outcomes included its correlation with CRT, predictive value for perfusion based fluid responsiveness (≥ 25% CRT reduction) [4], and association with hemodynamic and metabolic parameters.</p><p>Thirty-two patients were analyzed (median age: 62 [54–69] years, median SOFA score: 9 (6–11), SAPS II: 43 (33–51), and 84% on mechanical ventilation). Median GRT was 2.3 (1.6–3.2) s, and median CRT was 2.9 [2.4–3.8] s. Based on our linear regression model, the classical threshold of 3 s to define abnormal CRT corresponds to an estimated GRT of approximately 2.12 s. GRT was feasible in all patients, with a slightly lower interobserver coefficient of variation (5.2% [95% CI 0.9–9.6]) compared to CRT (7.3% [95% CI 3.9–10.2]). The median Fitzpatrick skin phototype was 3, GRT was easier to read in patients with phototype 1 and 4 as illustrated in Fig. 1. GRT was successfully measured in 97% of patients. No major adverse events were reported, except mild discomfort in one patient.</p><figure><figcaption><b data-test=\"figure-caption-text\">Fig. 1</b></figcaption><picture><source srcset=\"//media.springernature.com/lw685/springer-static/image/art%3A10.1186%2Fs13054-025-05555-9/MediaObjects/13054_2025_5555_Fig1_HTML.png?as=webp\" type=\"image/webp\"/><img alt=\"figure 1\" aria-describedby=\"Fig1\" height=\"533\" loading=\"lazy\" src=\"//media.springernature.com/lw685/springer-static/image/art%3A10.1186%2Fs13054-025-05555-9/MediaObjects/13054_2025_5555_Fig1_HTML.png\" width=\"685\"/></picture><p>Visual representation of GRT and CRT dynamics in a phototype I and IV patients</p><span>Full size image</span><svg aria-hidden=\"true\" focusable=\"false\" height=\"16\" role=\"img\" width=\"16\"><use xlink:href=\"#icon-eds-i-chevron-right-small\" xmlns:xlink=\"http://www.w3.org/1999/xlink\"></use></svg></figure><p>GRT strongly correlated with CRT at baseline (R²=0.621, <i>p</i> < 0.001) and after VE (R²=0.609, <i>p</i> < 0.001). GRT and CRT increased when body temperature decreased, GRT was less influenced by body temperature (R²=0.159, <i>p</i> = 0.054) compared to CRT (R²=0.322, <i>p</i> = 0.004).</p><p>Patients with a high GRT (> 2.3s) had significantly lower systolic arterial pressure (93 mmHg vs. 108 mmHg, <i>p</i> = 0.014) and higher central venous pressure (9 mmHg vs. 5 mmHg, <i>p</i> = 0.047) compared to those with a low GRT (≤ 2.3s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², <i>p</i> = 0.027). Patients with high CRT(> 2.9 s) had significantly lower systolic arterial pressure (94 mmHg vs. 108 mmHg, <i>p</i> = 0.028) and similar central venous pressure (9 mmHg vs. 7 mmHg, <i>p</i> = 0.364) compared to those with a low CRT (≤ 2.9s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², <i>p</i> = 0.006).</p><p>The diagnostic accuracy of ΔGRT for predicting perfusion-based fluid responsiveness, with 13 patients (42%) identified as perfusion-based responders, was excellent (AUC-ROC 0.94 [95% CI 0.84–0.99]). However, neither GRT (AUC-ROC of 0.65 (95% CI [0.44–0.82])) nor CRT (AUC-ROC of 0.55 (95% CI [0.33–0.76]).) reliably predicted cardiac index-based fluid responsiveness (≥ 15% increase in CI), with 12 patients (38%) classified as cardiac index-based responders.</p><p>Our study demonstrates that GRT is feasible, reproducible, and strongly correlated with CRT. Moreover, GRT shows a weaker association with hemodynamic variables such as MAP, CO, and CVP. These findings support the classification of GRT as a perfusion-related parameter that is closely linked to CRT yet partially independent of macrocirculatory influences—consistent with other indices of tissue perfusion or microcirculation. Additionally, the reduced association between GRT and body thermoregulation suggests its potential utility in prehospital settings, where environmental factors can compromise the reliability of CRT measurements. Importantly, GRT may offer advantages over CRT in patients with very dark or light skin, where CRT assessment is challenging. Examples provided herein suggest that GRT may be easier to assess in patients with light and dark skin. However, further evaluation is needed in phototypes 5 and 6, as this study included only phototypes 1 to 4. In acute circulatory failure, monitoring tissue perfusion in vital organs is crucial, with gut perfusion playing a key role in multiple organ dysfunction syndrome. Although oral mucosal and gut perfusion are not identical, mucosal perfusion is generally more closely aligned with organ perfusion than skin perfusion. This holds true even though an association between gut perfusion and CRT has been suggested [5]. Since CRT may underdiagnose circulatory failure in some populations, developing equitable diagnostic methods remains essential [6]. Additionally, GRT’s diagnostic accuracy for perfusion-based fluid responsiveness suggests that it could be an alternative to CRT in guiding resuscitation strategies. However, further studies are needed to validate its clinical application across diverse patient populations and investigate its prognostic value beyond fluid responsiveness assessment.</p><p>GRT is a promising alternative to CRT for assessing tissue perfusion in critically ill patients, offering potential advantages in reliability and applicability across diverse skin pigmentations. Given that minority and ethnic populations are often underserved by traditional bedside tools like CRT, GRT may provide a more equitable and accurate method of evaluation for all patient groups. These findings highlight the need for further research to validate GRT’s feasibility and clinical utility in diverse populations.</p><p>As shown herein, the first image illustrates the compression of the skin of the chest (using a 10 mL air-filled syringe compressed to 7 mL, functioning as a piston to compress the skin for 7 s) (A) or gingival mucosa (using a 2 mL air-filled syringe compressed to 1 mL, functioning as a piston to compress the mucosa for 7 s)(B). The subsequent images depict time-stamped frames capturing the progression of both the CRT and GRT sequences in the same patient. Images of two patients are displayed (1.A, B and 2.A, B). In both patients—Patient 1 with light skin and phototype I, and Patient 2 with dark skin and phototype IV—the recoloration is more clearly observed in the GRT sequence compared to the CRT sequence.</p><p>No datasets were generated or analysed during the current study.</p><ol data-track-component=\"outbound reference\" data-track-context=\"references section\"><li data-counter=\"1.\"><p>Jacquet-Lagrèze M, Wiart C, Schweizer R, Didier L, Ruste M, Coutrot M, et al. Capillary refill time for the management of acute circulatory failure: a survey among pediatric and adult intensivists. BMC Emerg Med. 2022;22:131.</p><p>Google Scholar </p></li><li data-counter=\"2.\"><p>Jacquet-Lagrèze M, Pernollet A, Kattan E, Ait-Oufella H, Chesnel D, Ruste M, et al. Prognostic value of capillary refill time in adult patients: a systematic review with meta-analysis. Crit Care Lond Engl. 2023;27:473.</p><p>Google Scholar </p></li><li data-counter=\"3.\"><p>Chalifoux NV, Spielvogel CF, Stefanovski D, Silverstein DC. Standardized capillary refill time and relation to clinical parameters in hospitalized dogs. J Vet Emerg Crit Care San Antonio Tex. 2001. 2021;31:585–94.</p></li><li data-counter=\"4.\"><p>Jacquet-Lagrèze M, Bouhamri N, Portran P, Schweizer R, Baudin F, Lilot M, et al. Capillary refill time variation induced by passive leg Raising predicts capillary refill time response to volume expansion. Crit Care Lond Engl. 2019;23:281.</p><p>Google Scholar </p></li><li data-counter=\"5.\"><p>Brunauer A, Koköfer A, Bataar O, Gradwohl-Matis I, Dankl D, Bakker J, et al. Changes in peripheral perfusion relate to visceral organ perfusion in early septic shock: A pilot study. J Crit Care. 2016;35:105–9.</p><p>Google Scholar </p></li><li data-counter=\"6.\"><p>Sjoding MW, Dickson RP, Iwashyna TJ, Gay SE, Valley TS. Racial Bias in pulse oximetry measurement. N Engl J Med. 2020;383:2477–8.</p><p>Google Scholar </p></li></ol><p>Download references<svg aria-hidden=\"true\" focusable=\"false\" height=\"16\" role=\"img\" width=\"16\"><use xlink:href=\"#icon-eds-i-download-medium\" xmlns:xlink=\"http://www.w3.org/1999/xlink\"></use></svg></p><p>Not applicable.</p><p>No funding source.</p><h3>Authors and Affiliations</h3><ol><li><p>Département d’Anesthésie Réanimation, Centre Hospitalier Louis Pradel, Hospices Civils de Lyon, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran & Jean-Luc Fellahi</p></li><li><p>Université Claude-Bernard, Lyon 1, Campus Lyon Santé Est, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste, Philippe Portran & Jean-Luc Fellahi</p></li><li><p>CarMeN Laboratoire, Inserm UMR 1060, Université Claude Bernard Lyon 1, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste & Jean-Luc Fellahi</p></li><li><p>Département d’anesthésie réanimation de l’hôpital Cardiologique Louis Pradel, 59 Boulevard Pinel, Bron, 69500, France</p><p>Matthias Jacquet-Lagrèze</p></li></ol><span>Authors</span><ol><li><span>Matthias Jacquet-Lagrèze</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Martin Ruste</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Elodia Noumedem</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Nourredine Bouhamri</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Philippe Portran</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Jean-Luc Fellahi</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li></ol><h3>Contributions</h3><p>Substantial Contributions to Study Concept and Design: Acquisition of data, MJL, NB, PPAnalysis of data, MJL, MR, JLFInterpretation of data: MJL, EN, JLF Drafting the Manuscript or Revising It: MJL, MR, EN, NB, PP, JLFFinal Approval of the Version to Be Published: MJL, MR, EN, NB, PP, JLFAccountability for All Aspects of the Work: MJL, MR, EN, NB, PP, JLF.</p><h3>Corresponding author</h3><p>Correspondence to Matthias Jacquet-Lagrèze.</p><h3>Ethics approval and consent to participate </h3>\n<p>The experimental protocol was approved by the Institutional Review Board (IRB) for human projects (CPP Lyon Sud-Est, ANSM: 2014-A01034-43). It was registered a priori in Clinicaltrial.gov: (NCT02248025). Oral and written information was given to all patients or relatives. The need to obtain signed informed consent was waived by the IRB.</p>\n<h3>Consent for publication</h3>\n<p>Oral and written information was provided to all patients or their representatives, including details about video recordings of gingival and skin assessments, with no identifying features captured. The institutional review board waived the requirement for signed informed consent.</p>\n<h3>Competing interests</h3>\n<p>The authors declare no competing interests.</p><h3>Publisher’s note</h3><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p><p><b>Open Access</b> This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.</p>\n<p>Reprints and permissions</p><img alt=\"Check for updates. 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Gingival capillary refill time: a new approach to assess tissue perfusion. <i>Crit Care</i> <b>29</b>, 331 (2025). https://doi.org/10.1186/s13054-025-05555-9</p><p>Download citation<svg aria-hidden=\"true\" focusable=\"false\" height=\"16\" role=\"img\" width=\"16\"><use xlink:href=\"#icon-eds-i-download-medium\" xmlns:xlink=\"http://www.w3.org/1999/xlink\"></use></svg></p><ul data-test=\"publication-history\"><li><p>Received<span>: </span><span><time datetime=\"2025-05-23\">23 May 2025</time></span></p></li><li><p>Accepted<span>: </span><span><time datetime=\"2025-07-09\">09 July 2025</time></span></p></li><li><p>Published<span>: </span><span><time datetime=\"2025-07-28\">28 July 2025</time></span></p></li><li><p>DOI</abbr><span>: </span><span>https://doi.org/10.1186/s13054-025-05555-9</span></p></li></ul><h3>Share this article</h3><p>Anyone you share the following link with will be able to read this content:</p><button data-track=\"click\" data-track-action=\"get shareable link\" data-track-external=\"\" data-track-label=\"button\" type=\"button\">Get shareable link</button><p>Sorry, a shareable link is not currently available for this article.</p><p data-track=\"click\" data-track-action=\"select share url\" data-track-label=\"button\"></p><button data-track=\"click\" data-track-action=\"copy share url\" data-track-external=\"\" data-track-label=\"button\" type=\"button\">Copy to clipboard</button><p> Provided by the Springer Nature SharedIt content-sharing initiative </p>","PeriodicalId":10811,"journal":{"name":"Critical Care","volume":"27 1","pages":""},"PeriodicalIF":9.3000,"publicationDate":"2025-07-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Gingival capillary refill time: a new approach to assess tissue perfusion\",\"authors\":\"Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran, Jean-Luc Fellahi\",\"doi\":\"10.1186/s13054-025-05555-9\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Acute circulatory is a life-threatening condition, marked by inadequate tissue perfusion and oxygen delivery, leading to cellular dysfunction. Capillary refill time (CRT) is a widely used bedside marker of tissue perfusion but has limitations due to its sensitivity to temperature, pigmentation, and peripheral vascular disease [1, 2]. In veterinary medicine, gingival capillary refill time (GRT) is used to assess circulatory status via mucosal microcirculation, but its relevance in humans is unexplored [3]. GRT may provide a more robust alternative by directly assessing mucosal microcirculation and mitigating CRT limitations.</p><p>We conducted an ancillary analysis of the PeachCART cohort (NCT02248025) [4] to evaluate the feasibility, reproducibility, and clinical relevance of GRT in critically ill patients receiving fluid resuscitation for acute circulatory failure. We hypothesized that GRT would be feasible, correlate with CRT, and be a reliable predictor of perfusion-based fluid responsiveness.</p><p>The protocol was approved by the institutional review board; Oral and written information was given to all patients or relatives. Signed consent was waived by the ethics committee. GRT and CRT were recorded using an iPhone 6™ (8 MP camera). GRT involved applying calibrated pressure to the gingival mucosa with a 2 mL air-filled syringe compressed to 1 mL for 7 s. Four videos were taken per step by a single investigator and analyzed by two blinded readers. CRT was measured on chest skin using a 10 mL syringe compressed to 7 mL, as previously described. Volume expansion consisted of 500 mL lactated Ringer over 20 min, without changes in sedation or vasoactive drugs. Patients were monitored with PiCCO™ and thermodilution was performed before and after volume expansion. Metabolic and hemodynamic parameters, general patient characteristics, and Fitzpatrick skin phototype were also recorded. Primary outcomes were GRT feasibility and reproducibility; secondary outcomes included its correlation with CRT, predictive value for perfusion based fluid responsiveness (≥ 25% CRT reduction) [4], and association with hemodynamic and metabolic parameters.</p><p>Thirty-two patients were analyzed (median age: 62 [54–69] years, median SOFA score: 9 (6–11), SAPS II: 43 (33–51), and 84% on mechanical ventilation). Median GRT was 2.3 (1.6–3.2) s, and median CRT was 2.9 [2.4–3.8] s. Based on our linear regression model, the classical threshold of 3 s to define abnormal CRT corresponds to an estimated GRT of approximately 2.12 s. GRT was feasible in all patients, with a slightly lower interobserver coefficient of variation (5.2% [95% CI 0.9–9.6]) compared to CRT (7.3% [95% CI 3.9–10.2]). The median Fitzpatrick skin phototype was 3, GRT was easier to read in patients with phototype 1 and 4 as illustrated in Fig. 1. GRT was successfully measured in 97% of patients. No major adverse events were reported, except mild discomfort in one patient.</p><figure><figcaption><b data-test=\\\"figure-caption-text\\\">Fig. 1</b></figcaption><picture><source srcset=\\\"//media.springernature.com/lw685/springer-static/image/art%3A10.1186%2Fs13054-025-05555-9/MediaObjects/13054_2025_5555_Fig1_HTML.png?as=webp\\\" type=\\\"image/webp\\\"/><img alt=\\\"figure 1\\\" aria-describedby=\\\"Fig1\\\" height=\\\"533\\\" loading=\\\"lazy\\\" src=\\\"//media.springernature.com/lw685/springer-static/image/art%3A10.1186%2Fs13054-025-05555-9/MediaObjects/13054_2025_5555_Fig1_HTML.png\\\" width=\\\"685\\\"/></picture><p>Visual representation of GRT and CRT dynamics in a phototype I and IV patients</p><span>Full size image</span><svg aria-hidden=\\\"true\\\" focusable=\\\"false\\\" height=\\\"16\\\" role=\\\"img\\\" width=\\\"16\\\"><use xlink:href=\\\"#icon-eds-i-chevron-right-small\\\" xmlns:xlink=\\\"http://www.w3.org/1999/xlink\\\"></use></svg></figure><p>GRT strongly correlated with CRT at baseline (R²=0.621, <i>p</i> < 0.001) and after VE (R²=0.609, <i>p</i> < 0.001). GRT and CRT increased when body temperature decreased, GRT was less influenced by body temperature (R²=0.159, <i>p</i> = 0.054) compared to CRT (R²=0.322, <i>p</i> = 0.004).</p><p>Patients with a high GRT (> 2.3s) had significantly lower systolic arterial pressure (93 mmHg vs. 108 mmHg, <i>p</i> = 0.014) and higher central venous pressure (9 mmHg vs. 5 mmHg, <i>p</i> = 0.047) compared to those with a low GRT (≤ 2.3s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², <i>p</i> = 0.027). Patients with high CRT(> 2.9 s) had significantly lower systolic arterial pressure (94 mmHg vs. 108 mmHg, <i>p</i> = 0.028) and similar central venous pressure (9 mmHg vs. 7 mmHg, <i>p</i> = 0.364) compared to those with a low CRT (≤ 2.9s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², <i>p</i> = 0.006).</p><p>The diagnostic accuracy of ΔGRT for predicting perfusion-based fluid responsiveness, with 13 patients (42%) identified as perfusion-based responders, was excellent (AUC-ROC 0.94 [95% CI 0.84–0.99]). However, neither GRT (AUC-ROC of 0.65 (95% CI [0.44–0.82])) nor CRT (AUC-ROC of 0.55 (95% CI [0.33–0.76]).) reliably predicted cardiac index-based fluid responsiveness (≥ 15% increase in CI), with 12 patients (38%) classified as cardiac index-based responders.</p><p>Our study demonstrates that GRT is feasible, reproducible, and strongly correlated with CRT. Moreover, GRT shows a weaker association with hemodynamic variables such as MAP, CO, and CVP. These findings support the classification of GRT as a perfusion-related parameter that is closely linked to CRT yet partially independent of macrocirculatory influences—consistent with other indices of tissue perfusion or microcirculation. Additionally, the reduced association between GRT and body thermoregulation suggests its potential utility in prehospital settings, where environmental factors can compromise the reliability of CRT measurements. Importantly, GRT may offer advantages over CRT in patients with very dark or light skin, where CRT assessment is challenging. Examples provided herein suggest that GRT may be easier to assess in patients with light and dark skin. However, further evaluation is needed in phototypes 5 and 6, as this study included only phototypes 1 to 4. In acute circulatory failure, monitoring tissue perfusion in vital organs is crucial, with gut perfusion playing a key role in multiple organ dysfunction syndrome. Although oral mucosal and gut perfusion are not identical, mucosal perfusion is generally more closely aligned with organ perfusion than skin perfusion. This holds true even though an association between gut perfusion and CRT has been suggested [5]. Since CRT may underdiagnose circulatory failure in some populations, developing equitable diagnostic methods remains essential [6]. Additionally, GRT’s diagnostic accuracy for perfusion-based fluid responsiveness suggests that it could be an alternative to CRT in guiding resuscitation strategies. However, further studies are needed to validate its clinical application across diverse patient populations and investigate its prognostic value beyond fluid responsiveness assessment.</p><p>GRT is a promising alternative to CRT for assessing tissue perfusion in critically ill patients, offering potential advantages in reliability and applicability across diverse skin pigmentations. Given that minority and ethnic populations are often underserved by traditional bedside tools like CRT, GRT may provide a more equitable and accurate method of evaluation for all patient groups. These findings highlight the need for further research to validate GRT’s feasibility and clinical utility in diverse populations.</p><p>As shown herein, the first image illustrates the compression of the skin of the chest (using a 10 mL air-filled syringe compressed to 7 mL, functioning as a piston to compress the skin for 7 s) (A) or gingival mucosa (using a 2 mL air-filled syringe compressed to 1 mL, functioning as a piston to compress the mucosa for 7 s)(B). The subsequent images depict time-stamped frames capturing the progression of both the CRT and GRT sequences in the same patient. Images of two patients are displayed (1.A, B and 2.A, B). In both patients—Patient 1 with light skin and phototype I, and Patient 2 with dark skin and phototype IV—the recoloration is more clearly observed in the GRT sequence compared to the CRT sequence.</p><p>No datasets were generated or analysed during the current study.</p><ol data-track-component=\\\"outbound reference\\\" data-track-context=\\\"references section\\\"><li data-counter=\\\"1.\\\"><p>Jacquet-Lagrèze M, Wiart C, Schweizer R, Didier L, Ruste M, Coutrot M, et al. Capillary refill time for the management of acute circulatory failure: a survey among pediatric and adult intensivists. BMC Emerg Med. 2022;22:131.</p><p>Google Scholar </p></li><li data-counter=\\\"2.\\\"><p>Jacquet-Lagrèze M, Pernollet A, Kattan E, Ait-Oufella H, Chesnel D, Ruste M, et al. Prognostic value of capillary refill time in adult patients: a systematic review with meta-analysis. 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Racial Bias in pulse oximetry measurement. N Engl J Med. 2020;383:2477–8.</p><p>Google Scholar </p></li></ol><p>Download references<svg aria-hidden=\\\"true\\\" focusable=\\\"false\\\" height=\\\"16\\\" role=\\\"img\\\" width=\\\"16\\\"><use xlink:href=\\\"#icon-eds-i-download-medium\\\" xmlns:xlink=\\\"http://www.w3.org/1999/xlink\\\"></use></svg></p><p>Not applicable.</p><p>No funding source.</p><h3>Authors and Affiliations</h3><ol><li><p>Département d’Anesthésie Réanimation, Centre Hospitalier Louis Pradel, Hospices Civils de Lyon, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran & Jean-Luc Fellahi</p></li><li><p>Université Claude-Bernard, Lyon 1, Campus Lyon Santé Est, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste, Philippe Portran & Jean-Luc Fellahi</p></li><li><p>CarMeN Laboratoire, Inserm UMR 1060, Université Claude Bernard Lyon 1, Lyon, France</p><p>Matthias Jacquet-Lagrèze, Martin Ruste & Jean-Luc Fellahi</p></li><li><p>Département d’anesthésie réanimation de l’hôpital Cardiologique Louis Pradel, 59 Boulevard Pinel, Bron, 69500, France</p><p>Matthias Jacquet-Lagrèze</p></li></ol><span>Authors</span><ol><li><span>Matthias Jacquet-Lagrèze</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Martin Ruste</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Elodia Noumedem</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Nourredine Bouhamri</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Philippe Portran</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li><li><span>Jean-Luc Fellahi</span>View author publications<p><span>Search author on:</span><span>PubMed<span> </span>Google Scholar</span></p></li></ol><h3>Contributions</h3><p>Substantial Contributions to Study Concept and Design: Acquisition of data, MJL, NB, PPAnalysis of data, MJL, MR, JLFInterpretation of data: MJL, EN, JLF Drafting the Manuscript or Revising It: MJL, MR, EN, NB, PP, JLFFinal Approval of the Version to Be Published: MJL, MR, EN, NB, PP, JLFAccountability for All Aspects of the Work: MJL, MR, EN, NB, PP, JLF.</p><h3>Corresponding author</h3><p>Correspondence to Matthias Jacquet-Lagrèze.</p><h3>Ethics approval and consent to participate </h3>\\n<p>The experimental protocol was approved by the Institutional Review Board (IRB) for human projects (CPP Lyon Sud-Est, ANSM: 2014-A01034-43). It was registered a priori in Clinicaltrial.gov: (NCT02248025). Oral and written information was given to all patients or relatives. The need to obtain signed informed consent was waived by the IRB.</p>\\n<h3>Consent for publication</h3>\\n<p>Oral and written information was provided to all patients or their representatives, including details about video recordings of gingival and skin assessments, with no identifying features captured. The institutional review board waived the requirement for signed informed consent.</p>\\n<h3>Competing interests</h3>\\n<p>The authors declare no competing interests.</p><h3>Publisher’s note</h3><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p><p><b>Open Access</b> This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.</p>\\n<p>Reprints and permissions</p><img alt=\\\"Check for updates. 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0-.92-.08-1.33-.25-.41-.16-.77-.4-1.08-.7-.3-.31-.54-.69-.72-1.13-.17-.44-.26-.95-.26-1.52zm4.61-.62c0-.55-.11-.98-.34-1.28-.23-.31-.58-.47-1.06-.47-.41 0-.77.15-1.08.45-.31.29-.5.73-.57 1.3zm3.01 2.23c.31.24.61.43.92.57.3.13.63.2.98.2.38 0 .65-.08.83-.23s.27-.35.27-.6c0-.14-.05-.26-.13-.37-.08-.1-.2-.2-.34-.28-.14-.09-.29-.16-.47-.23l-.53-.22c-.23-.09-.46-.18-.69-.3-.23-.11-.44-.24-.62-.4s-.33-.35-.45-.55c-.12-.21-.18-.46-.18-.75 0-.61.23-1.1.68-1.49.44-.38 1.06-.57 1.83-.57.48 0 .91.08 1.29.25s.71.36.99.57l-.74.98c-.24-.17-.49-.32-.73-.42-.25-.11-.51-.16-.78-.16-.35 0-.6.07-.76.21-.17.15-.25.33-.25.54 0 .14.04.26.12.36s.18.18.31.26c.14.07.29.14.46.21l.54.19c.23.09.47.18.7.29s.44.24.64.4c.19.16.34.35.46.58.11.23.17.5.17.82 0 .3-.06.58-.17.83-.12.26-.29.48-.51.68-.23.19-.51.34-.84.45-.34.11-.72.17-1.15.17-.48 0-.95-.09-1.41-.27-.46-.19-.86-.41-1.2-.68z" fill="#535353"/></g></svg>\\\" width=\\\"57\\\"/><h3>Cite this article</h3><p>Jacquet-Lagrèze, M., Ruste, M., Noumedem, E. <i>et al.</i> Gingival capillary refill time: a new approach to assess tissue perfusion. <i>Crit Care</i> <b>29</b>, 331 (2025). https://doi.org/10.1186/s13054-025-05555-9</p><p>Download citation<svg aria-hidden=\\\"true\\\" focusable=\\\"false\\\" height=\\\"16\\\" role=\\\"img\\\" width=\\\"16\\\"><use xlink:href=\\\"#icon-eds-i-download-medium\\\" xmlns:xlink=\\\"http://www.w3.org/1999/xlink\\\"></use></svg></p><ul data-test=\\\"publication-history\\\"><li><p>Received<span>: </span><span><time datetime=\\\"2025-05-23\\\">23 May 2025</time></span></p></li><li><p>Accepted<span>: </span><span><time datetime=\\\"2025-07-09\\\">09 July 2025</time></span></p></li><li><p>Published<span>: </span><span><time datetime=\\\"2025-07-28\\\">28 July 2025</time></span></p></li><li><p>DOI</abbr><span>: </span><span>https://doi.org/10.1186/s13054-025-05555-9</span></p></li></ul><h3>Share this article</h3><p>Anyone you share the following link with will be able to read this content:</p><button 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摘要
此外,GRT与体温调节之间的相关性降低表明其在院前环境中的潜在效用,在院前环境因素可能会损害CRT测量的可靠性。重要的是,对于皮肤很黑或很浅的患者,GRT可能比CRT更有优势,而CRT的评估是有挑战性的。本文提供的例子表明,在皮肤浅色和深色的患者中,GRT可能更容易评估。然而,由于本研究仅包括1至4型光型,因此需要进一步评估5和6型光型。在急性循环衰竭中,监测重要器官的组织灌注是至关重要的,而肠道灌注在多器官功能障碍综合征中起着关键作用。虽然口腔粘膜和肠道灌注不完全相同,但粘膜灌注通常比皮肤灌注更接近器官灌注。这是正确的,即使肠灌注和CRT之间的关联已被认为是b[5]。由于CRT可能对某些人群的循环衰竭诊断不足,因此开发公平的诊断方法仍然至关重要。此外,GRT对基于灌注的液体反应的诊断准确性表明,它可以替代CRT指导复苏策略。然而,需要进一步的研究来验证其在不同患者群体中的临床应用,并调查其在液体反应性评估之外的预后价值。GRT是评估危重患者组织灌注的一种有希望的替代CRT,在可靠性和适用性方面具有潜在的优势,适用于不同的皮肤色素。考虑到像CRT这样的传统床边工具往往无法为少数族裔人群提供服务,GRT可能为所有患者群体提供更公平、更准确的评估方法。这些发现强调需要进一步的研究来验证GRT在不同人群中的可行性和临床应用。如图所示,第一张图像显示了胸部皮肤的压缩(使用10ml充气注射器压缩到7ml,作为活塞压缩皮肤7 s)(a)或牙龈粘膜(使用2ml充气注射器压缩到1ml,作为活塞压缩粘膜7 s)(B)。随后的图像描述了同一患者的CRT和GRT序列的时间戳帧。显示两名患者的图像(1)。A B和2。A、B)。在这两例患者中,患者1为浅色皮肤和光型I,患者2为深色皮肤和光型iv,与CRT序列相比,在GRT序列中更清楚地观察到重新着色。在本研究中没有生成或分析数据集。刘建军,刘建军,刘建军,等。急性循环衰竭管理的毛细血管再充血时间:一项儿科和成人重症医师的调查。中华医学杂志,2022;22:131。[10][学者jacquet - lagr<e:1> M, Pernollet A, Kattan E, Ait-Oufella H, Chesnel D, Ruste M,等。]成人患者毛细血管再充血时间的预后价值:一项系统综述和荟萃分析。危重护理与护理杂志,2009;27:473。学者Chalifoux NV, Spielvogel CF, Stefanovski D, Silverstein DC。住院犬标准化毛细血管再充血时间及其与临床参数的关系。[J]圣安东尼奥急诊急救中心,2001。2021; 31:585 - 94。李建军,李建军,李建军,等。被动抬腿引起的毛细血管再充盈时间变化预测了毛细血管再充盈时间对体积膨胀的响应。危重护理与护理,2019;23:28 . 1。[10]学者Brunauer A, Koköfer A, Bataar O, Gradwohl-Matis I, Dankl D, Bakker J,等。脓毒性休克早期外周灌注变化与内脏器官灌注相关:一项初步研究。[J] .中国生物医学工程学报,2016;35(5):591 - 591。[10]学者Sjoding MW, Dickson RP, Iwashyna TJ, Gay SE, Valley TS.脉搏血氧测量中的种族偏见。中国生物医学工程学报,2016;22(3):391 - 391。b谷歌学者下载参考资料不适用。没有资金来源。 作者与单位:法国里昂里昂平民收容所,路易斯·普拉德尔医院,法国里昂,马赛亚斯·雅克-拉格伦兹,马丁·鲁斯特,埃洛迪亚·努米德姆,努尔雷丁·布哈姆里,菲利普·波特兰;Jean-Luc fellowahiuniversit<s:1> Claude-Bernard, Lyon 1, Campus Lyon santeest, Lyon, france里昂Jean-Luc fellaman实验室,Inserm UMR 1060, Claude Bernard Lyon 1, Lyon, france;Jean-Luc fellahi, <s:2> Louis Pradel Cardiologique, 59 Boulevard Pinel, Bron, 69500;francemaththias jacquet - lagr<s:1> authorsmatthias jacquet - lagr<e:1>查看作者出版物搜索作者on:PubMed谷歌ScholarMartin RusteView作者出版物搜索作者on:PubMed谷歌ScholarElodia NoumedemView作者出版物搜索作者on:PubMed谷歌ScholarNourredine BouhamriView作者出版物搜索作者on:PubMed谷歌ScholarPhilippe PortranView作者出版物搜索作者on:PubMed谷歌ScholarJean-Luc FellahiView作者出版物搜索作者对研究概念和设计的重大贡献:数据获取、MJL、NB、pp数据分析、MJL、MR、jl数据解读:MJL、EN、EN、NB、PP、jl起草或修改稿件:MJL、MR、EN、NB、PP、jl最终定稿:MJL、MR、EN、NB、PP、jl工作各方面的责任:MJL、MR、EN、NB、PP、JLF。通讯作者:Matthias jacquet - lagratisze本实验方案经机构审查委员会(IRB)批准,适用于人类项目(CPP Lyon Sud-Est, ANSM: 2014-A01034-43)。该药物已在Clinicaltrial.gov (NCT02248025)上先验注册。向所有患者或亲属提供口头和书面信息。内部审查委员会免除了获得签署的知情同意书的需要。发表同意向所有患者或其代表提供口头和书面信息,包括牙龈和皮肤评估的视频记录的细节,没有捕捉到识别特征。机构审查委员会放弃了签署知情同意书的要求。利益竞争作者声明没有利益竞争。出版方声明:对于已出版地图的管辖权要求和机构关系,普林格·自然保持中立。开放获取本文遵循知识共享署名-非商业-非衍生品4.0国际许可协议,该协议允许以任何媒介或格式进行非商业用途、共享、分发和复制,只要您适当注明原作者和来源,提供知识共享许可协议的链接,并注明您是否修改了许可材料。根据本许可协议,您无权分享源自本文或其部分内容的改编材料。本文中的图像或其他第三方材料包含在文章的知识共享许可协议中,除非在材料的署名中另有说明。如果材料未包含在文章的知识共享许可中,并且您的预期用途不被法律法规允许或超过允许的用途,您将需要直接获得版权所有者的许可。要查看本许可协议的副本,请访问http://creativecommons.org/licenses/by-nc-nd/4.0/.Reprints和permissionsCite这篇文章jacquet - lagr<e:1>, M., Ruste, M., Noumedem, E.等。牙龈毛细血管再充盈时间:评估组织灌注的新方法。危重症护理29,331(2025)。https://doi.org/10.1186/s13054-025-05555-9Download citation:收稿日期:2025年5月23日接受日期:2025年7月9日发布日期:2025年7月28日doi: https://doi.org/10.1186/s13054-025-05555-9Share这篇文章任何人与您分享以下链接将能够阅读此内容:获取可共享链接对不起,本文目前没有可共享链接。复制到剪贴板由施普林格自然共享内容倡议提供
Gingival capillary refill time: a new approach to assess tissue perfusion
Acute circulatory is a life-threatening condition, marked by inadequate tissue perfusion and oxygen delivery, leading to cellular dysfunction. Capillary refill time (CRT) is a widely used bedside marker of tissue perfusion but has limitations due to its sensitivity to temperature, pigmentation, and peripheral vascular disease [1, 2]. In veterinary medicine, gingival capillary refill time (GRT) is used to assess circulatory status via mucosal microcirculation, but its relevance in humans is unexplored [3]. GRT may provide a more robust alternative by directly assessing mucosal microcirculation and mitigating CRT limitations.
We conducted an ancillary analysis of the PeachCART cohort (NCT02248025) [4] to evaluate the feasibility, reproducibility, and clinical relevance of GRT in critically ill patients receiving fluid resuscitation for acute circulatory failure. We hypothesized that GRT would be feasible, correlate with CRT, and be a reliable predictor of perfusion-based fluid responsiveness.
The protocol was approved by the institutional review board; Oral and written information was given to all patients or relatives. Signed consent was waived by the ethics committee. GRT and CRT were recorded using an iPhone 6™ (8 MP camera). GRT involved applying calibrated pressure to the gingival mucosa with a 2 mL air-filled syringe compressed to 1 mL for 7 s. Four videos were taken per step by a single investigator and analyzed by two blinded readers. CRT was measured on chest skin using a 10 mL syringe compressed to 7 mL, as previously described. Volume expansion consisted of 500 mL lactated Ringer over 20 min, without changes in sedation or vasoactive drugs. Patients were monitored with PiCCO™ and thermodilution was performed before and after volume expansion. Metabolic and hemodynamic parameters, general patient characteristics, and Fitzpatrick skin phototype were also recorded. Primary outcomes were GRT feasibility and reproducibility; secondary outcomes included its correlation with CRT, predictive value for perfusion based fluid responsiveness (≥ 25% CRT reduction) [4], and association with hemodynamic and metabolic parameters.
Thirty-two patients were analyzed (median age: 62 [54–69] years, median SOFA score: 9 (6–11), SAPS II: 43 (33–51), and 84% on mechanical ventilation). Median GRT was 2.3 (1.6–3.2) s, and median CRT was 2.9 [2.4–3.8] s. Based on our linear regression model, the classical threshold of 3 s to define abnormal CRT corresponds to an estimated GRT of approximately 2.12 s. GRT was feasible in all patients, with a slightly lower interobserver coefficient of variation (5.2% [95% CI 0.9–9.6]) compared to CRT (7.3% [95% CI 3.9–10.2]). The median Fitzpatrick skin phototype was 3, GRT was easier to read in patients with phototype 1 and 4 as illustrated in Fig. 1. GRT was successfully measured in 97% of patients. No major adverse events were reported, except mild discomfort in one patient.
Fig. 1
Visual representation of GRT and CRT dynamics in a phototype I and IV patients
Full size image
GRT strongly correlated with CRT at baseline (R²=0.621, p < 0.001) and after VE (R²=0.609, p < 0.001). GRT and CRT increased when body temperature decreased, GRT was less influenced by body temperature (R²=0.159, p = 0.054) compared to CRT (R²=0.322, p = 0.004).
Patients with a high GRT (> 2.3s) had significantly lower systolic arterial pressure (93 mmHg vs. 108 mmHg, p = 0.014) and higher central venous pressure (9 mmHg vs. 5 mmHg, p = 0.047) compared to those with a low GRT (≤ 2.3s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², p = 0.027). Patients with high CRT(> 2.9 s) had significantly lower systolic arterial pressure (94 mmHg vs. 108 mmHg, p = 0.028) and similar central venous pressure (9 mmHg vs. 7 mmHg, p = 0.364) compared to those with a low CRT (≤ 2.9s). They also exhibited a lower cardiac index (2.3 vs. 2.9 L/min/m², p = 0.006).
The diagnostic accuracy of ΔGRT for predicting perfusion-based fluid responsiveness, with 13 patients (42%) identified as perfusion-based responders, was excellent (AUC-ROC 0.94 [95% CI 0.84–0.99]). However, neither GRT (AUC-ROC of 0.65 (95% CI [0.44–0.82])) nor CRT (AUC-ROC of 0.55 (95% CI [0.33–0.76]).) reliably predicted cardiac index-based fluid responsiveness (≥ 15% increase in CI), with 12 patients (38%) classified as cardiac index-based responders.
Our study demonstrates that GRT is feasible, reproducible, and strongly correlated with CRT. Moreover, GRT shows a weaker association with hemodynamic variables such as MAP, CO, and CVP. These findings support the classification of GRT as a perfusion-related parameter that is closely linked to CRT yet partially independent of macrocirculatory influences—consistent with other indices of tissue perfusion or microcirculation. Additionally, the reduced association between GRT and body thermoregulation suggests its potential utility in prehospital settings, where environmental factors can compromise the reliability of CRT measurements. Importantly, GRT may offer advantages over CRT in patients with very dark or light skin, where CRT assessment is challenging. Examples provided herein suggest that GRT may be easier to assess in patients with light and dark skin. However, further evaluation is needed in phototypes 5 and 6, as this study included only phototypes 1 to 4. In acute circulatory failure, monitoring tissue perfusion in vital organs is crucial, with gut perfusion playing a key role in multiple organ dysfunction syndrome. Although oral mucosal and gut perfusion are not identical, mucosal perfusion is generally more closely aligned with organ perfusion than skin perfusion. This holds true even though an association between gut perfusion and CRT has been suggested [5]. Since CRT may underdiagnose circulatory failure in some populations, developing equitable diagnostic methods remains essential [6]. Additionally, GRT’s diagnostic accuracy for perfusion-based fluid responsiveness suggests that it could be an alternative to CRT in guiding resuscitation strategies. However, further studies are needed to validate its clinical application across diverse patient populations and investigate its prognostic value beyond fluid responsiveness assessment.
GRT is a promising alternative to CRT for assessing tissue perfusion in critically ill patients, offering potential advantages in reliability and applicability across diverse skin pigmentations. Given that minority and ethnic populations are often underserved by traditional bedside tools like CRT, GRT may provide a more equitable and accurate method of evaluation for all patient groups. These findings highlight the need for further research to validate GRT’s feasibility and clinical utility in diverse populations.
As shown herein, the first image illustrates the compression of the skin of the chest (using a 10 mL air-filled syringe compressed to 7 mL, functioning as a piston to compress the skin for 7 s) (A) or gingival mucosa (using a 2 mL air-filled syringe compressed to 1 mL, functioning as a piston to compress the mucosa for 7 s)(B). The subsequent images depict time-stamped frames capturing the progression of both the CRT and GRT sequences in the same patient. Images of two patients are displayed (1.A, B and 2.A, B). In both patients—Patient 1 with light skin and phototype I, and Patient 2 with dark skin and phototype IV—the recoloration is more clearly observed in the GRT sequence compared to the CRT sequence.
No datasets were generated or analysed during the current study.
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Authors and Affiliations
Département d’Anesthésie Réanimation, Centre Hospitalier Louis Pradel, Hospices Civils de Lyon, Lyon, France
Matthias Jacquet-Lagrèze, Martin Ruste, Elodia Noumedem, Nourredine Bouhamri, Philippe Portran & Jean-Luc Fellahi
Université Claude-Bernard, Lyon 1, Campus Lyon Santé Est, Lyon, France
Matthias Jacquet-Lagrèze, Martin Ruste, Philippe Portran & Jean-Luc Fellahi
CarMeN Laboratoire, Inserm UMR 1060, Université Claude Bernard Lyon 1, Lyon, France
Matthias Jacquet-Lagrèze, Martin Ruste & Jean-Luc Fellahi
Département d’anesthésie réanimation de l’hôpital Cardiologique Louis Pradel, 59 Boulevard Pinel, Bron, 69500, France
Matthias Jacquet-Lagrèze
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Contributions
Substantial Contributions to Study Concept and Design: Acquisition of data, MJL, NB, PPAnalysis of data, MJL, MR, JLFInterpretation of data: MJL, EN, JLF Drafting the Manuscript or Revising It: MJL, MR, EN, NB, PP, JLFFinal Approval of the Version to Be Published: MJL, MR, EN, NB, PP, JLFAccountability for All Aspects of the Work: MJL, MR, EN, NB, PP, JLF.
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Correspondence to Matthias Jacquet-Lagrèze.
Ethics approval and consent to participate
The experimental protocol was approved by the Institutional Review Board (IRB) for human projects (CPP Lyon Sud-Est, ANSM: 2014-A01034-43). It was registered a priori in Clinicaltrial.gov: (NCT02248025). Oral and written information was given to all patients or relatives. The need to obtain signed informed consent was waived by the IRB.
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Oral and written information was provided to all patients or their representatives, including details about video recordings of gingival and skin assessments, with no identifying features captured. The institutional review board waived the requirement for signed informed consent.
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The authors declare no competing interests.
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Jacquet-Lagrèze, M., Ruste, M., Noumedem, E. et al. Gingival capillary refill time: a new approach to assess tissue perfusion. Crit Care29, 331 (2025). https://doi.org/10.1186/s13054-025-05555-9
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DOI: https://doi.org/10.1186/s13054-025-05555-9
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