Repair of Traumatic Tricuspid Valve Rupture in Loeys Dietz Type V

Repair of Traumatic Tricuspid Valve Rupture in Loeys Dietz Type V | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Case Report Repair of Traumatic Tricuspid Valve Rupture in Loeys Dietz Type V Carla Boyle, Natalie Dixon, Julie Doberne This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-9363599/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 16 You are reading this latest preprint version Abstract Background: Loeys-Dietz Syndrome (LDS) is a rare connective tissue disorder that often results in vascular fragility and valvular abnormalities, most commonly presenting with aortic dilation requiring intervention. Blunt cardiac trauma following chest injury is rare, and patients uncommonly experience isolated valvular injury. Here, we present a case of a patient with LDS type V who suffered chest trauma resulting in acute tricuspid regurgitation complicated by cardiogenic shock requiring surgical repair. Case Presentation: A 54-year-old woman with a history of cervical instability, obstructive sleep apnea, easy bruising and LDS type V with no relevant surgical history was brought to care after acute chest trauma. Initial management demonstrated a pericardial effusion for which a pericardial window was placed at an outside hospital. She was transferred to a higher level of care for worsening cardiogenic shock, and severe tricuspid regurgitation was demonstrated on imaging, secondary to a flail leaflet. The tricuspid valve was repaired surgically, and the patient was weaned off vasoactive agents before discharge. Conclusions: Intraoperative management of connective tissue disorders in cardiothoracic surgery patients is highly dependent on their subtype. In this case, the presenting patient was likely at increased risk for valvular rupture due to her underlying LDS; however, this was not noted to impact tissue quality during the surgical repair. Significant preoperative collaboration between the cardiothoracic and vascular surgical teams was imperative for anticipatory planning and should be the standard for patients with complex underlying connective tissue disorders. Loeys-Dietz Syndrome Tricuspid Valve Repair Connective Tissue Disorders Figures Figure 1 Figure 2 Figure 3 Background Blunt chest trauma leading to cardiac injury is uncommon, however when it occurs it most often affects the myocardium, leading to cardiac wall damage [ 1 ]. Given its anterior location, right sided cardiac injury is more common than left. Isolated valvular injury is uncommon and often due to pressure redistribution during acute blunt trauma. This includes papillary muscle and chordae tendinae rupture due to trauma occurring during systole, causing a rapid increase in intraventricular pressure [ 1 ]. If valvular injury occurs due to papillary muscle necrosis following cardiac wall damage, presentation may be delayed, leading to latent diagnosis and management of regurgitation. The mechanism of chest injury associated with tricuspid valve rupture is most commonly high velocity acceleration-deceleration accidents in motor vehicles [ 2 – 4 ]. Loeys-Dietz Syndrome (LDS) is a heritable angiopathy characterized by autosomal dominant mutations in the transforming growth factor beta receptor (TGFB) pathway, causing degeneration of the medial arterial layer and loss of elastic tissue [ 5 ]. This increases susceptibility to arterial pathologies such as aortic aneurysms, arterial tortuosity and cardiomyopathies, as well as craniofacial malformations and other cutaneous manifestations. Patients with LDS often exhibit aggressive aortopathies requiring early intervention. The patient was diagnosed with LDS type V with a mutation in TGFB3 (variant c. 487C > t p.Arg163Trp) after receiving targeted parental testing as her daughter was found to have a bicuspid aortic valve and aortic enlargement. Upon diagnosis, the patient had normal aortic root measurements, no valvular abnormalities, no significant aortic dilation, and no peripheral tortuosity. She also lacked any classic features of LDS, such as hypertelorism, or translucent skin. Case Presentation A 54-year-old woman with past medical history of cervical instability, obstructive sleep apnea, easy bruising, gastroesophageal reflux, and Loeys-Dietz Syndrome (LDS) was brought emergently to care after being kicked in the chest by a horse. Upon presentation, the patient was hypotensive and tachycardic, with distended neck veins and transthoracic echocardiogram (TTE) demonstrating a significant pericardial effusion and IVC distention. The patient received an urgent sub-xiphoid pericardial window placement, during which she was found to have a 200ml hemopericardium with clot formation. Intraoperative transesophageal echocardiogram (TEE) also demonstrated a ruptured tricuspid valve chord and moderate tricuspid valve regurgitation (Fig. 1 ). Following pericardial window placement, the patient developed recurrent hypotension refractory to fluid resuscitation with transthoracic echocardiograph revealing worsened severe tricuspid regurgitation and a flail tricuspid leaflet with flow reversal in the hepatic veins and flattening of the interventricular septum. Left ventricular ejection fraction was preserved. The patient required significant vasopressor support and was ultimately transferred to a higher level of care for continued management. Invasive hemodynamics demonstrated minimal right ventricle pulsatility, low pulmonary artery pulsatility index (PAPi score 0.56 at admission) and ventricularized right atrial waveform. She continued to require vasopressor and inotropic support and diuresis for 3 days until weaning was successful, and she was stable for intervention. Prior to intervention, she had a net fluid output of 6 liters. Repeat TTE following volume optimization continued to demonstrate severe TR due to a flail leaflet. Preoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating significant tricuspid regurgitation into the right atrium, with a mass (later demonstrated to be ruptured papillary muscle) visible on the tricuspid leaflet. Increased right atrial size also demonstrated. Given the severity of her tricuspid regurgitation, timely intervention following optimization was necessary. As the etiology of the TR was a flail leaflet, she was not a candidate for percutaneous annuloplasty devices. Other percutaneous options relying on coaptation were also rejected, as there was not enough tissue present to clasp due to the location of the papillary rupture. Vascular surgery was also consulted regarding risks related to the patient’s LDS subtype, and these were deemed to be non-prohibitive. Reports from interventions in LDS patients also affirm that surgery is not complicated by increased tissue fragility in this patient population [ 6 ]. Finally, her age, conditioning, and lack of surgical history suggested that she would be an appropriate candidate for open repair. Thus, surgical repair of the tricuspid valve was planned, with the option for bioprosthetic valve replacement if needed. The surgery was performed via median sternotomy with central aortic and bicaval venous cannulation. Cardiopulmonary bypass was initiated, and an aortic cross clamp was applied. A right atriotomy was performed, and the tricuspid valve was inspected. A flail segment of the anterior leaflet was noted. On further inspection, this was due to an anterior papillary muscle that has been avulsed from the ventricular attachments (Fig. 2 ). The papillary muscle was secured to the right ventricle using 2 − 0 plegdeted Ticron sutures. Interrupted 2 − 0 Ticron sutures were then placed horizontally and passed through a 32mm Tricuspid Edwards MC3 annuloplasty band. This was then seated and secured using Corknot. Upon further testing of the valve, a residual leak was noted from a small flail segment on the posterior leaflet with an adjacent small cleft. This cord had been avulsed from the right ventricle along the papillary muscle as well. The cleft was closed with running suture. Using an additional pledgeted 2 − 0 Ticron suture, the papillary attached to the posterior flail cord was reattached to the right ventricle. Medical photography of intraoperative visualization of tricuspid valve following bicaval cannulation, bypass initiation and tricuspid valve exposure. Papillary muscle is grasped and elevated demonstrating where rupture occurred, prior to reattachment. On final testing, a small amount of leak was noted centrally. Discussion was held regarding proceeding with closure vs replacing tricuspid valve. Given the risks of heart block with valve replacement as well as future bioprosthetic valve degeneration in the setting of a young, active individual, we chose to proceed with removal of cross clamp and wean from bypass. Postoperative TEE revealed mild to moderate TR, and normal left and right ventricular function (Fig. 3 ). In the following days, the patient was weaned off vasoactive medications, however remained hypotensive, so a beta blocker was not initiated. Postoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating mild-moderate tricuspid valve regurgitation into the right atrium following surgical repair. 4-weeks following the operation, a TTE demonstrated residual mild TR with a mean transvalvular pressure gradient of 2 mmHg. The right ventricle also appeared to exhibit reverse positive remodeling, returning to a cavity size within normal limits. Following her operation, the patient was found to have a right upper extremity deep vein thrombosis requiring anticoagulation. No other significant complications were noted in the postoperative period to date. Discussion and Conclusions LDS is a rare subtype of connective tissue disorder, and its phenotypic presentation spans from subclinical (such as seen in this patient) to severe. LDS subtypes are distinguished by their underlying mutations and phenotypic presentations; LDS type 5 is denoted by mutations in the TGFB ligand 3 and lower rates of aneurysmal and cardiac abnormalities than other subtypes [ 7 ]. Indeed, thresholds for intervention in children with these subtypes are higher [ 8 ]. Interestingly, one small study demonstrated that women with LDS had a significantly higher rate of tricuspid regurgitation than men with LDS, however further characterization of this sex-associated difference is needed [ 9 ]. In consideration of surgical approach, much of the concern for Loeys-Dietz patients is an increased rate of progressive dilation following graft placement, especially in cases of aneurysmal repair or aortic valve repair [ 10 ]. However, this patient did not have any evidence of vascular disease, suggesting that future dilation of the repaired area would be unlikely to occur. There are limited reports of traumatic blunt cardiac trauma in patients with connective tissue disorders, as much of the literature focuses on pathogenic aneurysmal disease associated with underlying mutations. There have been some case reports of tricuspid regurgitation following blunt chest trauma, with one case even highlighting a horse kick as the mechanism of injury, just as was seen here [ 11 ]. In both cases, the patient suffered anterior papillary muscle rupture; however, in the non-LDS case, the patient was asymptomatic, and the TR was discovered upon incidental TTE performed during admission. Both patients received surgical repair, and had residual postoperative TR. It is unclear why one patient would have more severe symptoms of TR compared to another, however given that the patient presented here had torn chordae in addition to an anterior papillary muscle rupture, and with underlying LDS, there may have been less ability to compensate. Tricuspid rupture following blunt cardiac trauma is often ascribed to an acute increase in intraventricular pressure due to external compression at the same time as systole, leading to a tear within the structures maintaining valve patency [ 1 ]. Other mechanisms involve ischemia due to injury, causing tearing of the papillary muscles. In this patient, the presence of a pericardial effusion with tamponade suggests she likely had significant myocardial injury following the impact of the horse kick. Given she progressed quickly to TR (visible during pericardial window placement), it is more likely the mechanism of the papillary rupture was an acute increase in pressure within the right ventricle rather than prolonged ischemia following myocardial contusion. As a result, in patients with acute cardiogenic shock following blunt cardiac trauma, with evidence of valvular dysfunction, rapid characterization with dedicated cardiac imaging and early decision making for repair is crucial for restoration of normal cardiac function. In patients with underlying connective tissue disorders, early multidisciplinary collaboration in order to fully characterize their condition (including subtype) is crucial for preoperative planning. Abbreviations Loeys-Dietz Syndrome – LDS Transthoracic Echocardiogram- TTE Transesophageal Echocardiogram- TEE Tricuspid Regurgitation- TR Declarations Informed Consent Statement: The patient’s informed consent was obtained prior to the publication of this Case Report. This case report was reviewed by the Institutional Review Board of Oregon Health & Science University and deemed not human research (IRB #29968). Disclosures : The authors have no disclosures. Ethics Approval and Consent to Participate The Oregon Health and Science University Institutional Review Board and Ethics Committee reviewed and approved this case report. All clinical procedures were performed in accordance with the standards of the institution. Consent for Publication Informed consent was obtained from the patient for the publication of the case report and any accompanying images. Availability of Data and Materials No datasets were generated or analyzed. Competing Interests The authors declare they have no competing interests Funding This study recieved no specific grant from any funding agency Authors contributions CB, ND, and JD, contributed equally to this work. All authors read and approved the final manuscript. Acknowledgements Not applicable References Huis in ', t Veld MA, Craft CA, Hood RE. Blunt Cardiac Trauma Review. Cardiol Clin. 2018;36(1):183–91. https://doi.org/10.1016/j.ccl.2017.08.010 . Dounis G, Matsakas E, Poularas J, et al. Traumatic tricuspid insufficiency: a case report with a review of the literature. Eur J Emerg Med. 2002;9(3):258–61. https://doi.org/10.1097/00063110-200209000-00010 . Meel R, Ngutshane B, Gonçalves R, Mogaladi S. A Case of Severe Tricuspid Regurgitation Related to Traumatic Papillary Muscle Rupture. Case Rep Cardiol. 2020;2020:8505894. https://doi.org/10.1155/2020/8505894 . Mehrotra D, Dalley P, Mahon B. Tricuspid valve avulsion after blunt chest trauma. Tex Heart Inst J. 2012;39(5):668–70. Loeys BL, Dietz HC et al. Loeys-Dietz Syndrome. In: Adam MP, Feldman J, Mirzaa GM, editors. GeneReviews®. Seattle (WA): University of Washington, Seattle; 1993–2026. Hiratzka LF, Bakris GL, Beckman JA et al. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM Guidelines for the Diagnosis and Management of Patients With Thoracic Aortic Disease. Circulation. 2010;121(13):e266-e369. https://doi.org/10.1161/CIR.0b013e3181d4739e Gouda P, Kay R, Habib M, et al. Clinical features and complications of Loeys-Dietz syndrome: A systematic review. Int J Cardiol. 2022;362:158–67. https://doi.org/10.1016/j.ijcard.2022.05.065 . Patel ND, Alejo D, Crawford T, et al. Aortic Root Replacement for Children With Loeys-Dietz Syndrome. Ann Thorac Surg. 2017;103(5):1513–8. https://doi.org/10.1016/j.athoracsur.2017.01.053 . Abdul Nabi H, Bcharah G, Dreher L, et al. Sex-based differences in patients with Loeys-Dietz syndrome: An analysis of arteriopathies and surgical interventions. Int J Cardiol. 2025;437:133477. https://doi.org/10.1016/j.ijcard.2025.133477 . Patel ND, Crawford T, Magruder JT, et al. Cardiovascular operations for Loeys-Dietz syndrome: Intermediate-term results. J Thorac Cardiovasc Surg. 2017;153(2):406–12. https://doi.org/10.1016/j.jtcvs.2016.10.088 . Dorge M, Deleuse R, Pouleur AC, Badii MC. Severe tricuspid regurgitation after a horse kick: a case report of a rare cause of acquired valvulopathy. Eur Heart J Case Rep. 2025;9(2):ytae691. https://doi.org/10.1093/ehjcr/ytae691 . Additional Declarations No competing interests reported. Cite Share Download PDF Status: Under Review Version 1 posted Reviews received at journal 10 May, 2026 Reviews received at journal 09 May, 2026 Reviews received at journal 07 May, 2026 Reviews received at journal 03 May, 2026 Reviewers agreed at journal 03 May, 2026 Reviewers agreed at journal 29 Apr, 2026 Reviews received at journal 28 Apr, 2026 Reviews received at journal 28 Apr, 2026 Reviewers agreed at journal 28 Apr, 2026 Reviewers agreed at journal 27 Apr, 2026 Reviewers agreed at journal 27 Apr, 2026 Reviewers agreed at journal 27 Apr, 2026 Reviewers invited by journal 27 Apr, 2026 Editor assigned by journal 14 Apr, 2026 Submission checks completed at journal 14 Apr, 2026 First submitted to journal 09 Apr, 2026 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-9363599","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Case Report","associatedPublications":[],"authors":[{"id":633694974,"identity":"d11c2145-fb76-4c4f-95a1-2789e2b23936","order_by":0,"name":"Carla Boyle","email":"","orcid":"","institution":"Oregon Health \u0026 Science University","correspondingAuthor":false,"prefix":"","firstName":"Carla","middleName":"","lastName":"Boyle","suffix":""},{"id":633694975,"identity":"d0b05c47-a10a-4ddd-aebe-11304a08345e","order_by":1,"name":"Natalie Dixon","email":"","orcid":"","institution":"Oregon Health \u0026 Science University","correspondingAuthor":false,"prefix":"","firstName":"Natalie","middleName":"","lastName":"Dixon","suffix":""},{"id":633694976,"identity":"80647eaa-f0cc-4e84-9c37-2894a9838150","order_by":2,"name":"Julie Doberne","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAtUlEQVRIiWNgGAWjYDCCAzxgSo5BAkwzE6/FmHQtiQ1Ea+E73nvwceUOm/R+6fZnEgwV1okNhLRInjmXbHj2TFruzDlnzCQYzqQT1mJwI8dMsrHtcO6GGzlsEoxth4nSYv6zse1/usGN9GcSjP+I02LG2Nh2IMHgRoKZBGMDEVpAfgE6LNlw5owcY4uEY+nGBLWAQuxjY5udPL9E+sMbH2qsZQlqQQUJpCkfBaNgFIyCUYALAAAWzEEVy+jcZgAAAABJRU5ErkJggg==","orcid":"","institution":"Oregon Health \u0026 Science University","correspondingAuthor":true,"prefix":"","firstName":"Julie","middleName":"","lastName":"Doberne","suffix":""}],"badges":[],"createdAt":"2026-04-09 05:40:25","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-9363599/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-9363599/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":108939432,"identity":"66cedf44-e16f-49d8-999e-d8ca3fcd3bfb","added_by":"auto","created_at":"2026-05-11 05:07:47","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":108047,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003ePreoperative Transesophageal Echocardiogram\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003ePreoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating significant tricuspid regurgitation into the right atrium, with a mass (later demonstrated to be ruptured papillary muscle) visible on the tricuspid leaflet. Increased right atrial size also demonstrated.\u003c/p\u003e","description":"","filename":"Fig1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9363599/v1/5889d248792ebf055a7b5edf.jpg"},{"id":108939433,"identity":"99f40dc7-d1b8-421e-9124-2d690560903d","added_by":"auto","created_at":"2026-05-11 05:07:47","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":115693,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eIntraoperative image of damaged tricuspid valve prior to repair\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eMedical photography of intraoperative visualization of tricuspid valve following bicaval cannulation, bypass initiation and tricuspid valve exposure. Papillary muscle is grasped and elevated demonstrating where rupture occurred, prior to reattachment.\u003c/p\u003e","description":"","filename":"Fig2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9363599/v1/6a1401cb0bdbdc7609199fdf.jpg"},{"id":108978103,"identity":"7b255f78-5b16-4aa5-9f55-5bab332b50b7","added_by":"auto","created_at":"2026-05-11 11:34:05","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":75911,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003ePostoperative Transesophageal Echocardiogram\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003ePostoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating mild-moderate tricuspid valve regurgitation into the right atrium following surgical repair.\u003c/p\u003e","description":"","filename":"Fig3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9363599/v1/26e48d8a89821cfea645b59c.jpg"},{"id":108979852,"identity":"c220db41-d314-4aec-9ec4-409691654ad9","added_by":"auto","created_at":"2026-05-11 12:02:00","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":438492,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-9363599/v1/714a984d-670d-476a-8c96-a1636c44be53.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Repair of Traumatic Tricuspid Valve Rupture in Loeys Dietz Type V","fulltext":[{"header":"Background","content":"\u003cp\u003eBlunt chest trauma leading to cardiac injury is uncommon, however when it occurs it most often affects the myocardium, leading to cardiac wall damage [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. Given its anterior location, right sided cardiac injury is more common than left. Isolated valvular injury is uncommon and often due to pressure redistribution during acute blunt trauma. This includes papillary muscle and chordae tendinae rupture due to trauma occurring during systole, causing a rapid increase in intraventricular pressure [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. If valvular injury occurs due to papillary muscle necrosis following cardiac wall damage, presentation may be delayed, leading to latent diagnosis and management of regurgitation. The mechanism of chest injury associated with tricuspid valve rupture is most commonly high velocity acceleration-deceleration accidents in motor vehicles [\u003cspan additionalcitationids=\"CR3\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eLoeys-Dietz Syndrome (LDS) is a heritable angiopathy characterized by autosomal dominant mutations in the transforming growth factor beta receptor (TGFB) pathway, causing degeneration of the medial arterial layer and loss of elastic tissue [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. This increases susceptibility to arterial pathologies such as aortic aneurysms, arterial tortuosity and cardiomyopathies, as well as craniofacial malformations and other cutaneous manifestations. Patients with LDS often exhibit aggressive aortopathies requiring early intervention.\u003c/p\u003e \u003cp\u003eThe patient was diagnosed with LDS type V with a mutation in TGFB3 (variant c. 487C\u0026thinsp;\u0026gt;\u0026thinsp;t p.Arg163Trp) after receiving targeted parental testing as her daughter was found to have a bicuspid aortic valve and aortic enlargement. Upon diagnosis, the patient had normal aortic root measurements, no valvular abnormalities, no significant aortic dilation, and no peripheral tortuosity. She also lacked any classic features of LDS, such as hypertelorism, or translucent skin.\u003c/p\u003e"},{"header":"Case Presentation","content":"\u003cp\u003eA 54-year-old woman with past medical history of cervical instability, obstructive sleep apnea, easy bruising, gastroesophageal reflux, and Loeys-Dietz Syndrome (LDS) was brought emergently to care after being kicked in the chest by a horse.\u003c/p\u003e \u003cp\u003eUpon presentation, the patient was hypotensive and tachycardic, with distended neck veins and transthoracic echocardiogram (TTE) demonstrating a significant pericardial effusion and IVC distention. The patient received an urgent sub-xiphoid pericardial window placement, during which she was found to have a 200ml hemopericardium with clot formation. Intraoperative transesophageal echocardiogram (TEE) also demonstrated a ruptured tricuspid valve chord and moderate tricuspid valve regurgitation (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). Following pericardial window placement, the patient developed recurrent hypotension refractory to fluid resuscitation with transthoracic echocardiograph revealing worsened severe tricuspid regurgitation and a flail tricuspid leaflet with flow reversal in the hepatic veins and flattening of the interventricular septum. Left ventricular ejection fraction was preserved.\u003c/p\u003e \u003cp\u003eThe patient required significant vasopressor support and was ultimately transferred to a higher level of care for continued management. Invasive hemodynamics demonstrated minimal right ventricle pulsatility, low pulmonary artery pulsatility index (PAPi score 0.56 at admission) and ventricularized right atrial waveform. She continued to require vasopressor and inotropic support and diuresis for 3 days until weaning was successful, and she was stable for intervention. Prior to intervention, she had a net fluid output of 6 liters. Repeat TTE following volume optimization continued to demonstrate severe TR due to a flail leaflet.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003ePreoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating significant tricuspid regurgitation into the right atrium, with a mass (later demonstrated to be ruptured papillary muscle) visible on the tricuspid leaflet. Increased right atrial size also demonstrated.\u003c/p\u003e \u003cp\u003eGiven the severity of her tricuspid regurgitation, timely intervention following optimization was necessary. As the etiology of the TR was a flail leaflet, she was not a candidate for percutaneous annuloplasty devices. Other percutaneous options relying on coaptation were also rejected, as there was not enough tissue present to clasp due to the location of the papillary rupture. Vascular surgery was also consulted regarding risks related to the patient’s LDS subtype, and these were deemed to be non-prohibitive. Reports from interventions in LDS patients also affirm that surgery is not complicated by increased tissue fragility in this patient population [\u003cspan class=\"CitationRef\"\u003e6\u003c/span\u003e]. Finally, her age, conditioning, and lack of surgical history suggested that she would be an appropriate candidate for open repair. Thus, surgical repair of the tricuspid valve was planned, with the option for bioprosthetic valve replacement if needed.\u003c/p\u003e \u003cp\u003eThe surgery was performed via median sternotomy with central aortic and bicaval venous cannulation. Cardiopulmonary bypass was initiated, and an aortic cross clamp was applied. A right atriotomy was performed, and the tricuspid valve was inspected. A flail segment of the anterior leaflet was noted. On further inspection, this was due to an anterior papillary muscle that has been avulsed from the ventricular attachments (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e). The papillary muscle was secured to the right ventricle using 2 − 0 plegdeted Ticron sutures. Interrupted 2 − 0 Ticron sutures were then placed horizontally and passed through a 32mm Tricuspid Edwards MC3 annuloplasty band. This was then seated and secured using Corknot. Upon further testing of the valve, a residual leak was noted from a small flail segment on the posterior leaflet with an adjacent small cleft. This cord had been avulsed from the right ventricle along the papillary muscle as well. The cleft was closed with running suture. Using an additional pledgeted 2 − 0 Ticron suture, the papillary attached to the posterior flail cord was reattached to the right ventricle.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eMedical photography of intraoperative visualization of tricuspid valve following bicaval cannulation, bypass initiation and tricuspid valve exposure. Papillary muscle is grasped and elevated demonstrating where rupture occurred, prior to reattachment.\u003c/p\u003e \u003cp\u003eOn final testing, a small amount of leak was noted centrally. Discussion was held regarding proceeding with closure vs replacing tricuspid valve. Given the risks of heart block with valve replacement as well as future bioprosthetic valve degeneration in the setting of a young, active individual, we chose to proceed with removal of cross clamp and wean from bypass. Postoperative TEE revealed mild to moderate TR, and normal left and right ventricular function (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e). In the following days, the patient was weaned off vasoactive medications, however remained hypotensive, so a beta blocker was not initiated.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003ePostoperative transesophageal echocardiogram visualizing the right atrium and right ventricle with Doppler color wave overlaid. Image is taken during systole demonstrating mild-moderate tricuspid valve regurgitation into the right atrium following surgical repair.\u003c/p\u003e \u003cp\u003e4-weeks following the operation, a TTE demonstrated residual mild TR with a mean transvalvular pressure gradient of 2 mmHg. The right ventricle also appeared to exhibit reverse positive remodeling, returning to a cavity size within normal limits. Following her operation, the patient was found to have a right upper extremity deep vein thrombosis requiring anticoagulation. No other significant complications were noted in the postoperative period to date.\u003c/p\u003e "},{"header":"Discussion and Conclusions","content":"\u003cp\u003eLDS is a rare subtype of connective tissue disorder, and its phenotypic presentation spans from subclinical (such as seen in this patient) to severe. LDS subtypes are distinguished by their underlying mutations and phenotypic presentations; LDS type 5 is denoted by mutations in the TGFB ligand 3 and lower rates of aneurysmal and cardiac abnormalities than other subtypes [\u003cspan class=\"CitationRef\"\u003e7\u003c/span\u003e]. Indeed, thresholds for intervention in children with these subtypes are higher [\u003cspan class=\"CitationRef\"\u003e8\u003c/span\u003e]. Interestingly, one small study demonstrated that women with LDS had a significantly higher rate of tricuspid regurgitation than men with LDS, however further characterization of this sex-associated difference is needed [\u003cspan class=\"CitationRef\"\u003e9\u003c/span\u003e]. In consideration of surgical approach, much of the concern for Loeys-Dietz patients is an increased rate of progressive dilation following graft placement, especially in cases of aneurysmal repair or aortic valve repair [\u003cspan class=\"CitationRef\"\u003e10\u003c/span\u003e]. However, this patient did not have any evidence of vascular disease, suggesting that future dilation of the repaired area would be unlikely to occur.\u003c/p\u003e\u003cp\u003eThere are limited reports of traumatic blunt cardiac trauma in patients with connective tissue disorders, as much of the literature focuses on pathogenic aneurysmal disease associated with underlying mutations. There have been some case reports of tricuspid regurgitation following blunt chest trauma, with one case even highlighting a horse kick as the mechanism of injury, just as was seen here [\u003cspan class=\"CitationRef\"\u003e11\u003c/span\u003e]. In both cases, the patient suffered anterior papillary muscle rupture; however, in the non-LDS case, the patient was asymptomatic, and the TR was discovered upon incidental TTE performed during admission. Both patients received surgical repair, and had residual postoperative TR. It is unclear why one patient would have more severe symptoms of TR compared to another, however given that the patient presented here had torn chordae in addition to an anterior papillary muscle rupture, and with underlying LDS, there may have been less ability to compensate.\u003c/p\u003e\u003cp\u003eTricuspid rupture following blunt cardiac trauma is often ascribed to an acute increase in intraventricular pressure due to external compression at the same time as systole, leading to a tear within the structures maintaining valve patency [\u003cspan class=\"CitationRef\"\u003e1\u003c/span\u003e]. Other mechanisms involve ischemia due to injury, causing tearing of the papillary muscles. In this patient, the presence of a pericardial effusion with tamponade suggests she likely had significant myocardial injury following the impact of the horse kick. Given she progressed quickly to TR (visible during pericardial window placement), it is more likely the mechanism of the papillary rupture was an acute increase in pressure within the right ventricle rather than prolonged ischemia following myocardial contusion. As a result, in patients with acute cardiogenic shock following blunt cardiac trauma, with evidence of valvular dysfunction, rapid characterization with dedicated cardiac imaging and early decision making for repair is crucial for restoration of normal cardiac function. In patients with underlying connective tissue disorders, early multidisciplinary collaboration in order to fully characterize their condition (including subtype) is crucial for preoperative planning.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eLoeys-Dietz Syndrome \u0026ndash; LDS\u003c/p\u003e\n\u003cp\u003eTransthoracic Echocardiogram- TTE\u003c/p\u003e\n\u003cp\u003eTransesophageal Echocardiogram- TEE\u003c/p\u003e\n\u003cp\u003eTricuspid Regurgitation- TR\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eInformed Consent Statement: The patient\u0026rsquo;s informed consent was obtained prior to the publication of this Case Report.\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis case report was reviewed by the Institutional Review Board of Oregon Health \u0026amp; Science University and deemed not human research (IRB #29968).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eDisclosures\u003c/strong\u003e:\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe authors have no disclosures.\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eEthics Approval and Consent to Participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe Oregon Health and Science University Institutional Review Board and Ethics Committee reviewed and approved this case report. All clinical procedures were performed in accordance with the standards of the institution.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for Publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eInformed consent was obtained from the patient for the publication of the case report and any accompanying images.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of Data and Materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNo datasets were generated or analyzed.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare they have no competing interests\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study recieved no specific grant from any funding agency\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eCB, ND, and JD, contributed equally to this work. All authors read and approved the final manuscript.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eHuis in ', t Veld MA, Craft CA, Hood RE. Blunt Cardiac Trauma Review. Cardiol Clin. 2018;36(1):183\u0026ndash;91. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.ccl.2017.08.010\u003c/span\u003e\u003cspan address=\"10.1016/j.ccl.2017.08.010\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDounis G, Matsakas E, Poularas J, et al. Traumatic tricuspid insufficiency: a case report with a review of the literature. 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Tex Heart Inst J. 2012;39(5):668\u0026ndash;70.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLoeys BL, Dietz HC et al. Loeys-Dietz Syndrome. In: Adam MP, Feldman J, Mirzaa GM, editors. GeneReviews\u0026reg;. Seattle (WA): University of Washington, Seattle; 1993\u0026ndash;2026.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHiratzka LF, Bakris GL, Beckman JA et al. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM Guidelines for the Diagnosis and Management of Patients With Thoracic Aortic Disease. Circulation. 2010;121(13):e266-e369. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1161/CIR.0b013e3181d4739e\u003c/span\u003e\u003cspan address=\"10.1161/CIR.0b013e3181d4739e\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGouda P, Kay R, Habib M, et al. Clinical features and complications of Loeys-Dietz syndrome: A systematic review. Int J Cardiol. 2022;362:158\u0026ndash;67. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.ijcard.2022.05.065\u003c/span\u003e\u003cspan address=\"10.1016/j.ijcard.2022.05.065\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePatel ND, Alejo D, Crawford T, et al. Aortic Root Replacement for Children With Loeys-Dietz Syndrome. Ann Thorac Surg. 2017;103(5):1513\u0026ndash;8. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.athoracsur.2017.01.053\u003c/span\u003e\u003cspan address=\"10.1016/j.athoracsur.2017.01.053\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAbdul Nabi H, Bcharah G, Dreher L, et al. Sex-based differences in patients with Loeys-Dietz syndrome: An analysis of arteriopathies and surgical interventions. Int J Cardiol. 2025;437:133477. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.ijcard.2025.133477\u003c/span\u003e\u003cspan address=\"10.1016/j.ijcard.2025.133477\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePatel ND, Crawford T, Magruder JT, et al. Cardiovascular operations for Loeys-Dietz syndrome: Intermediate-term results. J Thorac Cardiovasc Surg. 2017;153(2):406\u0026ndash;12. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.jtcvs.2016.10.088\u003c/span\u003e\u003cspan address=\"10.1016/j.jtcvs.2016.10.088\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eDorge M, Deleuse R, Pouleur AC, Badii MC. Severe tricuspid regurgitation after a horse kick: a case report of a rare cause of acquired valvulopathy. Eur Heart J Case Rep. 2025;9(2):ytae691. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1093/ehjcr/ytae691\u003c/span\u003e\u003cspan address=\"10.1093/ehjcr/ytae691\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"journal-of-cardiothoracic-surgery","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"jcts","sideBox":"Learn more about [Journal of Cardiothoracic Surgery](http://cardiothoracicsurgery.biomedcentral.com)","snPcode":"13019","submissionUrl":"https://submission.nature.com/new-submission/13019/3","title":"Journal of Cardiothoracic Surgery","twitterHandle":"@BioMedCentral","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Loeys-Dietz Syndrome, Tricuspid Valve Repair, Connective Tissue Disorders","lastPublishedDoi":"10.21203/rs.3.rs-9363599/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-9363599/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground:\u003c/h2\u003e \u003cp\u003eLoeys-Dietz Syndrome (LDS) is a rare connective tissue disorder that often results in vascular fragility and valvular abnormalities, most commonly presenting with aortic dilation requiring intervention. Blunt cardiac trauma following chest injury is rare, and patients uncommonly experience isolated valvular injury. Here, we present a case of a patient with LDS type V who suffered chest trauma resulting in acute tricuspid regurgitation complicated by cardiogenic shock requiring surgical repair.\u003c/p\u003e\u003ch2\u003eCase Presentation:\u003c/h2\u003e \u003cp\u003eA 54-year-old woman with a history of cervical instability, obstructive sleep apnea, easy bruising and LDS type V with no relevant surgical history was brought to care after acute chest trauma. Initial management demonstrated a pericardial effusion for which a pericardial window was placed at an outside hospital. She was transferred to a higher level of care for worsening cardiogenic shock, and severe tricuspid regurgitation was demonstrated on imaging, secondary to a flail leaflet. The tricuspid valve was repaired surgically, and the patient was weaned off vasoactive agents before discharge.\u003c/p\u003e\u003ch2\u003eConclusions:\u003c/h2\u003e \u003cp\u003eIntraoperative management of connective tissue disorders in cardiothoracic surgery patients is highly dependent on their subtype. In this case, the presenting patient was likely at increased risk for valvular rupture due to her underlying LDS; however, this was not noted to impact tissue quality during the surgical repair. Significant preoperative collaboration between the cardiothoracic and vascular surgical teams was imperative for anticipatory planning and should be the standard for patients with complex underlying connective tissue disorders.\u003c/p\u003e","manuscriptTitle":"Repair of Traumatic Tricuspid Valve Rupture in Loeys Dietz Type V","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-05-11 05:07:43","doi":"10.21203/rs.3.rs-9363599/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"editorInvitedReview","content":"","date":"2026-05-10T13:30:06+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-09T12:51:10+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-08T03:07:19+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-03T18:19:50+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"76261354277513761129127727242354973639","date":"2026-05-03T17:57:38+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"326533337480036684387001171639256686092","date":"2026-04-29T20:19:08+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-04-29T00:29:43+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-04-28T12:21:08+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"41281146304698673805753217251400510603","date":"2026-04-28T11:33:26+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"162881933677548819633651913085574565345","date":"2026-04-28T02:42:14+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"284826679374528274181272375602495195965","date":"2026-04-27T17:58:56+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"138990949105972405038642017270039370176","date":"2026-04-27T17:52:40+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-04-27T14:12:27+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2026-04-14T09:35:13+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2026-04-14T09:33:49+00:00","index":"","fulltext":""},{"type":"submitted","content":"Journal of Cardiothoracic Surgery","date":"2026-04-09T05:32:21+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"journal-of-cardiothoracic-surgery","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"jcts","sideBox":"Learn more about [Journal of Cardiothoracic Surgery](http://cardiothoracicsurgery.biomedcentral.com)","snPcode":"13019","submissionUrl":"https://submission.nature.com/new-submission/13019/3","title":"Journal of Cardiothoracic Surgery","twitterHandle":"@BioMedCentral","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"a29a417e-4ac2-4e0d-b1d9-c62bd66009a1","owner":[],"postedDate":"May 11th, 2026","published":true,"recentEditorialEvents":[{"type":"editorInvitedReview","content":"","date":"2026-05-10T13:30:06+00:00","index":58,"fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-09T12:51:10+00:00","index":57,"fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-08T03:07:19+00:00","index":56,"fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-03T18:19:50+00:00","index":55,"fulltext":""},{"type":"reviewerAgreed","content":"76261354277513761129127727242354973639","date":"2026-05-03T17:57:38+00:00","index":54,"fulltext":""},{"type":"reviewerAgreed","content":"326533337480036684387001171639256686092","date":"2026-04-29T20:19:08+00:00","index":52,"fulltext":""}],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-05-11T05:07:43+00:00","versionOfRecord":[],"versionCreatedAt":"2026-05-11 05:07:43","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-9363599","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-9363599","identity":"rs-9363599","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}