Preoperative Embolization of a Pulmonary Carcinoid Tumor with Unusual Arterial Supply: A Case Report

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Abstract Background Pulmonary carcinoid tumors are rare neuroendocrine neoplasms that carry a risk of bleeding. We report a case of a tumor with unusual arterial supply from multiple sources including collateral from the renal artery, successfully managed with preoperative embolization followed by surgical resection. Case presentation: A 39-year-old woman with no significant medical history presented with chronic cough. Chest radiography revealed an opacity in the right hilar region. Computed tomography (CT) showed a mass obstructing the right middle lobe bronchus. 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) demonstrated no abnormal uptake in the lesion. However, a Ga-68 DOTATATE somatostatin receptor scan (DOTA-PET) showed intense tracer uptake in the mass. Bronchoscopy identified a reddish endobronchial lesion completely occluding the middle lobe bronchus and causing distal collapse. Biopsy was deferred due to the lesion’s hypervascular appearance. With a presumptive diagnosis of carcinoid tumor, a multidisciplinary team planned for surgical resection. To mitigate intraoperative bleeding, preoperative angiographic evaluation was performed. Digital subtraction angiography (DSA) revealed that the blood supply originated from the right bronchial artery, right internal mammary artery and right renal artery. All identified feeding arteries were selectively catheterized and embolized with coils. The patient underwent a right middle lobectomy. Intraoperative blood loss was minimal, and the tumor was resected completely. Pathology confirmed carcinoid tumor. At two-year follow-up, the patient remains asymptomatic. Conclusions This case highlights a rare arterial supply to a lung tumor and demonstrates that preoperative embolization of multiple feeding vessels can facilitate safe resection of a hypervascular tumor. Awareness of vascular anomalies and multidisciplinary approach were key to successful management.
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Preoperative Embolization of a Pulmonary Carcinoid Tumor with Unusual Arterial Supply: A Case Report | 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 Preoperative Embolization of a Pulmonary Carcinoid Tumor with Unusual Arterial Supply: A Case Report Isa Cam, Aykut Eliçora, Almotasem Shatat, Hüseyin Fatih Sezer, and 5 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-6862855/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 04 Jan, 2026 Read the published version in Journal of Cardiothoracic Surgery → Version 1 posted 15 You are reading this latest preprint version Abstract Background Pulmonary carcinoid tumors are rare neuroendocrine neoplasms that carry a risk of bleeding. We report a case of a tumor with unusual arterial supply from multiple sources including collateral from the renal artery, successfully managed with preoperative embolization followed by surgical resection. Case presentation: A 39-year-old woman with no significant medical history presented with chronic cough. Chest radiography revealed an opacity in the right hilar region. Computed tomography (CT) showed a mass obstructing the right middle lobe bronchus. 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) demonstrated no abnormal uptake in the lesion. However, a Ga-68 DOTATATE somatostatin receptor scan (DOTA-PET) showed intense tracer uptake in the mass. Bronchoscopy identified a reddish endobronchial lesion completely occluding the middle lobe bronchus and causing distal collapse. Biopsy was deferred due to the lesion’s hypervascular appearance. With a presumptive diagnosis of carcinoid tumor, a multidisciplinary team planned for surgical resection. To mitigate intraoperative bleeding, preoperative angiographic evaluation was performed. Digital subtraction angiography (DSA) revealed that the blood supply originated from the right bronchial artery, right internal mammary artery and right renal artery. All identified feeding arteries were selectively catheterized and embolized with coils. The patient underwent a right middle lobectomy. Intraoperative blood loss was minimal, and the tumor was resected completely. Pathology confirmed carcinoid tumor. At two-year follow-up, the patient remains asymptomatic. Conclusions This case highlights a rare arterial supply to a lung tumor and demonstrates that preoperative embolization of multiple feeding vessels can facilitate safe resection of a hypervascular tumor. Awareness of vascular anomalies and multidisciplinary approach were key to successful management. Pulmonary carcinoid Hypervascular lung tumor Bronchial artery embolization Lobectomy Aberrant arterial supply Figures Figure 1 Figure 2 Figure 3 Background Pulmonary carcinoid tumors are rare neuroendocrine tumors of the lung, representing only about 1–2% of primary pulmonary neoplasms (1). They are typically low-grade, slow-growing neoplasms with relatively low metastatic potential. These tumors most often present in middle-aged adults and, unlike other lung cancers, have no strong association with smoking (1). Central bronchial carcinoids can cause airway obstruction leading to cough, wheezing, recurrent pneumonia or atelectasis, and occasionally hemoptysis, and many are discovered incidentally on imaging performed for unrelated reasons (1). A hallmark feature is rich vascularity; bronchial carcinoids appear as reddish endobronchial masses that bleed easily on contact (2). The blood supply is usually derived from the bronchial arteries, but larger or long-standing lesions can recruit additional “parasitic” supply from other systemic arteries, such as intercostal arteries, the internal mammary artery, or even branches of the abdominal aorta (3). Recognizing such aberrant arterial supply is important, as uncontrolled feeder vessels can result in severe hemorrhage during interventions. Definitive management of localized pulmonary carcinoid is surgical resection, which offers an excellent prognosis for these tumors, given the typical natural history. However, intraoperative bleeding is a major concern due to their hypervascular nature; even bronchoscopic biopsy can provoke significant hemorrhage (2). Therefore, when a carcinoid tumor is suspected, meticulous planning for bleeding control is warranted. Preoperative embolization of feeding arteries is one strategy that has been used to minimize hemorrhage risk in hypervascular thoracic tumors, including large bronchial carcinoids (4). Here, we report a case in which thorough angiographic mapping and coil embolization of an unusual multi-arterial tumor supply, including collaterals from the renal artery, permitted safe surgical resection of a bronchial carcinoid that might otherwise have posed a serious bleeding hazard. To the best of our knowledge, there is no previously documented case of a pulmonary carcinoid tumor receiving arterial supply from the renal artery in addition to the bronchial and internal mammary arteries and undergoing preoperative embolization to reduce the risk of bleeding. This appears to be the first reported instance, and highlights the importance of thorough angiographic evaluation for any hypervascular lung tumor. Case Presentation A 39-year-old female who had never smoked, was referred to pulmonary clinic with a 3-month history of persistent dry cough. She reported no hemoptysis, wheezing, fever, night sweats or weight loss. Physical examination was unremarkable except for diminished breath sounds in the right lung field. Routine laboratory tests were within normal limits. A chest X-ray revealed an ill-defined opacity in the right hilar region. Suspecting an airway lesion or an enlarged lymph node, thoracic CT was performed. The CT scan showed a well-defined round mass with millimetric calcifications, obstructing the right middle lobe bronchus, with complete collapse of the right middle lobe. The interface between the mass and the atelectatic lobe was indistinct, making it difficult to determine the exact tumor margins (Fig. 1 A). For further characterization, a PET-CT scan was performed. Interestingly, the lesion demonstrated no significant uptake of 18F-FDG, which is unusual for most malignant tumors (Fig. 1 B). This raised the possibility that the lesion could be a low-grade neoplasm, such as a carcinoid, which may be PET-negative. Therefore, a DOTA-PET scan was obtained to evaluate somatostatin receptor expression. On this DOTA-PET scan, the mass showed intense radiotracer uptake with an SUV-max of 46, increasing the possibility of a neuroendocrine tumor (Fig. 1 C). No other areas of abnormal uptake were seen, suggesting that the disease was localized to the lung. The patient subsequently underwent bronchoscopy for direct visualization and possible biopsy. Bronchoscopy revealed a vascular, reddish endobronchial tumor obliterating the right middle lobe bronchial orifice with evidence of complete middle lobe collapse distal to it. Given its friable appearance, the bronchoscopist judged that a biopsy would carry high risk of uncontrolled bleeding. In the interest of safety, no tissue sample was taken bronchoscopically. Based on the imaging findings and bronchoscopic appearance, the preliminary diagnosis was a typical bronchial carcinoid tumor causing right middle lobe atelectasis. Consistent with guidelines, surgical resection was indicated for this presumed carcinoid after discussion at a multidisciplinary tumor board. In light of the typical hypervascular nature of carcinoid tumors, the surgical team requested a preoperative CT angiographic evaluation and possible embolization to minimize intraoperative bleeding. The patient consented to this plan. Contrary to expectations, CT angiography showed that the tumor was not only supplied by the right bronchial artery and the right internal mammary artery but also by an arterial branch originating from the proximal right renal artery (Fig. 2 ). Digital subtraction angiography (DSA) was performed via a femoral approach. Initial bronchial arteriography showed a markedly hypertrophied right bronchial artery (Fig. 3 A) feeding the tumor alongside potential non-bronchial collaterals from the right internal mammary artery (Fig. 3 C) and another branch originating from the proximal right renal artery (Fig. 3 B). The latter finding was unusual, suggesting an aberrant transdiaphragmatic collateral possibly via an inferior phrenic artery branch originating from the renal artery. No pulmonary arterial blush or arteriovenous shunting was seen on the angiogram. After delineating the blood supply, embolization of the feeding arteries proceeded using a coaxial microcatheter technique. The right bronchial artery branch to the tumor was catheterized and occluded using multiple coils until stasis was achieved (Fig. 3 D). Next, the feeding artery arising from the renal artery was carefully catheterized; multiple coils were deployed, effectively cutting off flow to the tumor (Fig. 3 E). Finally, the branch from the right internal mammary artery was embolized with coils placed just distal to its origin, resulting in cessation of flow to the tumor (Fig. 3 F). A completion arteriogram showed no residual arterial perfusion of the tumor. The embolization procedure was tolerated well, with no immediate complications. The patient was observed overnight and had no chest pain, hemoptysis, or evidence of infarction to surrounding organs. Approximately one week later, a right thoracotomy and middle lobectomy was carried out. Notably the operation was performed successfully with minimal bleeding from the tumor bed, attesting to the efficacy of the prior embolization. On gross examination the tumor was well-circumscribed, red-brown, and appeared to be confined to the bronchus with extension into adjacent lung parenchyma causing collapse. Histopathological analysis of the resected specimen confirmed a typical carcinoid tumor. Tumor invasion was limited to the bronchus and immediately surrounding lung; the visceral pleura was intact. All surgical resection margins were clear of tumor with no lymph node involvement. The patient had an uncomplicated postoperative recovery. She was discharged on postoperative day six with instructions for routine follow-up. At her 2-year follow-up visit, she remained asymptomatic with no evidence of recurrence on clinical exam or on surveillance imaging (Fig. 1 D). Discussion and Conclusions Carcinoid tumors are highly vascular tumors supplied by systemic arteries, and even a small biopsy may lead to profuse bleeding (2). The most salient aspects of this case are the unusual arterial supply and the use of preoperative arterial embolization to mitigate bleeding risk. Bronchial carcinoid tumors can be extremely vascular, and have rarely been reported to recruit blood supply from multiple sources beyond the normal bronchial circulation (3). This case illustrates an extreme example of this phenomenon, since it had systemic feeders from the right internal mammary artery and even a branch arising from the right renal artery. Such aberrant arterial contributions have been described in other hypervascular intrathoracic tumors, although they are uncommon (3,5). If unrecognized, these collateral vessels could cause massive hemorrhage during surgery or even during bronchoscopic interventions. In the context of management of hemoptysis, it is crucial to search for and embolize non-bronchial systemic collaterals when bronchial artery embolization alone is not sufficient. Studies have shown that up to 45% of patients with severe hemoptysis have significant collateral supply to lung lesions from sources such as intercostal or phrenic arteries (5). Hemothorax is a serious complication associated with thoracic surgeries which increase morbidity and potentially necessitate reoperation. Several studies have highlighted the risks of perioperative bleeding and hemothorax, and have recommended preventive measures, such as preoperative embolization which can significantly reduce these risks. Rea et al. reported hemothorax requiring blood transfusions among postoperative complications in patients undergoing surgery for bronchial carcinoid tumors, underscoring the importance of minimizing intraoperative bleeding (6). Machuca et al. identified postoperative complications related to hemothorax, with some cases severe enough to require surgical reintervention (7). Similarly, Kasprzyk et al. observed that hemothorax was a significant postoperative complication in a case series of bronchial carcinoid tumors that often required reoperation, once again stressing the clinical significance of perioperative bleeding (8). Fadel et al., evaluating sleeve lobectomy procedures, also reported hemothorax as a major complication that could lead to substantial patient morbidity (9). Although rare, Filosso et al. reported one case of perioperative mortality associated with the surgical management of a bronchial carcinoid tumor (10). Therefore, embolization techniques may provide an essential intervention to control tumor-related vascularity, reducing the risk of perioperative bleeding and even mortality. There are some published reports in which preoperative embolization was used successfully for pulmonary carcinoids and other thoracic tumors with a high risk of bleeding. Jiang et al. described a case of a giant thymic carcinoid in which preoperative embolization of internal mammary arteries was performed one day prior to surgery, resulting in minimal intraoperative blood loss and an uncomplicated resection (11). A recent case series by Lucarelli et al. reported the use of preoperative embolization in a variety of giant thoracic tumors, including an atypical lung carcinoid; in all cases, embolization was technically successful and it significantly reduced tumor vascularity to facilitate safer surgery (3). The collective evidence from such reports suggests that if a pulmonary tumor is known to be highly vascular, such as a carcinoid or paraganglioma, then preoperative angiography and embolization should be considered to prevent hemorrhagic complications (3). It should be noted that preoperative embolization carries its own risks and should be undertaken by experienced operators. In the case series by Lucarelli et al., careful techniques were employed to avoid embolizing an artery that might supply the spinal cord (the artery of Adamkiewicz) (3). In the presented case, we took care to embolize the internal mammary branch distal to its origin to preserve the parent vessel and to super-selectively embolize the feeder from the renal artery to avoid any non-target embolization. Thus, a detailed understanding of thoracic vascular anatomy and meticulous angiographic technique are essential when using this strategy. In situations where a feeder artery also supplies normal tissue that cannot be compromised, one might choose to either embolize only distal branches or manage that vessel intraoperatively via surgical ligation under direct vision. In conclusion, hypervascular lung tumors, such as carcinoid tumors, may have unusual arterial supplies. Clinicians and surgeons should be vigilant for multiple systemic feeders to mitigate the risk of catastrophic bleeding, severe morbidity and potentially mortality. Abbreviations ● CT Computed tomography ● FDG Fluorodeoxyglucose ● PET Positron emission tomography ● SUV Standardized uptake value ● DOTA-PET Gallium-68 DOTA-peptide positron emission tomography (somatostatin receptor PET scan) ● DSA Digital subtraction angiography ● NET Neuroendocrine tumor ● IMA Internal mammary artery (also known as internal thoracic artery) Declarations Ethics approval and consent to participate: Not applicable. Institutional review board approval was not required for a single-patient case report. The patient provided informed consent to all treatments and to the use of her clinical information in this report. Consent for publication: Written informed consent was obtained from the patient for publication of this case report and accompanying images. Availability of data and materials: All relevant data are presented in the case report. Additional clinical details can be made available from the corresponding author upon reasonable request. Competing interests: The authors declare that they have no competing interests. Funding: No external funding was received for this study. All medical care and investigations were part of routine patient management. Authors’ contributions: AE, ST, HFS and SAB managed the patient’s workup and follow-up. IC carried out the arterial embolization and contributed details of the angiographic findings. IC, AY, EC, AS and BYB conducted the literature review and drafted the manuscript. All authors contributed to editing the report, and all approved the final manuscript. Acknowledgements: The authors thank the multidisciplinary team at our institution for their roles in managing this patient. We also extend our gratitude to the patient for allowing us to share her case for the benefit of medical education. References Limaiem F, Tariq MA, Ismail U, Wallen JM. Lung Carcinoid Tumors. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023. Mancini MC. Carcinoid Lung Tumors. Medscape Reference [Internet]. Updated May 13, 2024. Available from: https://emedicine.medscape.com/article/280104-overview. Lucarelli NM, Maggialetti N, Marulli G. Preoperative Embolization in the Management of Giant Thoracic Tumors: A Case Series. J Pers Med. 2024;14(10):1019. Utpat K, Basu S, Joshi JM. Dual Tracer PET Imaging (⁶⁸Ga-DOTATATE and ¹⁸F-FDG) Features in Pulmonary Carcinoid: Correlation with Tumor Proliferation Index. Indian J Nucl Med. 2017;32(1):39–41. Keller FS, Rosch J, Loflin TG, Nath PH, McElvein RB. Nonbronchial systemic collateral arteries: significance in percutaneous embolotherapy for hemoptysis. Radiology. 1987;164(3):687–692. Rea F, Rizzardi G, Zuin A, Marulli G, Nicotra S, Bulf R, Schiavon M, Sartori F. Outcome and surgical strategy in bronchial carcinoid tumors: single institution experience with 252 patients. Eur J Cardiothorac Surg. 2007;31(2):186–191. Machuca TN, Cardoso PFG, Camargo SM, et al. Surgical treatment of bronchial carcinoid tumors: A single-center experience. Lung Cancer. 2010;70(2):158–162 Kasprzyk M, Musiałkiewicz J, Kolasiński M, Jagiełka K, Dyszkiewicz W. Pulmonary carcinoids – analysis of early and long-term surgical treatment outcomes in a group of 90 patients. Kardiochir Torakochirurgia Pol. 2017;14(4):225–229. Fadel E, Yildizeli B, Chapelier AR, Dicenta I, Mussot S, Dartevelle PG. Sleeve lobectomy for bronchogenic cancers: Factors affecting survival. Ann Thorac Surg. 2002;74(3):851–859. Filosso PL, Rena O, Donati G, Casadio C, Ruffini E, Papalia E, et al. Bronchial carcinoid tumors: Surgical management and long-term outcome. J Thorac Cardiovasc Surg. 2002;123(2):303–309. Jiang G, Zhu Y, Zhou Y, Chen C. Preoperative embolization followed by surgical excision of a giant thymic carcinoid. Interact Cardiovasc Thorac Surg. 2013;16(4):541–543. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 04 Jan, 2026 Read the published version in Journal of Cardiothoracic Surgery → Version 1 posted Editorial decision: Revision requested 27 Sep, 2025 Reviews received at journal 21 Aug, 2025 Reviewers agreed at journal 18 Aug, 2025 Reviews received at journal 18 Aug, 2025 Reviewers agreed at journal 17 Aug, 2025 Reviews received at journal 15 Aug, 2025 Reviews received at journal 13 Aug, 2025 Reviewers agreed at journal 12 Aug, 2025 Reviewers agreed at journal 12 Aug, 2025 Reviewers agreed at journal 12 Aug, 2025 Reviewers agreed at journal 12 Aug, 2025 Reviewers invited by journal 12 Aug, 2025 Editor assigned by journal 19 Jun, 2025 Submission checks completed at journal 19 Jun, 2025 First submitted to journal 10 Jun, 2025 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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12:08:13","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-6862855/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-6862855/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s13019-025-03825-9","type":"published","date":"2026-01-04T15:57:52+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":89544246,"identity":"e9b3470c-aa23-4b61-9685-7ed767609595","added_by":"auto","created_at":"2025-08-21 06:58:21","extension":"jpeg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":59253,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003e(A)\u003c/strong\u003e Axial non-contrast CT scan demonstrates a mass obstructing the right middle lobe bronchus (arrows). \u003cstrong\u003e(B)\u003c/strong\u003eFDG PET-CT image reveals no significant radiotracer uptake. \u003cstrong\u003e(C)\u003c/strong\u003e Ga-68 DOTATATE PET-CT scan shows intense radiotracer uptake within the mass(arrow). \u003cstrong\u003e(D)\u003c/strong\u003e Two-year follow-up Ga-68 DOTATATE PET-CT shows no radiotracer uptake, with hyperdense surgical materials on the right side (arrowheads).\u003c/p\u003e","description":"","filename":"floatimage1.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-6862855/v1/211a37b8311196323656de18.jpeg"},{"id":89544247,"identity":"06fa5df3-d5bd-476a-86dd-877d35c73758","added_by":"auto","created_at":"2025-08-21 06:58:21","extension":"jpeg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":104565,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eCT Angiography of the Tumor’s Arterial Supply\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e(A) Coronal CT image demonstrating an arterial branch arising from the right bronchial artery (Arrow) and arterial branch originating from proximal right renal artery (Arrowheads) supplying the tumor (arrow).\u003c/p\u003e\n\u003cp\u003e(B) Sagittal CT image delineating an arterial branch originating from the right internal mammary artery contributing to the tumor’s vascularity (arrowheads).\u003c/p\u003e","description":"","filename":"floatimage2.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-6862855/v1/b7c47493c50d3f8900e79bf0.jpeg"},{"id":89544253,"identity":"a1dbe68d-e638-4324-9e5a-88e8fd734dfb","added_by":"auto","created_at":"2025-08-21 06:58:21","extension":"jpeg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":77729,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003e(A–C)\u003c/strong\u003e Arteriograms depict the tumor supplied by multiple feeding arteries:\u003cstrong\u003e(A)\u003c/strong\u003e Right bronchial artery (arrow). \u003cstrong\u003e(B)\u003c/strong\u003e Aberrant branch arising from the renal artery (arrow). \u003cstrong\u003e(C)\u003c/strong\u003eBranch from the right internal mammary artery (arrow).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e(D–F)\u003c/strong\u003e Post-embolization arteriograms demonstrate successful coil embolization of the feeding arteries: \u003cstrong\u003e(D)\u003c/strong\u003eRight bronchial artery post-embolization (arrowhead). \u003cstrong\u003e(E)\u003c/strong\u003e Renal artery branch post-embolization (arrowhead). \u003cstrong\u003e(F)\u003c/strong\u003e Internal mammary artery branch post-embolization (arrowhead).\u003c/p\u003e","description":"","filename":"floatimage3.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-6862855/v1/e2a70165760ef6615c86a2a1.jpeg"},{"id":99545274,"identity":"d90777e8-526e-4929-84b9-9b80d7ec10fb","added_by":"auto","created_at":"2026-01-05 16:05:02","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1076333,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-6862855/v1/a853b5fa-b640-4c90-bba6-2a7bb3c09019.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Preoperative Embolization of a Pulmonary Carcinoid Tumor with Unusual Arterial Supply: A Case Report","fulltext":[{"header":"Background","content":"\u003cp\u003ePulmonary carcinoid tumors are rare neuroendocrine tumors of the lung, representing only about 1\u0026ndash;2% of primary pulmonary neoplasms (1). They are typically low-grade, slow-growing neoplasms with relatively low metastatic potential. These tumors most often present in middle-aged adults and, unlike other lung cancers, have no strong association with smoking (1). Central bronchial carcinoids can cause airway obstruction leading to cough, wheezing, recurrent pneumonia or atelectasis, and occasionally hemoptysis, and many are discovered incidentally on imaging performed for unrelated reasons (1). A hallmark feature is rich vascularity; bronchial carcinoids appear as reddish endobronchial masses that bleed easily on contact (2). The blood supply is usually derived from the bronchial arteries, but larger or long-standing lesions can recruit additional \u0026ldquo;parasitic\u0026rdquo; supply from other systemic arteries, such as intercostal arteries, the internal mammary artery, or even branches of the abdominal aorta (3). Recognizing such aberrant arterial supply is important, as uncontrolled feeder vessels can result in severe hemorrhage during interventions. Definitive management of localized pulmonary carcinoid is surgical resection, which offers an excellent prognosis for these tumors, given the typical natural history. However, intraoperative bleeding is a major concern due to their hypervascular nature; even bronchoscopic biopsy can provoke significant hemorrhage (2). Therefore, when a carcinoid tumor is suspected, meticulous planning for bleeding control is warranted. Preoperative embolization of feeding arteries is one strategy that has been used to minimize hemorrhage risk in hypervascular thoracic tumors, including large bronchial carcinoids (4). Here, we report a case in which thorough angiographic mapping and coil embolization of an unusual multi-arterial tumor supply, including collaterals from the renal artery, permitted safe surgical resection of a bronchial carcinoid that might otherwise have posed a serious bleeding hazard. To the best of our knowledge, there is no previously documented case of a pulmonary carcinoid tumor receiving arterial supply from the renal artery in addition to the bronchial and internal mammary arteries and undergoing preoperative embolization to reduce the risk of bleeding. This appears to be the first reported instance, and highlights the importance of thorough angiographic evaluation for any hypervascular lung tumor.\u003c/p\u003e"},{"header":"Case Presentation","content":"\u003cp\u003eA 39-year-old female who had never smoked, was referred to pulmonary clinic with a 3-month history of persistent dry cough. She reported no hemoptysis, wheezing, fever, night sweats or weight loss. Physical examination was unremarkable except for diminished breath sounds in the right lung field. Routine laboratory tests were within normal limits.\u003c/p\u003e\n\u003cp\u003eA chest X-ray revealed an ill-defined opacity in the right hilar region. Suspecting an airway lesion or an enlarged lymph node, thoracic CT was performed. The CT scan showed a well-defined round mass with millimetric calcifications, obstructing the right middle lobe bronchus, with complete collapse of the right middle lobe. The interface between the mass and the atelectatic lobe was indistinct, making it difficult to determine the exact tumor margins (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003eA).\u003c/p\u003e\n\u003cp\u003eFor further characterization, a PET-CT scan was performed. Interestingly, the lesion demonstrated no significant uptake of 18F-FDG, which is unusual for most malignant tumors (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003eB). This raised the possibility that the lesion could be a low-grade neoplasm, such as a carcinoid, which may be PET-negative. Therefore, a DOTA-PET scan was obtained to evaluate somatostatin receptor expression. On this DOTA-PET scan, the mass showed intense radiotracer uptake with an SUV-max of 46, increasing the possibility of a neuroendocrine tumor (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003eC). No other areas of abnormal uptake were seen, suggesting that the disease was localized to the lung.\u003c/p\u003e\n\u003cp\u003eThe patient subsequently underwent bronchoscopy for direct visualization and possible biopsy. Bronchoscopy revealed a vascular, reddish endobronchial tumor obliterating the right middle lobe bronchial orifice with evidence of complete middle lobe collapse distal to it. Given its friable appearance, the bronchoscopist judged that a biopsy would carry high risk of uncontrolled bleeding. In the interest of safety, no tissue sample was taken bronchoscopically. Based on the imaging findings and bronchoscopic appearance, the preliminary diagnosis was a typical bronchial carcinoid tumor causing right middle lobe atelectasis.\u003c/p\u003e\n\u003cp\u003eConsistent with guidelines, surgical resection was indicated for this presumed carcinoid after discussion at a multidisciplinary tumor board. In light of the typical hypervascular nature of carcinoid tumors, the surgical team requested a preoperative CT angiographic evaluation and possible embolization to minimize intraoperative bleeding. The patient consented to this plan. Contrary to expectations, CT angiography showed that the tumor was not only supplied by the right bronchial artery and the right internal mammary artery but also by an arterial branch originating from the proximal right renal artery (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003eDigital subtraction angiography (DSA) was performed via a femoral approach. Initial bronchial arteriography showed a markedly hypertrophied right bronchial artery (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eA) feeding the tumor alongside potential non-bronchial collaterals from the right internal mammary artery (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eC) and another branch originating from the proximal right renal artery (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eB). The latter finding was unusual, suggesting an aberrant transdiaphragmatic collateral possibly via an inferior phrenic artery branch originating from the renal artery. No pulmonary arterial blush or arteriovenous shunting was seen on the angiogram.\u003c/p\u003e\n\u003cp\u003eAfter delineating the blood supply, embolization of the feeding arteries proceeded using a coaxial microcatheter technique. The right bronchial artery branch to the tumor was catheterized and occluded using multiple coils until stasis was achieved (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eD).\u003c/p\u003e\n\u003cp\u003eNext, the feeding artery arising from the renal artery was carefully catheterized; multiple coils were deployed, effectively cutting off flow to the tumor (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eE). Finally, the branch from the right internal mammary artery was embolized with coils placed just distal to its origin, resulting in cessation of flow to the tumor (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eF). A completion arteriogram showed no residual arterial perfusion of the tumor. The embolization procedure was tolerated well, with no immediate complications. The patient was observed overnight and had no chest pain, hemoptysis, or evidence of infarction to surrounding organs.\u003c/p\u003e\n\u003cp\u003eApproximately one week later, a right thoracotomy and middle lobectomy was carried out. Notably the operation was performed successfully with minimal bleeding from the tumor bed, attesting to the efficacy of the prior embolization. On gross examination the tumor was well-circumscribed, red-brown, and appeared to be confined to the bronchus with extension into adjacent lung parenchyma causing collapse.\u003c/p\u003e\n\u003cp\u003eHistopathological analysis of the resected specimen confirmed a typical carcinoid tumor. Tumor invasion was limited to the bronchus and immediately surrounding lung; the visceral pleura was intact. All surgical resection margins were clear of tumor with no lymph node involvement.\u003c/p\u003e\n\u003cp\u003eThe patient had an uncomplicated postoperative recovery. She was discharged on postoperative day six with instructions for routine follow-up. At her 2-year follow-up visit, she remained asymptomatic with no evidence of recurrence on clinical exam or on surveillance imaging (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003eD).\u003c/p\u003e"},{"header":"Discussion and Conclusions","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e\n \u003cp\u003eCarcinoid tumors are highly vascular tumors supplied by systemic arteries, and even a small biopsy may lead to profuse bleeding (2). The most salient aspects of this case are the unusual arterial supply and the use of preoperative arterial embolization to mitigate bleeding risk. Bronchial carcinoid tumors can be extremely vascular, and have rarely been reported to recruit blood supply from multiple sources beyond the normal bronchial circulation (3). This case illustrates an extreme example of this phenomenon, since it had systemic feeders from the right internal mammary artery and even a branch arising from the right renal artery. Such aberrant arterial contributions have been described in other hypervascular intrathoracic tumors, although they are uncommon (3,5). If unrecognized, these collateral vessels could cause massive hemorrhage during surgery or even during bronchoscopic interventions.\u003c/p\u003e\n \u003cp\u003eIn the context of management of hemoptysis, it is crucial to search for and embolize non-bronchial systemic collaterals when bronchial artery embolization alone is not sufficient. Studies have shown that up to 45% of patients with severe hemoptysis have significant collateral supply to lung lesions from sources such as intercostal or phrenic arteries (5).\u003c/p\u003e\n \u003cp\u003eHemothorax is a serious complication associated with thoracic surgeries which increase morbidity and potentially necessitate reoperation. Several studies have highlighted the risks of perioperative bleeding and hemothorax, and have recommended preventive measures, such as preoperative embolization which can significantly reduce these risks. Rea et al. reported hemothorax requiring blood transfusions among postoperative complications in patients undergoing surgery for bronchial carcinoid tumors, underscoring the importance of minimizing intraoperative bleeding (6). Machuca et al. identified postoperative complications related to hemothorax, with some cases severe enough to require surgical reintervention (7). Similarly, Kasprzyk et al. observed that hemothorax was a significant postoperative complication in a case series of bronchial carcinoid tumors that often required reoperation, once again stressing the clinical significance of perioperative bleeding (8). Fadel et al., evaluating sleeve lobectomy procedures, also reported hemothorax as a major complication that could lead to substantial patient morbidity (9). Although rare, Filosso et al. reported one case of perioperative mortality associated with the surgical management of a bronchial carcinoid tumor (10). Therefore, embolization techniques may provide an essential intervention to control tumor-related vascularity, reducing the risk of perioperative bleeding and even mortality.\u003c/p\u003e\n \u003cp\u003eThere are some published reports in which preoperative embolization was used successfully for pulmonary carcinoids and other thoracic tumors with a high risk of bleeding. Jiang et al. described a case of a giant thymic carcinoid in which preoperative embolization of internal mammary arteries was performed one day prior to surgery, resulting in minimal intraoperative blood loss and an uncomplicated resection (11). A recent case series by Lucarelli et al. reported the use of preoperative embolization in a variety of giant thoracic tumors, including an atypical lung carcinoid; in all cases, embolization was technically successful and it significantly reduced tumor vascularity to facilitate safer surgery (3). The collective evidence from such reports suggests that if a pulmonary tumor is known to be highly vascular, such as a carcinoid or paraganglioma, then preoperative angiography and embolization should be considered to prevent hemorrhagic complications (3).\u003c/p\u003e\n \u003cp\u003eIt should be noted that preoperative embolization carries its own risks and should be undertaken by experienced operators. In the case series by Lucarelli et al., careful techniques were employed to avoid embolizing an artery that might supply the spinal cord (the artery of Adamkiewicz) (3). In the presented case, we took care to embolize the internal mammary branch distal to its origin to preserve the parent vessel and to super-selectively embolize the feeder from the renal artery to avoid any non-target embolization. Thus, a detailed understanding of thoracic vascular anatomy and meticulous angiographic technique are essential when using this strategy. In situations where a feeder artery also supplies normal tissue that cannot be compromised, one might choose to either embolize only distal branches or manage that vessel intraoperatively via surgical ligation under direct vision.\u003c/p\u003e\n \u003cp\u003eIn conclusion, hypervascular lung tumors, such as carcinoid tumors, may have unusual arterial supplies. Clinicians and surgeons should be vigilant for multiple systemic feeders to mitigate the risk of catastrophic bleeding, severe morbidity and potentially mortality.\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Abbreviations","content":"\u003cdiv class=\"DefinitionList\"\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eCT\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eComputed tomography\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eFDG\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eFluorodeoxyglucose\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003ePET\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003ePositron emission tomography\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eSUV\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eStandardized uptake value\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eDOTA-PET\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eGallium-68 DOTA-peptide positron emission tomography (somatostatin receptor PET scan)\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eDSA\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eDigital subtraction angiography\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eNET\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eNeuroendocrine tumor\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv class=\"DefinitionListEntry\"\u003e\u003cdiv class=\"Term\"\u003e● \u003cb\u003eIMA\u003c/b\u003e\u003c/div\u003e\u003cdiv class=\"Description\"\u003e\u003cp\u003eInternal mammary artery (also known as internal thoracic artery)\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate:\u003c/strong\u003e Not applicable. Institutional review board approval was not required for a single-patient case report. The patient provided informed consent to all treatments and to the use of her clinical information in this report.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication:\u003c/strong\u003e Written informed consent was obtained from the patient for publication of this case report and accompanying images.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials:\u003c/strong\u003e All relevant data are presented in the case report. Additional clinical details can be made available from the corresponding author upon reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests:\u003c/strong\u003e The authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding:\u003c/strong\u003e No external funding was received for this study. All medical care and investigations were part of routine patient management.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors’ contributions:\u0026nbsp;\u003c/strong\u003eAE, ST, HFS and SAB managed the patient’s workup and follow-up. IC carried out the arterial embolization and contributed details of the angiographic findings. IC, AY, EC, AS and BYB conducted the literature review and drafted the manuscript. All authors contributed to editing the report, and all approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements:\u003c/strong\u003e The authors thank the multidisciplinary team at our institution for their roles in managing this patient. We also extend our gratitude to the patient for allowing us to share her case for the benefit of medical education.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eLimaiem F, Tariq MA, Ismail U, Wallen JM. \u003cb\u003eLung Carcinoid Tumors.\u003c/b\u003e StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023.\u003c/li\u003e\n\u003cli\u003eMancini MC. \u003cb\u003eCarcinoid Lung Tumors.\u003c/b\u003e Medscape Reference [Internet]. Updated May 13, 2024. Available from: https://emedicine.medscape.com/article/280104-overview.\u003c/li\u003e\n\u003cli\u003eLucarelli NM, Maggialetti N, Marulli G. \u003cb\u003ePreoperative Embolization in the Management of Giant Thoracic Tumors: A Case Series.\u003c/b\u003e J Pers Med. 2024;14(10):1019.\u003c/li\u003e\n\u003cli\u003eUtpat K, Basu S, Joshi JM. \u003cb\u003eDual Tracer PET Imaging (⁶⁸Ga-DOTATATE and ¹⁸F-FDG) Features in Pulmonary Carcinoid: Correlation with Tumor Proliferation Index.\u003c/b\u003e Indian J Nucl Med. 2017;32(1):39–41.\u003c/li\u003e\n\u003cli\u003eKeller FS, Rosch J, Loflin TG, Nath PH, McElvein RB. \u003cb\u003eNonbronchial systemic collateral arteries: significance in percutaneous embolotherapy for hemoptysis.\u003c/b\u003e Radiology. 1987;164(3):687–692.\u003c/li\u003e\n\u003cli\u003eRea F, Rizzardi G, Zuin A, Marulli G, Nicotra S, Bulf R, Schiavon M, Sartori F. \u003cb\u003eOutcome and surgical strategy in bronchial carcinoid tumors: single institution experience with 252 patients.\u003c/b\u003e Eur J Cardiothorac Surg. 2007;31(2):186–191.\u003c/li\u003e\n\u003cli\u003eMachuca TN, Cardoso PFG, Camargo SM, et al. \u003cb\u003eSurgical treatment of bronchial carcinoid tumors: A single-center experience.\u003c/b\u003e Lung Cancer. 2010;70(2):158–162\u003c/li\u003e\n\u003cli\u003eKasprzyk M, Musiałkiewicz J, Kolasiński M, Jagiełka K, Dyszkiewicz W. \u003cb\u003ePulmonary carcinoids – analysis of early and long-term surgical treatment outcomes in a group of 90 patients.\u003c/b\u003e Kardiochir Torakochirurgia Pol. 2017;14(4):225–229.\u003c/li\u003e\n\u003cli\u003eFadel E, Yildizeli B, Chapelier AR, Dicenta I, Mussot S, Dartevelle PG. \u003cb\u003eSleeve lobectomy for bronchogenic cancers: Factors affecting survival.\u003c/b\u003e Ann Thorac Surg. 2002;74(3):851–859.\u003c/li\u003e\n\u003cli\u003eFilosso PL, Rena O, Donati G, Casadio C, Ruffini E, Papalia E, et al. \u003cb\u003eBronchial carcinoid tumors: Surgical management and long-term outcome.\u003c/b\u003e J Thorac Cardiovasc Surg. 2002;123(2):303–309.\u003c/li\u003e\n\u003cli\u003eJiang G, Zhu Y, Zhou Y, Chen C. \u003cb\u003ePreoperative embolization followed by surgical excision of a giant thymic carcinoid.\u003c/b\u003e Interact Cardiovasc Thorac Surg. 2013;16(4):541–543.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"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":"Pulmonary carcinoid, Hypervascular lung tumor, Bronchial artery embolization, Lobectomy, Aberrant arterial supply","lastPublishedDoi":"10.21203/rs.3.rs-6862855/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-6862855/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e\u003cp\u003ePulmonary carcinoid tumors are rare neuroendocrine neoplasms that carry a risk of bleeding. We report a case of a tumor with unusual arterial supply from multiple sources including collateral from the renal artery, successfully managed with preoperative embolization followed by surgical resection.\u003c/p\u003e\u003ch2\u003eCase presentation:\u003c/h2\u003e\u003cp\u003eA 39-year-old woman with no significant medical history presented with chronic cough. Chest radiography revealed an opacity in the right hilar region. Computed tomography (CT) showed a mass obstructing the right middle lobe bronchus. 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) demonstrated no abnormal uptake in the lesion. However, a Ga-68 DOTATATE somatostatin receptor scan (DOTA-PET) showed intense tracer uptake in the mass. Bronchoscopy identified a reddish endobronchial lesion completely occluding the middle lobe bronchus and causing distal collapse. Biopsy was deferred due to the lesion\u0026rsquo;s hypervascular appearance. With a presumptive diagnosis of carcinoid tumor, a multidisciplinary team planned for surgical resection. To mitigate intraoperative bleeding, preoperative angiographic evaluation was performed. Digital subtraction angiography (DSA) revealed that the blood supply originated from the right bronchial artery, right internal mammary artery and right renal artery. All identified feeding arteries were selectively catheterized and embolized with coils. The patient underwent a right middle lobectomy. Intraoperative blood loss was minimal, and the tumor was resected completely. Pathology confirmed carcinoid tumor. At two-year follow-up, the patient remains asymptomatic.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e\u003cp\u003eThis case highlights a rare arterial supply to a lung tumor and demonstrates that preoperative embolization of multiple feeding vessels can facilitate safe resection of a hypervascular tumor. Awareness of vascular anomalies and multidisciplinary approach were key to successful management.\u003c/p\u003e","manuscriptTitle":"Preoperative Embolization of a Pulmonary Carcinoid Tumor with Unusual Arterial Supply: A Case Report","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-08-21 06:58:16","doi":"10.21203/rs.3.rs-6862855/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2025-09-28T03:59:41+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-21T16:58:23+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"144310985432113139923744086528881253343","date":"2025-08-18T23:46:28+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-18T12:30:27+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"80729863070793430246324682544666440149","date":"2025-08-17T21:38:17+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-15T17:41:11+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-08-13T21:55:33+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"303698016885364565789448861863381030401","date":"2025-08-12T16:56:17+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"204859944878764462429974059323259303927","date":"2025-08-12T15:55:15+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"207932145867995252269218010815579556204","date":"2025-08-12T12:57:55+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"95216115099476747491633016999315171510","date":"2025-08-12T11:08:14+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-08-12T11:03:45+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-06-19T12:48:16+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-06-19T12:45:05+00:00","index":"","fulltext":""},{"type":"submitted","content":"Journal of Cardiothoracic Surgery","date":"2025-06-10T11:53:52+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":"18bdb044-04f7-4377-b1a4-f5bea267cddc","owner":[],"postedDate":"August 21st, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2026-01-05T16:00:33+00:00","versionOfRecord":{"articleIdentity":"rs-6862855","link":"https://doi.org/10.1186/s13019-025-03825-9","journal":{"identity":"journal-of-cardiothoracic-surgery","isVorOnly":false,"title":"Journal of Cardiothoracic Surgery"},"publishedOn":"2026-01-04 15:57:52","publishedOnDateReadable":"January 4th, 2026"},"versionCreatedAt":"2025-08-21 06:58:16","video":"","vorDoi":"10.1186/s13019-025-03825-9","vorDoiUrl":"https://doi.org/10.1186/s13019-025-03825-9","workflowStages":[]},"version":"v1","identity":"rs-6862855","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-6862855","identity":"rs-6862855","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}

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