학술논문

Effect of the COVID-19 pandemic on surgery for indeterminate thyroid nodules (THYCOVID): a retrospective, international, multicentre, cross-sectional study.
Document Type
Academic Journal
Author
Medas F; Department of Surgical Sciences, University of Cagliari, Cagliari, Italy. Electronic address: fabiomedas@unica.it.; Dobrinja C; Department of Medical and Surgical Sciences, University of Trieste, Cattinara Teaching Hospital, Trieste, Italy.; Al-Suhaimi EA; Biology Department, College of Science, Institute for Research and Medical Consultations, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia.; Altmeier J; Endocrine Surgery, Diakonie-Klinikum Stuttgart, Stuttgart, Germany.; Anajar S; Department of Otolaryngology-Head and Neck Surgery, Cheikh Khalifa International University Hospital, Mohammed VI University of Health Sciences, Casablanca, Morocco.; Arikan AE; Department of General Surgery, Acibadem Mehmet Ali Aydinlar University, School of Medicine, Istanbul, Türkiye.; Azaryan I; Division of Endocrinology, Diabetes and Metabolism, Department of Internal Medicine, The Ohio State University Wexner Medical Center, Columbus, OH, USA.; Bains L; Department of Surgery, Maulana Azad Medical College, New Delhi, India.; Basili G; Azienda USL Toscana Nord-Ovest, UOSD Chirurgia della Tiroide, Toscana, Italy.; Bolukbasi H; General Surgery, University of Health Sciences, Kanuni Sultan Suleyman Training and Research Hospital, Istanbul, Türkiye.; Bononi M; Dipartimento di Chirurgia Pietro Valdoni, Policlinico Umberto I Sapienza, Rome, Italy.; Borumandi F; Department of Oral and Maxillofacial Surgery, University Hospitals Sussex NHS Foundation Trust, St Richard's Hospital, Chichester and Worthing Hospital, Worthing, UK.; Bozan MB; General Surgery, Kahramanmaras Sutcu Imam University, Faculty of Medicine, Kahramanmaras, Türkiye.; Brenta G; Endocrinology Department, Unidad Asistencial Dr César Milstein, Buenos Aires, Argentina.; Brunaud L; Department of Surgery CVMC, CHU Nancy-Brabois, Université de Lorraine, Nancy, France.; Brunner M; Department of General and Visceral Surgery, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.; Buemi A; Department of Surgery, Cliniques Universitaires Saint Luc, Bruxelles, Belgium.; Canu GL; Department of Surgical Sciences, University of Cagliari, Cagliari, Italy.; Cappellacci F; Department of Surgical Sciences, University of Cagliari, Cagliari, Italy.; Cartwright SB; Department of Surgery, University of Nebraska Medical Center, Omaha, NE, USA.; Castells Fusté I; Endocrinology Department, Granollers General Hospital, Barcelona, Spain.; Cavalheiro B; Departamento de Cirurgia de Cabeça e Pescoço, Hospital São Camilo Oncologia-Instituto Brasileiro de Controle do Câncer, São Paulo, Brazil.; Cavallaro G; Department of Surgery, Sapienza University of Rome, Rome, Italy.; Chala A; Head and Neck Department Oncologos del Occidente, Universidad de Caldas, Manizales, Colombia.; Chan SYB; Department of Surgery, Tseung Kwan O Hospital, Hong Kong Special Administrative Region, China.; Chaplin J; Department of Otolaryngology Head and Neck Surgery, Auckland City Hospital, Auckland, New Zealand.; Cheema MS; CMH Lahore Medical College and Institute of Dentistry, Lahore, Pakistan.; Chiapponi C; Department of General, Visceral, Cancer and Transplant Surgery, University Hospital Cologne, Cologne, Germany; Department of Endocrine Surgery, Evangelisches Klinikum Cologne Weyertal, Cologne, Germany.; Chiofalo MG; Head and Neck Cancer Medical Oncology Department, Istituto Nazionale Tumori, IRCCS Fondazione G Pascale, Napoli, Italy.; Chrysos E; Department of Surgery, University Hospital of Heraklion, Medical School, University of Crete, Crete, Greece.; D'Amore A; Division of Endocrine Surgery, Department of Gastroenterologic, Endocrine-Metabolic and Nephro-Urologic Sciences, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, Rome, Italy.; de Cillia M; Department of Surgery, Saint John of God Hospital, Salzburg, Austria.; De Crea C; UOC Chirurgia Endocrina e Metabolica, Fondazione Policlinico Universitario A Gemelli IRCCS, Rome, Italy.; de Manzini N; Department of Medical and Surgical Sciences, University of Trieste, Cattinara Teaching Hospital, Trieste, Italy.; de Matos LL; Department of Head and Neck Surgery, Hospital das Clínicas, University of São Paulo, São Paulo, Brazil.; De Pasquale L; Thyroid and Parathyroid Surgery Unit-Otolaryngology Unit, ASST Santi Paolo e Carlo, Department of Health Sciences, Università degli Studi di Milano, Milan, Italy.; Del Rio P; General Surgery Unit, Department of Medicine and Surgery, Parma University Hospital, Parma, Italy.; Demarchi MS; Department of Thoracic and Endocrine Surgery, Geneva University Hospitals and University of Geneva, Geneva, Switzerland.; Dhiwakar M; Department of Otolaryngology-Head and Neck Surgery, Kovai Medical Center and Hospital, Coimbatore, India.; Donatini G; General and Endocrine Surgery, CHU Poitiers, Poitiers, France.; Dora JM; Thyroid Unit, Hospital de Clínicas de Porto Alegre and Federal University of Rio Grande do Sul, Porto Alegre, Brazil.; D'Orazi V; Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy; Division of General Surgery-Section of Endocrine and Diabetic Foot Surgery, 'Fabia Mater' Hospital, Rome, Italy.; Doulatram Gamgaram VK; Endocrinology and Nutrition, Hospital Regional Universitario, Málaga, Spain.; Eismontas V; Department of Surgery, Klaipeda University Hospital, Klaipeda, Lithuania; Health Research and Innovation Science Center, Faculty of Health Sciences, Klaipeda University, Klaipeda, Lithuania.; Kabiri EH; Department of Thoracic Surgery, Mohammed V Military Teaching Hospital, Rabat, Morocco.; El Malki HO; Surgery Department 'A', Ibn Sina Hospital, Medical School, Mohammed V University, Rabat, Morocco.; Elzahaby I; Surgical Oncology, Mansoura University, Mansoura, Egypt.; Enciu O; Elias University Emergency Hospital, Carol Davila University of Medicine and Pharmacy, Bucharest, Romania.; Eskander A; Department of Otolaryngology-Head and Neck Surgery, University of Toronto, Toronto, ON, Canada.; Feroci F; Department of Surgery, General Surgery Unit, S Stefano Hospital, Prato, Italy.; Figueroa-Bohorquez D; Head and Neck Surgery, Hospital Universitario Nacional de Colombia, Bogotá DC, Colombia.; Filis D; Department of Surgery, Saint Andrew Hospital of Patras, Patras, Greece.; François G; Otolaryngology and Head and Neck Surgery, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland.; Frías-Fernández P; Surgical Oncology, Tula's General Hospital, Tula de Allende, Mexico.; Gamboa-Dominguez A; Departamento de Patología, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.; Genc V; Department of Surgery, Ankara University Faculty of Medicine, Ankara, Turkey.; Giordano D; Otorhinolaryngology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.; Gómez-Pedraza A; National Cancer Institute of Mexico, Mexico City, Mexico.; Graceffa G; Department of Surgical, Oncological and Oral Sciences, University of Palermo, Palermo, Italy.; Griffin J; Otolaryngology, Midlands Regional Hospital Tullamore, Tullamore, Ireland.; Guerreiro SC; Endocrine Surgery, University Hospital Center of Central Lisbon, Hospital Curry Cabral, Lisboa, Portugal.; Gupta K; Department of Head and Neck Surgery, Medanta, Gurugram, India.; Gupta KK; Department of ENT, University Hospitals Birmingham NHS Trust, Birmingham, UK.; Gurrado A; Department of Precision and Regenerative Medicine and Ionian Area, University of Bari 'Aldo Moro', Bari, Italy.; Hajiioannou J; ENT Department, University Hospital of Larissa, Larissa, Greece.; Hakala T; Department of Surgery, Tampere University Hospital, Tampere, Finland.; Harahap WA; Department of Surgery, Faculty of Medicine, Universitas Andalas, Padang City, Indonesia.; Hargitai L; Department of General Surgery, Division of Visceral Surgery, Medical University Vienna, Vienna, Austria.; Hartl D; Department of Surgery, Anesthesia and Interventional Radiology, Head and Neck Oncology Service, Thyroid Surgery Unit, Gustave Roussy, Villejuif, France.; Hellmann A; Department of General, Endocrine and Transplant Surgery, Medical University of Gdańsk, Gdańsk, Poland.; Hlozek J; Department of Otorhinolaryngology and Maxillofacial Surgery, Military University Hospital, Prague, Czech Republic; Third Faculty of Medicine, Charles University, Prague, Czech Republic.; Hoang VT; Department of Radiology, Thien Hanh Hospital, Buon Ma Thuot, Vietnam.; Iacobone M; Endocrine Surgery Unit, Department of Surgery, Oncology and Gastroenterology, University of Padova, Padova, Italy.; Innaro N; Unit of Endocrine Surgery, AOU Mater Domini, Catanzaro, Italy.; Ioannidis O; Fourth Department of Surgery, Medical School, Aristotle University of Thessaloniki, General Hospital 'Georgios Papanikolaou', Thessaloniki, Greece.; Jang JHI; Department of Otorhinolaryngology-Head and Neck Surgery, Singapore General Hospital, Singapore.; Xavier-Junior JC; Surgical Pathology Department, Instituto de Patologia de Araçatuba, Araçatuba, Brazil.; Jovanovic M; Clinic for Endocrine Surgery, University Clinical Center of Serbia, Belgrade, Serbia; School of Medicine, Belgrade, Serbia.; Kaderli RM; Department of Visceral Surgery and Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.; Kakamad F; Department of Scientific Affairs, Smart Health Tower, Sulaimani, Iraq.; Kaliszewski K; Department of General, Minimally Invasive and Endocrine Surgery, Wroclaw Medical University, Wroclaw, Poland.; Karamanliev M; Department of Surgical Oncology, University Hospital 'Georgi Stranski', Faculty of Medicine, Medical University of Pleven, Pleven, Bulgaria.; Katoh H; Department of Breast and Endocrine Surgery, Kitasato University Hospital, Sagamihara, Japan.; Košec A; Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Center Sestre Milosrdnice, Zagreb, Croatia.; Kovacevic B; Institute of Pathology and Forensic Medicine, Medical Military Academy, Belgrade, Serbia.; Kowalski LP; Department of Head and Neck Surgry and Otorhinolaryngology, AC Camargo Cancer Center, São Paulo, Brazil.; Králik R; Department of Surgical Oncology, St Elisabeth Cancer Institute, Medical Faculty of Comenius University, Bratislava, Slovakia.; Yadav SK; Department of Surgery, NSCB Medical College, Jabalpur, India.; Kumorová A; Clinic of Otorhinolaryngology and Head and Neck Surgery, Central Military Hospital Ružomberok, Ružomberok, Slovakia.; Lampridis S; Department of Thoracic Surgery, 424 General Military Hospital, Thessaloniki, Greece.; Lasithiotakis K; Department of Surgery, University Hospital of Heraklion, Medical School, University of Crete, Crete, Greece.; Leclere JC; Head and Neck Surgery, Brest University Hospital, Brest, France.; Leong EKF; Department of Surgery, National University Hospital, Singapore.; Leow MK; Department of Endocrinology, Tan Tock Seng Hospital, Singapore.; Lim JY; Department of Surgery and Otolaryngology, Oregon Health and Science University, Portland, OR, USA.; Lino-Silva LS; Oncology Center, Medica Sur Hospital, Mexico City, Mexico.; Liu SYW; Department of Surgery, Chinese University of Hong Kong, Hong Kong Special Administrative Region, China.; Llorach NP; Unit of Endocrine Surgery Head and Neck Parc Tauli, Hospital Universitari, Sabadell, Spain.; Lombardi CP; Division of Endocrine Surgery, Department of Gastroenterologic, Endocrine-Metabolic and Nephro-Urologic Sciences, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, Rome, Italy.; López-Gómez J; Head and Neck Department, Hospital de Oncología Centro Médico Nacional Siglo XXI, Mexico City, Mexico.; Lori E; Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.; Quintanilla-Dieck L; Department of Pediatric Otolaryngology, Head and Neck Surgery, Oregon Health and Science University, Portland, OR, USA.; Lucchini R; Endocrine Surgery Unit, University of Perugia, Santa Maria Hospital, Terni, Italy.; Madani A; Department of Surgery, University of Toronto, Toronto, ON, Canada.; Manatakis D; Second Department of Surgery, Athens Naval and Veterans Hospital, Athens, Greece.; Markovic I; Clinic for Surgical Oncology, Institute of Oncology and Radiology of Serbia, Belgrade, Serbia.; Materazzi G; Endocrine Surgery Unit, University Hospital of Pisa, Pisa, Italy.; Mazeh H; Department of Surgery, Hadassah Medical Center, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.; Mercante G; Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy; Department of Otorhinolaryngology-Head and Neck Surgery, IRCCS Humanitas Research Hospital, Rozzano, Italy.; Meyer-Rochow GY; Endocrine Surgery, Department of General Surgery, Waikato Hospital, Hamilton, New Zealand.; Mihaljevic O; Department of Pathophysiology, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia.; Miller JA; The Royal Melbourne Hospital and Epworth Hospital, Melbourne, VIC, Australia.; Minuto M; Department of Surgical Sciences and Integrated Diagnostics, University of Genoa, Genova, Italy.; Monacelli M; Thoracic Surgery, Azienda Ospedaliera di Perugia, Perugia, Italy.; Mulita F; Department of Surgery, General University Hospital of Patras, Patras, Greece.; Mullineris B; Department of General, Emergency and New Technologies, University Hospital of Modena, Baggiovara Civil Hospital, Modena, Italy.; Muñoz-de-Nova JL; Department of General and Digestive Surgery, Hospital Universitario de La Princesa, Madrid, Spain.; Muradás Girardi F; Head and Neck Surgery Department, Hospital Ana Nery, Santa Cruz do Sul, Brazil.; Nader S; Otolaryngology Department, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.; Napadon T; Department of Otolaryngology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.; Nastos C; Third Department of Surgery, Attikon University Hospital, Athens, Greece.; Offi C; Department of Endocrine and Ultrasound-Guided Surgery, Ospedale del Mare, ASl Napoli 1 Centro, Naples, Italy.; Ronen O; Galilee Medical Center, Azrieli Faculty of Medicine Bar Ilan University, Safed, Israel.; Oragano L; ASL VCO, Ospedale San Biagio, Domodossola, Italy.; Orois A; Department of Endocrinology and Nutrition, Hospital Universitari Mútua Terrassa, Terrassa, Spain.; Pan Y; Department of Thyroid Surgery, The First Affiliated Hospital of Jinan University, Guangzhou, China.; Panagiotidis E; Department of Nuclear Medicine/PET CT, Theageneio Cancer Hospital of Thessaloniki, Thessaloniki, Greece.; Panchangam RB; Endocrine and Metabolic Surgery, Bhargav Endocrine Hospital, Vijayawada, India.; Papavramidis T; First Propedeutic Department of Surgery, Aristotle University of Thessaloniki, AHEPA University Hospital, Thessaloniki, Greece.; Parida PK; Department of ENT-Head and Neck Surgery, All India Institute of Medical Sciences, Bhubaneswar, India.; Paspala A; Department of Surgery, Eugenideio Hospital, Athens, Greece.; Pérez ÒV; General Surgery Department, Universitat de Barcelona, Hospital Clínic de Barcelona, Barcelona, Spain.; Petrovic S; Surgery Bitenc, Ljubljana, Slovenia.; Raffaelli M; UOC Chirurgia Endocrina e Metabolica, Fondazione Policlinico Universitario A Gemelli IRCCS, Rome, Italy.; Ramacciotti CF; Service of Endocrinology, Hospital Privado Universitario de Córdoba, Córdoba, Argentina.; Ratia Gimenez T; General Surgery, Hospital Universitario Principe de Asturias, Alcala de Henares, Spain.; Rivo Vázquez Á; Department of General and Digestive Surgery, Division of Endocrine Surgery, Complexo Hospitalario Universitario de Vigo, Vigo, Spain.; Roh JL; Department of Otorhinolaryngology-Head and Neck Surgery, CHA Bundang Medical Center, CHA University, Seongnam, South Korea.; Rossi L; Endocrine Surgery Unit, University Hospital of Pisa, Pisa, Italy.; Sanabria A; Department of Surgery, Universidad de Antioquia, CEXCA Centro de Excelencia en Enfermedades de Cabeza y Cuello, Medellín, Colombia.; Santeerapharp A; Department of Otolaryngology-Head and Neck Surgery, Faculty of Medicine, Srinakharinwirot University, Bangkok, Thailand.; Semenov A; Endocrine Surgery Department, Saint Petersburg State University Hospital, Saint Petersburg, Russia.; Seneviratne S; Faculty of Medicine, University of Colombo, Colombo, Sri Lanka.; Serdar A; Department of Endocrin Pathology Unit, University of Health Sciences, Faculty of Medicine, Bakırköy Dr Sadi Konuk Training and Research Hospital, Istanbul, Turkey.; Sheahan P; South Infirmary Victoria University Hospital, Cork, Ireland.; Sheppard SC; Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital of Nîmes, Nîmes, France.; Slotcavage RL; Department of Surgery and Department of Internal Medicine, University of Arkansas for Medical Sciences, Little Rock, AR, USA.; Smaxwil C; Endocrine Surgery, Diakonie-Klinikum Stuttgart, Stuttgart, Germany.; Kim SY; Department of Surgery, Ajou University School of Medicine, Suwon, South Korea.; Sorrenti S; Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy.; Spartalis E; Department of Thyroid Surgery, REA Hospital, Athens, Greece.; Sriphrapradang C; Department of Medicine, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.; Testini M; Department of Precision and Regenerative Medicine and Ionian Area, University of Bari 'Aldo Moro', Bari, Italy.; Turk Y; Division of Endocrine Surgery, General Surgery Department, Ege University Hospital, Izmir, Turkey.; Tzikos G; First Propedeutic Department of Surgery, Aristotle University of Thessaloniki, AHEPA University Hospital, Thessaloniki, Greece.; Vabalayte K; Endocrine Surgery Department, Saint Petersburg State University Hospital, Saint Petersburg, Russia.; Vargas-Osorio K; Clinical University Hospital Santiago de Compostela University of Santiago de Compostela, Santiago de Compostela, Spain.; Vázquez Rentería RS; Departamento de Cabeza y Cuello, Instituto Nacional de Cancerología, Mexico City, Mexico.; Velázquez-Fernández D; Endocrine Surgery Unit, Department of Surgery, National Institute for Medical Sciences and Nutrition, Mexico City, Mexico.; Vithana SMP; Department of Surgery, National Hospital Kandy, Kandy, Sri Lanka.; Yücel L; Department of Otorhinolaryngology, University of Health Sciences, Gülhane Research and Training Hospital, Ankara, Turkey.; Yulian ED; Division of Surgical Oncology, Department of Surgery, Dr Cipto Mangunkusumo General Hospital, Jakarta, Indonesia.; Zahradnikova P; Department of Paediatric Surgery, Medical Faculty of Comenius University, National Institute of Children's Diseases, Bratislava, Slovakia.; Zarogoulidis P; Third Surgery Department, Aristotle University of Thessaloniki, Thessaloniki, Greece.; Ziablitskaia E; Central Research Laboratory, Clinical Medical Multidisciplinary Center of St Luke VI Vernadsky Crimean Federal University, Simferopol, Russia.; Zolotoukho A; Endocrine Surgery Department, Saint Petersburg State University Hospital, Saint Petersburg, Russia.; Calò PG; Department of Surgical Sciences, University of Cagliari, Cagliari, Italy.
Source
Publisher: The Lancet, Diabetes & Endocrinology Country of Publication: England NLM ID: 101618821 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2213-8595 (Electronic) Linking ISSN: 22138587 NLM ISO Abbreviation: Lancet Diabetes Endocrinol Subsets: MEDLINE
Subject
Language
English
Abstract
Background: Since its outbreak in early 2020, the COVID-19 pandemic has diverted resources from non-urgent and elective procedures, leading to diagnosis and treatment delays, with an increased number of neoplasms at advanced stages worldwide. The aims of this study were to quantify the reduction in surgical activity for indeterminate thyroid nodules during the COVID-19 pandemic; and to evaluate whether delays in surgery led to an increased occurrence of aggressive tumours.
Methods: In this retrospective, international, cross-sectional study, centres were invited to participate in June 22, 2022; each centre joining the study was asked to provide data from medical records on all surgical thyroidectomies consecutively performed from Jan 1, 2019, to Dec 31, 2021. Patients with indeterminate thyroid nodules were divided into three groups according to when they underwent surgery: from Jan 1, 2019, to Feb 29, 2020 (global prepandemic phase), from March 1, 2020, to May 31, 2021 (pandemic escalation phase), and from June 1 to Dec 31, 2021 (pandemic decrease phase). The main outcomes were, for each phase, the number of surgeries for indeterminate thyroid nodules, and in patients with a postoperative diagnosis of thyroid cancers, the occurrence of tumours larger than 10 mm, extrathyroidal extension, lymph node metastases, vascular invasion, distant metastases, and tumours at high risk of structural disease recurrence. Univariate analysis was used to compare the probability of aggressive thyroid features between the first and third study phases. The study was registered on ClinicalTrials.gov, NCT05178186.
Findings: Data from 157 centres (n=49 countries) on 87 467 patients who underwent surgery for benign and malignant thyroid disease were collected, of whom 22 974 patients (18 052 [78·6%] female patients and 4922 [21·4%] male patients) received surgery for indeterminate thyroid nodules. We observed a significant reduction in surgery for indeterminate thyroid nodules during the pandemic escalation phase (median monthly surgeries per centre, 1·4 [IQR 0·6-3·4]) compared with the prepandemic phase (2·0 [0·9-3·7]; p<0·0001) and pandemic decrease phase (2·3 [1·0-5·0]; p<0·0001). Compared with the prepandemic phase, in the pandemic decrease phase we observed an increased occurrence of thyroid tumours larger than 10 mm (2554 [69·0%] of 3704 vs 1515 [71·5%] of 2119; OR 1·1 [95% CI 1·0-1·3]; p=0·042), lymph node metastases (343 [9·3%] vs 264 [12·5%]; OR 1·4 [1·2-1·7]; p=0·0001), and tumours at high risk of structural disease recurrence (203 [5·7%] of 3584 vs 155 [7·7%] of 2006; OR 1·4 [1·1-1·7]; p=0·0039).
Interpretation: Our study suggests that the reduction in surgical activity for indeterminate thyroid nodules during the COVID-19 pandemic period could have led to an increased occurrence of aggressive thyroid tumours. However, other compelling hypotheses, including increased selection of patients with aggressive malignancies during this period, should be considered. We suggest that surgery for indeterminate thyroid nodules should no longer be postponed even in future instances of pandemic escalation.
Funding: None.
Competing Interests: Declaration of interests We declare no competing interests.
(Copyright © 2023 Elsevier Ltd. All rights reserved.)