Severe Acute Respiratory Syndrome Coronavirus 2 Infection and Thrombosis: Phlegmasia Cerulea Dolens Presenting with Venous Gangrene in a Child
2020; Elsevier BV; Volume: 226; Linguagem: Inglês
10.1016/j.jpeds.2020.07.032
ISSN1097-6833
AutoresGautam Visveswaran, Kavita Morparia, Shalu Narang, Cindy Sturt, Michael DiVita, Brett Voigt, Amer Hawatmeh, Derrick McQueen, Marc Cohen,
Tópico(s)Thermal Regulation in Medicine
ResumoA 12-year-old girl with severe acute respiratory syndrome coronavirus 2 infection presented as phlegmasia cerulea dolens with venous gangrene. Emergent mechanical thrombectomy was complicated by a massive pulmonary embolism and cardiac arrest, for which extracorporeal cardiopulmonary resuscitation and therapeutic hypothermia were used. Staged ultrasound-assisted catheter-directed thrombolysis was used for treatment of bilateral pulmonary emboli and the extensive lower extremity deep vein thrombosis while the patient received extracorporeal membrane oxygenation support. We highlight the need for heightened suspicion for occult severe acute respiratory syndrome coronavirus 2 infection among children presenting with unusual thrombotic complications. A 12-year-old girl with severe acute respiratory syndrome coronavirus 2 infection presented as phlegmasia cerulea dolens with venous gangrene. Emergent mechanical thrombectomy was complicated by a massive pulmonary embolism and cardiac arrest, for which extracorporeal cardiopulmonary resuscitation and therapeutic hypothermia were used. Staged ultrasound-assisted catheter-directed thrombolysis was used for treatment of bilateral pulmonary emboli and the extensive lower extremity deep vein thrombosis while the patient received extracorporeal membrane oxygenation support. We highlight the need for heightened suspicion for occult severe acute respiratory syndrome coronavirus 2 infection among children presenting with unusual thrombotic complications. Phlegmasia cerulea dolens (PCD) is characterized by extensive venous thrombosis and severe venous outflow obstruction presents with painful limb swelling, cyanosis, and gangrene in extreme cases. Occurrence of PCD in healthy pediatric patients is rare.1Kuo I. Smith J. Abou-Zamzam A.M. A multimodal therapeutic approach to phlegmasia cerulea dolens in a pediatric patient.J Vasc Surg. 2011; 53: 212-215Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar, 2Spentzouris G. Scriven R.J. Lee T.K. Labropoulos N. Pediatric venous thromboembolism in relation to adults.J Vasc Surg. 2012; 55: 1785-1793Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 3Tran J. Rafique Z. Phlegmasia cerulea dolens in the pediatric population: a life-threatening condition.J Emerg Med. 2015; 49: e111-e114Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar Potential protective mechanisms cited include a decreased capacity for thrombin generation, increased alpha-2 macroglobulin inhibition of thrombin, and the antithrombotic potential of the vessel wall.2Spentzouris G. Scriven R.J. Lee T.K. Labropoulos N. Pediatric venous thromboembolism in relation to adults.J Vasc Surg. 2012; 55: 1785-1793Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar Among adult and pediatric patients, malignancy, sepsis, surgery, hypercoagulable state, and vascular injury (indwelling central lines) predispose to PCD.2Spentzouris G. Scriven R.J. Lee T.K. Labropoulos N. Pediatric venous thromboembolism in relation to adults.J Vasc Surg. 2012; 55: 1785-1793Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 3Tran J. Rafique Z. Phlegmasia cerulea dolens in the pediatric population: a life-threatening condition.J Emerg Med. 2015; 49: e111-e114Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar, 4Ibrahim H. Krouskop R. Jeroudi M. McCulloch C. Parupia H. Dhanireddy R. Venous gangrene of lower extremities and Staphylococcus aureus sepsis.J Perinatol. 2001; 21: 136-140Crossref PubMed Scopus (9) Google Scholar Coronavirus disease associated with the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is associated with a hypercoagulable state among adults, as is the multisystem inflammatory syndrome in children.5Middeldorp S. Coppens M. van Haaps T.F. Foppen M. Vlaar A.P. Müller M.C.A. et al.Incidence of venous thromboembolism in hospitalized patients with COVID-19.J Thromb Haemost. 2020; 18: 1995-2002Crossref PubMed Scopus (1106) Google Scholar, 6Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. Arbous M.S. Gommers D.A.M.P.J. Kant K.M. et al.Incidence of thrombotic complications in critically ill ICU patients with COVID-19.Thromb Res. 2020; 191: 145-147Abstract Full Text Full Text PDF PubMed Scopus (3333) Google Scholar, 7Capone C.A. Subramony A. Sweberg T. Schneider J. Shah S. Rubin L. et al.Characteristics, cardiac involvement, and outcomes of multisystem inflammatory syndrome of childhood associated with severe acute respiratory syndrome coronavirus 2 infection.J Pediatr. 2020; 224: 141-145Abstract Full Text Full Text PDF PubMed Scopus (173) Google Scholar, 8Kaushik S. Aydin S.I. Derespina K.R. Bansal P.B. Kowalsky S. Trachtman R. et al.Multisystem inflammatory syndrome in children associated with severe acute respiratory syndrome coronavirus 2 infection (MIS-C): a multi-institutional study from New York City.J Pediatr. 2020; 224: 24-29Abstract Full Text Full Text PDF PubMed Scopus (301) Google Scholar We report the case of a girl with PCD and venous gangrene in association with SARS-CoV-2 infection. A 12-year-old previously healthy girl (body mass index of 20.1 kg/m2) had acute onset of painful swelling of her left leg without dyspnea or fever. She was evaluated 5 days prior for painful erythema of the left thigh of 5 days' duration, which was diagnosed as cellulitis and treated with oral trimethoprim-sulfamethoxazole. No intercurrent illness, sick contacts, long distance travel, familial thrombophilia, or trauma were reported. Vital signs on admission were blood pressure of 135/76 mm Hg, heart rate of 140 b/minute (sinus tachycardia), respiratory rate of 20 breaths/minute, and temperature of 98.2°F. Examination revealed marked swelling of the entire left leg that was cool to the touch. Her left foot was ecchymotic with decreased sensation and inability to flex toes, but dorsalis pedis and posterior tibial pulses were palpable (Figure 1). Laboratory tests before unfractionated heparin administration showed thrombocytopenia (126 000/μL), prolonged prothrombin time of 18 seconds (normal high, 13.4 seconds), partial thromboplastin time of 88.3 seconds (normal high, 36.6 seconds), elevated d-dimer 1953 ng/mL (high normal, ≤243 ng/mL), and factor VIII activity 259.4% (normal range, 62%-194%). Her erythrocyte sedimentation rate was >130 mm/hour (normal high, 13 mm/hour) and C-reactive protein was 14.8 mg/dL (normal high, 0.5 mg/dL). Because catheter-directed lysis requires hours for revascularization, we proceeded to percutaneous mechanical venous thrombectomy. Venography confirmed extensive popliteal-to-common iliac vein thrombosis and excluded inferior vena cava (IVC) clot (Video 1 and Video 2; available at www.jpeds.com). ClotTriever mechanical thrombectomy (Inari Medical, Irvine, California) retrieved a white and red fibrin-rich clot. Thrombectomy was complicated by hypotension, bradycardia, and pulseless electrical activity, for which cardiopulmonary resuscitation was initiated. Echocardiogram revealed severe right ventricular (RV) dilation with severe hypokinesis consistent with acute massive pulmonary embolism (PE). A multidisciplinary decision was made to initiate peripheral venoarterial extracorporeal membrane oxygenation (ECMO). Unfractionated heparin adjusted to an activated clotting time of 190-200 seconds was continued throughout the ECMO run. Given prolonged resuscitation of about 30-45 minutes, we initiated therapeutic hypothermia via the ECMO circuit. Admission SARS-CoV-2 nasopharyngeal reverse transcriptase-polymerase chain reaction testing was negative. Fibrinogen level drawn post ECMO initiation was 191 mg/dL (normal range, 210-400 mg/dL). Her initial thrombophilia workup was negative for most risk factors but was positive for antiphospholipid antibodies (APLA) (Table).TableThrombophilia investigationThrombophilic risk factorsResultsFactor V LeidenNegativeProthrombin gene mutationNegativeMTHFR gene mutationPositive for 1 copy of C677T variantProtein C67% (67%-141%)Protein S, free28%∗Repeat in 4 weeks was normal at 89%. (55%-124%)Antithrombin III55% (72%-129%)Lupus anticoagulant: DRVVT; lupus anticoagulant ratio79.6 seconds (28-48); 1.5 (0.8-1.2)Cardiolipin antibodyIgA <11, IgG 73 (≤14), IgM 31 (≤12)Beta 2 glycoprotein 1IgA <9, IgG 58 (≤20), IgM <9Lipoprotein (a)67.3 nmol/L (<75)DRVVT, dilute Russell's viper venom time.Normal range, if applicable, in parentheses.∗ Repeat in 4 weeks was normal at 89%. Open table in a new tab DRVVT, dilute Russell's viper venom time. Normal range, if applicable, in parentheses. Day 1 echocardiogram revealed persistent severe RV systolic dysfunction. Continued need for high-dose epinephrine (0.08 μg/kg/min), milrinone (0.5 μg/kg/min) with narrow arterial pulse pressure (20 mm Hg) while on ECMO support (flow, 2.5-2.7 L/hour; 60 mL/kg/min) prompted us to undertake EkoSonic ultrasound-assisted catheter-directed thrombolysis (UCDT) of the PE. Pulmonary angiography confirmed extensive emboli in the superior, middle, and inferior segments of the right lung; the lingular segment of the left lung; and interlobular pulmonary arteries. Bilateral UCDT catheters infusing tissue plasminogen activator (TPA) at 1 mg/lung/hour for 6 hours (12 mg total dose) facilitated thrombolysis.9Tapson V.F. Sterling K. Jones N. Elder M. Tripathy U. Brower J. et al.A randomized trial of the optimum duration of acoustic pulse thrombolysis procedure in acute intermediate-risk pulmonary embolism: the OPTALYSE PE Trial.JACC Cardiovasc Interv. 2018; 11: 1401-1410Crossref PubMed Scopus (292) Google Scholar Epinephrine was discontinued within 24 hours of thrombolysis and a 40 mm Hg arterial pulse pressure was noted with echocardiogram confirming improvement in RV size and function. Given hemodynamic improvement, we undertook venous thrombolysis to improve limb prognosis. An infrahepatic venous filter was deployed after excluding an IVC clot. Venography confirmed extensive thrombosis from the posterior tibial vein to the common iliac vein (Figure 2, A-C; available at www.jpeds.com). Rheolytic thrombectomy (Angiojet [Boston Scientific, Marlborough, Massachusetts] with powerpulse) was undertaken using TPA in solution (20 mg total).10Rao A.S. Konig G. Leers S.A. Cho J. Rhee R.Y. Makaroun M.S. et al.Pharmacomechanical thrombectomy for iliofemoral deep vein thrombosis: an alternative in patients with contraindications to thrombolysis.J Vasc Surg. 2009; 50: 1092-1098Abstract Full Text Full Text PDF PubMed Scopus (88) Google Scholar EkoSonic UCDT catheters were positioned via the common femoral vein traversing beyond the common iliac vein, and a second catheter via the posterior tibial vein extending into the common femoral vein (0.5 mg/hour/catheter for an hourly dose of 1 mg). Mild acute disseminated intravascular coagulation (DIC) mandated TPA discontinuation at 7 hours of UCDT and transfusion support corrected the DIC. Venoarterial ECMO was decannulated after 64 hours of support with primary repair of the arteries. Venography demonstrated improved venous outflow into the IVC with markedly decreased thrombus burden. Paralytics and sedation were weaned on day 4 and she awoke, followed commands, and was successfully extubated to oxygen via nasal cannula. Complete normalization of her RV function was noted on day 7 echocardiogram (Video 3; available at www.jpeds.com). The patient was given solumedrol 1 g (23 mg/kg) daily for 3 doses, followed by a taper. Plasmapheresis was undertaken daily for 5 days, and 3 times afterward for a total of 8 treatments. Empiric antibiotics with vancomycin and cefepime were administered for 5 days. Cyanosis subsequently was isolated to the toes, with improved perfusion to the mid foot. The SARS-CoV-2 IgG and IgM antibody titers drawn on hospital day 5, after 3 plasmapheresis sessions, were negative. Repeat testing using paired sera (hospitalization day 16/day 20) revealed up trending positive SARS-CoV-2 IgM antibody titers 28.8 units (day16) to 43.2 units (day 20) (reference valve, <9.0 units) and negative SARS-CoV-2 IgG titers.11Sethuraman N. Jeremiah S.S. Ryo A. Interpreting Diagnostic Tests for SARS-CoV-2.JAMA. 2020; Crossref PubMed Scopus (1090) Google Scholar She underwent hyperbaric oxygen treatments with improvement in sensorimotor deficits, but with continued severe cyanosis of all toes. She was discharged home on day 20 of hospitalization without neurologic deficits (Pediatric Cerebral Performance Category 1) on amlodipine, a prednisone taper, therapeutic enoxaparin, and gabapentin for continued neuropathic pain. Coronavirus disease 19 (COVID)-19 respiratory syndrome is associated with a hypercoagulable state in adults.5Middeldorp S. Coppens M. van Haaps T.F. Foppen M. Vlaar A.P. Müller M.C.A. et al.Incidence of venous thromboembolism in hospitalized patients with COVID-19.J Thromb Haemost. 2020; 18: 1995-2002Crossref PubMed Scopus (1106) Google Scholar,6Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. Arbous M.S. Gommers D.A.M.P.J. 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Zinkernagel A.S. et al.Endothelial cell infection and endotheliitis in COVID-19.Lancet. 2020; 395: 1417-1418Abstract Full Text Full Text PDF PubMed Scopus (4567) Google Scholar An elevated d-dimer, low normal or normal fibrinogen level, elevated fibrin degradation products, mild thrombocytopenia, and mildly elevated partial thromboplastin time in adults with severe COVID-19 has led some investigators to postulate the occurrence of a compensated DIC syndrome.14Thachil J. Tang N. Gando S. Falanga A. Cattaneo M. Levi M. et al.ISTH interim guidance on recognition and management of coagulopathy in COVID-19.J Thromb Haemost. 2020; 18: 1023-1026Crossref PubMed Scopus (1313) Google Scholar,15Tang N. Li D. Wang X. Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia.J Thromb Haemost. 2020; 18: 844-847Crossref PubMed Scopus (4064) Google Scholar Nonsurvivors met International Society of Thrombosis and Hemostasis criteria for DIC in 71.4% of patients vs 0.6% among COVID-19 survivors in 1 intensive care unit study.15Tang N. Li D. Wang X. Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia.J Thromb Haemost. 2020; 18: 844-847Crossref PubMed Scopus (4064) Google Scholar Admission coagulation tests were markedly abnormal in our patient. She met International Society of Thrombosis and Hemostasis criteria for nonovert DIC; International Society of Thrombosis and Hemostasis DIC score 4: prolonged prothrombin time (1 point) and severely elevated d-dimer (3 points).16Taylor F. Toh C.-H. Hoots K. Wada H. Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation.Thromb Haemost. 2001; 86: 1327-1330Crossref PubMed Scopus (1751) Google Scholar Importantly, her investigation for acute infection was negative. Thrombophilia workup was positive for APLA. Pediatric primary antiphospholipid syndrome (APS) is rare, and disease onset before age 15 years is reported in only 2.8% of all pediatric APS. Although arterial thrombosis is more often associated with primary APS, deep vein thrombosis is predominantly seen with secondary APS.17Kenet G. Aronis S. Berkun Y. Bonduel M. Chan A. Goldenberg N.A. et al.Impact of persistent antiphospholipid antibodies on risk of incident symptomatic thromboembolism in children: a systematic review and meta-analysis.Semin Thromb Hemost. 2011; 37: 802-809Crossref PubMed Scopus (43) Google Scholar Adult COVID-19-associated APLA and lupus anticoagulant have been reported.18Zhang Y. Xiao M. Zhang S. Xia P. 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Ciofi Degli Atti M. et al.A clinical, histopathological and laboratory study of 19 consecutive Italian paediatric patients with chilblain-like lesions: lights and shadows on the relationship with COVID-19 infection.J Eur Acad Dermatology Venereol. 2020; ([Epub ahead of print])Crossref Scopus (114) Google Scholar,26Andina D. Noguera-Morel L. Bascuas-Arribas M. Gaitero-Tristán J. Alonso-Cadenas J.A. Escalada-Pellitero S. et al.Chilblains in children in the setting of COVID-19 pandemic.Pediatr Dermatol. 2020; 37: 406-411Crossref PubMed Scopus (166) Google Scholar Our patient presented with venous gangrene and an acutely threatened limb. Emergent mechanical thrombectomy was complicated by a massive PE and cardiac arrest. Absence of an IVC clot, her adolescent age, known complications of IVC filters, and the purported design advantages of the ClotTriever with a coring element and a nitinol collection bag for distal protection biased our decision not to insert a prophylactic IVC filter.27Mouawad N.J. Effective single-session percutaneous nonpharmacologic mechanical thrombectomy for phlegmasia cerulea dolens.J Vasc Surg Cases Innov Tech. 2020; 6: 212-215Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar,28Benarroch-Gampel J. Pujari A. Aizpuru M. Rajani R.R. Jordan W.D. Crawford R. Technical success and short-term outcomes after treatment of lower extremity deep vein thrombosis with the ClotTriever system: a preliminary experience.J Vasc Surg Venous Lymphat Disord. 2020; 8: 174-181Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar In retrospect, filter placement likely would have captured dislodged emboli and prevented cardiac arrest.29Lee S.H. Kim H.K. Hwang J.K. Kim S.D. 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Athrombolytic regimen for high-risk deep venous thrombosis may substantially reduce the risk of postthrombotic syndrome in children.Blood. 2007; 110: 45-53Crossref PubMed Scopus (132) Google Scholar Adjunctive corticosteroid therapy and plasmapheresis was undertaken upon the finding of APLA. Plasmapheresis likely confounded SARS-CoV-2 antibody testing. Repeated serology confirmed our suspicion of relationship to SARS-CoV-2 infection. SARS-CoV-2 infection should be considered in the differential diagnosis for children with unusual thrombotic presentations. Earlier detection and treatment of coagulopathy may prevent severe complications of the nature described here. We thank the dedicated nursing staff of the pediatric intensive care unit, surgical, and catheterization laboratory for the exceptional care delivered. eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiIxZDA5NDFkNWQ1ODdhMWFhNDQyZTdmOTk2YzgzYTQwNiIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNzIzODU1ODgyfQ.HScWIzWvL7khnVFfUn_mTAhV72EN80zMeOKirFwlaqLC30aMdz6Z38WLtD8W2pWtXv6-PHpHnbvqHmUjYhdXuJvVF6DNwujOHd_nIAwk0NRAiXU4BY9Dy8b-1mhTELSHuxdVS6PHESV_dFhcLtmY5IgDg_DaTr9zoXnM5mVWNakdttX6wp8-sf6l4iPKfBuGX-6wlCFRja0g4F6x2HJIJGaaV6r32dsL2F9uG8-rmz_5be7CQ0VJIzQKwQ6RpYefaG0vkvX3beDM-Bdn-Fav_kHnbH-O9BXi7wqR_u_nX7j8GIjv30SORQiWkxwb7K2D-4Vf_QwH3r1_Ll-rMUesKg Download .mp4 (0.96 MB) Help with .mp4 files Video 1eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI5N2YwMmZmNmYwN2VkN2U3NTk0NWVlODFiYTU5ZmQ2ZSIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNzIzODU1ODgyfQ.TayoWrXyFDPAl8YhZ2dKK84gfO2uWTkQsdI48cc6IS1zhE6P-Isj5jy6gbcQAuwBLSYpCsHGG2PXh5JabxqKRw4E9AvJe3J7poHi7J1Z21sHheYruAmbuSFfqyOvcrdC7TjcqAl4eCG3oHCBqc8cWZyiAsnlLbEI4hl17zjh6s8E03_KXfYZNZheaEg9aB-ygHeZ31rtNXavEr6-VHlqxpgIagOVnsXz8neVMgR2ZGzXeGNfNaMRgTOHbFvwL43mVOuFfh-MdPrRSaOzP-YyjMZ7y_hpwf9zSVASCYLPg2xcmMYKiHqqt8NVMlS3katDdAJNZQg3KCc1G-z-e5AyGw Download .mp4 (0.77 MB) Help with .mp4 files Video 2eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiIxZjM5MGQxOTVhNzRhNzhjNzUxYTQ3NDNlZWI0MmI5NiIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNzIzODU1ODgyfQ.oGaaNEnIWcoEQY8tiEUnviCNczy8kO-_9REKaTAOIR8137HqYm53nPvgsr0UwB0ZkAFqjGX5lImtYlaMjH6atG7DDbjB5fmlVcJAZ-hXHHKr93ZeMcAFXkh6OCojGsG291WcN1kGPl0Ua8slb749UGyDlzyEmiKqQ35wqcW25Fs2e0wPYfdP8C35J8mioNf5vPUo6mnWwLAEeaqcbPwQiu_gGHVy-u8h7C-crGMm-qAn9QI6iKsNtDRpbnVlB6B5qd-tCjBWFGsFTms4tnK8OikMxG3-Td9YgLIgbMZ88QCA8YqiirydFasmqe2WGa2eFz1Xw6XXmgnMBwNg_Fy91A Download .mp4 (0.98 MB) Help with .mp4 files Video 3
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