Prerpints.org logo
Preprint
Review

Capillary Leak Syndrome after SARS-CoV-2 Infection and COVID-19 Vaccines: A Comparative Review

Altmetrics

Downloads

434

Views

297

Comments

0

Submitted:

05 January 2023

Posted:

11 January 2023

You are already at the latest version

Alerts
Abstract
Systemic capillary leak syndrome (SCLS) is an uncommon, potentially life-threatening disorder defined as recurrent attacks of pseudo-shock. This syndrome occurs due to the disruption of endothelial cells, which leads to increased vascular permeability, causing intravascular fluid to leak into the extravascular space and albumin to be retained in the interstitial space. SCLS can lead to hypovolemia, peripheral hypoperfusion, and acute renal insufficiency. The syndrome is presented with fever, generalized edema, pleural effusions, dyspnea, hypovolemia, hemoconcentration, prerenal azotemia, shock, and syncope. After ruling out other causes of hypovolemic shock, the diagnosis of SCLS can be considered on the presence of the classical triad of hypotension, hemoconcentration, and hypoalbuminemia. Eliminating the precipitating factors is the cornerstone of SCLS management. It is advisable to be very cautious and weigh the risks and benefits of vaccination of people with a history of this condition. This review will discuss and compare different aspects of SLCS after SARS-CoV-2 infection and COVID-19 vaccination.
Keywords: 
Subject: Medicine and Pharmacology  -   Pharmacology and Toxicology

1. Introduction

The coronavirus disease 2019 (COVID-19) pandemic showed us that the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection is not merely a respiratory disease but it can lead to several disastrous extrapulmonary complications as a result of immune response dysregulation [1]. Systemic capillary leak syndrome (SCLS) is among the essential immune diseases triggered by the SARS-CoV-2. This condition had been observed with a high frequency in COVID-19 infected patients, so authorities believe that this life-threatening condition might be a variant of the COVID-19 related multisystemic inflammatory syndromes (MIS) [2]. Reviewing the COVID-19 related literature has revealed three SARS-CoV-2 related SCLS: 1) new-onset SCLS, 2) flare-up of the preexisting SCLS, and 3) vaccine-induced SCLS [3]. With the introduction of COVID-19 vaccines, rare similar cases have been reported following SARS-CoV-2 vaccination, some with fatal outcomes [4], and it is anticipated to be increasingly identified with the increase in the vaccinated population. Here, we have reviewed the literature and compared the capillary leak syndrome in the settings of SARS-CoV-2 infection and vaccination.

2. Definition and etiology

Systemic capillary leak syndrome is an uncommon, potentially life-threatening disorder defined as recurrent attacks of pseudo-shock, whose frequency, severity, and duration are variable, with each bout lasting 24-48 hours [5]. On the other hand, SCLSs are classified into acute or chronic and primary or secondary, based on the relapses of attacks, the severity of manifestations, and the presence of precipitating factors [6]. The primary, spontaneous, or idiopathic SCLS is Clarkson’s disease, while secondary cases occur due to certain precipitating factors, including hematologic malignancies, immune disorders, trauma, toxins or chemicals, medication, surgery, transplantation, and infections [7]. Among the aforementioned precipitating factors, we can name immune disorders such as Sjögren’s syndrome, systemic sclerosis, and juvenile dermatomyositis [8,9,10], malignancies, such as monoclonal gammopathies, lymphoma and myeloproliferative disorder [11,12], and medications such as G-CSF, interferons, rituximab and chemotherapeutic agents such as checkpoint inhibitors [13,14,15,16,17] as the most commonly reported triggers of SCLS in the literature.
Among infections responsible for SCLS, we can name influenza as the most common, and respiratory syncytial virus (RSV), West Nile virus (WNV), hantavirus, rotavirus, brucellosis, meningococcemia, malaria, Zika, Ebola, and dengue fever as the less prevalent ones [18,19,20,21,22,23,24,25]. It is demonstrated that viruses, like the influenza virus, causing upper respiratory tract infections are predominantly responsible for SCLS; coronaviruses are also believed to lead to this complication. Since the pandemic’s beginning, there have been great case reports of SCLS following SARS-CoV-2 infection is anticipated [26].
Vaccination is another crucial trigger for SCLS [27]. Previously, SCLS had been reported following influenza vaccination [28]. However, the introduction of SARS-CoV-2 vaccines has brought about several new or exacerbated cases of SCLS [29,30]. Most cases of SARS-CoV-2 vaccination-induced SCLS have been reported with adenoviral vector and mRNA vaccines [31].

3. Pathophysiology

Systemic capillary leak syndrome occurs due to the disruption of endothelial cells, which leads to increased vascular permeability, causing intravascular fluid to leak into the extravascular space and albumin to be retained in the interstitial space [32]. This phenomenon can lead to hypovolemia, peripheral hypoperfusion, and acute renal insufficiency [33]. In viral infections, this condition can be triggered by direct viral toxicity on the endothelial barrier of massive inflammatory mediators secretion [5,34]. This inflammatory response in the lungs leads to pulmonary capillary leak syndrome, which manifests as progressive hypoxemic respiratory failure and acute respiratory distress syndrome (ARDS) [35,36]. The elevation of proinflammatory cytokines and chemokines, like CCL2, IL-1, IL-6, IL8, IL-12, and TNF-α during the SARS-CoV-2 infection has a critical role in damaging the respiratory system and other organs [37]. The most significant injury occurs in angiotensin-converting enzyme 2 (ACE2) rich areas, which are entry gates of the virus [38]. On the other hand, the occurrence of SCLS in the settings of COVID-19 vaccines can be attributed to the SARS-CoV-2 spike glycoprotein encoded by the RNA or the viral vector [39].

4. Manifestations

A great majority of acute SCLSs are preceded by a nonspecific prodrome of the flu-like syndrome [40]. Nonetheless, some acute cases follow an episode of sepsis, anaphylaxis, or even an intense physical exertion [41]. This syndrome is presented with fever, generalized edema, pleural effusions, dyspnea, hypovolaemia, hemoconcentration, prerenal azotemia, shock, and syncope. Peripheral, periorbital, or facial edema may only be detected [6]. It is a form of vascular leak syndrome defined as the presence of at least two of the following: hypotension, edema, and hypoalbuminemia [42]. However, the chronic form is characterized by fluctuating episodes of diffuse edema, weight gain, and hypoalbuminemia rather than hypotension [43]. Interestingly, consciousness is preserved during the bouts of a chronic SCLS, even in severe attacks [40].

5. Laboratory findings

It is observed that polycythemia, hypoalbuminemia, and neutrophilic leukocytosis are the most common laboratory findings in SCLS cases. Other abnormalities are thrombocytosis, rhabdomyolysis, lactic acidosis, coagulopathy, paraproteinemia, and increased VEGF levels [44]. However, it should be considered that thrombocytosis was not observed in some previous studies. In a study, it was seen that a significant number of patients showed monoclonal plasma cell (PC) proliferation [6], and monoclonal protein was detected via electrophoresis in a group of patients [45]. Acute renal failure (known as a total elevation in creatinine of 0.3 mg/dL or a reduction in urine volume to less than 0.5 mL/kg/h for a period longer than 6 hours, observed within 48 hours of the beginning of symptoms) is another critical, noted an abnormality in SCLS patients [6].

6. Diagnosis

In any patient presenting with generalized edema, hypotension, hemoconcentration, or hypoalbuminemia shortly after being infected with SARS-CoV-2 or after receiving a SARS-CoV-2 vaccine, SCLS should be considered [46]. There are no specific diagnostic criteria and tests for SCLS. Therefore, the diagnosis of capillary leak syndrome is that of exclusion. After ruling out other causes of hypovolemic shock, the diagnosis of SCLS can be considered on the presence of the classical triad of hypotension, hemoconcentration, and hypoalbuminemia. For example, the pulmonary capillary leak syndrome diagnosis is based upon clinical and radiologic findings and exclusion of heart failure [5,35]. However, in deceased patients, postmortem electron microscopy examinations of lung tissues, showing loosening of interendothelial junctional complex and increase in protein concentrations and cytokine levels of the bronchoalveolar fluid (BALF), retrospectively confirms the diagnosis [47].

7. Differential diagnosis

The similarities between SCLS and Kawasaki disease (KD) in the context of COVID-19 is to the extent that it is sometimes known as SARS-CoV-2–induced Kawasaki-like hyperinflammatory syndrome (SCiKH syndrome) [48]. Moreover, COVID-19-related multisystem inflammatory syndrome (MIS) is another similar condition that predominantly occurs in the pediatric population. It usually occurs in the late phase of SARS-CoV-2 infection, is manifested by elevated inflammatory biomarkers, and is managed with anti-inflammatory agents such as corticosteroids and IV immunoglobulins (IVIg) [11,49]. Sepsis is another condition commonly mistaken for SCLS. However, procalcitonin levels, blood cultures, and evidence of active infection on the chest or abdominal imaging can help in differentiating it from other differential diagnoses [7]. Other conditions that can present with hemoconcentration, hypoalbuminemia, and hypotension include nephrotic syndrome, malnutrition, cirrhosis, angioedema, and anaphylaxis, which should be excluded on clinical and paraclinical findings [29].

8. Treatment

In general, eliminating the precipitating factor is the cornerstone of SCLS management. SCLS is predominantly managed conservatively in the early stages with osmotic drugs, diuretics, colchicine, renal replacement therapy, hemofiltration, and albumin transfusion [50,51]. However, in later phases, surgical drainage might be needed to extract the accumulated fluids from body cavities to restore vital organs function [52]. In order to better manage SCLS, some authorities classify this condition into 4 grades: grade 1 (hypotension responsive to oral fluid therapy), grade 2 (intravenous hydration without hospital admission), grade 3 (life-threatening and requiring ICU admission), and grade 4 (fatal) [7].
Pulmonary capillary leak syndrome can be managed with oxygen therapy non-invasive or invasive mechanical ventilation [53]. Steroids help suppress the hyperinflammatory response [54,55], whereas theophylline, beta 2 agonists, aminophylline, lisinopril, montelukast, imatinib, and chronic treatment with IVIg may prevent relapses [50,56,57].

9. Prognosis

Complications of SCLS, triggered by any condition, include thromboembolism caused by the hemoconcentration and hyperviscosity, renal failure, pericardial effusions, tamponade, and cardiac arrest [6]. Moreover, compartment syndrome and the resultant amputations, in addition to sensorimotor neuropathy, can occur as a result of severe peripheral anasarca [58]. Mortality could be due to hypovolemic shock, rhabdomyolysis, arrhythmia, pulmonary edema, renal failure, refractory shock, and thromboembolism [39].

10. Prevention

As a preexisting SCLS can be exacerbated following any precipitating factors, such as infection or vaccination [59], it is better to be vigilant and weigh the risks and benefits of vaccinating individuals with a history of this disorder. Some authorities even prohibit adenoviral vector vaccines in individuals with a history of SCLS. If vaccinated, close monitoring with regular blood pressure measurement, weight, urine output, and hemoglobin and albumin levels is reasonable. Furthermore, in patients with a history of severe episodes of SCLS, who are decided to be vaccinated, administering IVIg before vaccination or monthly IVIg infusions during the COVID-19 pandemic may prevent further attacks [60,61].

11. Conclusion

As previously mentioned, Systemic capillary leak syndrome (SCLS) is an uncommon disease defined by the presence of extreme hypotension, hemoconcentration, and hypoalbuminemia due to leakage of plasma fluid and proteins into the interstitial space. SCLS is among the most important immune diseases triggered by the SARS-CoV-2. According to existing evidence, SARS-CoV-2 infection and COVID-19 vaccination could cause this life-threatening condition. SCLS could lead to severe complications like thromboembolism (caused by hemoconcentration and hyperviscosity), renal failure, pericardial effusions, tamponade, and cardiac arrest. Since there are no specific diagnostic criteria and tests for determining SCLS, the diagnosis is excluded. After excluding other causes of hypovolemic shock, the diagnosis of SCLS can be considered on the presence of the classical triad of hypotension, hemoconcentration, and hypoalbuminemia. A wide range of conditions can be listed as the differential diagnosis for cases of suspected SCLS. The most important ones are septic shock, nephrotic syndrome, anaphylaxis, hereditary angioedema, drug reactions, exudative enteropathy, and ovarian hyperstimulation. Early stages of SCLS should primarily be managed conservatively with osmotic drugs, diuretics, colchicine, renal replacement therapy, hemofiltration, and albumin transfusion. While, in later phases, surgical drainage might be needed to extract the accumulated fluids from body cavities to restore vital organs’ function. Since SLCS has been observed in association with SARS-CoV-2 infection and COVID-19 vaccination, it should be considered a possible diagnosis in COVID-19 patients, and it is advisable to be very cautious and weigh the risks and benefits of vaccination of people with a history of this syndrome.

Author Contributions

Zeinab Mohseni Afshar: Conceptualization, Writing - Original Draft; Hossein Nazari Rostami: Investigation, Writing - Original Draft; Ali Tavakoli Pirzaman: Investigation, Writing - Original Draft; Rezvan Hosseinzadeh: Visualization, Writing - Review & Editing; Arefeh Babazadeh: Investigation, Writing - Original Draft; Dariush Hosseinzadeh: Investigation, Writing - Original Draft; Seyed Rouhollah Miri: Investigation, Writing - Original Draft; Terence T. Sio: Writing - Review & Editing; Mohammad Barary: Investigation, Writing - Original Draft, Writing - Review & Editing; Soheil Ebrahimpour: Conceptualization, Writing - Original Draft, Supervision.

Funding

This research received no funding.

Data Availability Statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

Acknowledgments

The authors would like to thank the clinical research development center of Imam Reza Hospital, Kermanshah University of Medical Sciences, for their kind support. Figures 1 and 2 are created with BioRender.com.

Conflicts of Interest

Terence T. Sio reports that he provides strategic and scientific recommendations as a member of the Advisory Board and speaker for Novocure, Inc. and also as a member of the Advisory Board to Galera Therapeutics, which are not in any way associated with the content or disease site as presented in this manuscript. All other authors have no conflict of interests to be declared.

References

  1. John, A.L.S.; Rathore, A.P. Early insights into immune responses during COVID-19. The Journal of Immunology 2020, 205, 555–564. [Google Scholar] [CrossRef]
  2. de Chambrun, M.P.; Constantin, J.-M.; Mathian, A.; Quemeneur, C.; Lepere, V.; Combes, A.; Luyt, C.-E.; Amoura, Z. Clarkson’s Disease Episode or Secondary Systemic Capillary Leak-Syndrome: That Is the Question! Chest 2021, 159, 441. [Google Scholar] [CrossRef]
  3. Knox, D.B.; Lee, V.; Leither, L.; Brown, S.M. New-Onset Systemic Capillary Leak Syndrome in an Adult Patient with COVID-19. Case Rep Crit Care 2021, 2021, 8098942. [Google Scholar] [CrossRef]
  4. Dimitrova, E. Vaxzevria (Previously COVID-19 Vaccine AstraZeneca); European Medicines Agency: 2021.
  5. Siddall, E.; Khatri, M.; Radhakrishnan, J. Capillary leak syndrome: etiologies, pathophysiology, and management. Kidney Int 2017, 92, 37–46. [Google Scholar] [CrossRef]
  6. Kapoor, P.; Greipp, P.T.; Schaefer, E.W.; Mandrekar, S.J.; Kamal, A.H.; Gonzalez-Paz, N.C.; Kumar, S.; Greipp, P.R. Idiopathic systemic capillary leak syndrome (Clarkson's disease): the Mayo clinic experience. In Proceedings of the Mayo Clinic Proceedings; 2010; pp. 905–912. [Google Scholar]
  7. Druey, K.M.; Greipp, P.R. Narrative review: the systemic capillary leak syndrome. Ann Intern Med 2010, 153, 90–98. [Google Scholar] [CrossRef]
  8. Cao, C.; Shao, Q.; Yang, H. Sjogren's syndrome concurrent with organizing pneumonia with secondary systemic capillary leak syndrome: a case report. Scand J Rheumatol 2021, 50, 322–324. [Google Scholar] [CrossRef]
  9. Martin, A.J.; Sen, E.S.; Emonts, M. Atypical juvenile dermatomyositis complicated by systemic capillary leak syndrome: case report and review of the literature. Rheumatology (Oxford) 2021, 60, e1–e2. [Google Scholar] [CrossRef]
  10. Hinchcliff, M.E.; Lomasney, J.; Johnson, J.A.; Varga, J. Fulminant capillary leak syndrome in a patient with systemic sclerosis treated with imatinib mesylate. Rheumatology (Oxford) 2016, 55, 1916–1918. [Google Scholar] [CrossRef]
  11. de Chambrun, M.P.; Gousseff, M.; Mauhin, W.; Lega, J.-C.; Lambert, M.; Rivière, S.; Dossier, A.; Ruivard, M.; Lhote, F.; Blaison, G. Intravenous immunoglobulins improve survival in monoclonal gammopathy-associated systemic capillary-leak syndrome. The American journal of medicine 2017, 130, 1219–e1219. [Google Scholar] [CrossRef]
  12. Guffroy, A.; Dervieux, B.; Gravier, S.; Martinez, C.; Deibener-Kaminsky, J.; Hachulla, E.; Michel, M.; Weber, J.-C.; Korganow, A.-S.; Arnaud, L. Systemic capillary leak syndrome and autoimmune diseases: a case series. In Proceedings of the Seminars in arthritis and rheumatism; 2017; pp. 509–512. [Google Scholar]
  13. Yamamoto, K.; Mizuno, M.; Tsuji, T.; Amano, T. Capillary leak syndrome after interferon treatment for chronic hepatitis C. Arch Intern Med 2002, 162, 481–482. [Google Scholar] [CrossRef]
  14. Umeda, Y.; Hayashi, H.; Sugiyama, S.; Aoyama, Y. Systemic capillary leak syndrome triggered by anti-programmed death 1 checkpoint inhibitor in psoriasis. J Dermatol 2020, 47, 1322–1325. [Google Scholar] [CrossRef]
  15. Jeong, G.H.; Lee, K.H.; Lee, I.R.; Oh, J.H.; Kim, D.W.; Shin, J.W.; Kronbichler, A.; Eisenhut, M.; van der Vliet, H.J.; Abdel-Rahman, O. Incidence of capillary leak syndrome as an adverse effect of drugs in cancer patients: a systematic review and meta-analysis. Journal of clinical medicine 2019, 8, 143. [Google Scholar] [CrossRef]
  16. Vedala, K.; Desikan, S.P.; McClain, C., 3rd; Jacob, D.; Desikan, R. Capillary Leak Syndrome From Rituximab Therapy of Lymphoma. J Investig Med High Impact Case Rep 2020, 8, 2324709620942372. [Google Scholar] [CrossRef]
  17. Dagdemir, A.; Albayrak, D.; Dilber, C.; Totan, M. G-CSF related capillary leak syndrome in a child with leukemia. Leuk Lymphoma 2001, 42, 1445–1447. [Google Scholar] [CrossRef]
  18. Ebdrup, L.; Druey, K.M.; Druey, K.; Mogensen, T.H. Severe capillary leak syndrome with cardiac arrest triggered by influenza virus infection. BMJ Case Rep 2018, 2018, bcr–2018. [Google Scholar] [CrossRef] [PubMed]
  19. Erkurt, M.A.; Sari, I.; Gul, H.C.; Coskun, O.; Eyigun, C.P.; Beyan, C. The first documented case of brucellosis manifested with pancytopenia and capillary leak syndrome. Intern Med 2008, 47, 863–865. [Google Scholar] [CrossRef]
  20. Verma, S.K.; Gutch, M.; Agarwal, A.; Vaish, A.K. Capillary leak syndrome in dengue fever. WHO Regional Office for South-East Asia. 2011.
  21. Aldemir-Kocabas, B.; Karbuz, A.; Ciftci, E.; Demir, M.; Ince, E. An unusual cause of secondary capillary leak syndrome in a child: rotavirus diarrhea. Turk J Pediatr 2013, 55, 90–93. [Google Scholar] [PubMed]
  22. Das, B.K.; Agasti, N.; Singh, Y.K.S.; Midya, A. Plasmodium vivax Malaria Presenting with Acute Systemic Capillary Leak Syndrome. J Assoc Physicians India 2019, 67, 86–87. [Google Scholar]
  23. Escutenaire, S.; Pastoret, P.P. Hantavirus infections. Rev Sci Tech 2000, 19, 64–78. [Google Scholar] [CrossRef]
  24. Milonovich, L.M. Meningococcemia: epidemiology, pathophysiology, and management. J Pediatr Health Care 2007, 21, 75–80. [Google Scholar] [CrossRef]
  25. Fosse, J.H.; Haraldsen, G.; Falk, K.; Edelmann, R. Endothelial Cells in Emerging Viral Infections. Front Cardiovasc Med 2021, 8, 619690. [Google Scholar] [CrossRef] [PubMed]
  26. Beber, A.; Dellai, F.; Abdel Jaber, M.; Peterlana, D.; Brunori, G.; Maino, A. Systemic Capillary Leak Syndrome triggered by SARS-CoV2 infection: Case Report and Systematic Review. Scand J Rheumatol 2022, 51, 67–69. [Google Scholar] [CrossRef] [PubMed]
  27. Batista-Duharte, A.; Portuondo, D.; Perez, O.; Carlos, I.Z. Systemic immunotoxicity reactions induced by adjuvanted vaccines. Int Immunopharmacol 2014, 20, 170–180. [Google Scholar] [CrossRef]
  28. Geerse, D.A.; Meynen, F.M.; Gelens, M.A.; Kooman, J.P.; Cornelis, T. Systemic Capillary Leak Syndrome after Influenza Vaccination in a Peritoneal Dialysis Patient. Perit Dial Int 2015, 35, 772–773. [Google Scholar] [CrossRef] [PubMed]
  29. Robichaud, J.; Cote, C.; Cote, F. Systemic capillary leak syndrome after ChAdOx1 nCOV-19 (Oxford-AstraZeneca) vaccination. CMAJ 2021, 193, E1341–E1344. [Google Scholar] [CrossRef] [PubMed]
  30. Choi, G.J.; Baek, S.H.; Kim, J.; Kim, J.H.; Kwon, G.Y.; Kim, D.K.; Jung, Y.H.; Kim, S. Fatal Systemic Capillary Leak Syndrome after SARS-CoV-2Vaccination in Patient with Multiple Myeloma. Emerg Infect Dis 2021, 27, 2973–2975. [Google Scholar] [CrossRef] [PubMed]
  31. Petric, D. Can a Multi-Epitope Vaccine be a solution for COVID-19 pandemic? Academia Letters 2021 2021, 4010. [Google Scholar] [CrossRef]
  32. Wu, M.A.; Tsvirkun, D.; Bureau, L.; Boccon-Gibod, I.; Inglebert, M.; Duperray, A.; Bouillet, L.; Misbah, C.; Cicardi, M. Paroxysmal Permeability Disorders: Development of a Microfluidic Device to Assess Endothelial Barrier Function. Front Med (Lausanne) 2019, 6, 89. [Google Scholar] [CrossRef]
  33. Balakumar, V.; Murugan, R.; Sileanu, F.E.; Palevsky, P.; Clermont, G.; Kellum, J.A. Both positive and negative fluid balance may be associated with reduced long-term survival in the critically ill. Critical care medicine 2017, 45, e749. [Google Scholar] [CrossRef]
  34. Mehta, P.; McAuley, D.F.; Brown, M.; Sanchez, E.; Tattersall, R.S.; Manson, J.J.; Hlh Across Speciality Collaboration, U.K. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020, 395, 1033–1034. [Google Scholar] [CrossRef]
  35. Bahloul, M.; Ketata, W.; Lahyeni, D.; Mayoufi, H.; Kotti, A.; Smaoui, F.; Kallel, N.; Daoud, E.; Bouaziz, M.; Kammoun, S. Pulmonary capillary leak syndrome following COVID-19 virus infection. J Med Virol 2021, 93, 94–96. [Google Scholar] [CrossRef] [PubMed]
  36. Wu, M.A.; Fossali, T.; Pandolfi, L.; Carsana, L.; Ottolina, D.; Frangipane, V.; Rech, R.; Tosoni, A.; Agarossi, A.; Cogliati, C. COVID-19: the key role of pulmonary capillary leakage. An observational cohort study. medRxiv 2020. [Google Scholar]
  37. Xie, Z.; Chan, E.; Yin, Y.; Ghosh, C.C.; Wisch, L.; Nelson, C.; Young, M.; Parikh, S.M.; Druey, K.M. Inflammatory Markers of the Systemic Capillary Leak Syndrome (Clarkson Disease). J Clin Cell Immunol 2014, 5, 1000213. [Google Scholar] [CrossRef]
  38. Li, H.; Liu, L.; Zhang, D.; Xu, J.; Dai, H.; Tang, N.; Su, X.; Cao, B. SARS-CoV-2 and viral sepsis: observations and hypotheses. Lancet 2020, 395, 1517–1520. [Google Scholar] [CrossRef] [PubMed]
  39. Roncati, L.; Gianotti, G.; Ambrogi, E.; Attolini, G. Capillary leak syndrome in COVID-19 and post COVID-19 vaccines. European Journal of Gynaecological Oncology 2021, 42, 829–831. [Google Scholar]
  40. Pineton de Chambrun, M.; Luyt, C.E.; Beloncle, F.; Gousseff, M.; Mauhin, W.; Argaud, L.; Ledochowski, S.; Moreau, A.S.; Sonneville, R.; Verdiere, B.; et al. The Clinical Picture of Severe Systemic Capillary-Leak Syndrome Episodes Requiring ICU Admission. Crit Care Med 2017, 45, 1216–1223. [Google Scholar] [CrossRef]
  41. Druey, K.M.; Parikh, S.M. Idiopathic systemic capillary leak syndrome (Clarkson disease). J Allergy Clin Immunol 2017, 140, 663–670. [Google Scholar] [CrossRef]
  42. Railan, D.; Fivenson, D.P.; Wittenberg, G. Capillary leak syndrome in a patient treated with interleukin 2 fusion toxin for cutaneous T-cell lymphoma. J Am Acad Dermatol 2000, 43, 323–324. [Google Scholar] [CrossRef]
  43. Airaghi, L.; Montori, D.; Santambrogio, L.; Miadonna, A.; Tedeschi, A. Chronic systemic capillary leak syndrome. Report of a case and review of the literature. J Intern Med 2000, 247, 731–735. [Google Scholar] [CrossRef]
  44. Baloch, N.U.; Bikak, M.; Rehman, A.; Rahman, O. Recognition and management of idiopathic systemic capillary leak syndrome: an evidence-based review. Expert Rev Cardiovasc Ther 2018, 16, 331–340. [Google Scholar] [CrossRef]
  45. Dhir, V.; Arya, V.; Malav, I.C.; Suryanarayanan, B.S.; Gupta, R.; Dey, A.B. Idiopathic systemic capillary leak syndrome (SCLS): case report and systematic review of cases reported in the last 16 years. Intern Med 2007, 46, 899–904. [Google Scholar] [CrossRef]
  46. Tanabe, M.; Hikone, M.; Sugiyama, K.; Hamabe, Y. Systemic capillary leak syndrome complicated by laryngeal edema after severe acute respiratory syndrome coronavirus 2 vaccination. Acute Med Surg 2021, 8, e700. [Google Scholar] [CrossRef] [PubMed]
  47. Wu, M.A.; Fossali, T.; Pandolfi, L.; Carsana, L.; Ottolina, D.; Frangipane, V.; Rech, R.; Tosoni, A.; Lopez, G.; Agarossi, A.; et al. Hypoalbuminemia in COVID-19: assessing the hypothesis for underlying pulmonary capillary leakage. J Intern Med 2021, 289, 861–872. [Google Scholar] [CrossRef] [PubMed]
  48. Licciardi, F.; Pruccoli, G.; Denina, M.; Parodi, E.; Taglietto, M.; Rosati, S.; Montin, D. SARS-CoV-2-Induced Kawasaki-Like Hyperinflammatory Syndrome: A Novel COVID Phenotype in Children. Pediatrics 2020, 146. [Google Scholar] [CrossRef] [PubMed]
  49. Dufort, E.M.; Koumans, E.H.; Chow, E.J.; Rosenthal, E.M.; Muse, A.; Rowlands, J.; Barranco, M.A.; Maxted, A.M.; Rosenberg, E.S.; Easton, D.; et al. Multisystem Inflammatory Syndrome in Children in New York State. N Engl J Med 2020, 383, 347–358. [Google Scholar] [CrossRef] [PubMed]
  50. Cocchi, E.; Chiale, F.; Gianoglio, B.; Deorsola, L.; Pace Napoleone, C.; Fagioli, F.; Peruzzi, L. Colchicine: An Impressive Effect on Posttransplant Capillary Leak Syndrome and Renal Failure. Pediatrics 2019, 143. [Google Scholar] [CrossRef] [PubMed]
  51. Wu, M.A.; Colombo, R.; Podda, G.M.; Cicardi, M. Handling shock in idiopathic systemic capillary leak syndrome (Clarkson’s disease): less is more. Internal and emergency medicine 2019, 14, 723–730. [Google Scholar] [CrossRef] [PubMed]
  52. Saini, A.; Delius, R.E.; Seshadri, S.; Walters, H., 3rd; Mastropietro, C.W. Passive peritoneal drainage improves fluid balance after surgery for congenital heart disease. Eur J Cardiothorac Surg 2012, 41, 256–260. [Google Scholar] [CrossRef] [PubMed]
  53. Bahloul, M.; Dammak, H.; Chaari, A.; Allala, R.; Abid, L.; Haddar, S.; Chelly, H.; Ayoub, A.; Ben Hamida, C.; Bouaziz, M. Pulmonary capillary leak syndrome after influenza A (H1N1) virus infection. Am J Emerg Med 2010, 28, 1063–e1061-1066. [Google Scholar] [CrossRef]
  54. Chihrin, S.; Loutfy, M.R. Overview of antiviral and anti-inflammatory treatment for severe acute respiratory syndrome. Expert Rev Anti Infect Ther 2005, 3, 251–262. [Google Scholar] [CrossRef]
  55. Russell, B.; Moss, C.; George, G.; Santaolalla, A.; Cope, A.; Papa, S.; Van Hemelrijck, M. Associations between immune-suppressive and stimulating drugs and novel COVID-19—a systematic review of current evidence. ecancermedicalscience 2020, 14. [Google Scholar] [CrossRef]
  56. Lambert, M.; Launay, D.; Hachulla, E.; Morell-Dubois, S.; Soland, V.; Queyrel, V.; Fourrier, F.; Hatron, P.Y. High-dose intravenous immunoglobulins dramatically reverse systemic capillary leak syndrome. Crit Care Med 2008, 36, 2184–2187. [Google Scholar] [CrossRef] [PubMed]
  57. Xie, Z.; Chan, E.C.; Long, L.M.; Nelson, C.; Druey, K.M. High-dose intravenous immunoglobulin therapy for systemic capillary leak syndrome (Clarkson disease). Am J Med 2015, 128, 91–95. [Google Scholar] [CrossRef] [PubMed]
  58. Sanghavi, R.; Aneman, A.; Parr, M.; Dunlop, L.; Champion, D. Systemic capillary leak syndrome associated with compartment syndrome and rhabdomyolysis. Anaesth Intensive Care 2006, 34, 388–391. [Google Scholar] [CrossRef]
  59. Concistre, A.; Alessandri, F.; Rosato, E.; Pugliese, F.; Muscaritoli, M.; Letizia, C. A case of chronic systemic capillary leak syndrome (SCLS) exacerbated during SARS-CoV2 infection. Eur Rev Med Pharmacol Sci 2021, 25, 5922–5927. [Google Scholar] [CrossRef] [PubMed]
  60. de Chambrun, M.P.; Cohen-Aubart, F.; Donker, D.W.; Cariou, P.-L.; Luyt, C.-E.; Combes, A.; Amoura, Z. SARS-CoV-2 induces acute and refractory relapse of systemic capillary leak syndrome (Clarkson's disease). The American journal of medicine 2020, 133, e663–e664. [Google Scholar] [CrossRef]
  61. Abgueguen, P.; Chennebault, J.M.; Pichard, E. Immunoglobulins for treatment of systemic capillary leak syndrome. Am J Med 2010, 123, e3–4. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.
Prerpints.org logo

Preprints.org is a free preprint server supported by MDPI in Basel, Switzerland.

facebook logotwitter logolinkedin logo
MDPI Initiatives
Important Links
Subscribe

Disclaimer

Terms of Use

Privacy Policy

© 2024 MDPI (Basel, Switzerland) unless otherwise stated