Jornal Vascular Brasileiro
https://app.periodikos.com.br/journal/jvb/article/doi/10.1590/1677-5449.202301282
Jornal Vascular Brasileiro
Review Article

Portal-splenic-mesenteric venous thrombosis in COVID-19 patients: a systematic review

Trombose venosa porto-espleno-mesentérica em pacientes com COVID-19: uma revisão sistemática

Ricardo Zanetti Gomes; Matheus Von Jelita Salina; Vitor Hugo Moro Pironatto; Julia Kapp Lepinski; Tiago Daniel Gueiber; Beatriz Moreira Salles Juliatto; Milena Zadra Prestes; Camila Marinelli Martins

Downloads: 2
Views: 110

Abstract

The COVID-19 pandemic affected millions of people worldwide. In addition to respiratory impairment, this viral infection can also provoke gastrointestinal symptoms caused by vascular disorders, such as portal-splenic-mesenteric venous thrombosis (PSMVT). This systematic review aimed to investigate the profile of patients who developed PSMVT concomitant with or after viral infection and its predominant outcomes. The database searches returned 214 articles. Of these, 40 case reports were included in the review, presenting a total of 41 cases of PSMVT addressed. Males were more prevalent (n=27; 65.85%), mean age was 51.54 years, and 19.57% had a previous history of endocrine diseases. Statistically significant relationships (p<0.05) were found between patient death and tachypnea at hospital admission (p=0.043) and between patient death and age (p=0.019). It was therefore possible to identify the main profiles and risk factors for PSMVT development and mortality of COVID-19 infected patients.

Keywords

SARS-CoV-2; inflammation; mesenteric ischemia; thrombosis; mesenteric venous thrombosis; splanchnic circulation

Resumo

A pandemia de covid-19 afetou milhões de pessoas no mundo todo. A infecção pelo vírus, além de comprometer o sistema respiratório, pode promover sintomas gastrointestinais decorrentes de afecções vasculares, como a trombose venosa porto-espleno-mesentérica (TVPEM). A presente revisão sistemática teve como objetivo investigar o perfil dos pacientes que desenvolveram TVPEM concomitantemente ou subsequente à infecção por covid-19, bem como os desfechos predominantes. De 214 artigos identificados nas bases de dados, 40 relatos de casos foram incluídos na revisão, incluindo 41 casos de TVPEM. O sexo masculino foi o mais prevalente (n=27; 65,85%), com média de idade de 51,54 anos, sendo que 19,57% dos pacientes tinham doença endocrinológica prévia. Foi encontrada relação estatisticamente significativa (p<0,05) entre óbito dos pacientes e a presença de taquipneia na admissão (p=0,043), assim como entre óbito e a idade dos pacientes (p=0,019). Assim, foi possível identificar os principais perfis e fatores de risco para o desenvolvimento e mortalidade da TVPEM em pacientes com covid-19.

Palavras-chave

SARS-CoV-2; inflamação; isquemia mesentérica; trombose; trombose venosa mesentérica; circulação esplâncnica

References

1 Our World in Data [Internet]. Oxford: University of Oxford; 2022 [cited 2022 Sept 18]. https://ourworldindata.org/explorers/coronavirus-data-explorer

2 Harnik IG, Brandt LJ. Mesenteric venous thrombosis. Vasc Med. 2010;15(5):407-18. http://doi.org/10.1177/1358863X10379673. PMid:20926500.

3 Pang JHQ, Tang JH, Eugene-Fan B, Lee CL, Low JK. A peculiar case of small bowel stricture in a coronavirus disease 2019 patient with congenital adhesion band and superior mesenteric vein thrombosis. Ann Vasc Surg. 2021;70:286-9. http://doi.org/10.1016/j.avsg.2020.08.084. PMid:32861849.

4 Parry AH, Wani AH, Yaseen M. Acute mesenteric ischemia in severe coronavirus-19 (COVID-19): possible mechanisms and diagnostic pathway. Acad Radiol. 2020;27(8):1190. http://doi.org/10.1016/j.acra.2020.05.016. PMid:32475635.

5 Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. http://doi.org/10.1136/bmj.n71. PMid:33782057.

6 Biblioteca Virtual em Saúde – BVS. DeCS: Descritores em Ciências da Saúde [Internet]. 2022 [cited 2022 Sept 15]. https://decs.bvsalud.org

7 Mendeley Ltd. Mendeley Desktop version 1.19.8 [Software]. London: Elsevier; 2020.

8 Microsoft Corporation. Microsoft Excel version 16.0 [Software]. Redmond: Microsoft; 2018.

9 Murad MH, Sultan S, Haffar S, Bazerbachi F. Methodological quality and synthesis of case series and case reports. BMJ Evid Based Med. 2018;23(2):60-3. http://doi.org/10.1136/bmjebm-2017-110853. PMid:29420178.

10 R Core Team. R: the R project for statistical computing version 4.2.1 [Software]. Vienna: R Foundation for Statistical Computing; 2020.

11 Carmo A Fo, Cunha BS. Inferior mesenteric vein thrombosis and COVID-19. Rev Soc Bras Med Trop. 2020;53:e20200412. http://doi.org/10.1590/0037-8682-0412-2020. PMid:32965451.

12 Alemán W, Cevallos LC. Subacute mesenteric venous thrombosis secondary to COVID-19: a late thrombotic complication in a nonsevere patient. Radiol Case Rep. 2021;16(4):899-902. http://doi.org/10.1016/j.radcr.2021.01.039. PMid:33495703.

13 Fan BE, Chang CCR, Teo CHY, Yap ES. COVID-19 Coagulopathy with superior mesenteric vein thrombosis complicated by an ischaemic Bowel. Hamostaseologie. 2020;40(5):592-3. http://doi.org/10.1055/a-1232-7446. PMid:32894875.

14 Amaravathi U, Balamurugan N, Muthu Pillai V, Ayyan SM. Superior mesenteric arterial and venous thrombosis in COVID-19. J Emerg Med. 2021;60(5):e103-7. http://doi.org/10.1016/j.jemermed.2020.12.016. PMid:33581991.

15 Goodfellow M, Courtney M, Upadhyay Y, Marsh R, Mahawar K. Mesenteric venous thrombosis due to coronavirus in a post Roux-en-Y gastric bypass patient: a case report. Obes Surg. 2021;31(5):2308-10. http://doi.org/10.1007/s11695-020-05214-8. PMid:33415609.

16 Ebrahiminik H, Nikpour S, Yazdi HR, Mohammadi A, Mirza-Aghazadeh-Attari M. Successful vascular interventional management of superior mesenteric vein thrombosis in a patient with COVID-19: a case report and review of literature. Radiol Case Rep. 2021;16(6):1539-42. http://doi.org/10.1016/j.radcr.2021.03.038. PMid:33777280.

17 Hosoda T, Orikasa H. A fatal case of extensive gastrointestinal necrosis due to portal and mesenteric vein thrombosis in the post-acute phase of COVID-19. J Infect Chemother. 2022;28(1):108-11. http://doi.org/10.1016/j.jiac.2021.10.015. PMid:34711507.

18 De Barry O, Mekki A, Diffre C, Seror M, El Hajjam M, Carlier RY. Arterial and venous abdominal thrombosis in a 79-year-old woman with COVID-19 pneumonia. Radiol Case Rep. 2020;15(7):1054-7. http://doi.org/10.1016/j.radcr.2020.04.055. PMid:32351657.

19 Navarro-Martínez S, Diez Ares JA, Peris Tomás N, Gonzálvez Guardiola P, Pérez-Rubio A. Superior mesenteric vein thrombosis as the only manifestation of SARS-CoV-2 infection. Cir Esp. 2021;100(4):245-7. http://doi.org/10.1016/j.ciresp.2021.03.007. PMid:33849706.

20 Marsafi O, Ijim F, Elkourchi M, Chahbi Z, Adnor S, Wakrim S. Acute venous mesenteric ischemia in a young COVID-19 positive subject: a case report. Pan Afr Med J. 2021;39:273. PMid:34754350.

21 Randhawa J, Kaur J, Randhawa HS, Kaur S, Singh H. Thrombosis of the portal vein and superior mesenteric vein in a patient with subclinical COVID-19 infection. Cureus. 2021;13(4):e14366. http://doi.org/10.7759/cureus.14366. PMid:33976989.

22 Calcagno E, Sogunro O, Nepal P, Assaker R, Sapire J. COVID-19 induced mesenteric venous infarction. Radiol Case Rep. 2021;16(8):1999-2002. http://doi.org/10.1016/j.radcr.2021.04.083. PMid:33995746.

23 Jeilani M, Hill R, Riad M, Abdulaal Y. Superior mesenteric vein and portal vein thrombosis in a patient with COVID-19: a rare case. BMJ Case Rep. 2021;14(6):e244049. http://doi.org/10.1136/bcr-2021-244049. PMid:34158339.

24 Thuluva SK, Zhu H, Tan MML, et al. A 29-year-old male construction worker from India who presented with left- sided abdominal pain due to isolated superior mesenteric vein thrombosis associated with SARS-CoV-2 infection. Am J Case Rep. 2020;21:e926785. http://doi.org/10.12659/AJCR.926785. PMid:32970653.

25 Mazariegos-Rubi MA, Borregón-Rivilla M, Gómez- Palmero C, Díez-de los Ríos M. Gómez- Palmero C, Díez-de los Ríos M. Pileflebitis mesentérica secundaria a infección por coronavirus. Atención Primaria Práctica. 2021;3(2):100087. http://doi.org/10.1016/j.appr.2021.100087.

26 Dağıstanlı S, Sönmez S. Spleen infarct secondary to thrombus in COVID-19-related splenic vein: a case report. Arab J Gastroenterol. 2021;22(2):180-3. http://doi.org/10.1016/j.ajg.2021.03.003. PMid:34088621.

27 Agarwal M, Singh S, Sinha U, Bhushan D. Extrahepatic portal vein thrombosis in a pregnant patient with COVID-19: a rare thrombotic event survivor. BMJ Case Rep. 2021;14(8):e243697. http://doi.org/10.1136/bcr-2021-243697. PMid:34385221.

28 Vidali S, Morosetti D, Granai AV, Legramante JM, Buonomo OC, Argirò R. Splenoportal-mesenteric axis thrombosis and splenic artery occlusion as initial presentations of COVID-19 disease. Eur Rev Med Pharmacol Sci. 2021;25(3):1680-3. PMid:33629338.

29 Mitchell JM, Rakheja D, Gopal P. SARS-CoV-2-related hypercoagulable state leading to ischemic enteritis secondary to superior mesenteric artery thrombosis. Clin Gastroenterol Hepatol. 2021;19(11):e111. http://doi.org/10.1016/j.cgh.2020.06.024. PMid:32562891.

30 Levolger S, Bokkers RPH, Wille J, Kropman RHJ, de Vries JPPM. Arterial thrombotic complications in COVID-19 patients. J Vasc Surg Cases Innov Tech. 2020;6(3):454-9. http://doi.org/10.1016/j.jvscit.2020.06.012. PMid:32835150.

31 Beccara L, Pacioni C, Ponton S, Francavilla S, Cuzzoli A. Arterial mesenteric thrombosis as a complication of SARS-CoV-2 infection. Eur J Case Rep Intern Med. 2020;7(5):001690. http://doi.org/10.12890/2020_001690. PMid:32399456.

32 Cheung S, Quiwa JC, Pillai A, Onwu C, Tharayil ZJ, Gupta R. Superior mesenteric artery thrombosis and acute intestinal ischemia as a consequence of COVID-19 infection. Am J Case Rep. 2020;21:e925753. http://doi.org/10.12659/AJCR.925753. PMid:32724028.

33 Hassan A, Desai P, Al Abady A, Baawain S. Superior mesenteric artery thrombosis for emergency laparotomy in COVID-19 patient: a case report. Oman Med J. 2021;36(5):e299. http://doi.org/10.5001/omj.2022.27. PMid:34631158.

34 Bannazadeh M, Tassiopoulos A, Koullias G. Acute superior mesenteric artery thrombosis seven days after discharge for novel coronavirus pneumonia. J Vasc Surg Cases Innov Tech. 2021;7(3):586-8. http://doi.org/10.1016/j.jvscit.2020.12.002. PMid:33623835.

35 Azouz E, Yang S, Monnier-Cholley L, Arrivé L. Systemic arterial thrombosis and acute mesenteric ischemia in a patient with COVID-19. Intensive Care Med. 2020;46(7):1464-5. http://doi.org/10.1007/s00134-020-06079-2. PMid:32424482.

36 Ucpinar BA, Sahin C. Superior mesenteric artery thrombosis in a patient with COVID-19: a unique presentation. J Coll Physicians Surg Pak. 2020;30(10):112-4. PMid:33115582.

37 Dinoto E, Ferlito F, La Marca MA, Mirabella D, Bajardi G, Pecoraro F. Staged acute mesenteric and peripheral ischemia treatment in COVID-19 patient: case report. Int J Surg Case Rep. 2021;84:106105. http://doi.org/10.1016/j.ijscr.2021.106105. PMid:34119938.

38 Macedo VSO, Moreira GB, Albuquerque ACF, Oliveira SCS, Esmeraldo MA, Barbosa FCB. Late mesenteric ischemia after Sars-Cov-2 infection: case report. J Vasc Bras. 2021;20:e20200105. http://doi.org/10.1590/1677-5449.200105. PMid:34093678.

39 Balani P, Bhuiyan AS, Dalal VN, Maheshwari GS. Early detection and successful management of acute mesenteric ischaemia in symptomatic COVID-19 patient. Indian J Surg. 2022;84(1):209-11. http://doi.org/10.1007/s12262-021-02839-6. PMid:33867749.

40 Asghari A, Adeli SH, Vafaeimanesh J, Bagheri H, Riahi M, Mirdamadi M. Intestinal ischemia due to mesenteric vascular thrombosis in a patient with positive SARS-Cov-2 RNA without primary pulmonary symptom: a case report. Middle East J Dig Dis. 2021;13(1):75-9. http://doi.org/10.34172/mejdd.2021.208. PMid:34712443.

41 Abeysekera KW, Karteszi H, Clark A, Gordon FH. Spontaneous portomesenteric thrombosis in a non-cirrhotic patient with SARS-CoV-2 infection. BMJ Case Rep. 2020;13(12):e238906. http://doi.org/10.1136/bcr-2020-238906. PMid:33371000.

42 Kukreja Y, Mohanty Z, Kumar S, Tripathy S. Mesenteric ischemia in a patient with COVID-19 infection. Mod Med. 2021;28(1):89-91. http://doi.org/10.31689/rmm.2021.28.1.89.

43 Lari E, Lari A, AlQinai S, et al. Severe ischemic complications in COVID-19: a case series. Int J Surg Case Rep. 2020;75:131-5. http://doi.org/10.1016/j.ijscr.2020.09.009. PMid:32934901.

44 Mir MZ, Mashhadi A, Jahantigh M, Seyedi SJ. Bowel necrosis associated with COVID-19 pneumonia: a report of two cases. Radiol Case Rep. 2021;16(4):819-23. http://doi.org/10.1016/j.radcr.2021.01.043. PMid:33520046.

45 Rodriguez-Nakamura RM, Gonzalez-Calatayud M, Martinez Martinez AR. Acute mesenteric thrombosis in two patients with COVID-19: two cases report and literature review. Int J Surg Case Rep. 2020;76:409-14. http://doi.org/10.1016/j.ijscr.2020.10.040. PMid:33083204.

46 Sehhat S, Talebzadeh H, Hakamifard A, et al. Acute mesenteric ischemia in a patient with COVID-19: a case report. Arch Iran Med. 2020;23(9):639-43. http://doi.org/10.34172/aim.2020.77. PMid:32979913.

47 Singh B, Mechineni A, Kaur P, et al. Acute intestinal ischemia in a patient with COVID-19 infection. Korean J Gastroenterol. 2020;76(3):164-6. http://doi.org/10.4166/kjg.2020.76.3.164. PMid:32969365.

48 Tripolino C, Pizzini AM, Zaccaroni S, et al. Is SARS-CoV-2 infection an emerging risk factor for splanchnic venous thrombosis? Clin Hemorheol Microcirc. 2021;79(2):347-55. http://doi.org/10.3233/CH-211256. PMid:34511494.

49 Ignat M, Philouze G, Aussenac-Belle L, et al. Small bowel ischemia and SARS-CoV-2 infection: an underdiagnosed distinct clinical entity. Surgery. 2020;168(1):14-6. http://doi.org/10.1016/j.surg.2020.04.035. PMid:32473831.

50 Strauss SA, Seo C, Carrier M, Jetty P. From cellular function to global impact: the vascular perspective on COVID-19. Can J Surg. 2020;64(3):E289-97. http://doi.org/10.1503/cjs.023820. PMid:33978563.

51 Guillet H, Gallet R, Pham V, et al. Clinical spectrum of ischaemic arterial diseases associated with COVID-19: a series of four illustrative cases. Eur Heart J Case Rep. 2021;5(1):a488. http://doi.org/10.1093/ehjcr/ytaa488. PMid:33542975.

52 Dane B, Smereka P, Wain R, Kim D, Katz D. Hypercoagulability in patients with coronavirus disease (COVID-19): identification of arterial and venous thromboembolism in the abdomen, pelvis, and lower extremities. AJR Am J Roentgenol. 2021;216(1):104-5. http://doi.org/10.2214/AJR.20.23617. PMid:32603220.

53 Ali Ahmed SM, Robinson CS, Sharmila DN, Balaji SK, Yalamuru SR. Peripheral vascular system thrombosis and COVID-19: a chilling revelation. Indian J Vasc Endovasc Surg. 2021;8(3):208-12. http://doi.org/10.4103/ijves.ijves_150_20.

54 Cheruiyot I, Kipkorir V, Ngure B, Misiani M, Munguti J, Ogeng’o J. Arterial thrombosis in coronavirus disease 2019 patients: a rapid systematic review. Ann Vasc Surg. 2021;70:273-81. http://doi.org/10.1016/j.avsg.2020.08.087. PMid:32866574.

55 Keshavarz P, Rafiee F, Kavandi H, Goudarzi S, Heidari F, Gholamrezanezhad A. Ischemic gastrointestinal complications of COVID-19: a systematic review on imaging presentation. Clin Imaging. 2021;73:86-95. http://doi.org/10.1016/j.clinimag.2020.11.054. PMid:33341452.

56 Omar SF, Habib RM, Motawea AM. Radiological findings of COVID-19-related thromboembolic complications. Egypt J Radiol Nucl Med. 2021;52(1):99. http://doi.org/10.1186/s43055-021-00446-9.

57 Pirola L, Palermo A, Mulinacci G, et al. Acute mesenteric ischemia and small bowel imaging findings in COVID-19: a comprehensive review of the literature. World J Gastrointest Surg. 2021;13(7):702-16. http://doi.org/10.4240/wjgs.v13.i7.702. PMid:34354803.

58 Singh B, Kaur P, Maroules M. Splanchnic vein thrombosis in COVID-19: a review of literature. Dig Liver Dis. 2020;52(12):1407-9. http://doi.org/10.1016/j.dld.2020.09.025. PMid:33067157.

59 Hmoud B, Singal AK, Kamath PS. Mesenteric venous thrombosis. J Clin Exp Hepatol. 2014;4(3):257-63. http://doi.org/10.1016/j.jceh.2014.03.052. PMid:25755568.

60 Guan WJ, Ni Z, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382(18):1708-20. http://doi.org/10.1056/NEJMoa2002032. PMid:32109013.

61 Lee TH, Lee JS, Jo Y, et al. Superior mesenteric artery syndrome: where do we stand today? J Gastrointest Surg. 2012;16(12):2203-11. http://doi.org/10.1007/s11605-012-2049-5. PMid:23076975.

62 Associação Médica Brasileira – AMB. Diretrizes sobre diagnóstico, prevenção e tratamento de complicações tromboembólicas na COVID-19 [Internet]. São Paulo: AMB; 2022 [cited 2022 Sept 19]. https://amb.org.br/wp-content/uploads/2021/04/DIAGN%C3%93STICO-PREVEN%C3%87%C3%83O-E-TRATAMENTO-DE-COMPLICA%C3%87%C3%95ES-TROMBOEMB%C3%93LICAS-NA-COVID-19-FINAL-01.07.2020.pdf

63 Cuker A, Tseng EK, Nieuwlaat R, et al. American Society of Hematology living guidelines on the use of anticoagulation for thromboprophylaxis in patients with COVID-19: July 2021 update on postdischarge thromboprophylaxis. Blood Adv. 2022;6(2):664-71. http://doi.org/10.1182/bloodadvances.2021005945. PMid:34727173.

64 Adams RB. Enterectomy. In: Evans SRT, editor. Surgical pitfalls: prevention and management [Internet]. Washington: Georgetown University Medical Center; 2009; p. 237-46 [cited 2022 Nov 19]. https://www.sciencedirect.com/science/article/pii/B978141602951950030X

65 Al-Taee A, Ahmed Z, Dhedhi A, Giacaman M. Mesenteric venous thrombosis masquerading as small bowel obstruction. ACG Case Rep J. 2019;6(9):e00210. http://doi.org/10.14309/crj.0000000000000210. PMid:31750378.

66 Bonanad C, García-Blas S, Tarazona-Santabalbina F, et al. The effect of age on mortality in patients with COVID-19: a meta-analysis with 611,583 subjects. J Am Med Dir Assoc. 2020;21(7):915-8. http://doi.org/10.1016/j.jamda.2020.05.045. PMid:32674819.

67 Oldenburg WA, Lau LL, Rodenberg TJ, Edmonds HJ, Burger CD. Acute mesenteric ischemia: a clinical review. Arch Intern Med. 2004;164(10):1054-62. http://doi.org/10.1001/archinte.164.10.1054. PMid:15159262.

68 Warkentin TE, Kaatz S. COVID-19 versus HIT hypercoagulability. Thromb Res. 2020;196:38-51. http://doi.org/10.1016/j.thromres.2020.08.017. PMid:32841919.

69 Garnier M, Curado A, Billoir P, Barbay V, Demeyere M, Dacher JN. Imaging of Oxford/AstraZeneca® COVID-19 vaccine-induced immune thrombotic thrombocytopenia. Diagn Interv Imaging. 2021;102(10):649-50. http://doi.org/10.1016/j.diii.2021.04.005. PMid:33962903.

70 Aladdin Y, Algahtani H, Shirah B. Vaccine-induced immune thrombotic thrombocytopenia with disseminated intravascular coagulation and death following the ChAdOx1 nCoV-19 vaccine. J Stroke Cerebrovasc Dis. 2021;30(9):105938. http://doi.org/10.1016/j.jstrokecerebrovasdis.2021.105938. PMid:34171649.

71 Umbrello M, Brena N, Vercelli R, et al. Successful treatment of acute spleno-porto-mesenteric vein thrombosis after ChAdOx1 nCoV-19 vaccine: a case report. J Crit Care. 2021;65:72-5. http://doi.org/10.1016/j.jcrc.2021.05.021. PMid:34111682.

72 Graça LL, Amaral MJ, Serôdio M, Costa B. Extensive thrombosis after COVID-19 vaccine: cause or coincidence? BMJ Case Rep. 2021;14(8):e244878. http://doi.org/10.1136/bcr-2021-244878. PMid:34400433.

73 Asmat H, Fayeye F, Alshakaty H, Patel J. A rare case of COVID-19 vaccine-induced thrombotic thrombocytopaenia (VITT) involving the veno-splanchnic and pulmonary arterial circulation, from a UK district general hospital. BMJ Case Rep. 2021;14(9):e244223. http://doi.org/10.1136/bcr-2021-244223. PMid:34535492.
 


Submitted date:
07/24/2024

Accepted date:
10/17/2024

Sociedade Brasileira de Angiologia e Cirurgia Vascular (SBACV)"> Sociedade Brasileira de Angiologia e Cirurgia Vascular (SBACV)">
67a4d932a9539561a47ccc46 jvb Articles
Links & Downloads

J Vasc Bras

Share this page
Page Sections