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Case report

Spontaneous retroperitoneal hematoma in a COVID-19 patient

Ana Sekulić1,2, Olivera Marinković1, Davor Mrda1, Borislav Tošković1,2, Marija Zdravković1,2, Predrag Đuran1
  • University Hospital Medical Center Bežanijska kosa, Belgrade, Serbia
  • Faculty of Medicine, University of Belgrade, Belgrade, Serbia

ABSTRACT

Introduction: The infection caused by the SARS-CoV-2 virus is known to cause a hypercoagulable condition resulting in acute thrombotic events. Thromboembolic events occur in as many as 21.0% of cases with a mortality rate of about 74.0% in persons infected with COVID-19. Anticoagulant therapy is used in severe COVID-19 infections in order to prevent thrombosis and has been shown to reduce mortality. The use of anticoagulants is not without risks. Bleeding complications can range from mild to severe or even life-threatening, such as retroperitoneal bleeding into the psoas muscle.

Case report: We present a case of a patient who developed a complication of bleeding into the retroperitoneal space during the treatment of bilateral bronchopneumonia caused by the SARS-CoV-2 virus. After the diagnosis was established, on the basis of a clinical examination, laboratory and radiological examinations, and after initial conservative treatment at the UHMC Bežanijska kosa, the patient underwent embolization of the left lumbar arteries from the right inguinal fossa, during procedural analgosedation. After the radiological procedure, the recovery was satisfactory, but due to the impossibility of resorption of an encapsulated hematoma with a zone of central necrosis, a mini left lumbotomy and evacuation of the hematoma were performed. The patient was discharged from the hospital on the 23rd day of admission in stable general condition.

Conclusion: The effect of anticoagulant therapy, especially in patients with existing risk factors, early diagnosis, and prompt therapy of spontaneous retroperitoneal hematomas is imperative to reduce mortality from this severe complication, in patients with the COVID-19 infection.


INTRODUCTION

Since the beginning of the pandemic of the SARS-CoV-2 virus, on December 12, 2019, until now, the COVID-19 disease has shown many different clinical manifestations. Respiratory symptoms and fever are common in most patients infected with SARS-CoV-2. However, other systems may be involved as well [1]. It is known that COVID-19 causes the hypercoagulable state, resulting in acute thrombotic events, including venous thromboembolism, acute myocardial infarction, acute stroke, and acute ischemia of the extremities. Thromboembolic events occur in as many as 21.0% of patients, with a mortality rate of around 74.0% in COVID-19 patients [2].

Anticoagulants are used in severe forms of the COVID-19 infection for preventing thrombosis and they have proven to reduce mortality. At the moment, in Serbia, the 12th version of the Protocol for Treating Patients with the COVID-19 Infection is in use and it clearly defines indications for the application of anticoagulant therapy in prophylactic and therapeutic doses (Table 1).

The application of anticoagulants is not without risk. Complications of bleeding may vary from mild to severe or even life-threatening. Retroperitoneal bleeding into the psoas muscle may be lethal, due to profuse bleeding that occurs before symptoms appear. It is very important to be cautious in the diagnosis and treatment of this complication. Clinically, retroperitoneal bleeding can manifest in the form of hypotension, abdominal pain or a drop in hemoglobin. Monitoring the effect of anticoagulants is an imperative for decreasing the risk of hemorrhagic events. Hemodynamically unstable patients on anticoagulant therapy with unpredictable large hematoma of the soft tissues may be treated with arterial embolization, as it is a minimally invasive procedure with a rapid therapeutic effect, as compared to surgical treatment.

Since the beginning of the COVID-19 pandemic until now, at the University Hospital Medical Center Bežanijska kosa, a total of approximately 20 arterial embolization procedures was performed, in patients with diagnosed retroperitoneal hematoma resulting from the COVID-19 infection. In this case report, we present the case of a patient who, during treatment of bilateral pneumonia caused by SARS-CoV-2, developed the complication of bleeding into the retroperitoneal space.

CASE REPORT

Due to a large retroperitoneal hematoma on the left side, a 65-year-old male patient was admitted to our hospital, UHMC Bežanijska kosa, from the temporary COVID-19 hospital at the Belgrade Fair, where he had been treated for 21 days for bilateral pneumonia caused by SARS-CoV-2. The patient had previously been on antihypertensive and oral anticoagulant therapy, due to a triple bypass and an aortic valve replacement. During the treatment of COVID-19 pneumonia, he was on low molecular heparin treatment, in therapeutic doses. The patient had previously displayed an allergy to penicillin.

Table 1. Protocol for Treating Patients with COVID-19, Version 12

07t01

At admission, the patient was conscious, communicative, oriented, afebrile, and his skin and mucosa were pale. He was breathing on his own, and with the help of an oxygen mask with a 10 L/min flow, he was achieving a satisfactory partial pressure of oxygen. The monitoring of hemodynamic parameters revealed hypotension with sinus tachycardia. The patient had a preserved satisfactory spontaneous 24-hour urine output. Physical examination revealed large hematomas in the lumbar region and significant swelling of the lower extremities. The following signs and symptoms were also present: severe pain in the side, hypovolemia, and a palpable mass in the abdomen. In terms of antibiotic therapy, treatment with meropenem, vancomycin, and metronidazole was continued, together with standard cardiological therapy. the patient was X-rayed while lying down in the AP position.

The chest X-ray showed evidence of previous median sternotomy, a visible shadow of the artificial valve, and a central venous catheter (CVC) placed in the right internal jugular vein (vena jugularis interna dextra). In a smaller portion of the pulmonary parenchyma, fibrous lesions were registered, as well as bilateral pleural effusions, the larger one positioned on the left side (Figure 1).

07f01

Figure 1. Chest X-ray on admission to hospital In a smaller part of the pleural parenchyma fibrous changes are visible. Bilateral pleural effusions are present, the larger one can be seen on the left

CT finding: perihepatically, subhepatically, perisplenically, subsplenically, bilaterally pericollically interstitially, in the rectovesical space – a large quantity of free fluid with a density of 20 H; in the left hemiabdomen, pericollically – a heterodense, predominantly hypodense tumor mass with central signs of necrosis, clear margins, an approximate diameter of 143x164x243 mm, and a density of 40 H (Figure 2).

07f02

Figure 2. CT scan of the abdomen with a large retroperitoneal hematoma on the left In the left hemiabdomen, a heterodense, predominantly hypodense tumor mass with central signs of necrosis is present, clearly limited to an approximate diameter of 143x164x243 mm, and with a density of up to 40 HU

Blood work revealed marked anemia, thrombocytopenia, leukocytosis with neutrophilia and lymphopenia. The CRP level was 38.4 mg/L. Biochemical analyses showed the following: hypoproteinemia, increased levels of nitrogen compounds and transaminases, normal electrolyte status. The D-dimer was elevated and amounted to 1,324 ng/mL.

After brief and appropriate preparation, with the patient under procedural analgosedation, an interventional therapeutic procedure was performed – embolization of the lumbar arteries on the left, approached from the right inguinal fossa, by puncturing the right femoral artery (arteria femoralis communis - AFC), applying the Seldinger technique. After the abdominal aorta was catheterized, only two lumbar arteries were angiographically detected on the left side. The first infrarenal lumbar artery was entered via catheter. Upon angiography, several smaller “blush” phenomena were detected. The artery was closed with one package of 600 μm HydroPearl embolization particles and one package of 400 μm HydroPearl embolization particles. Then, selective embolization of the distal lumbar artery was performed, and, after the appropriate positioning of the catheter, this artery was closed with four packages of 600 μm HydroPearl embolization particles. Both arteries were closed until complete stasis of the contrast medium was achieved. The immediate effects of the embolization were satisfactory.

The procedure was completed without complications. During the procedure, the patient was under analgosedation, he was hemodynamically stable, tachycardic; he was receiving intravenous supplementation of the circulating volume through crystalloid solutions and transfusion of concentrated erythrocytes. After the procedure, the patient was returned to the intensive care unit, where treatment was continued. In the further course of recovery, the patient was hemodynamically stable, and breathing consciously. Blood work continued to show anemia, which was treated with transfusion of concentrated erythrocytes, and thrombocytopenia. The ROTEM test showed an insufficient platelet function; mild to medium hyperfibrinolysis was present; fibrinogenic activity was functional, as was the activity of plasma factors; D-dimer was rising, while AT III had normal values. Antibiotic treatment, according to the antibiogram, was continued. However, on the third day of treatment in our hospital, the patient developed diarrhea and Clostridium difficile was isolated. The antibiotic treatment was adjusted. Targeted peroral therapy with vancomycin and metronidazole was applied, in keeping with the national guidelines for treating the bacterium Clostridium difficile.

Laboratory analyses for this patient gradually improved, and, after the transfusion of blood and blood derivatives, the blood count was normalized; the platelet count rose; the D-dimer level decreased, which is why, on the sixth day after the procedure, a therapeutic dose of low molecular weight heparin (LMWH) was introduced. The patient was on combined enteral hyperproteic and parenteral nutrition. He was stabilized in terms of electrolytes and the metabolism and had satisfactory glucoregulation. Early rehabilitation treatment was carried out with the patient, and K-tape was used for large hematomas on the abdomen and legs, after retroperitoneal hematoma. In this phase, the patient regained flexion and extension of the hips and knees, which he did not have previously, due to excessive swelling of the extremities. Exercises in bed were continued as well as exercises of verticalization. In stable general condition, the patient was transferred to a surgical ward for further treatment, seven days after admission.

While on the ward, the patient still had high levels of CRP and D-dimer. Other laboratory analyses were without significant deviation from the reference ranges.

Repeated multidetector computed tomography (MDCT) imaging of the thorax, abdomen, and the lesser pelvis, on the eleventh and eighteenth day of hospitalization, revealed a persisting hematoma, 26x17x12 mm in diameter, in the left retroperitoneum, distally to the kidney. It was imbibing the left psoas muscle and could not be separated from it. The hematoma did not display signs of active bleeding and was pushing the abdominal structures medially and towards the front. There was no ascites. There were linear fibrous lesions consistent with resorptive scarring following viral pneumonia. Pleural effusion was present bilaterally, with lesser compressive areas of atelectasis.

On the nineteenth day of hospitalization, indication for surgical treatment was established. The following planned surgical procedure was carried out under general endotracheal anesthesia: After the surgical field was prepared, left mini lumbotomy was carried out. After passing though the muscular layer, a massive encapsulated retroperitoneal hematoma was encountered. Upon penetration of the capsule, evacuation of a large quantity of coagulum and old blood was performed. A drain was then placed, and the surgical wound was closed by anatomical layers.

Postoperative recovery was uneventful, without surgical complications. The wound healed per primam intentionem, and the drain was removed. The patient was discharged to recover at home on the twenty-third day of hospitalization, in good general condition, afebrile, hemodynamically stable, and with normal bowel function.

DISCUSSION

Although patients with severe form of COVID-19 tend to develop thrombotic complications, they can also have bleeding as a complication of the disease [3]. Coagulopathy in COVID-19 is significantly different from coagulopathy occurring in severe sepsis of other etiology. A combination of thrombocytopenia, prolonged prothrombin time (PT), and elevated D-dimer may indicate disseminated intravascular coagulopathy (DIC), although it differs from DIC seen in sepsis of other etiology. In sepsis, thrombocytopenia is more pronounced, while the level of D-dimer does not reach such high values as has been noted in COVID-19 patients. According to the International Society on Thrombosis and Haemostasis DIC score, most COVID-19 patients would not be classified as DIC [4]. What we know, at the moment, is that pulmonary thrombi in COVID-19 develop as the result of vascular damage related to viral infection and severe inflammation. This belief is substantiated by the levels of D-dimer and inflammatory markers, as well as by the elevation of multiple thrombolytic factors, such as IL-6 and antiphospholipid antibodies, in all of the patients. Autopsies of patients who had died of COVID-19 have revealed severe injury to the blood vessel endothelium, widespread thrombosis with microangiopathy and alveolar capillary microthrombi, as well as increased angiogenesis [5].

The frequency of bleeding is far lesser and is usually connected to the application of antithrombotic agents and anticoagulants. The total percentage of patients with complications of bleeding ranges from 4.8% to 8.0%, of whom approximately 3.5% had major bleeding [6]. However, Erdinc and Raina described a COVID-19 patient who developed spontaneous retroperitoneal hematoma (SRH) without receiving anticoagulant therapy [7]. The exact frequency of spontaneous retroperitoneal hematomas in COVID-19 patients remains unclear. Initially, a small number of patients was reported – 3.8 cases per 1,000 admissions to intensive care units (ICU) [8]. While Italian authors, participants in the Recovery study, reported 7.6 cases per 1,000 hospitalizations [9]. Bearing in mind the high mortality rate, doctors should closely monitor for first signs of illness, primarily for thrombocytopenia (platelet count <150×103 cells/mL) and for elevated D-dimer levels (>2.5 mg/mL). Monitoring the effect of anticoagulants is imperative for decreasing the risk of hemorrhagic events [10]. Risk factors for spontaneous retroperitoneal hematoma are as follows: anticoagulant therapy, older age, obesity, underlying comorbidities – most commonly hypertension and diabetes mellitus, as well as hemodialysis. Our patient had multiple risk factors – age (65 years); the fact that due to the underlying comorbidity he was on standard oral anticoagulant therapy; bronchopneumonia caused by COVID-19; therapeutic dosage of LMWH; bacterial intrahospital superinfection, infection caused by Clostridium difficile.

While the exact pathogenesis and pathophysiology of retroperitoneal bleeding is unknown, it is assumed retroperitoneal microvascular atherosclerosis may increase susceptibility to rupture, with the involvement of large blood vessels. Anticoagulant therapy and microtraumas, such as coughing and vomiting, can also lead to retroperitoneal bleeding [11]. The SARS-CoV-2 itself has an affinity for the ACE2 receptor in endothelial cells, which may directly damage blood vessels and cause bleeding. Conversely, dysregulation of the renin-angiotensin-aldosterone system, may contribute to elevated blood pressure, causing hemorrhagic events. The psoas muscle can accumulate up to ten times its own volume, which is clinically significant, as patients may lose a large volume of blood without this being noticed, unless laboratory analyses are performed and monitored regularly, and physical examinations are carried out routinely. Clinically, retroperitoneal bleeding can manifest as hypotension, abdominal pain, or a drop in the hemoglobin level [12],[13]. Our patient was hypotensive, tachycardic, he was complaining of pain in the left lumbar region, where a large hematoma was visible. The dominant findings in his blood work were, as follows: anemia, with a drop in the hemoglobin (Hb) level to 81 g/L; thrombocytopenia, amounting to 75x109 /L; and a high level of D-dimer, amounting to 1,324 ng/L (cut-off – 500 ng/L).

MDCT imaging of the abdomen and the lesser pelvis is an initial diagnostic procedure applied when there is suspicion of retroperitoneal bleeding. Initial treatment begins with discontinuing anticoagulant therapy, performing transfusion of blood and blood derivatives, providing blood volume supplementation through solutions administered via infusion therapy, and other measures of hemodynamic support and oxygenotherapy. Hemodynamically unstable patients on anticoagulant therapy with unpredictable large hematomas of the soft tissues may be treated by arterial embolization, as this is a minimally invasive procedure with rapid therapeutic effect, as compared to surgical treatment. When active bleeding is discovered in the psoas muscle, arterial embolization of the third and fourth lumbar artery is justified, which poses a technical challenge, as it requires selective catheterization of the artery, embolization, as well as assessment after embolization, in order to confirm the success of the procedure [14]. In our patient, embolization of lumbar arteries on the left was successfully performed.

Analysis of available literature shows that precedence is given to conservative treatment, in combination with the interventional radiological procedure of the embolization of damaged blood vessels. It seems that surgery is indicated when the patient remains unstable, despite the application of measures of intensive reanimation, in cases when interventional radiology is not successful or is not available, or in case of the development of compartment syndrome [15]. In our case, after radiological therapy and conservative treatment, the patient was operated on with the application of mini-laparotomy for the purpose of evacuating a necrotizing hematoma, which could not be reabsorbed spontaneously.

CONCLUSION

The application of anticoagulant therapy may cause severe hemorrhagic complications in COVID-19 patients. Monitoring the effect of anticoagulant therapy, especially in patients with risk factors, early diagnostics, as well as timely treatment of spontaneous retroperitoneal hematomas, is imperative for decreasing mortality from this severe complication in COVID-19 patients.

LIST OF ABBREVIATIONS AND ACRONYMS

SARS-CoV-2 - severe acute respiratory syndrome coronavirus 2
COVID-19 - coronavirus disease of 2019
DIC – disseminated intravascular coagulation
CT – computerized tomography
SpO2 – oxygen saturation of the patient’s blood
CVC – central venous catheter
ROTEM – rotational thromboelastometry
LMWH – low molecular weight heparin
CRP – C-reactive protein

  • Conflict of interest:
    None declared.

Informations

Volume 2 No 4

December 2021

Pages 377-385
  • Keywords:
    retroperitoneal hematoma, COVID-19, arterial embolization
  • Received:
    16 November 2021
  • Revised:
    26 November 2021
  • Accepted:
    28 November 2021
  • Online first:
    13 December 2021
  • DOI:
  • Cite this article:
    Sekulić A, Marinković O, Mrda D, Tošković B, Zdravković M, Đuran P. Spontaneous retroperitoneal hematoma in a COVID-19 patient. Serbian Journal of the Medical Chamber. 2021;2(4):377-85. doi: 10.5937/smclk2-34956
Corresponding author

Ana Sekulić
University Hospital Medical Center "Bežanijska kosa"
Dr Žorža Matea Street, 11000 Belgrade, Serbia
E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.


  • 1. Scialpi M, Russo P, Piane E, Gallo E, Scalera GB. First case of retroperitoneal hematoma in COVID-19. Turk J Urol. 2020 Sep;46(5):407-9. doi: 10.5152/tud.2020.20302.[CROSSREF]

    2. Malas MB, Naazie IN, Elsayed N, Mathlouthi A, Marmor R, Clary B. Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: A systematic review and meta-analysis. EClinicalMedicine. 2020 Dec;29:100639. doi: 10.1016/j.eclinm.2020.100639.[CROSSREF]

    3. Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020 Jul 23;136(4):489-500. doi: 10.1182/blood.2020006520.[CROSSREF]

    4. Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol. 2020 Jun;7(6):e438-e40. doi: 10.1016/S2352-3026(20)30145-9.[CROSSREF]

    5. Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, et al. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med. 2020 Jul 9;383(2):120-8. doi: 10.1056/NEJMoa2015432.[CROSSREF]

    6. Shah A, Donovan K, McHugh A, Pandey M, Aaron L, Bradbury CA, et al. Thrombotic and haemorrhagic complications in critically ill patients with COVID-19: a multicentre observational study. Crit Care. 2020 Sep 18;24(1):561. doi: 10.1186/s13054-020-03260-3.[CROSSREF]

    7. Erdinc B, Raina JS. Spontaneous Retroperitoneal Bleed Coincided With Massive Acute Deep Vein Thrombosis as Initial Presentation of COVID-19. Cureus. 2020 Aug 15;12(8):e9772. doi: 10.7759/cureus.9772.[CROSSREF]

    8. Artzner T, Clere-Jehl R, Schenck M, Greget M, Merdji H, De Marini P, et al. Spontaneous ilio-psoas hematomas complicating intensive care unit hospitalizations. PLoS One. 2019 Feb 22;14(2):e0211680. doi: 10.1371/journal.pone.0211680.[CROSSREF]

    9. Vergori A, Pianura E, Lorenzini P, D'Abramo A, Di Stefano F, Grisetti S, et al.; ReCOVeRI Study Group. Spontaneous ilio-psoas haematomas (IPHs): a warning for COVID-19 inpatients. Ann Med. 2021 Dec;53(1):295-301. doi: 10.1080/07853890.2021.1875498.[CROSSREF]

    10. Patel I, Akoluk A, Douedi S, Upadhyaya V, Mazahir U, Costanzo E, et al. Life-Threatening Psoas Hematoma due to Retroperitoneal Hemorrhage in a COVID-19 Patient on Enoxaparin Treated with Arterial Embolization: A Case Report. J Clin Med Res. 2020 Jul;12(7):458-61. doi: 10.14740/jocmr4256.[CROSSREF]

    11. Llitjos JF, Daviaud F, Grimaldi D, Legriel S, Georges JL, Guerot E, et al. Ilio-psoas hematoma in the intensive care unit: a multicentric study. Ann Intensive Care. 2016 Dec;6(1):8. doi: 10.1186/s13613-016-0106-z.[CROSSREF]

    12. Surani S, Estement B, Manchandan S, Sudhakaran S, Varon J. Spontaneous extraperitoneal lumbar artery hemorrhage. J Emerg Med. 2011 Jun;40(6):e111-4. doi: 10.1016/j.jemermed.2008.01.029.[CROSSREF]

    13. Qanadli SD, El Hajjam M, Mignon F, Bruckert F, Chagnon S, Lacombe P. Life-threatening spontaneous psoas haematoma treated by transcatheter arterial embolization. Eur Radiol. 1999;9(6):1231-4. doi: 10.1007/s003300050824.[CROSSREF]

    14. Amole AO, Kathuria MK, Ozkan OS, Gill AS, Ozkan EO. Lumbar artery laceration with retroperitoneal hematoma after placement of a G-2 inferior vena cava filter. Cardiovasc Intervent Radiol. 2008 Nov-Dec;31(6):1257-9. doi: 10.1007/s00270-008-9365-x.[CROSSREF]

    15. Chan YC, Morales JP, Reidy JF, Taylor PR. Management of spontaneous and iatrogenic retroperitoneal haemorrhage: conservative management, endovascular intervention or open surgery? Int J Clin Pract. 2008 Oct;62(10):1604- 13. doi: 10.1111/j.1742-1241.2007.01494.x.[CROSSREF]


REFERENCES

1. Scialpi M, Russo P, Piane E, Gallo E, Scalera GB. First case of retroperitoneal hematoma in COVID-19. Turk J Urol. 2020 Sep;46(5):407-9. doi: 10.5152/tud.2020.20302.[CROSSREF]

2. Malas MB, Naazie IN, Elsayed N, Mathlouthi A, Marmor R, Clary B. Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: A systematic review and meta-analysis. EClinicalMedicine. 2020 Dec;29:100639. doi: 10.1016/j.eclinm.2020.100639.[CROSSREF]

3. Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020 Jul 23;136(4):489-500. doi: 10.1182/blood.2020006520.[CROSSREF]

4. Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol. 2020 Jun;7(6):e438-e40. doi: 10.1016/S2352-3026(20)30145-9.[CROSSREF]

5. Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, et al. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med. 2020 Jul 9;383(2):120-8. doi: 10.1056/NEJMoa2015432.[CROSSREF]

6. Shah A, Donovan K, McHugh A, Pandey M, Aaron L, Bradbury CA, et al. Thrombotic and haemorrhagic complications in critically ill patients with COVID-19: a multicentre observational study. Crit Care. 2020 Sep 18;24(1):561. doi: 10.1186/s13054-020-03260-3.[CROSSREF]

7. Erdinc B, Raina JS. Spontaneous Retroperitoneal Bleed Coincided With Massive Acute Deep Vein Thrombosis as Initial Presentation of COVID-19. Cureus. 2020 Aug 15;12(8):e9772. doi: 10.7759/cureus.9772.[CROSSREF]

8. Artzner T, Clere-Jehl R, Schenck M, Greget M, Merdji H, De Marini P, et al. Spontaneous ilio-psoas hematomas complicating intensive care unit hospitalizations. PLoS One. 2019 Feb 22;14(2):e0211680. doi: 10.1371/journal.pone.0211680.[CROSSREF]

9. Vergori A, Pianura E, Lorenzini P, D'Abramo A, Di Stefano F, Grisetti S, et al.; ReCOVeRI Study Group. Spontaneous ilio-psoas haematomas (IPHs): a warning for COVID-19 inpatients. Ann Med. 2021 Dec;53(1):295-301. doi: 10.1080/07853890.2021.1875498.[CROSSREF]

10. Patel I, Akoluk A, Douedi S, Upadhyaya V, Mazahir U, Costanzo E, et al. Life-Threatening Psoas Hematoma due to Retroperitoneal Hemorrhage in a COVID-19 Patient on Enoxaparin Treated with Arterial Embolization: A Case Report. J Clin Med Res. 2020 Jul;12(7):458-61. doi: 10.14740/jocmr4256.[CROSSREF]

11. Llitjos JF, Daviaud F, Grimaldi D, Legriel S, Georges JL, Guerot E, et al. Ilio-psoas hematoma in the intensive care unit: a multicentric study. Ann Intensive Care. 2016 Dec;6(1):8. doi: 10.1186/s13613-016-0106-z.[CROSSREF]

12. Surani S, Estement B, Manchandan S, Sudhakaran S, Varon J. Spontaneous extraperitoneal lumbar artery hemorrhage. J Emerg Med. 2011 Jun;40(6):e111-4. doi: 10.1016/j.jemermed.2008.01.029.[CROSSREF]

13. Qanadli SD, El Hajjam M, Mignon F, Bruckert F, Chagnon S, Lacombe P. Life-threatening spontaneous psoas haematoma treated by transcatheter arterial embolization. Eur Radiol. 1999;9(6):1231-4. doi: 10.1007/s003300050824.[CROSSREF]

14. Amole AO, Kathuria MK, Ozkan OS, Gill AS, Ozkan EO. Lumbar artery laceration with retroperitoneal hematoma after placement of a G-2 inferior vena cava filter. Cardiovasc Intervent Radiol. 2008 Nov-Dec;31(6):1257-9. doi: 10.1007/s00270-008-9365-x.[CROSSREF]

15. Chan YC, Morales JP, Reidy JF, Taylor PR. Management of spontaneous and iatrogenic retroperitoneal haemorrhage: conservative management, endovascular intervention or open surgery? Int J Clin Pract. 2008 Oct;62(10):1604- 13. doi: 10.1111/j.1742-1241.2007.01494.x.[CROSSREF]

1. Scialpi M, Russo P, Piane E, Gallo E, Scalera GB. First case of retroperitoneal hematoma in COVID-19. Turk J Urol. 2020 Sep;46(5):407-9. doi: 10.5152/tud.2020.20302.[CROSSREF]

2. Malas MB, Naazie IN, Elsayed N, Mathlouthi A, Marmor R, Clary B. Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: A systematic review and meta-analysis. EClinicalMedicine. 2020 Dec;29:100639. doi: 10.1016/j.eclinm.2020.100639.[CROSSREF]

3. Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020 Jul 23;136(4):489-500. doi: 10.1182/blood.2020006520.[CROSSREF]

4. Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol. 2020 Jun;7(6):e438-e40. doi: 10.1016/S2352-3026(20)30145-9.[CROSSREF]

5. Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, et al. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med. 2020 Jul 9;383(2):120-8. doi: 10.1056/NEJMoa2015432.[CROSSREF]

6. Shah A, Donovan K, McHugh A, Pandey M, Aaron L, Bradbury CA, et al. Thrombotic and haemorrhagic complications in critically ill patients with COVID-19: a multicentre observational study. Crit Care. 2020 Sep 18;24(1):561. doi: 10.1186/s13054-020-03260-3.[CROSSREF]

7. Erdinc B, Raina JS. Spontaneous Retroperitoneal Bleed Coincided With Massive Acute Deep Vein Thrombosis as Initial Presentation of COVID-19. Cureus. 2020 Aug 15;12(8):e9772. doi: 10.7759/cureus.9772.[CROSSREF]

8. Artzner T, Clere-Jehl R, Schenck M, Greget M, Merdji H, De Marini P, et al. Spontaneous ilio-psoas hematomas complicating intensive care unit hospitalizations. PLoS One. 2019 Feb 22;14(2):e0211680. doi: 10.1371/journal.pone.0211680.[CROSSREF]

9. Vergori A, Pianura E, Lorenzini P, D'Abramo A, Di Stefano F, Grisetti S, et al.; ReCOVeRI Study Group. Spontaneous ilio-psoas haematomas (IPHs): a warning for COVID-19 inpatients. Ann Med. 2021 Dec;53(1):295-301. doi: 10.1080/07853890.2021.1875498.[CROSSREF]

10. Patel I, Akoluk A, Douedi S, Upadhyaya V, Mazahir U, Costanzo E, et al. Life-Threatening Psoas Hematoma due to Retroperitoneal Hemorrhage in a COVID-19 Patient on Enoxaparin Treated with Arterial Embolization: A Case Report. J Clin Med Res. 2020 Jul;12(7):458-61. doi: 10.14740/jocmr4256.[CROSSREF]

11. Llitjos JF, Daviaud F, Grimaldi D, Legriel S, Georges JL, Guerot E, et al. Ilio-psoas hematoma in the intensive care unit: a multicentric study. Ann Intensive Care. 2016 Dec;6(1):8. doi: 10.1186/s13613-016-0106-z.[CROSSREF]

12. Surani S, Estement B, Manchandan S, Sudhakaran S, Varon J. Spontaneous extraperitoneal lumbar artery hemorrhage. J Emerg Med. 2011 Jun;40(6):e111-4. doi: 10.1016/j.jemermed.2008.01.029.[CROSSREF]

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