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Open Access

Serial rotational thromboelastography (ROTEM) in mechanically ventilated patients with COVID-19 demonstrates hypercoagulopathy despite therapeutic heparinization

James K Choi, Kartik Prabhakaran, Rifat Latifi, Abbas Smiley, Joshua Klein, Gary Lombardo, Peter Rhee
DOI: 10.1136/tsaco-2020-000603 Published 10 March 2022
James K Choi
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Kartik Prabhakaran
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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  • ORCID record for Kartik Prabhakaran
Rifat Latifi
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Abbas Smiley
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Joshua Klein
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Gary Lombardo
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Peter Rhee
Department of Surgery, Westchester Medical Center, Valhalla, New York, USA
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Figures

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  • Figure 1
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    Figure 1

    Rotational thromboelastography (ROTEM) and thromboembolic event timeline.

  • Figure 2
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    Figure 2

    (A and B) CTEX and IN and (C and D) CFTEX and IN for patients with and without coagulopathic complications. Outliers are represented by a circle (mild outlier) or an asterisk (severe outlier). CFT, clot formation time; CT, clotting time; EX, EXTEM; IN, INTEM.

  • Figure 3
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    Figure 3

    (A, B, and C) MCFEX, IN and FIB for patients with and without coagulopathic complications. Outliers are represented by a circle (mild outlier) or an asterisk (severe outlier). EX, EXTEM; FIB, FIBTEM; IN, INTEM; MCF, maximum clot firmness.

  • Figure 4
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    Figure 4

    (A and B) CTEX and IN and (C and D) CFTEX and IN for patients with and without heparin drip administration. Outliers are represented by a circle (mild outlier) or an asterisk (severe outlier). CFT, clot formation time; CT, clotting time; EX, EXTEM; IN, INTEM.

  • Figure 5
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    Figure 5

    (A, B, and C) MCFEX, IN and FIB for patients with and without heparin drip administration. Outliers are represented by a circle (mild outlier) or an asterisk (severe outlier). EX, EXTEM; FIB, FIBTEM; IN, INTEM; MCF, maximum clot firmness.

Tables

  • Figures
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  • Table 1

    Rotational thromboelastography parameters

    Clot initiationClotting time
    Clot kineticsClot formation time
    Clot strengthAmplitude at 10 minutes
    Maximum clot firmness
    FibrinolysisMaximum lysis
  • Table 2

    Patient demographics, admission vital signs, and presenting symptoms

    Demographics, n (%)
     Age, mean (SD)57.9 (14.4)
     Male16 (76.2)
     BMI kg/m2, mean (SD)32.3 (9.2)
     Mortality3 (14.3)
    Admission vitals, mean (SD)
     Temperature, °F99.6 (2.1)
     Pulse, beats per minute98.6 (25.1)
     RR, breaths per minute25.3 (8.8)
     O2 saturation (%)91.6 (6.3)
     Systolic, mm Hg132.6 (19.6)
     Diastolic, mm Hg75.6 (14.9)
    Symptoms, n (%)
     Febrile16 (76.2)
     Lethargy5 (23.8)
     Shortness of breath15 (71.4)
     Headache1 (4.8)
     Anorexia0 (0)
     Rhinorrhea0 (0)
     Sputum3 (14.3)
     Sore throat1 (4.8)
     Cough15 (71.4)
     Emesis1 (4.8)
     Myalgia2 (9.5)
     Diarrhea3 (14.3)
     Recent travel0 (0)
     Known sick contacts2 (9.5)
    Length of symptoms, mean days (SD)5.2 (3.1)
    • BMI, body mass index; RR, respiratory rate.

  • Table 3

    Acute phase reactants and coagulation markers

    Laboratory values, mean (SD)Reference rangeMean (SD)Peak, meanNo HC, mean (SD)
    n=14
    HC, mean (SD)
    n=7
    P value
    Prothrombin time, seconds9.8–12.012.7 (1.9)18.712.6 (1.6)13.0 (2.5)0.6
    Partial thromboplastin time, seconds25.0–32.036.3 (7.7)53.335.5 (8.4)38.1 (6.5)0.5
    INR1.2 (0.2)1.851.1 (0.1)1.2 (0.3)0.4
    Platelet count, k/mm3160–410181.2 (56.8)336.8178.9 (45.6)185.7 (78.9)0.8
    D-dimer, mg/L<0.5910.8 (6.4)24.710.9 (5.6)10.4 (8.4)0.8
    Ferritin, µg/L18.0–370.01743.1 (1568.4)5268.91396.9 (1313.1)2435.5 (1904.1)0.1
    C-reactive protein, mg/dL0.00–0.5013.4 (26.3)26.812.7 (6.5)14.7 (6.5)0.5
    LDH, U/L125–220469.6 (175.1)874.9440.3 (141.8)528.2 (229.4)0.3
    Fibrinogen, mg/dL180–400406.3 (162.0)732.1360.8 (126.3)474.5 (196.8)0.2
    • HC, hypercoagulopathic complications; INR, international normalized ratio; LDH, lactate dehydrogenase.

  • Table 4

    Description of hypercoagulopathic complications (confirmed DVT and catheter thrombosis (≥3 episodes), stroke, and use of therapeutic anticoagulation)

    Patient numberDVTDVT locationClotted central venous cathetersConfirmed strokeTherapeutic anticoagulationAnticoagulation use (days)HDComorbidities
    1––Y–Y4YMG
    2–––––––HLD, HTN
    3––Y–Y24–HTN, DM
    4––––Y6–None
    5–––––––HTN, TIA
    6––––––YHTN
    7YBrachial vein–YY6–None
    8––––Y2–CP
    9––––Y3–DA
    10–––––––CILI
    11YInternal jugular––Y7–HTN, EtOH
    12––––Y23YHLD, PVD, SZ
    13––––Y3YHTN, CHF
    14–––––––HTN
    15––––Y9YHTN, DM, MG
    16–––––––CILI, EtOH
    17–––YY14–ARF, HTN, DM
    18––––Y15–HTN, DM, TIA
    19––––Y11YHTN, DM
    20––––Y6–HLD, CHF, HTN, COPD, CAD
    21–––YY2YHLD, HTN, DM
    • CAD, coronary artery disease; CHF, congestive heart failure; CILI, cirrhosis of the liver; COPD, chronic obstructive pulmonary disease; CP, cerebral palsy; DA, drug abuse; DM, diabetes; DVT, deep vein thrombosis; EtOH, alcohol use; HD, hemodialysis; HLD, hyperlipidemia; HTN, hypertension; MG, myasthenia gravis; PVD, peripheral vascular disease; SZ, seizure; TIA, transient ischemic attack; Y, yes.

  • Table 5

    ROTEM parameters and PTT by median and mean quartile of patients with hypercoagulopathy versus patients without coagulopathy

    HC (no=0, yes=1)nReference rangeMinimumQ1MedianQ3Maximum95% median CI
    CTEX04043–8249597186.749564.3 to 121.2
    121064.58010731162.6 to 115.2
    CTIN040122–208123150.2162.5215482168.2 to 213.4
    121123172.5209228.5572176.2 to 261.1
    CFTEX04048–1273961.78111529576.3 to 106.6
    12142485674.533147.2 to 105.3
    CFTIN04045–1103558.276111.530172.5 to 101.4
    12144515880.529452.5 to 104.9
    A10EX04040–603050.258.567.77854.7 to 61.4
    1212857.564697456.1 to 66.1
    A10IN04040–602947.55663.77453.6 to 59.7
    1212954.563657252.8 to 63.2
    MCFEX04052–704359.266728363.1 to 68.5
    1213967.57073.57965.2 to 72.8
    MCFIN04051–723958.264717961.1 to 66.6
    1213863.567727761.8 to 70.1
    MCFFIB0407–2451523284019.8 to 25.6
    12172232384123.8 to 33.9
    PTT04025–32 (seconds)192629.335.57729.5 to 36
    1212532.74148.66336.8 to 46.9
    • A10, amplitude at 10 minutes; CFT, clot formation time; CT, clotting time; EX, EXTEM; FIB, FIBTEM; HC, hypercoagulopathic complications; IN, INTEM; MCF, maximum clot firmness; n, number of ROTEM test results; PTT, partial thromboplastin time; ROTEM, rotational thromboelastography.

  • Table 6

    ROTEM parameters and PTT by median and mean quartile of patients with and without therapeutic heparin administration

    Heparin drip use (no=0, yes=1)nReference rangeMinimumQ1MedianQ3Maximum95% median CI
    CTEX01843–82495768.5768961.3 to 74.1
    1430627910749572.9 to 129.8
    CTIN018122–208130150.5160173.2222152.2 to 172.9
    143123157196229572188.6 to 216.2
    CFTEX01848–12752748511319478.6 to 111.3
    1433948619533163.9 to 101.0
    CFTIN01845–1105167.78111012175.1 to 96.0
    1433551599330165.5 to 101.2
    A10EX01840–604150.75559.57051.4 to 58.8
    143285563707857.3 to 64.3
    A10IN01840–604649.754.559.26651.5 to 57.2
    143295060687454.8 to 61.8
    MCFEX01852–705059.764.567.57660.8 to 67.2
    143396470748365.3 to 70.9
    MCFIN01851–725459.762.566.27360.4 to 65.2
    143385967737962.3 to 68.3
    MCFFIB0187–241112.718253715.6 to 22.9
    14352129364124.1 to 30.3
    PTT01825–32 (seconds)1925.12728.72925.4 to 27.9
    1432532.635.648.17736.3 to 43.3
    • A10, amplitude at 10 minutes; CFT, clot formation time; CT, clotting time; EX, EXTEM; FIB, FIBTEM; IN, INTEM; MCF, maximum clot firmness; PTT, partial thromboplastin time; ROTEM, rotational thromboelastography.

Supplementary Materials

  • Figures
  • Tables
  • Additional Files
  • Supplementary data

    [tsaco-2020-000603supp001.pdf]

  • Supplementary data

    [tsaco-2020-000603supp002.pdf]

  • Supplementary data

    [tsaco-2020-000603supp003.pdf]

Additional Files

  • Figures
  • Tables
  • Supplementary Materials
  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    • Data supplement 1
    • Data supplement 2
    • Data supplement 3
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Serial rotational thromboelastography (ROTEM) in mechanically ventilated patients with COVID-19 demonstrates hypercoagulopathy despite therapeutic heparinization
James K Choi, Kartik Prabhakaran, Rifat Latifi, Abbas Smiley, Joshua Klein, Gary Lombardo, Peter Rhee
Trauma Surg Acute Care Open Mar 2022, 7 (1) e000603; DOI: 10.1136/tsaco-2020-000603

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Serial rotational thromboelastography (ROTEM) in mechanically ventilated patients with COVID-19 demonstrates hypercoagulopathy despite therapeutic heparinization
James K Choi, Kartik Prabhakaran, Rifat Latifi, Abbas Smiley, Joshua Klein, Gary Lombardo, Peter Rhee
Trauma Surg Acute Care Open Mar 2022, 7 (1) e000603; DOI: 10.1136/tsaco-2020-000603
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Serial rotational thromboelastography (ROTEM) in mechanically ventilated patients with COVID-19 demonstrates hypercoagulopathy despite therapeutic heparinization
James K Choi, Kartik Prabhakaran, Rifat Latifi, Abbas Smiley, Joshua Klein, Gary Lombardo, Peter Rhee
Trauma Surgery & Acute Care Open Mar 2022, 7 (1) e000603; DOI: 10.1136/tsaco-2020-000603
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