Deep venous thrombosis: Difference between revisions
 
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==Background==
==Background==
===Clinical Spectrum of Venous Thromboembolism===
{{Venous thromboembolism types}}
{{Venous thromboembolism types}}


==Diagnosis==
{{Venous system anatomy leg}}
===Modified Wells Score===
#Active cancer (<6 mo) - 1pt
#Paralysis, paresis, or immob of extremity - 1pt
#Bedridden >3 d b/c of sx (w/in 4 wk) - 1pt
#TTP along deep venous system - 1pt
#Entire leg swollen - 1pt
#Unilateral calf swelling >3cm below tibial tuberosity - 1pt
#Unilateral pitting edema - 1pt
#Collateral superficial veins (not varicose) - 1pt
#Previously documented DVT - 1pt
#Alternative dx as likely or more likely than DVT - (-)2pts


==Clinical Features==
[[File:Deep vein thrombosis of the right leg.jpg|thumbnail|DVT of right leg]]
[[File:Deep vein thrombosis of the right leg.jpg|thumbnail|DVT of right leg]]
[[File:DVT.jpeg|thumbnail|Large DVT of left leg]]
[[File:DVT.jpeg|thumbnail|Large [[DVT]] of left leg]]
 
*Leg swelling with circumference >3cm more than unaffected side
====Probability====
*Tenderness over calf muscle
*0-1 = Low probability
*Homan's sign - pain during dorsiflexion of foot (SN 60-96% and SP 20-72%)<ref>Anand SS, et al. Does this patient have deep vein thrombosis? JAMA. 1998; 279(14):1094-9.</ref>
*≥2 = High probability
 
=====Low Probability=====
*Send d-dimer
**If pos obtain utz
 
=====High Probability=====
*Send d-dimer AND obtain utz
**If both negative done
**If utz positive done
**If pos d-dimer but neg UTZ:
***Repeat utz in 1wk


==Differential Diagnosis==
==Differential Diagnosis==
*Arterial embolism
*[[Acute arterial ischemia|Arterial thrombosis]]
*[[Septic Joint]]
*Arteritis
*[[Arthritis]]
*[[Buerger disease]]
*[[Cellulitis]]
*[[Compartment syndrome]]
*[[Complex regional pain syndrome]]
*[[Fractures (main)|Fracture]]
*[[Gout and Pseudogout|Gout]]
*[[Lymphangitis]]
*Myositis
*[[Necrotizing fasciitis]]
*Nerve entrapment
*[[Neuropathy]]
*[[Osteomyelitis]]
*[[Osteomyelitis]]
*[[Compartment Syndrome]]
*[[Paget-Schroetter syndrome]]
*[[Nec fasc]]
*[[Gout]]
*Neuropathy
*Nerve entrapment
*Sciatica
*Sciatica
*[[Fracture]]
*[[Septic Arthritis (General)|Septic Joint]]
*Reflex Sympathetic Dystrophy
*Lymphangitis
*Buerger's disease
*Arthritis
*Tendonitis
*Tendonitis
*Myositis
*Arteritis
*[[Paget-Schroetter Syndrome]]


==Treatment==
{{Calf pain DDX}}
'''Contraindications to A/C'''
{{Unilateral leg swelling DDX}}
* Active hemorrhage
 
* Plt < 50
==Evaluation==
* h/o intracerebral hemorrhage
[[File:DVT-clinical-algorithm.jpg|thumbnail|ACEP DVT Evaluation Algorithm]]
'''Proximal DVT'''  
[[File:DVT in the Femoral Vein.png|thumb|DVT of the femoral vein on [[DVT ultrasound]]]]
* If NO phlegmasia cerulea dolens:
[[File:Deep vein thrombosis distally to the great saphenous vein, labeled.jpg|thumb|DVT of the common femoral vein on [[DVT ultrasound]].]]
** Anticoagulate with heparin/coumadin x 3 months
[[ File:Iliac vein deep vein thrombosis.jpg|thumb|Iliac vein vein thrombosis, which constitutes a DVT in the pelvis.]]
* If phlegmasia cerulea dolens:
===Lower Extremity===
** Consider thrombolytics +/- thrombectomy  
*Clinical exam
** Anticoagulate with heparin/coumadin x 3 months
*Risk stratification for further testing indicated using (e.g., see Modified Wells Score below)
* If A/C contraindicated:
**Consider [[D-dimer]]
** IVC filter  
**Consider [[DVT ultrasound]]
'''Distal DVT'''  
 
* Symptomatic  
{{Modified Wells Score}}
** Anticoagulate with heparin/coumadin x 3 months
 
* Asymptomatic with extension of thrombus toward proximal veins
===Upper Extremity===
** Anticoagulate with heparin/coumadin x 3 months
''Requires [[DVT ultrasound|ultrasound]] for diagnosis.  Cannot be ruled out with d-dimer.<ref>Kucher N. Clinical practice Deep-vein thrombosis of the upper extremities. N Engl J Med. 2011;364:861–869.</ref>''
* Asymptomatic without extension
*Generally involves axillary or subclavian veins
** d/c with compressive U/S q2weeks
*Primary upper extremity DVT typically presents in young healthy individuals
'''Therapy'''
*Secondary upper extremity DVT often due to indwelling catheters
* Standard anticoagulation regimen
*Obtain a chest x-ray to rule out bony abnormalities that may be causing venous obstruction
**[[Enoxaparin]] 1 mg/kg q12h 4-5 days
 
**[[Coumadin]]
==Management==
***typical starting dose 5 mg/day
''The distinction between distal and proximal relates to veins below and above the knee respectively.<ref>Gualtiero P. How I treat isolated distal deep vein thrombosis (IDDVT). Blood 2014 123:1802-1809; doi: https://doi.org/10.1182/blood-2013-10-512616</ref> Patients with '''superficial venous thromboses such as the long saphenous and short saphenous are at risk of developing a DV'''T, especially in patients who have a history of prior [[DVT]] although management with anticoagulation is controversial.<ref>Litzendorf ME. Satiani B. Superficial Venous thrombosis:disease progression and evolving treatment approaches. Vasc Health Risk Manag. 2011(7). 569-575</ref>''
***give 7d supply with first dose in ED
===Proximal DVT===
* For pts with GFR < 30 and/or potentially requiring reversal
''Proximal veins are the '''external iliac''', '''common femoral''', '''greater saphenous''', '''profound (deep) femoral''', '''(superficial) femoral vein''', '''popliteal vein'''''
**[[Unfractionated Heparin]] 80 units/kg bolus then 18 units/kg/hour  
*If NO phlegmasia cerulea dolens:
***Check PTT after 6hr; adjust infusion to maintain PTT at 1.5-2.5x control
**Anticoagulate with [[apixaban]], [[rivaroxaban]], or [[heparin]]/[[coumadin]] x 3 months
** Coumadin as above
*If phlegmasia cerulea dolens:
**Consider thrombolytics +/- thrombectomy  
**Anticoagulate with [[apixaban]], [[rivaroxaban]], or [[heparin]]/[[coumadin]] x 3 months
*If anticoagulation contraindicated:
**[[IVC filter]]
 
====Mechanical Thrombectomy====
Consider pharmaco-mechanical (IR) management of proximal DVTs with the following charateristics:
*Objectively diagnosed (i.e., CT or US)
*Acute (≤14 days)
*Symptomatic (at least one):
**rVCSS Pain Score ≥2
**New edema of calf or thigh (CEAP ≥3)
**Limited mobility or bed bound due to pain / swelling
**Impairment of the tissue perfusion (phlegmasia)
 
===Distal DVT===
''Distal veins are the '''anterior tibial''', '''posterior tibial''', '''peroneal''', '''gastrocnemius, soleus.'''''
*Symptomatic  
**Anticoagulate with [[apixaban]], [[rivaroxaban]], or [[heparin]]/[[coumadin]] x 3 months
*Asymptomatic with extension of thrombus toward proximal veins
**Anticoagulate with [[apixaban]], [[rivaroxaban]], or [[heparin]]/[[coumadin]] x 3 months
*Asymptomatic without extension
**Discharge with compressive U/S q2 weeks
*2020 review from JAMA<ref>Diagnosis and Treatment of Lower Extremity Venous Thromboembolism: A Review.  JAMA. 2020 Nov 3;324(17):1765-1776. doi: https://doi.org/10.1001/jama.2020.17272</ref> recommend treat calf DVT if "severe symptoms or risk factors for pulmonary embolism or extension to proximal veins (such as hospitalization, history of VTE, and cancer)."
 
===VTE in Pregnancy<ref>DʼAlton ME et al. National Partnership for Maternal Safety: Consensus bundle on venous thromboembolism. Obstet Gynecol 2016 Oct; 128:688.</ref>===
*Therapeutic [[Enoxaparin|LMWH]] or [[Unfractionated_heparin|unfractionated heparin]] anticoagulation dose in:
**Antepartum outpatient with multiple prior VTEs or any VTE with high-risk thrombophilia until ''6 weeks postpartum''
**Postpartum inpatient with prior unprovoked, estrogen-provoked VTE, or low-risk thrombophilia ''for duration of admission''
*Lower prophylactic anticoagulation dose in:
**Antepartum outpatient with prior unprovoked, estrogen-provoked VTE, or low-risk thrombophilia until''6 weeks postpartum''
**Patients admitted > 72 hrs, not at high risk for bleeding or imminent delivery
**Resume 12 hours after C-section and removal of epidural / spinal needle in indicated patients
*Halt anticoagulation if imminent delivery, C-section, epidural / spinal needle
 
===Recurrent DVT on Therapeutic Anticoagulation===
*Admit patients for vascular surgery and hematologist consult
*Consider Greenfield IVC filter placement
*Typically start heparin for additional anticoagulation
 
===Upper extremity DVT===
*If secondary to catheter, do not necessarily have to remove <ref> Kovacs MJ et al. A pilot study of central venous catheter survival in cancer patients using low-molecular-weight heparin (dalteparin) and warfarin without catheter removal for the treatment of upper extremity deep vein thrombosis (the catheter study) JTH. 2007;5:1650–1653. </ref>
*Anticoagulation as per lower extremity DVTs.
*Consider admission for catheter directed thrombolysis or mechanical thrombectomy, especially with any of the following characteristics<ref>Kearon C, Akl EA, Ornelas J, et al. Antithrombotic therapy for VTE disease: CHEST guideline and expert panel report. Chest 2016;149:315-52.</ref>
**Severe symptoms
**Thrombus extending from subclavian to axillary vein
**Other features that suggest success for thrombolysis and decrease risk:
***Symptoms <14 days
***Life expectancy >1 yr
***Low risk for bleeding
 
==Anticoagulation Options==
{| {{table}}
| align="center" style="background:#f0f0f0;"|'''Medication'''
| align="center" style="background:#f0f0f0;"|'''[[Warfarin]] (Coumadin)'''
| align="center" style="background:#f0f0f0;"|'''[[Rivaroxaban]] (Xarelto)'''
| align="center" style="background:#f0f0f0;"|'''[[Apixaban]] (Eliquis)'''
| align="center" style="background:#f0f0f0;"|'''[[Dabigatran]] (Pradaxa)'''
|-
| Standard Dosing||
*[[Enoxaparin]] 1mg/kg q12h x 4-5 days  
*[[Warfarin]]  
**Starting dose of 5mg/day  
**Give 7d supply with first dose in ED
||
*15mg PO BID x 21 days
**Then 20mg PO daily (duration depending on risk factors)
||
*10mg PO BID x 7 days
**Then 5mg PO BID daily (duration depending on risk factors)
||
*[[Enoxaparin]] 1mg/kg q12h x 4-5 days
*Pradaxa 150mg BID <ref> https://pubmed.ncbi.nlm.nih.gov/19966341/ </ref>
|-
| Renal Dosing||
*[[Unfractionated Heparin]] 80 units/kg bolus
**Then 18 units/kg/hour  
**Check PTT after 6hr; adjust infusion to maintain PTT at 1.5-2.5x control  
*[[Warfarin]] as above
||
*Check creatinine on all patients prior to initiation
*CrCl <30 avoid use
||
*No dosage adjustments necessary for renal impairment
**However, CrCl <25 mL/minute were excluded from clinical trials
||
*CrCl<50 avoid use
|}
 
===Contraindications to anticoagulation===
*Active hemorrhage
*Platelets <50
*History of [[intracerebral hemorrhage]]


==Disposition==
==Disposition==
'''Inpatient therapy for pts with ANY of the following:'''
===Discharge===
* Iliofemoral DVT
Consider if all of the following are present:
* Phlegmasia cerulea dolens
*Ambulatory
* High risk of bleeding on A/C
*Hemodynamically stable
* Significant comorbidities
*Low risk of bleeding in patient
* Symptoms of concurrent PE
*Absence of renal failure
* Recent (within 2 weeks) stroke or transient ischemic attack
*Able to administer anticoagulation with appropriate monitoring
* Severe renal dysfunction (GFR < 30)
*Able to arrange for 2-3 day follow-up
* History of heparin sensitivity or [[Heparin-Induced Thrombocytopenia]]
 
* Weight > 150kg
===Admit===
'''Outpatient therapy for pts with ALL of the following:'''
For any of the following:
* Ambulatory
*Ileofemoral DVT that is a candidate for thrombectomy (should have the following):<ref>https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4646749/</ref>
* Hemodynamically stable
**Acute iliofemoral DVT (symptom duration <21 days)
* Low risk of bleeding in patient
**Low risk of bleeding
* Absence of renal failure
**Good functional status and reasonable life expectancy
* Able to administer (or have administered) LMWH +/- coumadin with appropriate monitoring
*[[Phlegmasia cerulea dolens]]
Arrange for 2-3 day follow-up in anticoagulation clinic
*High risk of bleeding on anticoagulation
*Significant comorbidities
*Symptoms of concurrent [[PE]]
*Recent (within 2 weeks) stroke or transient ischemic attack
*Severe renal dysfunction (GFR < 30)
*History of heparin sensitivity or [[Heparin-Induced Thrombocytopenia]]
*Weight > 150kg
*Upper extremity DVT, if indicated for thrombolysis vs outpatient for anticoagulation alone if low risk


==See Also==
==See Also==
*[[Ultrasound: DVT]]
*[[Anticoagulants]]
*[[Paget-Schroetter Syndrome]]
*[[Pulmonary embolism]]
*[[DVT ultrasound]]
*[[Paget-Schroetter syndrome]]


==External Links==
==External Links==
*[http://www.mdcalc.com/wells-criteria-for-dvt/ MDCalc - Wells' Criteria for DVT]
*[http://www.mdcalc.com/wells-criteria-for-dvt/ MDCalc - Wells' Criteria for DVT]
*[https://rebelem.com/tag/deep-vein-thrombosis/ REBEL EM - Should I Stay or Should I Go: Outpatient Treatment of Venous Thromboembolism]
*[https://coreem.net/core/deep-venous-thrombosis-dvt/ CORE EM - Deep Venous Thrombosis (DVT)]


==Source ==
==References==
*Tintinalli
<references/>
*UpToDate


[[Category:Cards]]
[[Category:Cardiology]]
[[Category:Ortho]]
[[Category:Vascular]]

Latest revision as of 19:37, 5 February 2025

Background

Clinical Spectrum of Venous thromboembolism

Only 40% of ambulatory ED patients with PE have concomitant DVT[1][2]

Leg Vein Anatomy

Blausen 0609 LegVeins.png

Significant risk of PE:

  • Common femoral vein
  • (Superficial) femoral vein
    • (Superficial) femoral vein is part of the deep system, not the superficial system as the name suggests!
  • Popliteal veins

Clinical Features

DVT of right leg
Large DVT of left leg
  • Leg swelling with circumference >3cm more than unaffected side
  • Tenderness over calf muscle
  • Homan's sign - pain during dorsiflexion of foot (SN 60-96% and SP 20-72%)[3]

Differential Diagnosis

Calf pain

Unilateral leg swelling

Differential Diagnosis of Pedal Edema

Evaluation

ACEP DVT Evaluation Algorithm
DVT of the femoral vein on DVT ultrasound
DVT of the common femoral vein on DVT ultrasound.
Iliac vein vein thrombosis, which constitutes a DVT in the pelvis.

Lower Extremity

  • Clinical exam
  • Risk stratification for further testing indicated using (e.g., see Modified Wells Score below)

Modified Wells Score

Can be applied for patients whose clinical presentation is concerning for a DVT in order to risk stratify.

  • Active cancer (<6 mo) (1pt)
  • Paralysis, paresis, or immobility of extremity (1pt)
  • Bedridden >3 days because of symptoms within 4 weeks (1pt)
  • TTP along deep venous system (1pt)
  • Entire leg swollen (1pt)
  • Unilateral calf swelling >3cm below tibial tuberosity (1pt)
  • Unilateral pitting edema (1pt)
  • Collateral superficial veins, not varicose (1pt)
  • Previously documented DVT (1pt)
  • Alternative diagnosis as likely or more likely than DVT (-2pts)

Scoring:

  • A score of 0 or lower → minimal risk - DVT prevalence of 5%. D-dimer testing is safe in this group - negative d-dimer decreases the probability of disease to <1% allowing an ultrasound to be deferred.
  • A score of 1-2 → moderate risk - DVT prevalence of 17%. D-dimer testing still effective and a negative test decreases post-test probability disease to <1%
  • A score of 3 or higher → high risk - DVT prevalence of 17-53% → patients should receive an ultrasound[4]

Upper Extremity

Requires ultrasound for diagnosis. Cannot be ruled out with d-dimer.[5]

  • Generally involves axillary or subclavian veins
  • Primary upper extremity DVT typically presents in young healthy individuals
  • Secondary upper extremity DVT often due to indwelling catheters
  • Obtain a chest x-ray to rule out bony abnormalities that may be causing venous obstruction

Management

The distinction between distal and proximal relates to veins below and above the knee respectively.[6] Patients with superficial venous thromboses such as the long saphenous and short saphenous are at risk of developing a DVT, especially in patients who have a history of prior DVT although management with anticoagulation is controversial.[7]

Proximal DVT

Proximal veins are the external iliac, common femoral, greater saphenous, profound (deep) femoral, (superficial) femoral vein, popliteal vein

Mechanical Thrombectomy

Consider pharmaco-mechanical (IR) management of proximal DVTs with the following charateristics:

  • Objectively diagnosed (i.e., CT or US)
  • Acute (≤14 days)
  • Symptomatic (at least one):
    • rVCSS Pain Score ≥2
    • New edema of calf or thigh (CEAP ≥3)
    • Limited mobility or bed bound due to pain / swelling
    • Impairment of the tissue perfusion (phlegmasia)

Distal DVT

Distal veins are the anterior tibial, posterior tibial, peroneal, gastrocnemius, soleus.

  • Symptomatic
  • Asymptomatic with extension of thrombus toward proximal veins
  • Asymptomatic without extension
    • Discharge with compressive U/S q2 weeks
  • 2020 review from JAMA[8] recommend treat calf DVT if "severe symptoms or risk factors for pulmonary embolism or extension to proximal veins (such as hospitalization, history of VTE, and cancer)."

VTE in Pregnancy[9]

  • Therapeutic LMWH or unfractionated heparin anticoagulation dose in:
    • Antepartum outpatient with multiple prior VTEs or any VTE with high-risk thrombophilia until 6 weeks postpartum
    • Postpartum inpatient with prior unprovoked, estrogen-provoked VTE, or low-risk thrombophilia for duration of admission
  • Lower prophylactic anticoagulation dose in:
    • Antepartum outpatient with prior unprovoked, estrogen-provoked VTE, or low-risk thrombophilia until6 weeks postpartum
    • Patients admitted > 72 hrs, not at high risk for bleeding or imminent delivery
    • Resume 12 hours after C-section and removal of epidural / spinal needle in indicated patients
  • Halt anticoagulation if imminent delivery, C-section, epidural / spinal needle

Recurrent DVT on Therapeutic Anticoagulation

  • Admit patients for vascular surgery and hematologist consult
  • Consider Greenfield IVC filter placement
  • Typically start heparin for additional anticoagulation

Upper extremity DVT

  • If secondary to catheter, do not necessarily have to remove [10]
  • Anticoagulation as per lower extremity DVTs.
  • Consider admission for catheter directed thrombolysis or mechanical thrombectomy, especially with any of the following characteristics[11]
    • Severe symptoms
    • Thrombus extending from subclavian to axillary vein
    • Other features that suggest success for thrombolysis and decrease risk:
      • Symptoms <14 days
      • Life expectancy >1 yr
      • Low risk for bleeding

Anticoagulation Options

Medication Warfarin (Coumadin) Rivaroxaban (Xarelto) Apixaban (Eliquis) Dabigatran (Pradaxa)
Standard Dosing
  • Enoxaparin 1mg/kg q12h x 4-5 days
  • Warfarin
    • Starting dose of 5mg/day
    • Give 7d supply with first dose in ED
  • 15mg PO BID x 21 days
    • Then 20mg PO daily (duration depending on risk factors)
  • 10mg PO BID x 7 days
    • Then 5mg PO BID daily (duration depending on risk factors)
Renal Dosing
  • Unfractionated Heparin 80 units/kg bolus
    • Then 18 units/kg/hour
    • Check PTT after 6hr; adjust infusion to maintain PTT at 1.5-2.5x control
  • Warfarin as above
  • Check creatinine on all patients prior to initiation
  • CrCl <30 avoid use
  • No dosage adjustments necessary for renal impairment
    • However, CrCl <25 mL/minute were excluded from clinical trials
  • CrCl<50 avoid use

Contraindications to anticoagulation

Disposition

Discharge

Consider if all of the following are present:

  • Ambulatory
  • Hemodynamically stable
  • Low risk of bleeding in patient
  • Absence of renal failure
  • Able to administer anticoagulation with appropriate monitoring
  • Able to arrange for 2-3 day follow-up

Admit

For any of the following:

  • Ileofemoral DVT that is a candidate for thrombectomy (should have the following):[13]
    • Acute iliofemoral DVT (symptom duration <21 days)
    • Low risk of bleeding
    • Good functional status and reasonable life expectancy
  • Phlegmasia cerulea dolens
  • High risk of bleeding on anticoagulation
  • Significant comorbidities
  • Symptoms of concurrent PE
  • Recent (within 2 weeks) stroke or transient ischemic attack
  • Severe renal dysfunction (GFR < 30)
  • History of heparin sensitivity or Heparin-Induced Thrombocytopenia
  • Weight > 150kg
  • Upper extremity DVT, if indicated for thrombolysis vs outpatient for anticoagulation alone if low risk

See Also

External Links

References

  1. ↑ Righini M, Le GG, Aujesky D, et al. Diagnosis of pulmonary embolism by multidetector CT alone or combined with venous ultrasonography of the leg: a randomised non-inferiority trial. Lancet. 2008; 371(9621):1343-1352.
  2. ↑ Daniel KR, Jackson RE, Kline JA. Utility of the lower extremity venous ultrasound in the diagnosis and exclusion of pulmonary embolism in outpatients. Ann Emerg Med. 2000; 35(6):547-554.
  3. ↑ Anand SS, et al. Does this patient have deep vein thrombosis? JAMA. 1998; 279(14):1094-9.
  4. ↑ Del Rios M et al. Focus on: Emergency Ultrasound For Deep Vein Thrombosis. ACEP News. March 2009. https://www.acep.org/clinical---practice-management/focus-on--emergency-ultrasound-for-deep-vein-thrombosis/
  5. ↑ Kucher N. Clinical practice Deep-vein thrombosis of the upper extremities. N Engl J Med. 2011;364:861–869.
  6. ↑ Gualtiero P. How I treat isolated distal deep vein thrombosis (IDDVT). Blood 2014 123:1802-1809; doi: https://doi.org/10.1182/blood-2013-10-512616
  7. ↑ Litzendorf ME. Satiani B. Superficial Venous thrombosis:disease progression and evolving treatment approaches. Vasc Health Risk Manag. 2011(7). 569-575
  8. ↑ Diagnosis and Treatment of Lower Extremity Venous Thromboembolism: A Review. JAMA. 2020 Nov 3;324(17):1765-1776. doi: https://doi.org/10.1001/jama.2020.17272
  9. ↑ DʼAlton ME et al. National Partnership for Maternal Safety: Consensus bundle on venous thromboembolism. Obstet Gynecol 2016 Oct; 128:688.
  10. ↑ Kovacs MJ et al. A pilot study of central venous catheter survival in cancer patients using low-molecular-weight heparin (dalteparin) and warfarin without catheter removal for the treatment of upper extremity deep vein thrombosis (the catheter study) JTH. 2007;5:1650–1653.
  11. ↑ Kearon C, Akl EA, Ornelas J, et al. Antithrombotic therapy for VTE disease: CHEST guideline and expert panel report. Chest 2016;149:315-52.
  12. ↑ https://pubmed.ncbi.nlm.nih.gov/19966341/
  13. ↑ https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4646749/
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