Dysfibrinogenemia

Back

Background

Dysfibrinogenemia is a rare coagulation disorder resulting from an abnormal or decreased level of fibrinogen, a 340 kDa glycoprotein produced in the liver. Fibrinogen necessary to form blood clots and control bleeding. Dysfibrinogenemia has two forms: congenital and acquired. The rare congenital form is asymptomatic in approximately 40% of cases, with the remainder of affected individuals experiencing bleeding (50%) or bleeding and thrombotic (clotting) episodes (10%).

Fibrinogen circulates in plasma at a concentration of 2-4 g/L and has a half-life of 4 days. The fibrinogen molecule is a hexamer consisting of three paired polypeptide chains: A-α, B-β, and γ. A and B refer to specific polypeptides on two of the chains. Synthesis of the protein in hepatocytes is under the control of three genes (one for each chain), the fibrinogen alpha, fibrinogen beta, or fibrinogen gamma genes (FGAFGB, or FGG, respectively), located within 50 kilobases (kb) on chromosome 4 (4q).

Congenital dysfibrinogenemia can be inherited as an autosomal-dominant, codominant, or autosomal-recessive disorder affecting FGAFGB, or FGG.

There are two types of congenital dysfibrinogenemia: type I, in which there is absence (afibrinogenemia) or low levels (hypofibrinogenemia) of circulating fibrinogen; and type II, in which fibrinogen levels are normal or low but the fibrinogen has low functional activity (dysfibrinogenemia).[1]  

The more common acquired form of dysfibrinogenemia is typically caused by liver diseases such as cirrhosis, hepatitis, or tumors.[2]  Other causes of acquired dysfibrinogenemia include autoimmune diseases. A case of acquired dysfibrinogenemia caused by an autoantibody that inhibited fibrin polymerization in a patient previously diagnosed with MELAS (mitochondrial myopathy, encephalopathy, lactic acidosis, strokelike episodes) has also been reported.[3]

When present, clinical manifestations of dysfibrinogenemia are generally mild. In some cases, however, they may be life-threatening. (See Presentation.)

While the majority of patients with dysfibrinogenemia require no treatment, those who experience clinically significant bleeding can benefit from fresh frozen plasma (FFP) or cryoprecipitate, depending on the severity of the bleeding. Anticoagulation is indicated for venous thromboembolism secondary to congenital dysfibrinogenemia. (See Treatment.)

Pathophysiology

In the clotting cascade, the various blood coagulation factors function in concert to produce a balance between fibrin clot formation and its subsequent degradation. When any factor in the cascade is absent, decreased, or abnormal, the delicate balance is disrupted, possibly leading to bleeding or thrombotic disorders. (For example, impaired fibrinopeptide B release results in abnormalities of polymerization that are associated with thrombotic events.) The clinical manifestations range from no symptoms to life-threatening events, depending on which coagulation factor is affected and the degree to which it is affected.

In normal fibrin clot formation, a fibrin monomer forms after thrombin cleaves fibrinopeptide A and B from the alpha and beta chains of the fibrinogen molecule. The fibrin monomer, which is insoluble, aggregates spontaneously into fibrin polymer. Factor XIIIa then catalyzes the cross-linkage between different fibrin chains, forming a stabilized fibrin polymer or clot. Eventually, plasmin lyses the fibrin clot.

As previously stated, fibrinogen is encoded by the FGA, FGB, and FGG genes. Causative mutations can occur in any of the three genes, but FGB mutations are the least common.[4, 5]

Acquired dysfibrinogenemia occurs most often in patients with severe liver disease. The impairment of fibrinogen, which is synthesized in the liver, is due to a structural defect caused by an increased carbohydrate content that interferes with the polymerization of the fibrin, depending on the degree of abnormality of the fibrinogen molecule. Rarely, dysfibrinogenemia may also be associated with malignancies, most commonly primary or secondary liver tumors, but acquired dysfibrinogenemia has also been reported in patients with renal cell carcinoma.

Congenital dysfibrinogenemia, a qualitative abnormality of the fibrin molecule, is one of the rarer coagulation disorders. Multiple variations of these dysfibrinogenemias have been elucidated. Each is named for the city where it was first discovered. With only rare exceptions, the congenital dysfibrinogenemias are inherited in an autosomal dominant or codominant fashion. Depending on the fibrinogen abnormality, defects may occur in one or more of the steps in fibrin clot formation, although the most common defect involves polymerization of the fibrin monomer.[6]

Bleeding may ensue when a fibrin clot forms that cannot be effectively stabilized. Bleeding in patients with congenital dysfibrinogenemia tends to be relatively mild or even absent; it is only a laboratory curiosity and is not life threatening. In contrast to the bleeding experienced by approximately half of the patients with congenital dysfibrinogenemia, one subset of patients (diagnosed with fibrinogen Oslo I) has an abnormal fibrinogen that is associated with thromboembolic complications that are often relatively mild. The abnormal fibrinogen in these patients forms a fibrin clot that is resistant to fibrinolysis by plasmin.[7]

Etiology

Congenital dysfibrinogenemias are most often inherited in an autosomal dominant or codominant fashion. Several variants are inherited autosomal recessively.  

Acquired dysfibrinogenemias occur in severe liver disease. The fibrinogen molecule produced by the impaired liver is not functional or able to form a stable fibrin clot.

Epidemiology

Transmission of congenital dysfibrinogenemia is autosomal dominant or codominant, except in a few cases that appear to be transmitted recessively.

Acquired abnormalities of fibrinogen may complicate liver disease; approximately 50% of patients with severe liver disease exhibit bleeding secondary to abnormal fibrinogen molecules.

Dysfibrinogenemia has no known predilection for race or sex.

Prognosis

The prognosis is good for patients with congenital dysfibrinogenemias, because bleeding or thrombotic events are rare and usually mild, though severe hemorrhagic episodes may characterize a few abnormal fibrinogen variants (eg, Imperate, Dettori, Detroit). On the other hand, patients with acquired dysfibrinogenemia often have a worse prognosis because it is associated with severe liver disease and individuals experience more severe bleeding episodes than do patients with the inherited type. The condition tends to worsen as the liver disease worsens.

During pregnancy, dysfibrinogenemia increases the risk for significant hemorrhage, thrombosis, and/or fetal loss.[8]

A multicenter study of 101 patients with congenital dysfibrinogenemia found that, over a mean 8.8-year follow-up period after diagnosis, the incidences of major bleeding and of thrombotic events were 2.5 and 18.7 per 1000 patient-years, respectively. By age 50 years, those cumulative incidences were estimated at 19.2% and 30.1%. In addition, of 111 pregnancies identified, the incidences of spontaneous abortion and postpartum hemorrhage were 19.8% and 21.4%, respectively. Abnormal bleeding was a complication in nine of 137 surgical procedures analyzed.[9]

A retrospective study by Mohsenian et al found that out of 68 pregnancies in persons with congenital fibrinogen deficiency, 31% resulted in spontaneous abortions, with 86% of them in patients with dysfibrinogenemia, and 14% in those with hypofibrinogenemia. The investigators culled information from the Prospective Rare Bleeding Disorders Database (PRO-RBDD).[10]

History

In congenital dysfibrinogenemia, bleeding is usually mild and may not manifest until after surgical procedures or major traumatic events. Rarely, however, patients can experience combined hemorrhagic and thrombotic tendencies. In female patients with congenital afibrinogenemia, recurrent, massive intra-abdominal bleeding due to rupture of Graafian follicles during ovulation has been reported.[11] In a review of 101 patients with congenital dysfibrinogenemia, the incidences of major bleeding and thrombotic events were 19.2% and 30.1%, respectively.[9]

Patients with acquired dysfibrinogenemia often have no history of bleeding or clotting, and family history is not significant for hematologic events.[12] When present, clinical manifestations of acquired dysfibrinogenemia are heterogeneous and include major bleeding or thrombosis, chronic thromboembolic pulmonary hypertension, and renal amyloidosis.[13]

Bleeding may involve any of the following:

Thrombotic events that may occur include the following:

Physical Examination

In the absence of bleeding or thrombosis. the physical examination provides no clues suggesting congenital or acquired dysfibrinogenemia.  

Laboratory Studies

The diagnosis is usually based on discrepancies between fibrinogen activity and antigen levels but could require more specialized techniques for the assessment of fibrinogen function, due to some limitations in routine assays.[14]  Recommended testing for fibrinogen disorders, and expected results, are as follows:

In the last of the above list, the reptilase time test, a snake venom that directly activates fibrinogen by cleaving fibrinopeptide A is used as a reagent. The advantage over the thrombin time is that this test is not affected by heparin. A prolonged reptilase time, in the presence of a normal fibrinogen concentration, provides strong evidence of a dysfibrinogenemia. However, this test does not detect all forms of dysfibrinogenemia. Elevated fibrinogen levels due to an acute phase reaction can be associated with prolonged reptilase times, possibly due to increased sialyation and/or phosphorylation.[15]

Genotype analysis, especially of the FGA gene, should be performed in asymptomatic patients with afibrinogenemia or hypofibrinogenemia[1]

Fibrinogen is measured in plasma using the Clauss method, based on the comparison of thrombin clotting times of dilutions of plasma against a plasma standard. The fibrinogen level may be low, within the reference range, or high. However, a level within the reference range or a high level does not imply that the fibrinogen molecule is fully functioning. For this reason, assess both the clottable (functional) fibrinogen, which should be decreased, and the antigenic fibrinogen (detected by immunoassay), which should be within the reference range. Definitive characterization of the abnormal fibrinogen can be performed in a research laboratory.[16]

Euglobulin clot lysis time may aid in the diagnosis. It is a crude measure of fibrinolytic potential. Elevated values occur when the abnormal fibrinogen results in markedly decreased fibrinolysis.

Although the TT reflects the conversion of fibrinogen to fibrin and is useful for diagnosing coagulation disorders involving abnormal fibrinogen, it does not distinguish between qualitative and quantitative defects. Examination of the amplitude of coagulation curves generated during TT tests may provide additional information to help distinguish between fibrinogen disorders following a low fibrinogen measurement by the Clauss method.[17]

In liver-associated acquired dysfibrinogenemia, fibrinogen levels are usually normal, as opposed to congenital dysfibrinogenemia, in which fibrinogen levels are low normal to deficient. In addition, genetic testing of patients with acquired dysfibrinogenemia will not reveal any mutations associated with the congenital variant.

Imaging Studies

In the investigation of suspected bleeding, appropriate imaging studies (eg, brain computed tomography [CT] scanning or magnetic resonance imaging [MRI]) may reveal the presence of suspected central nervous system (CNS) hemorrhage.

Other Tests

A retrospective, observational study by Kim et al suggested that thromboelastography (TEG) can be used to identify those emergency department patients with primary postpartum hemorrhage (PPH) who have hypofibrinogenemia. According to the investigators, multivariable analysis showed the alpha angle and maximum amplitude to be independently associated with hypofibrinogenemia, with optimum cutoff values for the angle and amplitude being under 63.8° (sensitivity of 83.6%, specificity of 81.2%) and below 56.1 mm, respectively.[18]

Approach Considerations

Treatment is not indicated in the majority of patients. When clinically significant bleeding occurs, replacement therapy is indicated. FFP or cryoprecipitate should be administered, depending on bleeding severity and product availability. 

Fibrinogen replacement therapy may prevent pregnancy complications.[8]

Venous thromboembolism secondary to congenital dysfibrinogenemia should be treated with low–molecular-weight heparin.[9] Patients with recurrent thrombotic events may require long-term anticoagulation with warfarin or subcutaneous heparin. Long-term treatment recommendations have not been established, and data are lacking to support the superiority of any one treatment modality.[12]

Educate patients with congenital dysfibrinogenemia that it is an inherited condition and that other family members may also be affected.

 

Medical Care

Hemorrhage

The half-life of fibrinogen is approximately 3.5 days, and afibrinogenemic patients can usually be managed postoperatively with infusion of replacement therapy every 2-3 days for major surgery.

The patient's personal and family history of bleeding and thrombosis should be taken into consideration for appropriate dosing of replacement therapy. In addition, the pharmacokinetics of fibrinogen after replacement therapy widely varies, and individual dose adjustment is recommended.

Children have more rapid plasma fibrinogen clearance and may require higher and more frequent dosing for surgery and major bleeding.

Acquired inhibitors have been reported after replacement therapy and should be considered in previously treated patients who demonstrate poor hemostasis with usual therapies.

Cryoprecipitate has been used as a source of fibrinogen; each bag of cryoprecipitate contains 100-250 mg of fibrinogen. The guidelines for dysfibrinogenemia are not standardized due to a lack of sufficient data in bleed management.

Fibrinogen dosage calculation

This is as follows[19] :

Consultations

Consultation with a hematologist/hemostasis specialist is advisable for patients who require fibrinogen replacement therapy. Genetic counseling and family studies should be part of a complete evaluation.

Surgical Care

To prevent excessive bleeding during surgical procedures, prophylactic treatment to raise fibrinogen levels to 1-1.5 g/L during the procedure is recommended. Replacement should be continued for 4-14 days following surgery, depending on the nature of the surgical procedure and time to complete healing.

Prevention

The obstetric complications of dysfibrinogenemia include first-trimester pregnancy loss, along with hemorrhage, placental abruption, and thrombosis. Administration of prophylactic cryoprecipitate may prevent recurrent miscarriages. Miesbach et al described the use of fibrinogen concentrates to avoid pregnancy loss in women with dysfibrinogenemia. The investigators performed a retrospective study of four women from the same family, each of whom had dysfibrinogenemia and a history of recurrent pregnancy loss. The patients received fibrinogen concentrates from the start of pregnancy until delivery, with three of the four women achieving delivery.[20]

Cryoprecipitate (CRYO)

Clinical Context:  The precipitate that forms when fresh frozen plasma (FFP) is thawed contains factor VIII, fibrinogen, von Willebrand factor, and fibronectin. Primarily used to treat bleeding in patients with fibrinogen deficiencies or abnormalities.

Fresh frozen plasma (FFP, Octaplas)

Clinical Context:  Plasma is the fluid compartment of blood containing the soluble clotting factors. Indications for using FFP include bleeding in patients with congenital coagulation defects and multiple coagulation factor deficiencies (severe liver disease).

Class Summary

These are used to replace the clotting factors needed when moderate-to-severe bleeding occurs. This most often occurs in acquired dysfibrinogenemias caused by a severely damaged liver that is unable to make clotting factors.[21]

Heparin

Clinical Context:  This is used in patients with thrombotic tendencies who develop deep venous thrombosis, arterial thrombosis, or pulmonary embolism.

Warfarin (Coumadin, Jantoven)

Clinical Context:  Warfarin interferes with hepatic synthesis of vitamin K–dependent coagulation factors. It is used for prophylaxis and treatment of venous thrombosis, pulmonary embolism, and thromboembolic disorders. Tailor dose to maintain an INR in the range of 2-3.

Enoxaparin (Lovenox)

Clinical Context:  Chronic subcutaneous therapy may be required in patients with recurrent thrombotic episodes.

Enhances inhibition of factor Xa and thrombin by increasing antithrombin III activity. In addition, preferentially increases inhibition of factor Xa.

Average duration of treatment is 7-14 d.

Class Summary

These prevent recurrent or ongoing thromboembolic occlusion.

Fibrinogen, human (Fibryga, RiaSTAP)

Clinical Context:  Approved by the US Food and Drug Administration (FDA) in 2009. Indicated for the treatment of acute bleeding episodes in patients with congenital fibrinogen deficiency, including afibrinogenemia and hypofibrinogenemia. Not indicated for dysfibrinogenemia. Available as single-use vials containing 900-1300 mg lyophilized fibrinogen concentrate powder for reconstitution. Actual fibrinogen potency for each lot is printed on vial label and carton.

Aminocaproic acid (Amicar)

Clinical Context:  Lysine analogue that inhibits fibrinolysis by blocking binding of plasmin or plasminogen activators to lysine residues on fibrin.

Tranexamic acid injection (Cyklokapron)

Clinical Context:  Alternative to aminocaproic acid. Inhibits fibrinolysis by displacing plasminogen from fibrin.

Class Summary

These are useful in conjunction with fibrinogen replacement for the treatment of mucosal bleeding, particularly bleeding involving the oronasopharynx. Inhibition of local fibrinolysis allows maintenance of the clot and decreases the frequency of rebleeding.

What is dysfibrinogenemia?What is the pathophysiology of dysfibrinogenemia?What causes dysfibrinogenemia?What is the prevalence of dysfibrinogenemia?What is the prognosis of dysfibrinogenemia?Which clinical history findings are characteristic of dysfibrinogenemia?How is bleeding characterized in dysfibrinogenemia?Which thrombotic events may occur in dysfibrinogenemia?What are the signs and symptoms of hereditary renal amyloidosis in dysfibrinogenemia?Which physical findings are characteristic of dysfibrinogenemia?Which conditions are included in the differential diagnoses of dysfibrinogenemia?What are the differential diagnoses for Dysfibrinogenemia?What is the Clauss method for measurement of plasma in the workup of dysfibrinogenemia?What is the role of lab tests in the workup of dysfibrinogenemia?How is dysfibrinogenemia treated?How are the obstetric complications of dysfibrinogenemia prevented?When are medications used in dysfibrinogenemia treatment?Which medications in the drug class Anticoagulants are used in the treatment of Dysfibrinogenemia?Which medications in the drug class Clotting factor replacement therapies are used in the treatment of Dysfibrinogenemia?

Author

Guy B Faguet, MD, Retired Professor, Department of Medicine, Section of Hematology and Oncology, Georgia Regents University

Disclosure: Nothing to disclose.

Specialty Editors

Francisco Talavera, PharmD, PhD, Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Received salary from Medscape for employment. for: Medscape.

Marcel E Conrad, MD, Distinguished Professor of Medicine (Retired), University of South Alabama College of Medicine

Disclosure: Partner received none from No financial interests for none.

Chief Editor

Perumal Thiagarajan, MD, Professor of Medicine and Pathology and Immunology, Baylor College of Medicine; Director, Hematology Laboratory and Transfusion Medicine, Michael E DeBakey Veterans Affairs Medical Center

Disclosure: Nothing to disclose.

Additional Contributors

Karen Seiter, MD, Professor, Department of Internal Medicine, Division of Oncology/Hematology, New York Medical College

Disclosure: Received honoraria from Novartis for speaking and teaching; Received consulting fee from Novartis for speaking and teaching; Received honoraria from Celgene for speaking and teaching.

Russell Burgess, MD, (Retired) Chief, Division of Hematology/Oncology, Eastern Carolina Internal Medicine, PA

Disclosure: Nothing to disclose.

Suchitra S Acharya, MD, MBBS, Associate Professor of Pediatrics and Pediatrics in Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell; Program Head, Bleeding Disorders and Thrombosis Program, Cohen Children's Medical Center of New York

Disclosure: Serve(d) as a director, officer, partner, employee, advisor, consultant or trustee for: Novonordisk, Shire <br/>Received research grant from: Bayer Pharmaceuticals .

Acknowledgements

Wendy Brick, MD Consulting Staff, Department of Internal Medicine, Division of Hematology and Oncology, Mecklenburg Medical Group

Wendy Brick, MD is a member of the following medical societies: Alpha Omega Alpha, American College of Physicians, American Medical Association, and American Society of Hematology

Disclosure: Nothing to disclose.

References

  1. de Moerloose P, Casini A, Neerman-Arbez M. Congenital fibrinogen disorders: an update. Semin Thromb Hemost. 2013 Jul. 39:585-595. [View Abstract]
  2. [Guideline] Dysfibrinogenemia. NIH Genetic and Rare Diseases Information Center. Available at https://rarediseases.info.nih.gov/diseases/2004/dysfibrinogenemia. Updated January 2025; Accessed: February 10, 2025.
  3. Lee N, Kim JE, Yoo HJ, Gu J, Kim H, Chung J, et al. Acquired Dysfibrinogenemia Caused by Autoantibody Inhibiting Fibrin Polymerization in a Patient with MELAS Syndrome and Bleeding Tendency. Ann Clin Lab Sci. 2016 Dec. 46 (6):696-700. [View Abstract]
  4. Ceznerová E, Kaufmanová J, Sovová Ž, Štikarová J, Loužil J, Kotlín R, et al. Structural and Functional Characterization of Four Novel Fibrinogen Mutations in FGB Causing Congenital Fibrinogen Disorder. Int J Mol Sci. 2022 Jan 10. 23 (2):[View Abstract]
  5. Richard M, Celeny D, Neerman-Arbez M. Mutations Accounting for Congenital Fibrinogen Disorders: An Update. Semin Thromb Hemost. 2022 Jan 24. [View Abstract]
  6. Kotlin R, Reicheltova Z, Maly M, et al. Two cases of congenital dysfibrinogenemia associated with thrombosis - Fibrinogen Praha III and Fibrinogen Plzen. Thromb Haemost. 2009 Sep. 102(3):479-86. [View Abstract]
  7. Morris TA, Marsh JJ, Chiles PG, et al. High prevalence of dysfibrinogenemia among patients with chronic thromboembolic pulmonary hypertension. Blood. 2009 Aug 27. 114(9):1929-36. [View Abstract]
  8. Langer M, Manire M, Clarkson M, Samhouri Y, Shah D, Bhagavatula R. Management of congenital dysfibrinogenemia in pregnancy: A challenging patient case. Res Pract Thromb Haemost. 2021 Dec. 5 (8):e12619. [View Abstract]
  9. Casini A, Blondon M, Lebreton A, Koegel J, Tintillier V, de Maistre E, et al. Natural history of patients with congenital dysfibrinogenemia. Blood. 2015 Jan 15. 125 (3):553-61. [View Abstract]
  10. Mohsenian S, Palla R, Menegatti M, et al. Congenital fibrinogen disorders: a retrospective clinical and genetic analysis of the Prospective Rare Bleeding Disorders Database. Blood Adv. 2024 Mar 26. 8 (6):1392-404. [View Abstract]
  11. Wang Y, Zhao L, Feng X, Li Q, Ma S, Liang D, et al. Two-Pronged Treatment of Hemoperitoneum and Abnormal Uterine Bleeding in an Adolescent Girl With Congenital Fibrinogen Deficiency. Front Med (Lausanne). 2020. 7:181. [View Abstract]
  12. Keinath K, Church T, Sadowski B, Perkins J. Acute renal artery infarction secondary to dysfibrinogenemia. BMJ Case Rep. 2017 Nov 8. 2017:[View Abstract]
  13. Casini A, de Moerloose P, Neerman-Arbez M. Clinical Features and Management of Congenital Fibrinogen Deficiencies. Semin Thromb Hemost. 2016 Jun. 42 (4):366-74. [View Abstract]
  14. Casini A, Neerman-Arbez M, Ariëns RA, de Moerloose P. Dysfibrinogenemia: from molecular anomalies to clinical manifestations and management. J Thromb Haemost. 2015 Jun. 13 (6):909-19. [View Abstract]
  15. Van Cott EM, Smith EY, Galanakis DK. Elevated fibrinogen in an acute phase reaction prolongs the reptilase time but typically not the thrombin time. Am J Clin Pathol. 2002 Aug. 118 (2):263-8. [View Abstract]
  16. Miesbach W, Schenk J, Alesci S, Lindhoff-Last E. Comparison of the fibrinogen Clauss assay and the fibrinogen PT derived method in patients with dysfibrinogenemia. Thromb Res. 2010 Dec. 126(6):e428-33. [View Abstract]
  17. Jacquemin M, Vanlinthout I, Van Horenbeeck I, Debasse M, Toelen J, Schoeters J, et al. The amplitude of coagulation curves from thrombin time tests allows dysfibrinogenemia caused by the common mutation FGG-Arg301 to be distinguished from hypofibrinogenemia. Int J Lab Hematol. 2017 Jun. 39 (3):301-307. [View Abstract]
  18. Kim SM, Sohn CH, Kwon H, et al. Thromboelastography as an early prediction method for hypofibrinogenemia in emergency department patients with primary postpartum hemorrhage. Scand J Trauma Resusc Emerg Med. 2024 Sep 13. 32 (1):85. [View Abstract]
  19. Acharya SS, Dimichele DM. Rare inherited disorders of fibrinogen. Haemophilia. 2008 Nov. 14 (6):1151-8. [View Abstract]
  20. Miesbach W, Galanakis D, Scharrer I. Treatment of patients with dysfibrinogenemia and a history of abortions during pregnancy. Blood Coagul Fibrinolysis. 2009 Jul. 20(5):366-70. [View Abstract]
  21. Bornikova L, Peyvandi F, Allen G, Bernstein J, Manco-Johnson MJ. Fibrinogen replacement therapy for congenital fibrinogen deficiency. J Thromb Haemost. 2011 Sep. 9(9):1687-704. [View Abstract]