Increased risk of venous thromboembolism in young and middle-aged individuals with hereditary angioedema: a family study

2.

Zöller

B

,

Li

X

,

Ohlsson

H

,

Ji

J

,

Sundquist

J

,

Sundquist

K

.

Family history of venous thromboembolism as a risk factor and genetic research tool

.

Thromb Haemost

.

2015

;

114

(

5

):

890

-

900

.

3.

Rosendaal

FR

.

Venous thrombosis: a multicausal disease

.

Lancet

.

1999

;

353

(

9159

):

1167

-

1173

.

4.

Zöller

B

,

García de Frutos

P

,

Hillarp

A

,

Dahlbäck

B

.

Thrombophilia as a multigenic disease

.

Haematologica

.

1999

;

84

(

1

):

59

-

70

.

5.

Zöller

B

,

Svensson

PJ

,

Dahlbäck

B

,

Lind-Hallden

C

,

Hallden

C

,

Elf

J

.

Genetic risk factors for venous thromboembolism

.

Expert Rev Hematol

.

2020

;

13

(

9

):

971

-

981

.

6.

Mannucci

PM

,

Franchini

M

.

Classic thrombophilic gene variants

.

Thromb Haemost

.

2015

;

114

(

5

):

885

-

889

.

7.

Morange

PE

,

Suchon

P

,

Trégouët

DA

.

Genetics of venous thrombosis: update in 2015

.

Thromb Haemost

.

2015

;

114

(

5

):

910

-

919

.

8.

Manderstedt

E

,

Lind-Halldén

C

,

Halldén

C

, et al;

Regeneron Genetics Center

.

Classic thrombophilias and thrombotic risk among middle-aged and older adults: a population-based cohort study

.

J Am Heart Assoc

.

2022

;

11

(

4

):

e023018

.

9.

Desch

KC

,

Ozel

AB

,

Halvorsen

M

, et al.

Whole-exome sequencing identifies rare variants in STAB2 associated with venous thromboembolic disease

.

Blood

.

2020

;

136

(

5

):

533

-

541

.

10.

Morange

PE

,

Peiretti

F

,

Gourhant

L

, et al.

A rare coding mutation in the MAST2 gene causes venous thrombosis in a French family with unexplained thrombophilia: the Breizh MAST2 Arg89Gln variant

.

PLoS Genet

.

2021

;

17

(

1

):

e1009284

.

11.

Manderstedt

E

,

Lind-Halldén

C

,

Halldén

C

, et al;

Regeneron Genetics Center

.

Genetic variation of the blood coagulation regulator tissue factor pathway inhibitor and venous thromboembolism among middle-aged and older adults: a population-based cohort study

.

Res Pract Thromb Haemost

.

2022

;

6

(

7

):

e12842

.

12.

Manderstedt

E

,

Halldén

C

,

Lind-Halldén

C

, et al.

Thrombomodulin (THBD) gene variants and thrombotic risk in a population-based cohort study

.

J Thromb Haemost

.

2022

;

20

(

4

):

929

-

935

.

13.

Manderstedt

E

,

Halldén

C

,

Lind-Halldén

C

, et al;

Regeneron Genetics Center

.

Thrombotic risk determined by rare and common SERPINA1 variants in a population-based cohort study

.

J Thromb Haemost

.

2022

;

20

(

6

):

1421

-

1427

.

14.

Miyata

T

,

Horiuchi

T

.

Biochemistry, molecular genetics, and clinical aspects of hereditary angioedema with and without C1 inhibitor deficiency

.

Allergol Int

.

2023

;

72

(

3

):

375

-

384

.

15.

Kerr

FK

,

Thomas

AR

,

Wijeyewickrema

LC

, et al.

Elucidation of the substrate specificity of the MASP-2 protease of the lectin complement pathway and identification of the enzyme as a major physiological target of the serpin, C1-inhibitor

.

Mol Immunol

.

2008

;

45

(

3

):

670

-

677

.

16.

Hansen

CB

,

Csuka

D

,

Munthe-Fog

L

, et al.

The levels of the lectin pathway serine protease MASP-1 and its complex formation with C1 inhibitor are linked to the severity of hereditary angioedema

.

J Immunol

.

2015

;

195

(

8

):

3596

-

3604

.

17.

Gailani

D

.

Hereditary angioedema and thrombosis

.

Blood

.

2023

;

141

(

19

):

2295

-

2297

.

18.

Cugno

M

,

Cicardi

M

,

Bottasso

B

, et al.

Activation of the coagulation cascade in C1-inhibitor deficiencies

.

Blood

.

1997

;

89

(

9

):

3213

-

3218

.

19.

Cugno

M

,

Zanichelli

A

,

Bellatorre

AG

,

Griffini

S

,

Cicardi

M

.

Plasma biomarkers of acute attacks in patients with angioedema due to C1-inhibitor deficiency

.

Allergy

.

2009

;

64

(

2

):

254

-

257

.

20.

Csuka

D

,

Veszeli

N

,

Imreh

É

, et al.

Comprehensive study into the activation of the plasma enzyme systems during attacks of hereditary angioedema due to C1-inhibitor deficiency

.

Orphanet J Rare Dis

.

2015

;

10

:

132

.

21.

Bork

K

,

Witzke

G

.

Shortened activated partial thromboplastin time may help in diagnosing hereditary and acquired angioedema

.

Int Arch Allergy Immunol

.

2016

;

170

(

2

):

101

-

107

.

22.

Grover

SP

,

Kawano

T

,

Wan

J

, et al.

C1 inhibitor deficiency enhances contact pathway-mediated activation of coagulation and venous thrombosis

.

Blood

.

2023

;

141

(

19

):

2390

-

2401

.

23.

Sundler Björkman

L

,

Persson

B

,

Aronsson

D

,

Skattum

L

,

Nordenfelt

P

,

Egesten

A

.

Comorbidities in hereditary angioedema-a population-based cohort study

.

Clin Transl Allergy

.

2022

;

12

(

3

):

e12135

.

24.

Grover

SP

,

Sundler Björkman

L

,

Egesten

A

,

Moll

S

,

Mackman

N

.

Hereditary angioedema is associated with an increased risk of venous thromboembolism

.

J Thromb Haemost

.

2022

;

20

(

11

):

2703

-

2706

.

25.

Allaart

CF

,

Poort

SR

,

Rosendaal

FR

,

Reitsma

PH

,

Bertina

RM

,

Briët

E

.

Increased risk of venous thrombosis in carriers of hereditary protein C deficiency defect

.

Lancet

.

1993

;

341

(

8838

):

134

-

138

.

26.

Zöller

B

,

Svensson

PJ

,

He

X

,

Dahlbäck

B

.

Identification of the same factor V gene mutation in 47 out of 50 thrombosis-prone families with inherited resistance to activated protein C

.

J Clin Invest

.

1994

;

94

(

6

):

2521

-

2524

.

27.

Zöller

B

,

Berntsdotter

A

,

García de Frutos

P

,

Dahlbäck

B

.

Resistance to activated protein C as an additional genetic risk factor in hereditary deficiency of protein S

.

Blood

.

1995

;

85

(

12

):

3518

-

3523

.

28.

van Boven

HH

,

Vandenbroucke

JP

,

Briët

E

,

Rosendaal

FR

.

Gene-gene and gene-environment interactions determine risk of thrombosis in families with inherited antithrombin deficiency

.

Blood

.

1999

;

94

(

8

):

2590

-

2594

.

29.

Rosen

M

,

Hakulinen

T

. Use of disease registers. In:

Ahrens

W

,

Pigeot

I

, eds.

Handbook of Epidemiology

.

Springer-Verlag

;

2005

:

231

-

252

.

30.

Ludvigsson

JF

,

Andersson

E

,

Ekbom

A

, et al.

External review and validation of the Swedish National Inpatient Register

.

BMC Public Health

.

2011

;

11

:

450

.

31.

Ekbom

A

.

The Swedish Multi-Generation Register

.

Methods Mol Biol

.

2011

;

675

:

215

-

220

.

32.

Zöller

B

.

Nationwide family studies of cardiovascular diseases – clinical and genetic implications of family history

.

EMJ Cardiol

.

2013

;

1(1)

:

102

-

113

.

33.

Ludvigsson

JF

,

Almqvist

C

,

Bonamy

AK

, et al.

Registers of the Swedish total population and their use in medical research

.

Eur J Epidemiol

.

2016

;

31

(

2

):

125

-

136

.

34.

Ludvigsson

JF

,

Otterblad-Olausson

P

,

Pettersson

BU

,

Ekbom

A

.

The Swedish personal identity number: possibilities and pitfalls in healthcare and medical research

.

Eur J Epidemiol

.

2009

;

24

(

11

):

659

-

667

.

35.

Ludvigsson

JF

,

Svedberg

P

,

Olén

O

,

Bruze

G

,

Neovius

M

.

The longitudinal integrated database for health insurance and labour market studies (LISA) and its use in medical research

.

Eur J Epidemiol

.

2019

;

34

(

4

):

423

-

437

.

36.

Zöller

B

,

Pirouzifard

M

,

Svensson

PJ

, et al.

Familial segregation of venous thromboembolism in Sweden: a nationwide family study of heritability and complex segregation analysis

.

J Am Heart Assoc

.

2021

;

10

(

24

):

e020323

.

37.

Zöller

B

,

Li

X

,

Sundquist

J

,

Sundquist

K

.

Age- and gender-specific familial risks for venous thromboembolism: a nationwide epidemiological study based on hospitalizations in Sweden

.

Circulation

.

2011

;

124

(

9

):

1012

-

1020

.

38.

Zöller

B

,

Ohlsson

H

,

Sundquist

J

,

Sundquist

K

.

Familial risk of venous thromboembolism in first-second- and third-degree relatives: a nationwide family study in Sweden

.

Thromb Haemost

.

2013

;

109

(

3

):

458

-

463

.

39.

Rosendahl

A

,

Mjörnheim

B

,

Eriksson

LC

.

Autopsies and quality of cause of death diagnoses

.

SAGE Open Med

.

2021

;

9

:

20503121211037169

.

40.

Rosengren

A

,

Fredén

M

,

Hansson

P-O

,

Wilhelmsen

L

,

Wedel

H

,

Eriksson

H

.

Psychosocial factors and venous thromboembolism: a long-term follow-up study of Swedish men

.

J Thromb Haemost

.

2008

;

6

(

4

):

558

-

564

.

41.

Breslow

NE

,

Day

NE

.

Statistical methods in cancer research, volume II: the design and analysis of cohort studies

.

IARC Sci Publ

.

1987

;

82

:

1

-

406

.

42.

Zöller

B

,

Li

X

,

Sundquist

J

,

Sundquist

K

.

Neighborhood deprivation and hospitalization for venous thromboembolism in Sweden

.

J Thromb Thrombolysis

.

2012

;

34

(

3

):

374

-

382

.

43.

Zöller

B

,

Li

X

,

Sundquist

J

,

Sundquist

K

.

Neighbourhood deprivation and hospitalization for atrial fibrillation in Sweden

.

Europace

.

2013

;

15

(

8

):

1119

-

1127

.

44.

Kleinbaum

DG

,

Klein

M

. Survival Analysis, A Self-Learning Text. 2nd ed..

Springer

;

2005

.

45.

Kozarcanin

H

,

Lood

C

,

Munthe-Fog

L

, et al.

The lectin complement pathway serine proteases (MASPs) represent a possible crossroad between the coagulation and complement systems in thromboinflammation

.

J Thromb Haemost

.

2016

;

14

(

3

):

531

-

545

.

46.

Gulla

KC

,

Gupta

K

,

Krarup

A

, et al.

Activation of mannan-binding lectin-associated serine proteases leads to generation of a fibrin clot

.

Immunology

.

2010

;

129

(

4

):

482

-

495

.

47.

Krarup

A

,

Wallis

R

,

Presanis

JS

,

Gál

P

,

Sim

RB

.

Simultaneous activation of complement and coagulation by MBL-associated serine protease 2

.

PLoS One

.

2007

;

2

(

7

):

e623

.

48.

Jenny

L

,

Dobó

J

,

Gál

P

,

Schroeder

V

.

MASP-1 induced clotting–the first model of prothrombin activation by MASP-1

.

PLoS One

.

2015

;

10

(

12

):

e0144633

.

49.

Conway

EM

.

Reincarnation of ancient links between coagulation and complement

.

J Thromb Haemost

.

2015

;

13

(

suppl 1

):

S121

-

S132

.

50.

Zöller

B

,

Holm

J

,

Svensson

P

,

Dahlbäck

B

.

Elevated levels of prothrombin activation fragment 1 + 2 in plasma from patients with heterozygous Arg506 to Gln mutation in the factor V gene (APC-resistance) and/or inherited protein S deficiency

.

Thromb Haemost

.

1996

;

75

(

2

):

270

-

274

.

51.

Rühl

H

,

Berens

C

,

Winterhagen

FI

, et al.

Increased activated protein C response rates reduce the thrombotic risk of Factor V Leiden carriers but not of prothrombin 20210G>A carriers

.

Circ Res

.

2019

;

125

(

5

):

523

-

534

.

52.

Martinelli

I

,

Mannucci

PM

,

De Stefano

V

, et al.

Different risks of thrombosis in four coagulation defects associated with inherited thrombophilia: a study of 150 families

.

Blood

.

1998

;

92

(

7

):

2353

-

2358

.

53.

Segal

JB

,

Brotman

DJ

,

Necochea

AJ

, et al.

Predictive value of factor V Leiden and prothrombin G20210A in adults with venous thromboembolism and in family members of those with a mutation: a systematic review

.

JAMA

.

2009

;

301

(

23

):

2472

-

2485

.

54.

Lindström

S

,

Wang

L

,

Smith

EN

, et al.

Genomic and transcriptomic association studies identify 16 novel susceptibility loci for venous thromboembolism

.

Blood

.

2019

;

134

(

19

):

1645

-

1657

.

55.

Klarin

D

,

Busenkell

E

,

Judy

R

, et al.

Genome-wide association analysis of venous thromboembolism identifies new risk loci and genetic overlap with arterial vascular disease

.

Nat Genet

.

2019

;

51

(

11

):

1574

-

1579

.

56.

Kalaria

S

,

Craig

T

.

Assessment of hereditary angioedema treatment risks

.

Allergy Asthma Proc

.

2013

;

34

(

6

):

519

-

522

.

57.

Gandhi

PK

,

Gentry

WM

,

Bottorff

MB

.

Thrombotic events associated with C1 esterase inhibitor products in patients with hereditary angioedema: investigation from the United States Food and Drug Administration adverse event reporting system database

.

Pharmacotherapy

.

2012

;

32

(

10

):

902

-

909

.

58.

Taeuber

I

,

Weibel

S

,

Herrmann

E

, et al.

Association of intravenous tranexamic acid with thromboembolic events and mortality: a systematic review, meta-analysis, and meta-regression

.

JAMA Surg

.

2021

;

156

(

6

):

e210884

.

59.

Farkas

H

,

Kőhalmi

KV

,

Veszeli

N

,

Zotter

Z

,

Várnai

K

,

Varga

L

.

Risk of thromboembolism in patients with hereditary angioedema treated with plasma-derived C1-inhibitor

.

Allergy Asthma Proc

.

2016

;

37

(

2

):

164

-

170

.

60.

Grover

SP

,

Snir

O

,

Hindberg

K

, et al.

High plasma levels of C1-inhibitor are associated with lower risk of future venous thromboembolism

.

J Thromb Haemost

.

2023

;

21

(

7

):

1849

-

1860

.

61.

Yuan

S

,

Xu

F

,

Zhang

H

, et al.

Proteomic insights into modifiable risk of venous thromboembolism and cardiovascular comorbidities

.

J Thromb Haemost

.

2024;22(3):738-748

.

62.

Preis

M

,

Hirsch

J

,

Kotler

A

, et al.

Factor XI deficiency is associated with lower risk for cardiovascular and venous thromboembolism events

.

Blood

.

2017

;

129

(

9

):

1210

-

1215

.

63.

Salomon

O

,

Steinberg

DM

,

Zucker

M

,

Varon

D

,

Zivelin

A

,

Seligsohn

U

.

Patients with severe factor XI deficiency have a reduced incidence of deep-vein thrombosis

.

Thromb Haemost

.

2011

;

105

(

2

):

269

-

273

.

64.

Meijers

JC

,

Tekelenburg

WL

,

Bouma

BN

,

Bertina

RM

,

Rosendaal

FR

.

High levels of coagulation factor XI as a risk factor for venous thrombosis

.

N Engl J Med

.

2000

;

342

(

10

):

696

-

701

.

65.

Cushman

M

,

O'Meara

ES

,

Folsom

AR

,

Heckbert

SR

.

Coagulation factors IX through XIII and the risk of future venous thrombosis: the Longitudinal Investigation of Thromboembolism Etiology

.

Blood

.

2009

;

114

(

14

):

2878

-

2883

.

66.

Elsheikh

S

,

Tidbury

N

,

Lip

GYH

.

A review of emerging factor XI inhibitors

.

Expert Opin Emerg Drugs

.

2023

;

28

(

1

):

43

-

53

.

67.

Nørgaard

I

,

Nielsen

SF

,

Nordestgaard

BG

.

Complement C3 and high risk of venous thromboembolism: 80517 individuals from the Copenhagen General Population Study

.

Clin Chem

.

2016

;

62

(

3

):

525

-

534

.

68.

Skjeflo

EW

,

Brækkan

SK

,

Ludviksen

JK

, et al.

Elevated plasma concentration of complement factor C5 is associated with risk of future venous thromboembolism

.

Blood

.

2021

;

138

(

21

):

2129

-

2137

.

69.

Damoah

CE

,

Snir

O

,

Hindberg

K

, et al.

High levels of complement activating enzyme MASP-2 are associated with the risk of future incident venous thromboembolism

.

Arterioscler Thromb Vasc Biol

.

2022

;

42

(

9

):

1186

-

1197

.

70.

Skjeflo

EW

,

Evensen

LH

,

Jensen

SB

, et al.

Complement factors B, D, C3bBbP and risk of future venous thromboembolism

.

Clin Immunol

.

2023

;

249

:

109278

.

71.

Aabom

A

,

Bygum

A

,

Koch

C

.

Complement factor C4 activation in patients with hereditary angioedema

.

Clin Biochem

.

2017

;

50

(

15

):

816

-

821

.

72.

Lander

ES

,

Schork

NJ

.

Genetic dissection of complex traits

.

Science

.

1994

;

265

(

5181

):

2037

-

2048

.

73.

Patel

H

,

Sun

H

,

Hussain

AN

,

Vakde

T

.

Advances in the diagnosis of venous thromboembolism: a literature review

.

Diagnostics (Basel)

.

2020

;

10

(

6

):

365

.

74.

Zöller

B

,

Li

X

,

Sundquist

J

,

Sundquist

K

.

Socioeconomic and occupational risk factors for venous thromboembolism in Sweden: a nationwide epidemiological study

.

Thromb Res

.

2012

;

129

(

5

):

577

-

582

.

75.

Winkleby

MA

,

Jatulis

DE

,

Frank

E

,

Fortmann

SP

.

Socioeconomic status and health: how education, income, and occupation contribute to risk factors for cardiovascular disease

.

Am J Public Health

.

1992

;

82

(

6

):

816

-

820

.

76.

Zöller

B

,

Li

X

,

Sundquist

J

,

Sundquist

K

.

Risk of venous thromboembolism in first- and second-generation immigrants in Sweden

.

Eur J Intern Med

.

2012

;

23

(

1

):

40

-

47

.

77.

Weinstock

MA

,

Brodsky

GL

.

Bias in the assessment of family history of melanoma and its association with dysplastic nevi in a case-control study

.

J Clin Epidemiol

.

1998

;

51

(

12

):

1299

-

1303

.

78.

Wettermark

B

,

Hammar

N

,

Fored

CM

, et al.

The new Swedish Prescribed Drug Register--opportunities for pharmacoepidemiological research and experience from the first six months

.

Pharmacoepidemiol Drug Saf

.

2007

;

16

(

7

):

726

-

735

.