Article, Cardiology

Floating right heart thrombi: A pooled analysis of cases reported over the past 10 years

a b s t r a c t

Introduction: Floating right heart thrombi (FRHTS) are a rare phenomenon associated with high mortality. Imme- diate treatment is mandatory, but optimal therapy is controversial.

Objective: To compare the clinical characteristics according to different treatment strategies and to identify pre- dictors of mortality on patients with FRHTS.

Methods: We conducted a systematic search of reported Clinical cases of TTRH from 2006 to 2016. Results: 207 patients were analyzed, median age was 60 years, 51.7% were men, 31.4% presented with shock. Pul- monary thromboembolism was present in 85% of the cases. The treatments administered were anticoagulation therapy in 44 patients (21.28%), Surgical embolectomy in 89 patients (43%), thrombolytic therapy in 66 patients (31.8%), percutaneous thrombectomy in 3 patients (1.93%) and fibrinolytic in situ in 4 (1.45%). The overall mor- tality rate was 21.3%. The mortality associated with anticoagulation alone was higher than surgical embolectomy or thrombolysis (36.4 vs 18% vs 18.2%, respectively, p = 0.03), and in percutaneous thrombectomy and fibrino- lytics in situ was 0%. At multivariate analysis, only anticoagulation alone (odds ratio [OR] 2.4, IC 95% 1.07-5.4, p = 0.03), and shock (OR 2.87 (IC 95% 1.3-5.9, p = 0.005) showed a statistically significant effect on mortality.

Conclusion: FRHTS represent a serious form of thromboembolism that requires rapid decisions to improve the

survival. Anticoagulation as the only strategy does not seem to be sufficient, while thrombolysis and Surgical thrombectomy show better and similar results. A proper individualization of the risk and benefits of both tech- niques is necessary to choose the most appropriate strategy for our patients.

(C) 2017

Introduction

Floating right heart thrombi (FRHTS) temporarily located in the atrium or ventricle are known as thrombi in transit [1]. They are rare and generally occur in the setting of venous thromboembolism, with a prevalence ranging from 7% to 18% in different reports of patients with pulmonary embolism (PE) [2-4]. The risk of imminent embolism of these large structures (5) with a mortality rate N 40% demands Urgent treatment [5-7].

The treatment of choice is still controversial due to lack of consensus. Most of the patients with FRHTS have been published as case reports or small case series. In 1989, Kinney et al. published a meta-analysis of 119

Abbreviations: FRHTS, floating right heart thrombi; DVT, deep venous thrombosis; PE, pulmonary embolism.

* Corresponding author at: Instituto Cardiovascular de Buenos Aires, Blanco Encalada 1543, Ciudad de Buenos Aires CP1428, Argentina.

E-mail addresses: [email protected] (L.M. Burgos), [email protected] (J.P. Costabel).

cases and reported that the efficacy of thrombolysis, heparin and surgi- cal thrombectomy was similar [8]. In 2002, Rose et al. demonstrated in a review of 177 cases that thrombolysis was associated with an improved survival rate compared with the rest of the treatments reported [9].To our knowledge there have been no published case studies and large studies in the last decade.

The aim of this study is to make an up-dated review about the clin- ical characteristics of patients with FRHTS, comparing the different treatment strategies and identifying predictors of mortality.

Methods

Search strategy

We performed a systematic search of the case reports published in the literature between January 1, 2006, and June 1, 2016, in the follow- ing scientific databases: MEDLINE, EMBASE, LILACS, Scielo, Redalyc and Cochrane Collaboration of Clinical Trials. The reference lists of the

https://doi.org/10.1016/j.ajem.2017.10.045

0735-6757/(C) 2017

relevant articles were checked to identify additional studies. Articles in Spanish, English, Portuguese and French were included.

Medical Subject Heading (MeSH), descriptors (DeCS), and the key- words “thrombus”, “thromboembolism”, “right ventricle”, “right atrium” and “right chambers” were used.

Population

Patients N 18 years with right heart thrombi in transit documented by any complementary test, with or without pulmonary embolism, were included in the study.

Selection criteria

Type of studies: We included case reports and case series describing the demographic characteristics of the patients (age, sex), treatments used (anticoagulation, fibrinolysis, surgical or percutaneous embolec- tomy) and in-hospital outcomes (mortality, bleeding). Studies with catheter-related thrombosis in patients with pacemakers or cardioverter defibrillator devices, central venous catheters, thrombi as- sociated with tumors or surgical implant, or uncertain diagnosis or Behcet disease were excluded as these thrombi require different treatment.

Data extraction and analysis

Two review authors independently examined the titles and abstracts of all the potential studies to be included, identified by the search strat- egy. In case of overlaps of the series notified by the same institution or author, only the most recent publication was included in the analysis. Then, the complete text of the relevant primary studies was evaluated and data were extracted. The information about the authors, name of the article, journal, year, issue and volume was included. The following data were retrieved from each case: age, sex, symptoms at admission (dyspnea, syncope, chest pain, others), baseline clinical characteristics (hypotension: blood pressure b 90/60 mm Hg, cardiogenic shock: blood pressure b 90/60 mm kg and requirements of vasoactive drugs; respiratory failure: pO2 b 60 mm Hg with fraction of inspired oxygen of 21%, requirements of orotracheal intubation or non-invasive mechan- ical ventilation; tachypnea: respiratory rate N 20 per minute), diagnostic tests, electrocardiogram, echocardiography, presence of pulmonary em- bolism or deep venous thrombosis, therapeutic strategy (according to the treatment received), outcomes (death) and complications (bleed- ing). When two treatments or more were used, the patients were clas- sified according to the final therapeutic strategy.

Statistical analysis

All the statistical calculations were performed using SPSS 21soft- ware package. Categorical variables were expressed as percentages, and were compared using the chi square test or the Fisher’s exact test, as applicable. Normality of distribution was assessed using the Kolmo- gorov-Smirnov test, and the Levene test was used to evaluate homosce- dasticity. Continuous variables were expressed as mean +- standard deviation and or mean and interquartile range, as applicable, and were compared with the Student’s t-test or with the Mann-Whitney U test, as applicable. The analysis of the variance (ANOVA) or the Kruskal-Wal- lis test was used to compare variability between groups, as applicable. Multivariate logistic regression analyses were performed to identify the association between the independent predictors and mortality using the variables with p b 0.1 on the univariate model. The results are presented as odds ratio (OR) with their corresponding 95% confi- dence intervals (CI). A two-tailed p value b 0.05 was considered statisti- cally significant.

Results

A total of 163 articles were analyzed during the study period (Sup- plementary material). Seven articles were excluded: 2 of them did not present full text, 1 did not report the baseline characteristics of the pa- tient, in 2 case reports the clinical characteristics could not be individu- alized with the treatment received and the results, and 2 articles were in a language that did not meet the inclusion criteria (Polish and Turkish). A total of 207 patients were included. Median age was 60 years (IQR 25-75: 49-79) and 51.7% were men. In 32.4% of the patients, hypoten- sion was the form of presentation, 48.8% had tachypnea, 42.5% pre- sented acute respiratory failure and 31.4% had cardiogenic shock. Dyspnea was the most common symptom on presentation (78.7%), followed by chest pain (26.6%), syncope (15.5%) and palpitations (9.2%) (Table 1). The ECG on presentation showed Right bundle branch block (RBBB) in 8.7%, inverted T waves in the inferior leads or right pre- cordial leads in 30.7% and signs of right ventricular overload (ST-seg- ment depression with inverted T waves in V1-V3 or DII, DIII and aVF)

in 26% of the patients.

The echocardiogram on admission showed reduced left ventricular ejection fraction (b 50%) in 25% of the patients, Right ventricular dilation in 93%, right ventricular dysfunction in 81% and a median systolic pul- monary artery pressure of 58 mm Hg (IQR = 19).

The association with PE was reported in 85% of the cases and the presence of Deep venous thrombosis in 33.3%. The diagnosis of FRHTS was made using transthoracic echocardiography in 88% of the cases, while transesophageal echocardiography or computed tomogra- phy scan were required in the rest of the patients.

Only 1 of 207 patients retrieved did not receive any treatment, 43% of the patients underwent surgical thrombectomy (n = 89), 31.8% re- ceived fibrinolysis (n = 66), 21.28% were only treated with heparin (n

= 44), 1.93% received in situ fibrinolysis and 1.45% percutaneous

thrombectomy.

The clinical characteristics of the patients were analyzed according to the treatment received. Those patients treated with anticoagulant agents and fibrinolysis presented on admission higher rate of hypoten- sion, tachypnea, respiratory failure and shock. There were no differ- ences in age and sex across the different treatments used. Patients with hemoptysis on admission received only anticoagulation (4.5%) or surgical thrombectomy (2.5%) and none of them were treated with local or systemic fibrinolysis. There were no differences according to the diagnostic method used (p = 0.5), electrocardiographic characteris- tics (p = 0.09) or presence of DVT. Patients who received fibrinolytic agents presented lower systolic pulmonary artery pressure compared with the other groups (p = 0.03), and those with diagnosis of PE were less likely to receive only anticoagulation therapy (p = 0.008).

Overall mortality was 21.3% (n = 207); 36.4% in the group of patients who received only anticoagulation, 18.2% in the group treated with thrombolysis and 18% in those treated with surgical thrombectomy (p = 0.03) (Fig. 1). As the number of in situ fibrinolysis and Percutaneous treatment patients were small, they were not consid- ered in multivariate mortality analysis. Mortality was greater in patients who received only anticoagulants (OR 2.57; 95% CI, 1.07-6.17 versus thrombolysis and OR 2.60;95% CI. 1.15-5.9 versus thrombectomy). We did not find significant differences between fibrinolysis and thrombectomy (p = 0.9; OR, 0.98; 95% CI, 0.43-2.25) (Table 2).

In patients with hemodynamic instability, mortality was 47.4% with surgery (n = 9), 40% with anticoagulation (n = 6), and 20.7% with fibrinolysis (n = 6), without statistically significant differences (p = 0.1). Stable patients had a trend toward less mortality with surgery: 9.4% with surgical thrombectomy (n = 6), 29.2% with anticoagulation (n = 7) and 14.7% with fibrinolysis (n = 5) (p = 0.06).

The univariate analysis identified treatment with anticoagulation

and cardiogenic shock as predictors of mortality. After multivariate logistic regression analysis, both variables remained as independent predictors of mortality: cardiogenic shock with an OR of 2.87 (95% CI,

Table 1

Baseline characteristics of the population according to the treatment received. The comparisons are between the 5 types of treatment.

Total (n =

Anticoagulation (n

Surgical thrombectomy

Systemic fibrinolysis

Percutaneous

In situ

p

207)

= 44)

(n = 66)

(n = 88)

thrombectomy (n = 3)

fibrinolysis

Value

Baseline characteristics

Age (median and IQR 25-75) (n =

60 (49-72)

65 (56-75)

57 (45-69)

61 (56-75)

62 (-)

65.5 (1)

0.06

207)

Male sex, (n = 207; n %)

107 (51.7%)

22 (55)

46 (51.7)

35 (53)

2 (66.7)

1 (25)

0.7

Hypotension (n = 192, n %)

67 (32.4%)

16 (41)

18 (21.7)

30 (48.4)

1 (33.3)

2 (50)

0.02

Tachypnea (n = 183; n %)

101 (48.8%)

27 (71.1)

29 (39.2)

40 (64.5)

1 (33.3)

4 (100)

0.002

Respiratory failure (n = 183; n %)

88 (42.5%)

23 (60.5)

26 (35.5%)

36 (57.1)

1 (33.3)

2 (50)

0.06

Shock (n = 193; n %)

65 (31.4%)

15 (38.5)

19 (22.9)

29 (46)

1 (33.3)

1 (25)

0.08

Clinical presentation

Dyspnea (n = 198; n %)

163 (78.7%)

36 (81.8)

66 (82.5)

53 (80.3)

3 (100)

4 (100)

0.8

Chest pain (n = 197; n %)

55 (26.6%)

12 (27.3)

23 (29.1)

16 (24.2)

1 (33.3)

2 (50)

0.5

Syncope (n = 196; n %)

32 (15.5%)

9 (20.9)

7 (8.8)

15 (23.1)

0 (0)

1 (25)

0.2

Palpitations (n = 197; n %)

19 (9.7%)

6 (13.6)

5 (6.3)

7 (10.8)

0 (0)

(0)

0.7

focal deficits (n = 197; n %)

9 (4.3%)

4 (9.1)

2 (2.5)

2 (3.1)

0 (0)

1 (25)

0.2

Hemoptysis (n = 197; n %)

5 (2.4%)

2 (4.5)

2 (2.5)

0 (0)

0 (0)

0 (0)

0.001

Cardiac arrest (n = 197; n %)

5 (2.4%)

2 (4.5%)

1 (1.3)

2 (3.1)

0 (0)

0 (0)

0.9

diagnostic methods

TTE (n = 201; n %)

177 (88.1%)

42 (94.5)

67 (80.7)

60 (90.9)

3 (100)

4 (100)

0.5

TEE (n = 201; n %)

13 (6.5%)

0 (0)

11 (13.3)

2 (3)

0 (0)

0 (0)

CT (n = 201; n %)

9 (4.5%)

1 (2.3)

4 (4.8)

4 (6.1)

0 (0)

0 (0)

Electrocardiographic characteristics

RBBB n = 127, n %)

11 (8.7%)

4 (12.1)

1 (2.6)

5 (9.8)

0 (0)

1 (50)

0.09

RV overload

33 (26%)

8 (24.2)

10 (26.3)

14 (27.5)

0 (0)

1 (50)

Inverted T wave inferior/right

39 (30.7%)

7 (21.1)

10 (26.3)

22 (43.1)

0 (0)

0 (0)

precordial leads

Echocardiographic characteristics

LVEF b 50% (n = 71; n %)

8 (17.4%)

4 (36.4)

2 (10)

1 (8.3)

0

1 (50)

0.2

Right ventricular dilation (n =

116 (93%)

31 (100)

33 (84.6)

47 (97.9)

1 (100)

4 (100)

0.001

124; n %)

Right ventricular dysfunction (n =

83 (81%)

25 (96.2)

24 (70.6)

29 (78.4)

1 (100)

4 (100)

0.049

103; n %)

PASP (n = 110)

58 (19)

65 (15)

60 (21)

51 (16)

65 (-)

64 (25)

0.015

Diagnosis during hospitalization

PE (n = 188; n %)

176 (85%)

34 (91.9)

77 (93.9)

58 (95.1)

3 (100)

4 (100)

0.008

DVT (n = 129; n %)

69 (33.3%)

12 (52.2)

27 (50)

27 (58.7)

1 (100)

2 (50)

0.7

Abbreviations: TTE: transthoracic echocardiography, TEE: transesophageal echocardiography, CT: computed tomography, RBBB: right bundle branch block, RV: right ventricle; LVEF: left ventricle ejection fraction; PSAP: pulmonary systolic artery pressure; PE: pulmonary embolism; DVT: deep vein thrombosis.

1.3-5.9; p = 0.005) and anticoagulation only with an OR of 2.4 (95% CI, 1.07-5.4; p = 0.03).

Discussion

This updated meta-analysis of a Rare condition which demands ur- gent resolution shows that FRHTS have a serious clinical presentation, evolve with unfavorable outcome and a mortality rate of 21.3% that may decrease with the use of aggressive treatments as surgical thrombectomy or systemic thrombolysis.

Fig. 1. Mortality rate by treatment received.

Similar to the study by Chartier et al. [1], the most common symp- tom on presentation in our pool analysis was dyspnea, followed by chest pain; syncope and palpitations were less common. We under- stand that dyspnea is due to embolization of thrombotic particles of dif- ferent sizes that are not always visualized by computed tomography scan or lung scintigraphy. In this sense, in most cases the diagnosis of FRHTS is made following the diagnosis of pulmonary embolism, as the risk of injection of Contrast agents for diagnosis once the presence of the thrombus is confirmed may be questioned. In PE registries, the pres- ence of FRHTS can range between 3% and 23%, and is particularly high in the groups of high-risk PE, with large emboli in the pulmonary arteries. Most FHRTS have been diagnosed in the setting of suspected PE, and only a few are found during echocardiographic evaluation of a patient hospitalized for other reason.

As in the series presented by Mollazadeh et al., the most prevalent finding in the ECG was T wave inversion in the Right precordial leads. The authors of this study speculate that this finding is more common in PE with FRHTS due to higher right ventricular overload secondary to elevated pulmonary artery pressure [10].

Most FRHTS have been diagnosed in the setting of suspected PE, and only a few are found during echocardiographic evaluation of a patient hospitalized for other reason. A high proportion of the patients in our meta-analysis had pulmonary embolism (85% of the cases), which is consistent with other reports published [4,6,7],

In this Pooled analysis, the diagnosis of FRHTS was made by trans- thoracic echocardiography in 88% of the cases and by computed tomog- raphy scan or transesophageal echocardiography in the rest of the

Table 2

Mortality analysis.

Mortality yes (n = 44)

Baseline characteristics

Age (median and IQR 25-75)

60 (47-72)

60 (55-74)

0.1

Male sex, (n = 207; n %)

26 (59.1%)

81 (49.7%)

0.26

Hypotension (n = 192, n %)

20 (51.3%)

47 (30.7%)

0.01

Tachypnea (n = 183; n%)

27 (67.6%)

76 (52.4%)

0.09

Respiratory failure (n = 183; n %)

23 (62.2%)

65 (44.5%)

0.055

Mortality no (n = 163)

p Value

in association with underlying heart anomalies, similar to the thrombi in the left heart chambers. Although the prevalence of type B thrombi is unknown, they have better outcomes than type A thrombi [14,15].

We found an overall mortality of 21.3%, which is similar to the one reported in the international PE registry by Torbicki et al. (21%, 42 cases) [16], slightly lower than that of the series by Rose et al. (27.1%, 177 cases), and definitely lower than the mortality reported by Chartier (44.7%, 38 cases) [1,9]. In this study, mortality rate decreases from 47.4% in patients with cardiogenic shock to 16% in patients without shock,

Shock (n = 193; n %)

Clinical presentation Dyspnea (n = 198; n %)

21 (53.8%)

39 (88.6%)

44 (28.6%)

123 (80.5%)

0.003 demonstrating that the outcome depends on the hemodynamic status. The optimal management of FRHTS remains controversial due to the

0.2 lack of prospective, randomized trials to answer this question. The bib-

Chest pain (n = 197; n %)

10 (22.7%)

45(29.4)

0.3

liography shows variable results of meta-analysis or case series. In 1989,

Syncope (n = 196; n %)

9 (20.9%)

23 (15%)

0.32

the meta-analysis published by Kinney did not show any difference in

Palpitations (n = 195; n %)

2 (4.5%)

16 (10.5%)

0.23

the efficacy of the different treatments used, with an estimated proba-

Focal deficits (n = 195; n %)

Hemoptysis (n = 197; n %)

1 (2.3%)

1 (2.3%)

8 (5.2%)

4 (2.6%)

0.4

0.8

bility of survival in patients with FRHTS and PE receiving heparin,

Cardiac arrest (n = 195; n %)

3 (6.8%)

2 (1.3%)

0.075 thrombolytic agents, surgical embolectomy, or none of the above of

Electrocardiographic characteristics RBBB (n = 127, n %)

RV strain (n = 127; n %)

3 (10.3%)

7 (24.1%)

8 (8.2%)

26 (26.5%)

0.7

0.7

70%, 62%, 62% and 19%, respectively [8]. In the analysis by Rose et al. in

2003, which included 177 patients with FRHTS, mortality was 100% in those who did not receive treatment, 28.6% in those receiving

Inverted T waves inferior/right

10 (34.5%)

29 (29.6%)

0.6

anticoagulation therapy, 23.8% in the surgical group and 11.3% in pa-

precordial leads (n = 127; n %)

tients treated with thrombolysis, demonstrating that thrombolytic ther-

Echocardiographic characteristics

apy was associated with an improved survival rate when compared

LVEF b 50% (n = 71; n %)

3 (25%)

15 (25.4%)

0.9

either with anticoagulation therapy or surgery [9]. The European Coop-

Right ventricular dilation (n = 124; n %)

25 (96%)

91 (92%)

0.5

erative Study reported a mortality rate of 60% for patients receiving

Right ventricular dysfunction

(n = 103; n %)

20 (95.2%)

62 (75.6%)

0.046

PASP (n = 110; median and IQR)

64 (17)

55 (21)

0.1

Diagnosis during hospitalization PE (n = 188; n %)

37 (92.5%)

139 (93.9%)

0.74

DVT (n = 69; n %)

5 (31.3%)

64 (56.6)

0.057

Treatment received None (n = 207; n%)

0 (0%)

1 (100%)

Anticoagulation (n = 207; n %)

16 (36.4%)

28 (63.6%)

0.03

Systemic fibrinolysis (n = 207; n %)

12 (18.2%)

54 (81.8%)

Surgical thrombectomy (n = 207; n %)

16 (18%)

73 (82%)

In situ fibrinolysis (n = 207; n %)

0 (0%)

4 (100%)

Percutaneous thrombectomy

0 (0%)

3 (100%)

(n = 207; n %)

Abbreviations: RBBB: right bundle branch block, RV: right ventricle; LVEF: left ventricle ejection fraction; PSAP: pulmonary systolic artery pressure; PE: pulmonary embolism; DVT: deep vein thrombosis.

patients. The diagnosis of FRHTS is feasible with transthoracic echocar- diography, and has a sensitivity of 50-60% to detect right heart thrombi; yet, the size of the clot may be underestimated. Transesophageal echo- cardiography has better resolution, and most of the time better acoustic window, reaching segments of the right ventricle that the transthoracic method cannot; allowing a more accurate diagnosis of FRHTS [11,12]. Transthoracic echocardiography is a simple method, widely available, and can be performed at the bed side without requiring anesthesia, while transesophageal echocardiography could provide better assess- ment of the clot size with the correct diagnosis of a patent foramen ovale which may put the patient at risk of systemic embolism.

In the studies included in the present meta-analysis, we found that the diagnosis of DVT was made in one out of three patients, suggesting that, although this condition could have been underestimated, clot for- mation could be due to a local phenomenon rather than to be the con- sequence of venous embolism. Two major thrombus types with different morphology, etiology and clinical significance have been iden- tified [6]. Type A thrombi have a spiral shape, are extremely mobile and are associated with deep venous thrombosis and pulmonary embolism. The hypothesis is that these clots are transferred from the great veins and are lodged in transit in the right heart chambers. The Predisposing factors include prominent eustachian valves, tricuspid regurgitation, low cardiac output and pulmonary artery hypertension [13]. Type B thrombi are not mobile and develop within the right heart chambers

anticoagulation drugs, 40% for those treated with thrombolytic therapy and 27% for patients undergoing surgery [6]. It is important to empha- size that in the last 30 years there has been few changes in the available therapeutic strategies. Percutaneous techniques for the administration of thrombolytic or material aspiration were recently introduced with scant case reports. In our series only 7 patients with techniques different from surgery, systemic fibrinolytics or anticoagulation were included. Our analysis demonstrated that the patients who received only anticoagulation therapy had poor outcome compared with those treated with systemic fibrinolysis or surgical thrombectomy. This find- ing is consistent with the different series, showing that anticoagulation per se seems to be sufficient to prevent embolism or to reperfuse large emboli, as in PE with hemodynamic impairment. Based on this analysis, it seems that the hemodynamic status guided the therapeutic manage- ment, as those patients with greater impairment did not undergo sur- gery. Although no differences were observed between the therapeutic strategies according to the hemodynamic status, the mortality rate in unstable patients was 47.4% with surgery, compared with the 40% Seen in patients treated with anticoagulation alone. On the other hand, stable patients undergoing surgery presented a mortality rate of 9.4%. Surgery is an effective strategy to remove FRHTS and clots from the main pulmonary arteries. However, surgery requires cardiopulmo- nary bypass, trained surgeons and a time interval that may limit the re- sults. Thrombolytic agents have the advantage that they can be administered rapidly, are effective in FRHTS, in thrombi in the proximal and distal pulmonary arteries and in venous thrombosis. Their disad- vantage is the risk of major bleeding and that, in case they fail, surgery should be postponed until they are eliminated. We did not find differ- ences in the outcome between both techniques, as it happened with other series in which thrombolysis seemed to have better results. Thus, we should define treatment based on the risk and benefits of each strategy for each of our patients. novel techniques, as aspiration thrombectomy, still lack sufficient number of patients to evaluate the results of this apparently promising strategy.

Conclusion

This study shows that FRHTS represent a serious form of thrombo- embolism that requires rapid decisions to improve the survival of the patients. Anticoagulation as the only strategy does not seem to be suffi- cient, while thrombolysis and surgical thrombectomy show better and

similar results. A proper individualization of the risk and benefits of both techniques is necessary to choose the most appropriate strategy for our patients.

Source(s) of support

None.

Conflict of interest declaration

None.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi. org/10.1016/j.ajem.2017.10.045.

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