Anda di halaman 1dari 16

Intensive Care Med

https://doi.org/10.1007/s00134-018-5211-z

SYSTEMATIC REVIEW

The use of echocardiographic indices


in defining and assessing right ventricular
systolic function in critical care research
Stephen J. Huang1*, Marek Nalos1, Louise Smith2, Arvind Rajamani1 and Anthony S. McLean1

© 2018 Springer-Verlag GmbH Germany, part of Springer Nature and ESICM

Abstract 
Purpose:  Many echocardiographic indices (or methods) for assessing right ventricular (RV) function are available, but
each has its strengths and limitations. In some cases, there might be discordance between the indices. We conducted
a systematic review to audit the echocardiographic RV assessments in critical care research to see if a consistent
pattern existed. We specifically looked into the kind and number of RV indices used, and how RV dysfunction was
defined in each study.
Methods:  Studies conducted in critical care settings and reported echocardiographic RV function indices from 1997
to 2017 were searched systematically from three databases. Non-adult studies, case reports, reviews and secondary
studies were excluded. These studies’ characteristics and RV indices reported were summarized.
Results:  Out of 495 non-duplicated publications found, 81 studies were included in our systematic review. There
has been an increasing trend of studying RV function by echocardiography since 2001, and most were conducted in
ICU. Thirty-one studies use a single index, mostly TAPSE, to define RV dysfunction; 33 used composite indices and the
combinations varied between studies. Seventeen studies did not define RV dysfunction. For those using composite
indices, many did not explain their choices.
Conclusions:  TAPSE seemed to be the most popular index in the last 2–3 years. Many studies used combinations of
indices but, apart from cor pulmonale, we could not find a consistent pattern of RV assessment and definition of RV
dysfunction amongst these studies.
Keywords:  Echocardiography, Right ventricular function, Critical care, Intensive care, Emergency, Anaesthetics

Introduction been reported as a predictor for mortality and morbidity


Acute right ventricular (RV) dysfunction is common in in critically ill patients [1, 2].
the critically ill population, especially where RV after- Assessment of RV function is part of patient care in
load is increased such as in patients with massive pulmo- the critical care setting. Traditionally, RV function has
nary embolism and acute respiratory distress syndrome been assessed by invasive right-heart catheterisation.
(ARDS). Other common causes of acute RV dysfunction However, the procedure of right-heart catheterisation is
are RV myocardial infarction and post-operative RV fail- cumbersome and risky [3], and RV function can only be
ure. RV dysfunction, including acute cor pulmonale, has inferred from intracardiac pressures and cardiac output
information [4]. Direct quantification of RV function is
*Correspondence: Stephen.huang@sydney.edu.au
impossible with this method. In the last 20  years, right-
1
Department of Intensive Care Medicine, Nepean Hospital, Sydney heart catheterisation has been gradually supplanted by
Medical School, The University of Sydney, Sydney, NSW, Australia non-invasive transthoracic echocardiography (TTE), or
Full author information is available at the end of the article
minimally invasive transoesophageal echocardiography
(TEE). Echocardiography offers many advantages in RV as ejection fraction cannot be based on a symmetrical
function assessment, including the ability to estimate conical shape [5]. Second, over the years many echocar-
intracardiac or pulmonary artery pressures, the quantifi- diographic RV function indices have been introduced
cation of RV function, the measurement of cardiac out- as surrogates of RV function (Table  1). Some of these
put and the ability to be performed at the bedside quickly indices measure the longitudinal (regional) function
and non-invasively. As such, critical care echocardiogra- of the RV (e.g. tricuspid annular plane systolic excur-
phy has become an essential part of patient care in the sion or TAPSE) while others measure the global func-
critical care setting. tion (e.g. fractional area change or FAC). Each index has
Echocardiographic assessment of RV function is not pros and cons (Table 1), but may not necessary yield the
without challenges. First, the geometry of the RV is com- same information. Third, the quality of images and tech-
plex; hence unlike the left ventricle (LV), assessment such nical limitations may preclude operators from obtaining

Table 1  Summary of common objective echocardiographic indices for RV function


Index Description Advantages Disadvantages (limitations)

Longitudinal function index


  TAPSE A single dimensional measurement of Easy to perform Angle-dependent
the longitudinal motion of the tricuspid Quick Maybe misleading if regional wall motion
annular plane Minimal training required abnormalities are present
Measured at lateral free wall Less dependent on image quality Subject to LV motion and translational
Averaging is easy to perform artefact
Good intra- and interoperator reproduc-
ibility
  St A single dimensional measurement of the Easy to perform Angle-dependent
peak longitudinal systolic velocity of the Quick Maybe misleading if regional wall motion
tricuspid annulus Less subject to 2D image quality abnormalities are present
Measured at lateral free wall Less dependent on image quality Subject to LV motion and translational
Averaging is easy to perform artefact
Good intra- and interoperator reproduc-
ibility
  RVS A single dimensional measurement of Not angle-dependent Requires good image quality
the percentage change in longitudinal Yields regional wall motion information Relatively time-consuming
length Not subject to translational artefact Requires off-line analysis
Measured at lateral free wall Requires extra and expensive software
Special training required
Poor interoperator variabilities
Global function index
  FAC A two dimensional measurement of the Not angle-dependent Requires good image quality
change in RV area Not subject to regional wall motion infor- Relatively time-consuming
Usually measured in the longitudinal view mation Some training required
but some use the cross-sectional view Not subject to translational artefact RVOT not included in assessment
Similar to and correlates with ejection Fair interoperator reproducibility Does not necessarily correlate with PASP
fraction
  Tei A Doppler (or tissue Doppler) measurement Not subject to regional wall motion Angle-dependent
­indexa of the ratio of sum of isovolumic times to abnormality Depends on good Doppler signal
ejection time Not subject to translational artefact Not recommended in irregular heart beats
Reflects both systolic and diastolic function Sensitive to loading conditions Moderate intra- and interoperator variabilities
(combined) Less subject to image quality
  EDA A two dimensional measurement of the Not angle-dependent A mild increase does not imply RV dysfunc-
ratio ratio of RV end-diastolic to LV end- Not subject to regional wall motion infor- tion
diastolic ratio mation Requires good image quality
A measure of how severe the RV is dilated Not subject to translational artefact Relatively time-consuming
compared to LV Sensitive to loading conditions Some training required
Severely dilated RV usually connotes RV Good intra- and interoperator variabilities
dysfunction
Usually used in conjunction with paradoxi-
cal septal motion in defining cor pulmo-
nale
TAPSE tricuspid annular plane systolic excursion, St tissue Doppler of the tricuspid annular systolic velocity, RVS right ventricular strain, FAC fractional area change, EDA
ratio RV end-diastolic area to LV end-diastolic area ratio
a
  Also known as RV index of myocardial performance (RVIMP)
certain RV function indices in the critical care setting. function indices. The following terms were accepted as an
Because of these challenges, we were curious to find out alternative to “RV systolic function” in the articles: “RV
how RV function was assessed and defined echocardio- function” (except diastolic function), “RV dysfunction” or
graphically in critical care research. As there is no sys- “cor pulmonale”. Studies types were classified objectively
tematic review available on this topic, we conducted a on the basis of how the investigators conducted the study,
narrative (descriptive) systematic review to summarize analysed the data and what was reported. Descriptive and
the echocardiographic assessments of RV function in summary statistics were provided where appropriate. All
critical care research (PROSPERO Registration Number: statistics and graphics were performed and produced
CRD42018092716). using the open statistical software R (version 3.4.3) (The
R Foundation for Statistical Computing, Austria, http://
Methods www.R-proje​ct.org/).
Eligibility criteria
All studies must have utilized echocardiography, either Results
transthoracic or transoesophageal, to assess RV systolic Number of studies included
function and been conducted in a critical care setting: The searches returned 592 studies, of which 97 studies
anaesthetic departments (AD), emergency departments were duplicated in more than one databases. A total of
(ED) or intensive care units (ICU). Both observational 414 studies were excluded for not meeting one or more
studies and clinical trials were eligible. Non-adult studies, of the criteria and 78 studies met all inclusion criteria
case studies/series, reviews and secondary studies were (Fig.  1). Three studies of the authors’ own works were
not eligible. also included [6–8]. Altogether, a total of 81 relevant
studies were included in this systematic review (Table 2).
Search strategy and databases
In order to capture most of the primary studies, we
employed a high sensitivity (broadened) strategy by Jan 1997 - June 2017:
searching the following text words: {[“right ventri*” OR
PubMed 319
“cor pulmonale” (Title and Abstract)] AND [“echocar- Embase + Medline 270
diogr*” (Title and Abstract)] AND [“critical care” OR Other sources 3
Total 592
“intensive care” OR “emergency” OR “anesth*” OR
“anaesth*” (All field)]}. To study the evolution of different
echocardiography measurements of RV function, pub- Excluded 97 duplicates
lications dating back 20  years (from 1997 to June 2017)
were searched (the search was performed in August
2017). Three databases, PubMed and EMBASE (with PubMed 316
Medline via Ovid), were used. The following filters were Embase + Medline 176
Other sources 3
applied: human, adult, English language, and journal Total 495
articles.

Excluded 414 from PubMed and Embase:


Studies selection
Two investigators (SJH and MN) manually screened all PubMed Embase
Case studies 132 68
the abstracts independently according to the predeter- Reviews 2 2
mined eligibility criteria (see above). Case studies, com- Guidelines 1 0
Non-critical care 62 10
mentaries, reviews and secondary studies were excluded. Non-echo 13 5
Full text articles were downloaded for screening if the No RV data 45 49
Non-adult 3 3
information provided in the abstract was not obvious. Study protocol 1 0
Any disagreements were resolved through discussion Irrelevant studies 0 1
Non-English 10 7
with a third independent investigator (ASM). Total 269 145

Data extraction and statistics


PubMed 47
The full text articles of all eligible studies were obtained, Embase + Medline 31
and the following information was extracted: study design Other sources 3
Total 81
and type of study, year of publication, setting, types and
number of subjects (patients), definition of RV function Fig. 1  Flow diagram showing the number of excluded and eligible
or dysfunction, and all reported echocardiography RV studies
Table 2  Details of included studies
No. First authors Patient ­typea Setting/country Sample Study ­typeb RV function surro- Basis for definition
size gates ­measuredc of RV dysfunction

1 Ochiai et al. [9] Cardiac surgery ICU/Japan 14 Association (PO) PA loops (Ees), FAC FAC
2 Ochiai et al. [10] Cardiac surgery ICU/Japan 11 Association (PO) PA loops (Ees), FAC FAC
3 Vieillard-Baron et al. ARDS ICU/France 75 Prognosis (PO) EDA ratio, PSM, FAC Conjunctive Cidx (EDA
[11] ratio + PSM)
4 Jackson et al. [12] PE ED/USA 124 Diagnosis (PO) RV contractility, PSM, Not defined
RV dilatation, PASP
5 Vieillard-Baron et al. PE ICU/France 98 Descriptive (RO) EDA ratio, PSM, FAC Conjunctive Cidx (EDA
[13] ratio + PSM)
6 Maslow et al. [14] Cardiac Anaesth/USA 41 Prognosis (RO) FAC, RVWM FAC
7 McLean et al. [6] Mixed ICU/Australia 84 Diagnosis (PO) TAPSE TAPSE
8 McLean et al. [7] Mixed ICU/Australia 121 Association (PO) TAPSE TAPSE
9 Catena et al. [15] Cardiac ICU/Italy 8 Descriptive (PO) FAC FAC
10 Mansencal et al. [16] PE ED/France 46 Diagnosis (PO) EDA ratio EDA ratio
11 Bal et al. [17] Shock ICU/France 41 Diagnosis (PO) EDA ratio EDA ratio
12 Lamia et al. [18] Mixed ICU/France 86 Association (PO) TAPSE, EDA ratio, FAC Not defined
13 Mokart et al. [19] Sepsis ICU/France 51 Prognosis (PO) RV dilatation, PSM, Permuted Cidx [EDA
PASP ratio + (PSM or
PASP)]
14 Gallotta et al. [20] PE ED/Italy 90 Prognosis (PO) RV dilatation, PSM, Compensatory Cidx
TAPSE
15 Aksay et al. [21] PE ED/Turkey 77 Prognosis (RO) RV dilatation, RVWM, Compensatory Cidx
PSM
16 Kline et al. [22] PE ED/USA 161 Prognosis (PO) RVWM Subjective RVWM
17 Sade et al. [23] Mixed ICU/Turkey 89 Agreement (PO) FAC, St FAC
18 Vieillard-Baron et al. ARDS ICU/France 42 Association (PO) EDA ratio, PSM Conjunctive Cidx
[24]
19 McLean and Huang Sepsis ICU/Australia 40 Prognosis (PO) St St
[8]
20 Kline et al. [25] PE ED/USA 152 Prognosis (PO) RVWM Subjective RVWM
21 Tousignant et al. [26] Cardiac Anaesth/Canada 24 Agreement (PO) St, RVS, RVSR, IVA Not defined
22 Palmieri et al. [27] PE ED/Italy 89 Association (PO) EDA ratio, PSM, TAPSE Conjunctive Cidx
23 Dessap et al. [28] ARDS ICU/France 11 Association (PO) EDA ratio, eccentricity Conjunctive Cidx
ratio
24 Tousignant et al. [29] Cardiac Anaesth/Canada 24 Descriptive (PO) TAPSE, St Not defined
25 Mahjoub et al. [30] Shock ICU/France 35 Diagnosis (PO) TAPSE, St Not defined
26 Gernoth et al. [31] ARDS ICU/Italy 12 Association (PO) Tei Tei
27 Ricci et al. [32] Cardiac ICU/USA 53 Prognosis (RO) FAC FAC
28 Matyal et al. [33] Lung surgery Anaest/USA 59 Prognosis (PO) Tei, St Tei
29 Karakilic et al. [34] AHF ED/Turkey 34 Association (PO) St, RVS St
30 Gackowski et al. [35] Cardiac surgery ICU/Poland 40 Prognosis (PO) TAPSE TAPSE
31 Rendina et al. [36] PE ED/Italy 211 Association (RO) PSM, RV dilatation, Compensatory Cidx
RVWM, PASP
32 Papaioannou et al. APO ICU/Greece 32 Prognosis (PO) FAC, TAPSE, St Not defined
[37]
33 Dessap et al. [38] ARDS ICU/France 203 Prevalence & progno- EDA ratio, PSM Conjunctive Cidx
sis (PO)
34 Fougéres et al. [39] ARDS ICU/France 21 Association (PO) EDA ratio, PSM Conjunctive Cidx
35 Haas et al. [40] Surgical Anaesth/Germany 10 Descriptive (PO) TAPSE, FAC, St, EDA Not defined
ratio
36 Albers et al. [41] Cardiac surgery ICU/Germany 73 Association (PO) St, RVS, RVSR Not defined
37 Park et al. [42] Respiratory ED/Korea 52 Diagnosis (PO) FAC, Tei, RVS Not defined
38 Golpe et al. [43] PE ED/Spain 103 Association (PO) RV dilatation, RVWM Compensatory Cidx
Table 2  continued
No. First authors Patient ­typea Setting/country Sample Study ­typeb RV function surro- Basis for definition
size gates ­measuredc of RV dysfunction
39 Brown et al. [44] Sepsis ICU/USA 23 Prevalence (PO) FAC, TAPSE Compensatory Cidx
40 Park et al. [42] PE ICU/Korea 24 Diagnosis (PO) FAC, Tei, RVS, St Not defined
41 Guervilly et al. [45] ARDS ICU/France 16 Interventional (PT) EDA ratio, PSM Conjunctive Cidx
42 Schuuring et al. [46] Cardiac surgery ICU/Netherlands 86 Descriptive (PO) TAPSE, St, Tei Compensatory Cidx
43 Furian et al. [47] Sepsis ICU/Brazil 45 Descriptive (PO) St St
44 Corciova et al. [48] Cardiac surgery ICU/Romania 171 Prognosis (RO) TAPSE TAPSE
45 Fichet et al. [49] ARDS ICU/France 50 Feasibility (PO) FAC, TAPSE, St, EDA Permuted Cidx
ratio, PSM
46 Harmankaya [50] Sepsis ICU/Turkey 55 Prognosis (PO) St, Tei Not defined
47 Fagnoul et al. [51] Sepsis ICU/Belgium 46 Descriptive (PO) St, EDA ratio EDA ratio
48 Franchi et al. [52] Mixed ICU/Italy 20 Association (PO) TAPSE, RVS RVS
49 Schuuring et al. [53] Cardiac surgery ICU/Netherlands 412 Association (RO) TAPSE, St Conjunctive Cidx
50 Lhéritier et al. [54] ARDS ICU/France 201 Prevalence & progno- EDA ratio, eccentricity Conjunctive Cidx
sis (PO) index, PSM
51 Boissier et al. [55] ARDS ICU/France 226 Prevalence & progno- EDA ratio, PSM Conjunctive Cidx
sis (PO)
52 Hyllen et al. [56] Cardiac surgery ICU/Sweden 40 Association (PO) FAC, TAPSE, St, Tei, Subjective
RVSP, RVS
53 Kusunose et al. [57] Lung surgery ICU/USA 89 Prognosis (RO) FAC, TAPSE, RVS Compensatory Cidx
54 Madhaven et al. [58] Respiratory Anaesth/India 20 Descriptive (PO) FAC, TAPSE, Tei, St Not defined
55 Yildirim et al. [59] Sepsis ED/Turkey 211 Association (PO) TAPSE TAPSE
56 Ramjee et al. [60] Cardiac ED/USA 291 Prognosis (RO) Subjective RV size and Subjective
RV systolic function
score
57 Bloomer et al. [61] PE ED/Netherlands 31 Descriptive (PO) Subjective RV systolic Subjective
function score
58 Denault et al. [62] Cardiac surgery ICU/Canada 120 Interventional (PT) FAC, TAPSE, St Compensatory Cidx
59 Guinot et al. [63] Cardiac surgery ICU/France 99 Prognosis (PO) St, TAPSE, RVEF, RV Permuted Cidx (any
dilatation two)
60 Denault et al. [64] Cardiac surgery Anaesth/Canada 110 Association (post hoc) TAPSE, FAC TAPSE
61 Imada et al. [65] Cardiac surgery Anaesth/Japan 54 Agreement (RO) FAC, RVEF Not defined
62 Khemasuwan et al. PE ICU/USA 211 Prognosis (RO) RV dilatation, PASP, Not defined
[66] TAPSE, RVS, RVSR
63 Azari et al. [67] PE ICU/Iran 30 Descriptive (PO) TAPSE Not defined
64 Perez-Teran et al. [68] Lung surgery ICU/Spain 120 Prognosis (RO) FAC, TAPSE, St, RVS Not defined
65 Russell et al. [69] Dyspnoea ED/USA 198 Descriptive (post hoc) RVWM Subjective RVWM
66 Legras et al. [70] ARDS ICU/France 195 Prevalence (PO) TAPSE, EDA ratio, FAC, Conjunctive Cidx (EDA
PSM, PASP ratio + PSM)
67 Dahhan et al. [71] PE ED/USA 69 Prognosis (RO) TAPSE, Tei, FAC, RVS Not defined
68 Nadziakiewicz et al. Cardiac ICU/Poland 23 Association (RO) TAPSE, FAC, RV dilata- Conjunctive Cidx
[72] tion, EDA ratio
69 Dessap et al. [2] ARDS ICU/France 752 Prevalence (PO) EDA ratio, PSM Conjunctive Cidx
70 Tuzovic et al. [73] PE ED/US 82 Association (RO) RVWM, RVS, FAC, Subjective (RVWM)
TAPSE
71 Biteker et al. [74] Sepsis ED/Turkey 111 Association (PO) TAPSE TAPSE
72 Lazzeri et al. [75] ARDS ICU/Italy 42 Prognosis (PO) TAPSE, EDA ratio TAPSE
73 Mishra et al. [76] Cardiac surgery ICU/India 40 Interventional (PT) TAPSE, St, Tei Permuted Cidx (any
combination)
74 Abtahi et al. [77] Cardiac ED/Iran 60 Association (PO) TAPSE, St, Tei Tei
75 Lazzeri et al. [78] ARDS ICU/Italy 74 Prognosis (PO) TAPSE TAPSE
Table 2  continued
No. First authors Patient ­typea Setting/country Sample Study ­typeb RV function surro- Basis for definition
size gates ­measuredc of RV dysfunction
76 Lazzeri et al. [79] ARDS ICU/France 46 Prognosis (PO) RV dilatation, PSM, Permuted Cidx (any
PASP, TAPSE one or combina-
tion of RV dilata-
tion + PSM)
77 Cecchini et al. [80] ARDS in sicklers ICU/France 362 Prevalence & progno- EDA ratio, PSM Conjunctive Cidx
sis (RO)
78 Dudzinski et al. [81] PE ED/USA 298 Diagnosis (PO) RVWM, RV dilatation, Compensatory Cidx
PSM
79 Jia et al. [82] PE ED/China 113 Diagnosis (RO) RVWM, EDA ratio, Permuted Cidx (any
PASP, TAPSE, RV combination)
dilatation
80 Diaz-Gomez et al. [83] Cardiac ICU/USA 45 Agreement (PO) TAPSE, SEATAK TAPSE
81 Weekes et al. [84] PE ED/USA 123 Prognosis (post hoc) TAPSE TAPSE
a
  AHF acute heart failure, APO acute pulmonary oedema, ARDS acute respiratory distress syndrome, PE pulmonary embolism
b
  Post hoc post hoc analysis of previous trial or observational study, PO prospective observational study, PT prospective trial, RO retrospective observational study
c
  Cidx composite index, EDA ratio RV end-diastolic area to LV end-diastolic area ratio, FAC fractional area change, IVA isovolumic acceleration, PA loop (Ees) pressure–
area loop (end-systolic elastance), PASP pulmonary artery systolic pressure, PSM paradoxical septal motion, RVS RV strain, RVSR RV strain rate, RVWM RV wall motion,
SEATAK subcostal echocardiographic assessment of tricuspid annular kick, St tricuspid annular systolic velocity, TAPSE tricuspid annular plane systolic excursion, Tei Tei
(myocardial performance) index

The total number of relevant publications per year descriptive in nature (37.5%), approximately two-thirds
is shown in Fig.  2a. The earliest studies that reported of the studies in ED and ICU were of prognosis and asso-
echocardiographic indices for RV function were found ciation types. Diagnostic studies were also common in
in 1998 and 1999 (n = 2) [9, 10]. There had been a sud- ED (22.7%). ICU had more variety of studies.
den increase in the number of studies from 2007, and
then another surge in 2015. The number of studies Cohorts and sample size
found in the first 6  months of 2017 was 4. Most studies The study populations were from a wide range of
(63.0%) were conducted in ICU (n = 51), followed by ED patients, and most were patients with pulmonary embo-
(n = 22 or 27.1%) and the rest were in AD (n = 8 or 9.9%) lism (PE), acute respiratory distress syndrome (ARDS),
(Fig. 2b). cardiac surgery, cardiac dysfunction or sepsis (Fig.  3a).
The distribution of patient types was also setting specific
Characteristics of studies (Fig. 3b): studies in AD were mostly surgical patients or
Sixty-one studies (75.3%) were prospective in design patients with underlying cardiac problems, studies in ED
and 17 (21.0%) were retrospective observational stud- were mostly with PE (n = 15), and ICU studies displayed
ies. Three of the 61 prospective studies were clinical tri- a wide spectrum of patients comprising both surgical and
als [45, 62, 76], the rest were observational studies. Three medical patients but mostly ARDS patients.
were post hoc analysis of previously conducted studies Supplementary Figure S2 shows the study sample sizes
[64, 69, 84]. over the last 20  years. The minimum sample size was 8
and the maximum was 752. Half of the studies had sam-
Types of studies ple sizes of 60 or less. There has been a trend of increas-
Most employed TTE (n = 54), 19 studies used TEE and ing sample size in the last 10 years, in particular ICU and
8 used both. Most studies were either prognosis (n = 23 ED studies. The median sample sizes for ICU and ED
or 28.4%) or association (n = 22 or 27.2%) studies. Twelve studies were 50 and 107, respectively. Sample sizes in AD
(14.8%) were descriptive and 9 (11.1%) were diagnos- studies were smaller (median = 32).
tic studies. Few were interventional (n = 3), agreements
between two or more methods (n = 4) or prevalence stud- Feasibility, intra‑ and interobserver agreements
ies (n = 3). Five studies had both prevalence and progno- Twenty-four studies reported feasibility as the number
sis characteristics (Supplementary Material Fig. S1). The of patients that the investigators  were unable to obtain
distributions of the types of studies in different settings echocardiograms. The average proportion of patients
were also slightly different (Supplementary Table  S1). reported to have poor acoustic views or images was 7.9%,
While the predominant type of studies in AD setting was ranging from 0% to 27%. Two studies which used TTE
a b
50

12
45

40
10

Total number of publications


Total number of publications

35

8
30

25
6

20

*
4 15

10
2
5

0 0

1995 2000 2005 2010 2015 Anesthetic ED ICU


Year Setting
Fig. 2  Characteristics of included studies. a Total number of relevant publications per year. b Total number of publications in each setting. *Up to
June 2017. ED emergency department, ICU intensive care unit

reported more than 25% of patients with poor acoustic than one indices for RV function. Among those which had
windows [65, 72]. Thirteen and sixteen studies reported clear definitions, 31 studies (50%) defined RV dysfunc-
intra- and interobserver agreements, respectively. tion based on a single index, including EDA ratio, FAC,
Another two studies did not report the agreements in RV strain (RVS), tissue Doppler tricuspid annular systolic
the studies but quoted the authors’ previous reports on velocity (St), TAPSE, Tei index, as well as subjective score
agreements. Agreements were reported as variabilities, of RV free wall motion (RVWM) (Fig. 5). TAPSE was the
Pearson correlations, kappa correlations or intraclass most common index used singly in defining RV dysfunc-
correlations. tion, followed by FAC and EDA ratio.
The use of more than one index, or composite indices
RV function indices (Cidx), to define RV dysfunction was also common among
Number of  indices measured per  study  Figure  4 shows studies (n = 33). The number of RV function indices meas-
the distribution of the number of RV indices measured per ured and the number used in defining RV dysfunction
study. Three AD studies used subjective scoring of RV sys- are shown in Table  3. The table shows that the number
tolic function, details of which were not available. Eighteen measured might not necessarily be the same as the num-
studies reported one RV function index. Sixty reported mul- ber used in defining RV dysfunction. Three types of Cidx
tiple (> 1) indices, amongst which six reported five or more. were reported: (1) compensatory Cidx (the “OR” rule),
i.e. the diagnosis of RV dysfunction was based on any one
Definitions of RV dysfunction  RV dysfunction or similar of the surrogates that was reported as abnormal (n = 11);
terms (see “Methods”) was clearly defined in 64 of the 81 (2) conjunctive Cidx (the “AND” rule), i.e. the diagno-
studies (79.0%) (Fig. 5). Seventeen studies (21.0%) did not sis of RV dysfunction required all surrogates reported as
define RV dysfunction and 16 of these measured more abnormal (n = 14); and (3) permuted Cidx which used any
a ca
l
rgi
Su ck
o
Sh
p sis
Se y
Study cohorts

r
ato
pir E
R es P
d
xe
Mi
i o n
c t
r e se a
t / e
lan yspn
sp
t ran
D
r g ery
ng su
Lu ac rdiac
rdi
Ca Ca S
D
AR
0 2 4 6 8 10 12 14 16 18 20
Total number of publications

b Anesthetic ED ICU
l
ca
rgi
Su ock
Sh is
ps
Se ry
Study cohorts

to
ira
sp PE
Re
d
xe
Mi n
ti o
ec
res ea
l a nt/ spn
p y
ns D ery
tra urg
u ng i a c s diac
L rd Car S
Ca D
AR
0 5 10 15 0 5 10 15 0 5 10 15
Total number of publications
Fig. 3  a Breakdown of study cohorts for all studies. b Breakdown of cohort for each setting. ARDS acute respiratory distress syndrome, PE pulmo-
nary embolism

combination of  at least two indices (n = 5). As a result of Discussion


the nature of pathophysiology, the use of Cidx was common Our systematic review evaluated 81 eligible studies over
amongst studies involving ARDS or pulmonary embolism the last 20  years and noticed an increased in interest in
(Table  2). The most common combination was the use of echocardiographic assessments of RV in research, espe-
EDA ratio and paradoxical septal motion (PSM) in defin- cially since late 2000. These studies could be categorized
ing cor pulmonale (n = 15). A significant number of stud- according to settings, study design as well as patient
ies (n = 16) did not define RV dysfunction clearly, although types. Large differences were seen in the number of
objective indices were measured. echocardiographic indices used and how RV dysfunction
was defined. While some studies used a single index to
Evolution of echocardiographic indices for RV function define RV dysfunction, many used Cidx or did not define
Supplementary Figure S3 shows the evolution of the usage RV dysfunction based on the indices they measured. The
of common RV function indices in the last 20  years. The emerging trend was the use of TAPSE.
indices shown in the figure were those measured in the
studies and were used in isolation or in combination with Study characteristics
other indices in defining RV function. The figure shows the Studies involving echocardiography in the critical care
frequency of each index being reported in published stud- setting were sparse prior to 2000 as echocardiography
ies per year. Several features are noticeable in the figure. was rarely available before 2000, and continued to be
First, there was a trend of increasing use of objective indices, very small in number in early 2000s (1–2 publications per
such as EDA ratio, FAC, TAPSE, St and Tei index. Subjective year) [85]. Among the three main areas of critical care,
RV wall motion (RVWM) assessment was seldom used in intensive care was the earliest to report the use of echo-
research. Second, there was also a rise in the use of FAC and cardiography in research [86, 87]. One of the earliest RV
TAPSE in recent years. The use of TAPSE started in 2003 studies using TTE was in 1987 [86], and the first TEE
and there has been a dramatic increase in the last 2–3 years. assessment of RV was reported in 1992 [88]. The number
30

25
Total number of publications

20

15

10

0 1 2 3 4 5 6
Number of different RV function indices reported
Fig. 4  Number of different RV function indices measured or reported per study

increased in the late 2000s, which might reflect the surge The ability to obtain echocardiographic images in criti-
in interest in RV function, coupled with the increasing cally ill patients was crucial for both clinical practice and
availability of ultrasound machines and training in the research. About one-third of the studies reported the
critical care setting. feasibility of performing echocardiography. Fortunately,
Our review also showed that the intensive care setting most studies were able to obtain optimal echocardio-
has been the most active in the use of echocardiography grams for most patients. As expected, those studies uti-
in RV assessment in research. This might be because ICU lizing TTE had the highest failure rates (some as high as
patients requiring echocardiography are more diverse 27%). The position of the patients, co-morbidities (e.g.
than those in AD and ED settings. Apart from ARDS, COPD), mechanical ventilation, wounds and/or experi-
which is the most common type of study population, the ence of the operators might contribute to the high failure
ICU cohorts also comprised shock, post-surgical, sepsis rates in TTE. The failure to obtain optimal studies might
or other patients reflecting a multipurpose and versatile have encouraged the use of compensatory or permuted
role of echocardiography in ICU, more so than in ED and Cidx (see below). Unfortunately, the proportions of miss-
AD. Echocardiography is commonly used for diagnosis, ing data for various indices were not reported in most
monitoring and management, and for prognosis in ICU. studies. Intra- and interobserver agreements are impor-
These led to more diverse research topics which was tant to understand the reliability and reproducibility of
reflected in the types of studies found. specific echocardiographic measurements. We found that
There was a high prevalence (or interest) of ARDS only about 15–20% of the studies reported intra- and/or
studies in ICU. This is consistent with the cause of RV interobserver agreements. However, there seemed to be a
dysfunction which is most often related to acute respira- lack of a standard way of reporting observer agreements.
tory failure and high RV afterload due to positive-pres- On the basis of the small sample size and variable eval-
sure ventilation. On the other hand, PE studies were the uation criteria, it may be safe to conclude that many of
most common in ED, suggesting that echocardiography the studies were of low to moderate quality. Over the
was commonly used as a screening tool in selected high- years, there was a gradual increase in sample size, per-
risk patients. haps due to better research training in recent years and/
20

18

16
Total number of publications

14

12

10

ati
o C S
tive
) St SE Te
i x idx idx ve ed
Ar FA RV P Cid C dC cti fin
jec TA tor
y
tive bje de
ED (su
b
sa nc ute Su No
t
en nju rm
W M
mp Co Pe
RV Co
Definitions of RV dysfunction
Fig. 5  Number of studies using the index/indices shown in defining RV dysfunction. White column: RV dysfunction was defined on the basis of a
single index. Grey column: definition was based on more than one indices or on subjective index. Black column: definition not stated. EDA ratio RV
end-diastolic area to LV end-diastolic area ratio, FAC fractional area change, RVS RV strain, RVWM RV wall motion, St tissue Doppler tricuspid annular
systolic velocity, TAPSE tricuspid annular plane systolic excursion, Tei Tei index, Cidx composite indices

Table 3  Number of RV function indices measured and used in defining RV dysfunction


Definition of RV dysfunction Subjective index used Number of objective RV function indices measured Total
1 2 3 4 5 6

Single index 1 17 11 1 1 0 0 31
> 1 indices 2 0 11 12 3 4 1 33
Not defined 0 1 4 4 7 1 0 17
Total 3 18 26 17 11 5 1 81

or a higher demand in research quality imposed by the global function indices are more difficult to perform but
funding body or the journal. may yield important information such as loading condi-
tion (afterload), a combination of systolic and diastolic
RV function indices function as well as overall RV dysfunction due to regional
Echocardiographic RV function indices can be divided wall motion abnormalities.
into two types: ones that measure longitudinal function
and those that measure global function (Table  1). The Longitudinal function indices
former type allows fast and easy methods of assessing RV To date, the most frequently used RV function indices
function but are inherently limited as they do not yield in critical care research are those which measure the
regional wall motion information. On the other hand, longitudinal motion of the RV. These indices are often
dichotomised to differentiate between normal and abnor- patients, 93 had suboptimal to poor echocardiographic
mal, and do not provide a graded classification of RV windows for RVS acquisition [102]. Other challenges are
dysfunction (mild vs moderate vs severe). We found that reproducibility and intervendor comparability. Hence,
the most popular index reported in critical care research although strain measurement is the state-of-the-art
was TAPSE probably owing to its ease of measurement, method, they were the least used and reported indices.
reproducibility and less reliance on image quality. Good Perhaps with industrial standardization of speckle track-
correlations between TAPSE, RV ejection fraction and ing algorithm, and with more training available, there
FAC have been reported [89, 90]. However, TAPSE meas- may be more applications of RVS in research.
ures the longitudinal motion of the whole RV segment in
the apical view and does not yield regional wall motion Global function indices
information [89]. The use of TAPSE as a measure of RV In terms of global function indices, commonly reported
function is recommended in the American, European were the Tei index, EDA ratio and FAC. Tei index (also
and Canadian Societies of Echocardiography joint guide- known as RV index of myocardial performance) is
lines [91]. Yet, the guidelines also highlight the limita- defined as the ratio of the summation of isovolumic con-
tions of TAPSE by stating that “TAPSE assumes that the traction and relaxation times to ejection time [103]. As
displacement of a single segment represents the func- the index incorporates both systolic and diastolic func-
tion of a complex 3D structure. Furthermore, it is angle tion, it provides a “global” functional measurement of RV
dependent…” [91]. TAPSE has also been reported to function. The Tei index has not been used extensively in
have a positive correlation with LV ejection fraction and critical care research partly because of the requirement
was reduced in patients with acute myocardial infarc- of adequate Doppler signals, the elaborate process of
tion, heart failure or with LV dyssynchrony [92–95]. In measurements and the index’s sensitivity to conduction
patients with pulmonary hypertension, TAPSE overes- delay. It is not suitable to use in situations where cardiac
timated FAC because of an abnormal rocking motion rhythm is irregular and where preload (right atrial pres-
of the lateral LV wall at the apex (translational artefact) sure) is high such as in PE.
[96]. This limitation was subsequently underscored in the Four studies used EDA ratio in isolation in defining RV
updated guidelines: “As a one-dimensional measurement dysfunction. EDA ratio is a good indicator of RV strain
relative to the transducer, TAPSE may over- or underesti- as a result of increased afterload and/or preload. An EDA
mate RV function because of cardiac translation…” [97]. ratio > 1 is associated with a 25% mortality in ARDS [11].
Of note, a new alternative index, subcostal echocardio- However, by itself EDA is not a sensitive surrogate for RV
graphic assessment of tricuspid annular kick (SEATAK), dysfunction, except in cases where EDA ratio > 1 [104].
has been proposed to measure TAPSE in the subcostal When used together with paradoxical septal motion
view. SEATAK displayed good correlation with TAPSE (PSM), EDA ratio is both specific and sensitive for detect-
but the feasibility of SEATAK was superior to TAPSE in ing cor pulmonale [11, 54, 105]. PSM is a specific sign of
ICU patients [98]. increased afterload, due to enhanced RV contractility and
St, also a longitudinal (lateral free wall) function index prolonged duration of systole. When LV starts to relax at
[37], was commonly used but less so than TAPSE. St was end-systole or onset of diastole, the RV is still in the con-
found to be associated with prolonged mechanical ven- traction phase and causes the interventricular septum to
tilation [50], and was related to severity of sepsis and bow towards the LV as a result of reversal of trans-septal
mortality [99]. Surprisingly, although St was commonly LV-to-RV pressure [11].
measured, it was seldom used in isolation in defining RV FAC, one of the reference standards often used for
dysfunction. Intervendor differences in measurement comparing RV function, has been shown to correlate well
methods and disagreement in results might account for with RV ejection fraction. It has been shown in many
the lack of attraction of St both in clinical and research studies that it has a strong association with patient out-
uses [100]. As the measurement is akin to TAPSE, all the comes. For example, reduced FAC was independently
limitations found in TAPSE measurements apply equally associated with increased risk of all-cause mortality, car-
to St. diovascular death, sudden death, heart failure and stroke
RV longitudinal strain (RVS) and strain rate (RVSR) after myocardial infarction [106, 107]. Physiologically,
are modern surrogates of RV longitudinal function [101]. although FAC is sensitive to loading conditions, it also
RVS is mostly used as a prognostic tool, although it has incorporates the effects of LV function and interventricu-
also been used for diagnostic purposes [42, 66]. Strain lar septal motion, rendering it one of the more reliable
measurements are time-consuming and rely on optimal indices for RV function. However, RV outflow tract is not
image quality. One study raised the issue of feasibility of included in the assessment and good image quality (to
RVS measurement in ICU patients: in a cohort of 211
define the endocardial border) required for measurement are on continuous scales. In these cases, the former case
is often not obtainable in the critically ill population. yields a dichotomous result whilst the latter presents
the gradation of outcomes. The two are not necessar-
Number of indices used in defining RV function ily compatible. As a result of imperfect correlations and
Only a relatively small number of studies (26.8%) agreements between the various indices, it is not uncom-
employed a single index, mostly dichotomised, to define mon to find between-study discrepancies in conclusion.
RV dysfunction, and many used composite (> 1) indi- We also found that nearly all of the studies that utilised
ces. Single index, especially when dichotomised, has the Cidx failed to report missing data. The failure to measure
benefit of simplicity where statistical analyses are made one or more indices as a result of various reasons, such as
simpler, and interpretation and presentations are made technical difficulties, could alter the outcomes.
easier. However, each index has pros and cons, and a sin-
gle index does not always portray the full picture [91]. Limitations
The reasons are twofold: First, a single index used may One of the commonest limitations of any systematic
not fit into the context of the problem. Some are better review is the failure to find all the eligible studies. To min-
suited to measure certain aspects of RV function (e.g. imize this problem, we used a “high sensitivity” approach
contractility), whilst some are better for other purposes in our literature search, i.e. we defined our search terms
(e.g. assessing preload and afterload). Other confounding as broad as possible and searched three databases.
factors may also be present and interfere with the inter- Despite this, we still could not guarantee that we were
pretations. Second, dichotomisation comes at some cost. able to find all eligible studies, especially for those studies
For example, dichotomisation leads to a loss of informa- that did not report any echocardiographic RV assessment
tion and inflates the false positive rate; the variability in their abstracts. We did not critically appraise the qual-
of the data and the non-linear relationship between the ity of the eligible studies and hence would have included
index and RV function are ignored [13]. studies of various quality in our systematic review. The
Cidx should theoretically give a better utility tool advantage of not excluding studies of lower quality was
than by using a single index. A substantial proportion that we were able to include more studies and to audit
of studies (69%) utilized Cidx in assessing RV function, different echocardiographic RV function indices used in
yet only a few explained the rationale behind using these critical care research, which was a reflection of clinical
[54, 108]. The choice of combination poses many chal- practice. Further, the evolution of each indices could also
lenges. Ideally, it should be based on a sound physiologi- be studied.
cal framework. For studies that used compensatory Cidx
(the “any one” or “OR” rule), each index is assumed to Conclusion
have the same weight. The advantage of compensatory Right ventricular assessment is an important part of criti-
Cidx is that missing data (often seen in critical care echo- cal care cardiopulmonary and haemodynamic studies.
cardiography measurements) will be compensated by the There are many echocardiographic RV function indices
presence of the others. Compensatory Cidx is also more and each has its strengths and limitations. Our system-
sensitive in detecting abnormality as it only requires one atic review found a plethora of study types and study
out of several indices to show a positive result. Yet, this designs in critical care research. The choice of index or
increases the risk of type I errors resulting in a higher indices for RV assessments and for defining RV dysfunc-
(false) prevalence rate [18, 109]. The situation is similar tion also varied from study to study. While some used
to multiple comparisons of outcomes in clinical trials. a single index, many used Cidx. The choice of Cidx is
On the other hand, conjunctive Cidx (the “must satisfy complicated and should be based on clinical context
all” or “AND” rule) gives a higher specificity but at the while keeping in mind potential technical difficulties in
expense of reducing sensitivity. For example, if TAPSE the critical care setting. As in cor pulmonale, the choice
and FAC are both required to be positive in defining RV should also be based on a sound pathophysiological
dysfunction, then in  situations where FAC is reduced framework.
but TAPSE is within normal range because of a normal
Electronic supplementary material
to hyperdynamic LV (see, for example, [12]), conjunc- The online version of this article (https​://doi.org/10.1007/s0013​4-018-5211-z)
tive Cidx would have misclassified (missed) the outcome contains supplementary material, which is available to authorized users.
because of the requirement that BOTH indices need to
be positive. This increases the chance of type II error Author details
rate especially in the less severe case. Another challenge 1
 Department of Intensive Care Medicine, Nepean Hospital, Sydney Medical
faced by the researchers (or clinicians) in using Cidx School, The University of Sydney, Sydney, NSW, Australia. 2 Cardiovascular
Ultrasound Laboratory, Intensive Care Unit, Nepean Hospital, Sydney, NSW,
is when some indices are on a binary scale while others Australia.
Compliance with Ethical Standards computed tomography. Am J Cardiol 95:1260–1263. https​://doi.
org/10.1016/j.amjca​rd.2005.01.064
Conflicts of interest 17. Bal L, Thierry S, Brocas E et al (2006) B-type natriuretic peptide (BNP)
The authors declare that they have no conflict of interest. and N-terminal-proBNP for heart failure diagnosis in shock or acute
respiratory distress. Acta Anaesthesiol Scand 50:340–347. https​://doi.
Ethics Approval org/10.1111/j.1399-6576.2006.00963​.x
Ethics approval for systematic review is not required. 18. Lamia B, Teboul J-L, Monnet X et al (2007) Relationship between the
tricuspid annular plane systolic excursion and right and left ventricular
function in critically ill patients. Intensive Care Med 33:2143–2149. https​
Received: 26 February 2018 Accepted: 5 May 2018 ://doi.org/10.1007/s0013​4-007-0881-y
19. Mokart D, Sannini A, Brun J-P et al (2007) N-terminal pro-brain natriu-
retic peptide as an early prognostic factor in cancer patients develop-
ing septic shock. Crit Care 11:R37. https​://doi.org/10.1186/cc572​1
20. Gallotta G, Palmieri V, Piedimonte V et al (2008) Increased troponin I
predicts in-hospital occurrence of hemodynamic instability in patients
References with sub-massive or non-massive pulmonary embolism independent
1. Mehta SR, Eikelboom JW, Natarajan MK et al (2001) Impact of right ven- to clinical, echocardiographic and laboratory information. Int J Cardiol
tricular involvement on mortality and morbidity in patients with inferior 124:351–357. https​://doi.org/10.1016/j.ijcar​d.2006.03.096
myocardial infarction. J Am Coll Cardiol 37:37–43 21. Aksay E, Yanturali S, Kiyan S (2007) Can elevated troponin I levels predict
2. Dessap AM, Dessap AM, Boissier F et al (2016) Acute cor pulmonale complicated clinical course and inhospitat mortality in patients with
during protective ventilation for acute respiratory distress syndrome: acute pulmonary embolism? Am J Emerg Med 25:138–143. https​://doi.
prevalence, predictors, and clinical impact. Intensive Care Med org/10.1016/j.ajem.2006.06.005
42:862–870. https​://doi.org/10.1007/s0013​4-015-4141-2 22. Kline JA, Hernandez-Nino J, Jones AE et al (2008) Prospective study of
3. Matthay MA, Chatterjee K (1988) Bedside catheterization of the pulmo- the clinical features and outcomes of emergency department patients
nary artery: risks compared with benefits. Ann Intern Med 109:826–834 with delayed diagnosis of pulmonary embolism. Acad Emerg Med
4. Osman D, Monnet X, Castelain V et al (2009) Incidence and prognostic 14:592–598. https​://doi.org/10.1111/j.1553-2712.2007.tb018​41.x
value of right ventricular failure in acute respiratory distress syn- 23. Sade LE, Gulmez O, Eroglu S et al (2007) Noninvasive estimation of right
drome. Intensive Care Med 35:69–76. https​://doi.org/10.1007/s0013​ ventricular filling pressure by ratio of early tricuspid inflow to annular
4-008-1307-1 diastolic velocity in patients with and without recent cardiac surgery.
5. Armour JA, Randall WC (1970) Structural basis for cardiac function. Am J JASE 20:982–988. https​://doi.org/10.1016/j.echo.2007.01.012
Physiol 218:1517–1523 24. Vieillard-Baron A, Charron C, Caille V et al (2007) Prone positioning
6. McLean AS, Tang B, Nalos M et al (2003) Increased B-type natriuretic unloads the right ventricle in severe ARDS. Chest 132:1440–1446. https​
peptide (BNP) level is a strong predictor for cardiac dysfunction in ://doi.org/10.1378/chest​.07-1013
intensive care unit patients. Anaesth Intensive Care 31:21–27 25. Kline JA, Zeitouni R, Marchick MR et al (2008) Comparison of 8 bio-
7. McLean AS, Huang SJ, Nalos M et al (2003) The confounding effects markers for prediction of right ventricular hypokinesis 6 months after
of age, gender, serum creatinine, and electrolyte concentrations on submassive pulmonary embolism. Am Heart J 156:308–314. https​://doi.
plasma B-type natriuretic peptide concentrations in critically ill patients. org/10.1016/j.ahj.2008.03.026
Crit Care Med 31:2611–2618. https​://doi.org/10.1097/01.CCM.00000​ 26. Tousignant CP, Bowry R, Levesque S, Denault AY (2008) Regional
94225​.18237​.20 differences in color tissue Doppler-derived measures of longitudinal
8. McLean AS, Huang SJ (2007) Prognostic value of natriuretic peptides right ventricular function using transesophageal and transthoracic
in severe sepsis—reply. Crit Care Med 35:1806–1806. https​://doi. echocardiography. J Cardiothorac Vasc Anesth 22:400–405. https​://doi.
org/10.1097/01.CCM.00002​69344​.37999​.8B org/10.1053/j.jvca.2007.07.014
9. Ochiai Y, Morita S, Tanoue Y et al (1999) Use of transesophageal echo- 27. Palmieri V, Gallotta G, Rendina D et al (2008) Troponin I and right
cardiography for postoperative evaluation of right ventricular function. ventricular dysfunction for risk assessment in patients with nonmassive
Ann Thorac Surg 67:146–152 pulmonary embolism in the emergency department in combination
10. Ochiai Y, Morita S, Tanoue Y et al (1998) Effects of amrinone, a phospho- with clinically based risk score. Intern Emerg Med 3:131–138. https​://
diesterase inhibitor, on right ventricular/arterial coupling immediately doi.org/10.1007/s1173​9-008-0134-2
after cardiac operations. J Thorac Cardiovasc Surg 116:139–147. https​:// 28. Dessap AM, Charron C, Devaquet J et al (2009) Impact of acute hyper-
doi.org/10.1016/S0022​-5223(98)70252​-1 capnia and augmented positive end-expiratory pressure on right ven-
11. Vieillard-Baron A, Schmitt JM, Augarde R et al (2001) Acute cor pulmo- tricle function in severe acute respiratory distress syndrome. Intensive
nale in acute respiratory distress syndrome submitted to protective Care Med 35:1850–1858. https​://doi.org/10.1007/s0013​4-009-1569-2
ventilation: incidence, clinical implications, and prognosis. Crit Care 29. Tousignant C, Bowry R, Cruz JD, Mazer CD (2009) Induction of anes-
Med 29:1551–1555 thesia does not alter tricuspid annular velocities: a tissue Doppler
12. Jackson RE, Rudoni RR, Hauser AM et al (2000) Prospective evaluation assessment. Can J Anaesth 56:757–762. https​://doi.org/10.1007/s1263​
of two-dimensional transthoracic echocardiography in emergency 0-009-9157-z
department patients with suspected pulmonary embolism. Acad 30. Mahjoub Y, Pila C, Friggeri A et al (2009) Assessing fluid responsiveness
Emerg Med 7:994–998 in critically ill patients: false-positive pulse pressure variation is detected
13. Vieillard-Baron A, Page B, Augarde R et al (2001) Acute cor pulmonale in by Doppler echocardiographic evaluation of the right ventricle. Crit
massive pulmonary embolism: incidence, echocardiographic pattern, Care Med 37:2570–2575. https​://doi.org/10.1097/CCM.0b013​e3181​
clinical implications and recovery rate. Intensive Care Med 27:1481– a380a​3
1486. https​://doi.org/10.1007/s0013​40101​032 31. Gernoth C, Wagner G, Pelosi P, Luecke T (2009) Respiratory and
14. Maslow AD, Regan MM, Panzica P et al (2002) Precardiopulmonary haemodynamic changes during decremental open lung positive end-
bypass right ventricular function is associated with poor outcome after expiratory pressure titration in patients with acute respiratory distress
coronary artery bypass grafting in patients with severe left ventricular syndrome. Crit Care 13:R59. https​://doi.org/10.1186/cc778​6
systolic dysfunction. Anesth Analg 95:1507–1518 (table of contents) 32. Ricci JM, Dukkipati SR, Pica MC et al (2009) Malignant ventricular
15. Catena E, Milazzo F, Merli M et al (2004) Echocardiographic evaluation arrhythmias in patients with acute right ventricular infarction undergo-
of patients receiving a new left ventricular assist device: the Impella ing mechanical reperfusion. Am J Cardiol 104:1678–1683. https​://doi.
recover 100. Eur J Echocardiogr 5:430–437. https​://doi.org/10.1016/j. org/10.1016/j.amjca​rd.2009.07.047
euje.2004.03.008 33. Matyal R, Mahmood F, Hess P et al (2010) Right ventricular echocardio-
16. Mansencal N, Joseph T, Vieillard-Baron A et al (2005) Diagnosis of right graphic predictors of postoperative supraventricular arrhythmias after
ventricular dysfunction in acute pulmonary embolism using helical
thoracic surgery: a pilot study. Ann Thorac Surg 90:1080–1087. https​:// 51. Fagnoul D, Pasquier P, Bodson L et al (2013) Myocardial dysfunction
doi.org/10.1016/j.athor​acsur​.2010.05.019 during H1N1 influenza infection. J Crit Care 28:321–327. https​://doi.
34. Karakilic E, Kepez A, Abali G et al (2010) The relationship between org/10.1016/j.jcrc.2013.01.010
B-type natriuretic peptide levels and echocardiographic parameters 52. Franchi F, Faltoni A, Cameli M et al (2013) Influence of positive end-
in patients with heart failure admitted to the emergency depart- expiratory pressure on myocardial strain assessed by speckle tracking
ment. Anadolu Kardiyol Derg 10:143–149. https​://doi.org/10.5152/ echocardiography in mechanically ventilated patients. Biomed Res Int
akd.2010.040 2013:918584–918588. https​://doi.org/10.1155/2013/91854​8
35. Gackowski A, Chrustowicz A, Kapelak B et al (2010) Forward stroke vol- 53. Schuuring MJ, van Gulik EC, Koolbergen DR et al (2013) Determinants of
ume is predictor of perioperative course in patients with mitral regurgi- clinical right ventricular failure after congenital heart surgery in adults.
tation undergoing mitral valve replacement. Cardiol J 17:386–389 J Cardiothorac Vasc Anesth 27:723–727. https​://doi.org/10.1053/j.
36. Rendina D, De Bonis S, Gallotta G et al (2010) Clinical, historical and jvca.2012.10.022
diagnostic findings associated with right ventricular dysfunction in 54. Lheritier G, Legras A, Caille A et al (2013) Prevalence and prognostic
patients with central and non-massive pulmonary embolism. Intern value of acute cor pulmonale and patent foramen ovale in ventilated
Emerg Med 5:53–59. https​://doi.org/10.1007/s1173​9-009-0330-8 patients with early acute respiratory distress syndrome: a multicenter
37. Papaioannou VE, Stakos DA, Dragoumanis CK, Pneumatikos IA (2010) study. Intensive Care Med 39:1734–1742. https​://doi.org/10.1007/s0013​
Relation of tricuspid annular displacement and tissue Doppler imaging 4-013-3017-6
velocities with duration of weaning in mechanically ventilated patients 55. Boissier F, Katsahian S, Razazi K et al (2013) Prevalence and prognosis
with acute pulmonary edema. BMC Cardiovasc Disord 10:20. https​:// of cor pulmonale during protective ventilation for acute respiratory
doi.org/10.1186/1471-2261-10-20 distress syndrome. Intensive Care Med 39:1725–1733. https​://doi.
38. Dessap AM, Boissier F, Leon R et al (2010) Prevalence and prognosis of org/10.1007/s0013​4-013-2941-9
shunting across patent foramen ovale during acute respiratory distress 56. Hyllen S, Nozohoor S, Ingvarsson A et al (2014) Right ventricular perfor-
syndrome. Crit Care Med 38:1786–1792. https​://doi.org/10.1097/ mance after valve repair for chronic degenerative mitral regurgitation.
CCM.0b013​e3181​eaa9c​8 Ann Thorac Surg 98:2023–2031. https​://doi.org/10.1016/j.athor​acsur​
39. Fougeres E, Teboul J-L, Richard C et al (2010) Hemodynamic impact of .2014.07.075
a positive end-expiratory pressure setting in acute respiratory distress 57. Kusunose K, Tsutsui RS, Bhatt K et al (2014) Prognostic value of RV
syndrome: importance of the volume status. Crit Care Med 38:802–807. function before and after lung transplantation. JACC Cardiovasc Imag
https​://doi.org/10.1097/CCM.0b013​e3181​c587f​d 7:1084–1094. https​://doi.org/10.1016/j.jcmg.2014.07.012
40. Haas S, Haese A, Goetz AE, Kubitz JC (2011) Haemodynamics and 58. Madhavan S, Dutt PG, Thingnam SKS, Rohit MK (2015) Perioperative
cardiac function during robotic-assisted laparoscopic prostatectomy in follow-up of patients with severe pulmonary artery hypertension
steep Trendelenburg position. Int J Med Robotics Comput Assist Surg secondary to left heart disease: a single center, prospective, obser-
7:408–413. https​://doi.org/10.1002/rcs.410 vational study. J Cardiothorac Vasc Anesth 29:1524–1532. https​://doi.
41. Albers J, Ister D, Kayhan N, Vahl CF (2011) Postoperative non-invasive org/10.1053/j.jvca.2015.08.009
assessment of pulmonary vascular resistance using Doppler echocar- 59. Yildirim B, Biteker FS, Basaran O et al (2015) Is there a potential role
diography. Interact Cardiovasc Thorac Surg 13:579–584. https​://doi. for echocardiography in adult patients with CAP? Am J Emerg Med
org/10.1510/icvts​.2011.27161​9 33:1672–1676. https​://doi.org/10.1016/j.ajem.2015.06.036
42. Park JH, Park YS, Kim YJ et al (2011) Differentiation between acute and 60. Ramjee V, Grossestreuer AV, Yao Y et al (2015) Right ventricular
chronic cor pulmonales with midventricular systolic strain of the right dysfunction after resuscitation predicts poor outcomes in cardiac
ventricle in the emergency department. Heart Vessels 26:435–439. arrest patients independent of left ventricular function. Resuscitation
https​://doi.org/10.1007/s0038​0-010-0072-6 96:186–191. https​://doi.org/10.1016/j.resus​citat​ion.2015.08.008
43. Golpe R, Castro-Anon O, Perez-de-Llano LA et al (2011) Electrocardio- 61. Bloomer TL, Thomassee EJ, Fong PP (2015) Acute pulmonary embolism
gram score predicts severity of pulmonary embolism in hemodynami- network and multidisciplinary response team approach to treatment.
cally stable patients. J Hosp Med 6:285–289. https​://doi.org/10.1002/ Crit Pathw Cardiol 14:90–96. https​://doi.org/10.1097/HPC.00000​00000​
jhm.868 00004​9
44. Brown SM, Pittman J, Miller RRI et al (2011) Right and left heart failure in 62. Denault AY, Couture P, Beaulieu Y et al (2015) Right ventricular depres-
severe H1N1 influenza A infection. Eur Respir J 37:112–118. https​://doi. sion after cardiopulmonary bypass for valvular surgery. J Cardiothorac
org/10.1183/09031​936.00008​210 Vasc Anesth 29:836–844. https​://doi.org/10.1053/j.jvca.2015.01.011
45. Guervilly C, Forel J-M, Hraiech S et al (2012) Right ventricular function 63. Guinot PG, Abou Arab O, Longrois D, Dupont H (2015) Right ventricular
during high-frequency oscillatory ventilation in adults with acute systolic dysfunction and vena cava dilatation precede alteration of renal
respiratory distress syndrome. Crit Care Med 40:1539–1545. https​://doi. function in adult patients undergoing cardiac surgery. An observa-
org/10.1097/CCM.0b013​e3182​451b4​a tional study. Eur J Anaesthesiol 32:535–542. https​://doi.org/10.1097/
46. Schuuring MJ, Bolmers PPM, Mulder BJM et al (2012) Right ventricular EJA.00000​00000​00014​9
function declines after cardiac surgery in adult patients with congenital 64. Denault AY, Beaulieu Y, Couture P et al (2015) Acute intraoperative
heart disease. Int J Cardiovasc Imaging 28:755–762. https​://doi. effect of intravenous amiodarone on right ventricular function in
org/10.1007/s1055​4-011-9892-4 patients undergoing valvular surgery. Eur Heart J Acute Cardiovasc Care
47. Furian T, Aguiar C, Prado K et al (2012) Ventricular dysfunction and 4:316–325. https​://doi.org/10.1177/20488​72614​54910​2
dilation in severe sepsis and septic shock: relation to endothelial 65. Imada T, Kannibayashi T, Ota C et al (2015) Intraoperative right ventricu-
function and mortality. J Crit Care 27:15. https​://doi.org/10.1016/j. lar fractional area change is a good indicator of right ventricular con-
jcrc.2011.06.017 tractility: a retrospective comparison using two- and three-dimensional
48. Corciova FC, Corciova C, Georgescu CA et al (2012) Echocardiographic echocardiography. J Cardiothorac Vasc Anesth 29:831–835. https​://doi.
predictors of adverse short-term outcomes after heart surgery in org/10.1053/j.jvca.2014.12.005
patients with mitral regurgitation and pulmonary hypertension. Heart 66. Khemasuwan D, Yingchoncharoen T, Tunsupon P et al (2015) Right
Surg Forum 15:127–132. https​://doi.org/10.1532/HSF98​.20121​008 ventricular echocardiographic parameters are associated with mortal-
49. Fichet J, Moreau L, Genee O et al (2012) Feasibility of right ventricular ity after acute pulmonary embolism. JASE 28:355–362. https​://doi.
longitudinal systolic function evaluation with transthoracic echocar- org/10.1016/j.echo.2014.11.012
diographic indices derived from tricuspid annular motion: a prelimi- 67. Azari A, Bigdelu L, Moravvej Z (2015) Surgical embolectomy in the
nary study in acute respiratory distress syndrome. Echocardiography management of massive and sub-massive pulmonary embolism: the
29:513–521. https​://doi.org/10.1111/j.1540-8175.2011.01650​.x results of 30 consecutive ill patients. ARYA Atheroscler 11:208–213
50. Harmankaya A, Akilli H, Gul M et al (2013) Assessment of right ventricu- 68. Perez-Teran P, Roca O, Rodriguez-Palomares J et al (2015) Influence of
lar functions in patients with sepsis, severe sepsis and septic shock and right ventricular function on the development of primary graft dysfunc-
its prognostic importance: a tissue Doppler study. J Crit Care 28:–1111. tion after Lung transplantation. J Heart Lung Transplant 34:1423–1429.
e11. https​://doi.org/10.1016/j.jcrc.2013.07.059 https​://doi.org/10.1016/j.healu​n.2015.05.026
69. Russell FM, Moore CL, Courtney DM et al (2015) Independent evalu- ventricle during positive-pressure ventilation with varying levels of
ation of a simple clinical prediction rule to identify right ventricular positive end-expiratory pressure. Crit Care Med 17:205–210. https​://doi.
dysfunction in patients with shortness of breath. Am J Emerg Med org/10.1097/00003​246-19890​3000-00001​
33:542–547. https​://doi.org/10.1016/j.ajem.2015.01.026 88. Poelaert JIT, Reichert CLA, Koolen JJ et al (1992) Transesophageal echo-
70. Legras A, Caille A, Bégot E et al (2015) Acute respiratory distress Doppler evaluation of the hemodynamic effects of positive-pressure
syndrome (ARDS)-associated acute cor pulmonale and patent foramen ventilation after coronary artery surgery. J Cardiothorac Vasc Anesth
ovale: a multicenter noninvasive hemodynamic study. Crit Care 19:174. 6:438–443. https​://doi.org/10.1016/1053-0770(92)90010​-5
https​://doi.org/10.1186/s1305​4-015-0898-5 89. Kaul S, Tei C, Hopkins JM, Shah PM (1984) Assessment of right ven-
71. Dahhan T, Siddiqui I, Tapson VF et al (2016) Clinical and echocardio- tricular function using two-dimensional echocardiography. Am Heart J
graphic predictors of mortality in acute pulmonary embolism. Cardio- 107:526–531
vasc Ultrasound 14:44. https​://doi.org/10.1186/s1294​7-016-0087-y 90. Saxena N, Rajagopalan N, Edelman K, López-Candales A (2006)
72. Nadziakiewicz P, Niklewski T, Szyguła-Jurkiewicz B et al (2016) Preop- Tricuspid annular systolic velocity: a useful measurement in determin-
erative echocardiography examination of right ventricle function in ing right ventricular systolic function regardless of pulmonary artery
patients scheduled for LVAD implantation correlates with postoperative pressures. Echocardiography 23:750–755. https​://doi.org/10.111
hemodynamic examinations. Ann Transplant 21:500–507 1/j.1540-8175.2006.00305​.x
73. Tuzovic M, Adigopula S, Amsallem M et al (2016) Regional right ventric- 91. Rudski LG, Lai WW, Afilalo J et al (2010) Guidelines for the echocar-
ular dysfunction in acute pulmonary embolism: relationship with clot diographic assessment of the right heart in adults: a report from the
burden and biomarker profile. Int J Cardiovasc Imaging 32:389–398. American Society of Echocardiography endorsed by the European
https​://doi.org/10.1007/s1055​4-015-0780-1 Association of Echocardiography, a registered branch of the European
74. Biteker FS, Basaran O, Dogan V et al (2016) Prognostic value of tran- Society of Cardiology, and the Canadian Society of Echocardiogra-
sthoracic echocardiography and biomarkers of cardiac dysfunction phy. J Am Soc Echocardiogr 23:685–713. https​://doi.org/10.1016/j.
in community-acquired pneumonia. Clin Microbiol Infect 22:1006. echo.2010.05.010
e1–1006.e6. https​://doi.org/10.1016/j.cmi.2016.08.016 92. Samad BA, Alam M, Jensen-Urstad K (2002) Prognostic impact of right
75. Lazzeri C, Cianchi G, Bonizzoli M et al (2016) Right ventricle dilation as ventricular involvement as assessed by tricuspid annular motion in
a prognostic factor in refractory acute respiratory distress syndrome patients with acute myocardial infarction. Am J Cardiol 90:778–781.
requiring veno-venous extracorporeal membrane oxygenation. Min- https​://doi.org/10.1016/S0002​-9149(02)02612​-7
erva Anestesiol 82:1043–1049 93. Gupta S, Khan F, Shapiro M et al (2008) The associations between tricus-
76. Mishra A, Kumar B, Dutta V et al (2016) Comparative effect of levosi- pid annular plane systolic excursion (TAPSE), ventricular dyssynchrony,
mendan and milrinone in cardiac surgery patients with pulmonary and ventricular interaction in heart failure patients. Eur J Echocardiogr
hypertension and left ventricular dysfunction. J Cardiothorac Vasc 9:766–771. https​://doi.org/10.1093/ejech​ocard​/jen14​7
Anesth 30:639–646. https​://doi.org/10.1053/j.jvca.2016.01.015 94. Kjaergaard J, Iversen KK, Akkan D et al (2009) Predictors of right
77. Abtahi F, Farmanesh M, Moaref A, Shekarforoush S (2016) Right ven- ventricular function as measured by tricuspid annular plane systolic
tricular involvement in either anterior or inferior myocardial infarction. excursion in heart failure. Cardiovasc Ultrasound 7:51
Int Cardiovasc Res J 10:67–71. https​://doi.org/10.17795​/icrj-10(2)67 95. Damy T, Kallvikbacka-Bennett A, Goode K et al (2012) Prevalence of,
78. Lazzeri C, Bonizzoli M, Cozzolino M et al (2016) Serial measurements of associations with, and prognostic value of tricuspid annular plane sys-
troponin and echocardiography in patients with moderate-to-severe tolic excursion (TAPSE) among out-patients referred for the evaluation
acute respiratory distress syndrome. J Crit Care 33:132–136. https​://doi. of heart failure. J Card Fail 18:216–225
org/10.1016/j.jcrc.2016.01.004 96. Giusca S, Dambrauskaite V, Scheurwegs C et al (2010) Deformation
79. Lazzeri C, Cianchi G, Bonizzoli M et al (2016) Pulmonary vascular imaging describes right ventricular function better than longitudinal
dysfunction in refractory acute respiratory distress syndrome before displacement of the tricuspid ring. Heart 96:281–288. https​://doi.
veno-venous extracorporeal membrane oxygenation. Acta Anaesthe- org/10.1136/hrt.2009.17172​8
siol Scand 60:485–491. https​://doi.org/10.1111/aas.12643​ 97. Lang RM, Badano LP, Mor-Avi V et al (2015) Recommendations for car-
80. Cecchini J, Boissier F, Gibelin A et al (2016) Pulmonary vascular dysfunc- diac chamber quantification by echocardiography in adults: an update
tion and cor pulmonale during acute respiratory distress syndrome in from the American Society of Echocardiography and the European
sicklers. Shock 46:358–364. https​://doi.org/10.1097/SHK.00000​00000​ Association of Cardiovascular Imaging. J Am Soc Echocardiogr 28:1–39.
00064​0 https​://doi.org/10.1016/j.echo.2014.10.003
81. Dudzinski DM, Hariharan P, Parry BA et al (2017) Assessment of right 98. Meluzín J (2001) Pulsed Doppler tissue imaging of the velocity of tri-
ventricular strain by computed tomography versus echocardiography cuspid annular systolic motion. A new, rapid, and non-invasive method
in acute pulmonary embolism. Acad Emerg Med 24:337–343. https​:// of evaluating right ventricular systolic function. Eur Heart J 22:340–348.
doi.org/10.1111/acem.13108​ https​://doi.org/10.1053/euhj.2000.2296
82. Jia D, Zhou X-M, Hou G (2017) Estimation of right ventricular dysfunc- 99. Dhutia NM, Zolgharni M, Willson K et al (2014) Guidance for accurate
tion by computed tomography pulmonary angiography: a valuable and consistent tissue Doppler velocity measurement: comparison
adjunct for evaluating the severity of acute pulmonary embolism. of echocardiographic methods using a simple vendor-independent
J Thromb Thrombolysis 43:271–278. https​://doi.org/10.1007/s1123​ method for local validation. Eur Heart J Cardiovasc Imaging 15:817–827.
9-016-1438-0 https​://doi.org/10.1093/ehjci​/jeu04​0
83. Diaz-Gomez JL, Alvarez AB, Danaraj JJ et al (2017) A novel semiquantita- 100. Pirat B, McCulloch ML, Zoghbi WA (2006) Evaluation of global and
tive assessment of right ventricular systolic function with a modified regional right ventricular systolic function in patients with pulmonary
subcostal echocardiographic view. Echocardiography 34:44–52. https​:// hypertension using a novel speckle tracking method. Am J Cardiol
doi.org/10.1111/echo.13400​ 98:699–704. https​://doi.org/10.1016/j.amjca​rd.2006.03.056
84. Weekes AJ, Johnson AK, Troha D et al (2017) Prognostic value of right 101. Park SJ, Park JH, Lee HS et al (2015) Impaired RV global longitudinal
ventricular dysfunction markers for serious adverse events in acute strain is associated with poor long-term clinical outcomes in patients
normotensive pulmonary embolism. J Emerg Med 52:137–150. https​:// with acute inferior STEMI. JACC Cardiovasc Imaging 8:161–169. https​://
doi.org/10.1016/j.jemer​med.2016.09.002 doi.org/10.1016/j.jcmg.2014.10.011
85. Vieillard-Baron A, Slama M, Cholley B et al (2007) Echocardiography in 102. Tei C, Ling LH, Hodge DO et al (1995) New index of combined systolic
the intensive care unit: from evolution to revolution? Intensive Care and diastolic myocardial performance: a simple and reproducible
Med 34:243–249. https​://doi.org/10.1007/s0013​4-007-0923-5 measure of cardiac function–a study in normals and dilated cardiomyo-
86. Jardin F, Dubourg O, Margairaz A, Bourdarias J-P (1987) Inspiratory pathy. J Cardiol 26:357–366
impairment in right ventricular performance during acute asthma. 103. Jardin F, Gueret P, Dubourg O et al (1985) Two-dimensional echocar-
Chest 92:789–795. https​://doi.org/10.1378/chest​.92.5.789 diographic evaluation of right ventricular size and contractility in acute
87. Mitaka C, Nagura T, Sakanishi N et al (1989) Two-dimensional echo- respiratory failure. Crit Care Med 13:952–956
cardiographic evaluation of inferior vena cava, right ventricle, and left
104. Jardin F, Dubourg O, Bourdarias JP (1997) Echocardiographic pattern of 107. Altman DG, Royston P (2006) The cost of dichotomising continuous
acute cor pulmonale. Chest 111:209–217 variables. BMJ 332:1080. https​://doi.org/10.1136/bmj.332.7549.1080
105. Zornoff L, Skali H, Pfeffer MA et al (2002) Right ventricular dysfunction 108. Prieto-Merino D, Smeeth L, Staa TPV, Roberts I (2013) Dangers of non-
and risk of heart failure and mortality after myocardial infarction. J Am specific composite outcome measures in clinical trials. BMJ 347:f6782.
Coll Cardiol 39:1450–1455 https​://doi.org/10.1136/bmj.f6782​
106. Anavekar NS, Skali H, Bourgoun M et al (2008) Usefulness of right ven- 109. Teixeira-Pinto A, Mauri L (2011) Statistical analysis of noncommensurate
tricular fractional area change to predict death, heart failure, and stroke multiple outcomes. Circulation 4:650–656. https​://doi.org/10.1161/circo​
following myocardial infarction (from the VALIANT ECHO study). Am J utcom​es.111.96158​1
Cardiol 101:607–612. https​://doi.org/10.1016/j.amjca​rd.2007.09.115