Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Open Access

Peer-reviewed

Research Article

Echocardiographic parameters of patients in the intensive care unit undergoing continuous renal replacement therapy

  • Panagiotis Kompotiatis,

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Writing – original draft

    Affiliation Division of Nephrology and Hypertension, Department of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

    ⨯
  • Brandon M. Wiley,

    Roles Conceptualization, Data curation, Resources, Writing – review & editing

    Affiliation Department of Cardiovascular Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

    ⨯
  • Jacob C. Jentzer,

    Roles Conceptualization, Data curation, Formal analysis, Writing – review & editing

    Affiliation Department of Cardiovascular Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

    ⨯
  • Kianoush B. Kashani

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing

    kashani.kianoush@mayo.edu

    Affiliations Division of Nephrology and Hypertension, Department of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

    ⨯

Abstract

Main objectives

Echocardiographic parameters have been used to predict outcomes for specific intensive care unit (ICU) populations. We sought to define echocardiographic parameters for ICU patients receiving continuous renal replacement therapy (CRRT).

Design, setting, participants, and measurements

This is a historical cohort study of consecutive ICU patients at Mayo Clinic (Rochester, Minnesota) who received CRRT from December 9, 2006, through November 13, 2015. Only patients with an echocardiographic examination within 7 days of CRRT initiation were considered.

Results

The study included 1,276 patients. Decreased left ventricular ejection fraction (LVEF; ≤45%) was noted in 361/1,120 (32%) and increased right ventricular systolic pressure (RVSP; ≥40 mm Hg) was noted in 529/798 (66%). Right ventricular systolic dysfunction was observed in 320/820 (39%). The most common valvular abnormality was tricuspid regurgitation (244/1,276 [19%]). Stratification of these parameters by ICU type (medical, surgical, cardiothoracic, cardiac) showed that most echocardiographic abnormalities were significantly more prevalent among cardiac ICU patients: LVEF ≤45% (67/105 [64%]), RVSP ≥40 mm Hg (63/79 [80%]) and tricuspid regurgitation (50/130 [38%]). We compared patients with acute kidney injury (AKI) vs end-stage renal disease and showed that decreased LVEF (284/921 [31%] vs 78/201 [39%]), was significantly less prevalent among patients with AKI, but increased RVSP was more prevalent (445/651 [68%] vs 84/147 [57%]) with AKI.

Conclusions

ICU patients who required CRRT had increased prevalence of pulmonary hypertension and right and left ventricular systolic dysfunction. Prediction of adverse outcomes with echocardiographic parameters in this patient population can lead to identification of modifiable risk factors.

Citation: Kompotiatis P, Wiley BM, Jentzer JC, Kashani KB (2019) Echocardiographic parameters of patients in the intensive care unit undergoing continuous renal replacement therapy. PLoS ONE 14(1): e0209994. https://doi.org/10.1371/journal.pone.0209994

Editor: Vincenzo Lionetti, Scuola Superiore Sant'Anna, ITALY

Received: October 19, 2018; Accepted: December 16, 2018; Published: January 11, 2019

Copyright: © 2019 Kompotiatis et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are in the paper and Supporting Information files.

Funding: This publication was made possible by CTSA Grant Number UL1 TR002377 from the National Center for Advancing Translational Sciences (NCATS), a component of the National Institutes of Health (NIH). This study was not funded, and the grant is for the first author’s training as part of the Clinical and Translational Science certificate program.

Competing interests: The authors have declared that no competing interests exist.

Abbreviations: AKI, acute kidney injury; APACHE III, Acute Physiology And Chronic Health Evaluation; CRRT, continuous renal replacement therapy; ESRD, end-stage renal disease; ICU, intensive care unit; IHD, intermittent hemodialysis; IQR, interquartile range; IVC, inferior vena cava; LV, left ventricle, left ventricular; LVEF, left ventricular ejection fraction; RV, right ventricle, right ventricular; RVSP, right ventricular systolic pressure; SOFA, Sequential Organ Failure Assessment

Introduction

Despite many advances in the care of critically ill patients and improvement in mortality rates during the past 20 years [1], the incidence of acute kidney injury (AKI) in patients in the intensive care unit (ICU) remains high (20%-57%) [2–4]. ICU patients with AKI have increased short- and long-term mortality rates (20%-27%) [3, 5], with the highest rates observed among patients with severe AKI who require acute initiation of renal replacement therapy. Of particular concern are patients whose hemodynamic instability necessitates initiation of continuous renal replacement therapy (CRRT). A 2015 meta-analysis reported an overall mortality rate of 46% for patients with AKI requiring CRRT [6], and individual studies have reported rates as high as 60% to 80% [7, 8].

CRRT was initially developed to treat patients who could not tolerate intermittent hemodialysis (IHD), either because of hemodynamic instability or because IHD could not efficiently correct acid-base and electrolyte disorders [9]. CRRT is also a practical tool in managing oligo-anuric critically patients with fluid overload or at risk of volume overload while requiring ongoing administration of parenteral drugs (e.g. vasopressors), blood products or parenteral nutrition [10, 11]. However, CRRT has not been proven superior to IHD in randomized control trials assessing mortality risk [12, 13]. Nevertheless, CRRT is often used in the ICU setting as a modality for renal replacement therapy, especially in clinical situations involving hemodynamic instability or intracranial hypertension, when IHD cannot be safely performed [13, 14].

Cardiac dysfunction, due to “cross-talk” between the heart and kidneys, is an important factor that often may contribute to development or worsening of AKI and progression to dialysis[15]. Echocardiography is the standard noninvasive method used to assess cardiac function in the ICU, and use of limited echocardiography to diagnose and guide therapy for patients with shock is associated with improved outcomes [16]. Further, the clinical relevance of various echocardiographic parameters has been described for patients in the ICU; these parameters include left ventricular ejection fraction (LVEF), diastolic function, right ventricle (RV) size, and tricuspid regurgitant jet velocity [17–19]. According to available evidence, RV size and tricuspid regurgitant jet velocity may be predictive of mortality risk [17, 18]. For patients receiving long-term hemodialysis, RV dysfunction is independently associated with increased mortality risk [20–22]. Pulmonary hypertension (assessed with echocardiography) also can indicate increased risk of death for patients with end-stage renal disease (ESRD) [21].

To our knowledge, the echocardiographic abnormalities in ICU patients receiving CRRT have not been characterized. We aimed to define the prevalence and patterns of echocardiographic abnormalities in ICU patients undergoing CRRT and to determine how these parameters differed among patients with AKI vs ESRD.

Materials and methods

Patient selection

The Mayo Clinic Institutional Review Board reviewed and approved this minimal-risk study with a waiver of informed consent (IRB # 15–008953). We retrospectively identified a historical cohort of all consecutive adults admitted to the ICUs at Mayo Clinic Hospital (Rochester, Minnesota), at the St. Marys and Methodist campuses, from December 9, 2006, through November 13, 2015. Patients were included in the study if they received CRRT during their ICU stay and had an echocardiogram within seven days (before or after) CRRT initiation. For individuals who had more than one echocardiogram performed within seven days of CRRT initiation, our analysis considered only the echocardiogram that was performed chronologically closest to the first CRRT session.

ESRD was defined per KDOQI[23] criteria as dialysis-dependent chronic kidney disease (CKD) stage 5 (Peritoneal or hemodialysis).

AKI was defined per KDIGO criteria based on both creatinine and urine output[14].

Data collection

We reviewed electronic medical records and abstracted baseline patient characteristics. The severity of illness was determined by Acute Physiology and Chronic Health Evaluation (APACHE III) scores and Sequential Organ Failure Assessment (SOFA) scores. ICU data were obtained from an Epidemiology and Translational Research in Intensive Care ICU DataMart database [24, 25]. Comorbidities were assessed with the Charlson comorbidity index [26]. Data were collected using a standardized process (S1 File).

Echocardiographic parameters were extracted from a separate institutional echocardiography database. Mean LVEF is reported if it was calculated with more than 1 method. Left ventricular (LV) mass was measured with the linear method, and increased mass was defined as greater than 115 g/m2 for men and 95 g/m2 for women [27]. LV diastolic function was assessed by using the American Society of Echocardiography guidelines [28]. Left atrial volume was measured with a 2-dimensional method (reported as mL/m2). RV systolic dysfunction was defined as a moderate or greater decrease in RV systolic function (23), with RV systolic pressure (RVSP) estimated from tricuspid regurgitant jet velocity. Inferior vena cava (IVC) dilation was defined as IVC diameter greater than 2.1 cm [29]. Pericardial effusion was categorized as none, mild, moderate, or large [30]. Finally, valvular diseases (aortic, mitral, tricuspid) were assessed with color flow Doppler imaging and categorized as normal, mild, moderate, or severe stenosis or regurgitation [31, 32]. Data on valvular diseases were extracted as text from the echocardiographic reports; if no information about valvular disease was available, the valve was considered normal.

Statistical analysis

Continuous variables are reported as mean (SD) or median (interquartile range [IQR]). Categorical variables are expressed as count (percent). Continuous variables were assessed by using the t-test, Wilcoxon rank sum test, analysis of variance, or Kruskal-Wallis test; categorical variables were assessed by using the χ2 test or Fisher exact test. JMP software (version 13.0.0; SAS Institute Inc.) was used for the analysis. P values < .05 were considered statistically significant.

Results

During the study period, 1,758 unique patients received CRRT (Fig 1). We excluded 482 patients (27%); 480 did not have an echocardiogram within seven days of CRRT initiation, and 2 declined research authorization. The final analysis included 1,276 patients (Baseline characteristics, comorbid conditions, and outcomes are shown in Table 1. Among all enrolled patients, CRRT 82% of cases (n = 1,040) were due to AKI, and 18% of cases (n = 236) were provided to the ESRD patients. Regarding the CRRT modality, continuous venovenous hemofiltration was used in most cases (n = 1,268 [99%]), and slow continuous ultrafiltration was used for the other 8 patients (1%).

thumbnail
Download:
Fig 1. Patient enrollment flowchart.

https://doi.org/10.1371/journal.pone.0209994.g001

thumbnail
Download:
Table 1. Baseline characteristics, comorbidities, and illness severity (N = 1,276)a.

https://doi.org/10.1371/journal.pone.0209994.t001

Echocardiographic parameters

The median time between echocardiography and CRRT initiation was 8 hours (IQR, −10 to 31 hours). Echocardiographic findings of this cohort are summarized in Table 2. Identified abnormalities included IVC dilation, diastolic dysfunction, RV systolic dysfunction, and increased LV mass. The most common valvular abnormalities were tricuspid regurgitation and mitral regurgitation.

thumbnail
Download:
Table 2. Echocardiographic parameters.

https://doi.org/10.1371/journal.pone.0209994.t002

Echocardiographic parameters, stratified by type of ICU admission (ie, medical, surgical, cardiothoracic, cardiac) are summarized in Table 3. The echocardiographic parameters that were statistically different between the different ICU types included median LVEF, diastolic dysfunction, IVC dilation, median RVSP, RV systolic dysfunction, moderate or greater aortic, mitral, and tricuspid regurgitation and left atrial volume index (Table 3). Lowest median LVEF, highest median RVSP and median left atrial volume index were noted in the cardiac ICU patients. IVC dilation, moderate or greater aortic, mitral, and tricuspid valves regurgitation were also more prevalent in cardiac ICU while RV systolic dysfunction was more prevalent in cardiothoracic surgery ICU.

thumbnail
Download:
Table 3. Echocardiographic data with statistical comparison between the different ICU types.

https://doi.org/10.1371/journal.pone.0209994.t003

We next compared echocardiographic parameters between patients with AKI vs. ESRD (Table 4). Compared with patients with AKI, patients with ESRD had a lower median ejection fraction (54 vs. 75%, p = 0.04,) and a higher median left atrial volume index (43 vs. 36 mL/m2, p = 0.002). Additionally, a higher percentage of patients with ESRD had moderate or greater aortic (4 vs. 0.96%, p = 0.004) or mitral stenosis (2 vs.0.19%, p = 0.01), but a lower percentage of patients with ESRD had RVSP ≥40 mm Hg (57 vs. 68%, p = 0.009). The relationship between elevated RVSP and AKI development persisted even after adjusting for the presence of acute respiratory distress syndrome or mechanical ventilation.

thumbnail
Download:
Table 4. Comparison of echocardiographic parameters for patients with AKI vs. ESRD.

https://doi.org/10.1371/journal.pone.0209994.t004

Discussion

In this study, we present a large cohort of ICU patients from a 9-year period who had an echocardiogram performed within 7 days of CRRT initiation. Our group has previously described the incidence of certain echocardiographic abnormalities and their associated outcomes in ICU patients with septic shock [33, 34]. To our knowledge, the current study is the first to describe the prevalence of echocardiographic parameters in ICU patients receiving CRRT. We identified a high prevalence of echocardiographic abnormalities that differed by the type of ICU. Type of ICU admission is a surrogate for the actual condition that necessitated ICU-level care, and therefore, our findings describe and compare the echocardiographic characteristics between ICU patients on CRRT with different underlying pathologic processes. Echocardiographic parameters were also different between patients when assessed regarding the indication for CRRT (AKI vs. ESRD). We identified a high prevalence of LV diastolic dysfunction and a substantial prevalence of RV and LV systolic dysfunction. Markers of volume overload, including IVC dilation and pulmonary hypertension, were also common.

Diastolic dysfunction was common in our cohort (62%). According to a meta-analysis published in 2015, the prevalence of diastolic dysfunction in ICU patients with sepsis and septic shock is 48%, and it is associated with increased mortality risk [35]. However, individual studies have reported a prevalence of diastolic dysfunction that ranges from 20% to 57% [36, 37], and although its association with mortality has been previously reported, outcomes have not been consistent across the studies [36–38]. LV systolic dysfunction (defined as LVEF ≤45%) was noted in 32% of our patients; this rate is higher than that previously reported in a study that used even higher threshold values to define LV systolic dysfunction [38].

Prevalence of pulmonary hypertension (defined as RVSP ≥40 mm Hg) was also higher in our patient population (66%) compared with rates reported previously. In a study that used Doppler echocardiography to evaluate pulmonary hypertension (tricuspid regurgitant jet velocity ≥3 m/sec, which typically corresponds to RVSP ≥40 mm Hg), the prevalence of pulmonary hypertension in patients in a medical ICU was 42% [18]. Several possible mechanisms could account for the increased RVSP in ICU patients undergoing CRRT [39]. The most common cause of pulmonary hypertension in ICU patients is volume overload causing interstitial pulmonary edema and hypoxia-induced pulmonary artery vasoconstriction; left-sided heart failure is also common [39]. Invasive mechanical ventilation, which was used in 73% of our cohort, also may have contributed to increased RVSP. Parenchymal lung disease, another cause of pulmonary hypertension, was present in 16% of patients. RV systolic dysfunction (moderate or greater decrease in RV systolic function) was noted in 39%; this rate is slightly higher than the prevalence previously observed in ICU patients (28%-31%) [17, 38].

Tricuspid regurgitation (moderate or greater) was noted in 19% of patients; this rate is considerably higher than that previously reported (~3%) [40]. This association probably is attributable to the higher prevalence of pulmonary hypertension and RV systolic dysfunction in our cohort [41, 42].

The most common echocardiographic abnormality was IVC dilation (71%), consistent with volume overload in most patients who received CRRT. However, the majority of patients (73%) also were receiving mechanical ventilation, which can increase the diameter of the IVC [43]. Similarly, the substantial rates of RV systolic dysfunction, pulmonary hypertension, and tricuspid regurgitation may have contributed to IVC dilation. Notably, elevated central venous pressure, which may be reflected by a dilated IVC, is a known contributor to AKI because it is a component of the cardiorenal syndrome [44, 45].

Compared with patients in the noncardiac ICUs, patients admitted to the cardiac ICU more commonly had echocardiographic abnormalities, including diastolic dysfunction, IVC dilation, and valvular disease (aortic regurgitation and stenosis, tricuspid valve regurgitation). They also had a higher prevalence of LV systolic dysfunction and pulmonary hypertension. These findings are probably intrinsic to the cardiac causes that led to their admission to a cardiac ICU and possibly also to CRRT initiation (eg, cardiorenal syndrome).

Comparison of echocardiographic parameters between patients with AKI vs. ESRD showed a higher prevalence of LV systolic dysfunction (defined as LVEF ≤45%) in patients with ESRD, which likely reflects the high prevalence of cardiovascular disease and congestive heart failure in this patient population [46, 47]. In contrast, the prevalence of pulmonary hypertension (defined as RVSP ≥40 mm Hg) was higher in patients with AKI; high RVSP is a known causative factor of AKI because it indicates venous congestion and RV dysfunction (cardiorenal syndrome) [48, 49].

Our investigation has a number of important limitations inherent to its design as a retrospective, single-center, cross-sectional study; as a result, these findings may have limited generalizability. This study can only provide information regarding the association (not causation) between the prevalence of echocardiographic parameters and the different ICU patient populations (AKI vs. ESRD; type of ICU). Additionally, some of the echocardiographic parameters were assessed only in a small fraction of the patients including diastolic dysfunction (22% of patients) and left atrial volume index (19% of patients) which limits the internal validity of these parameters in our cohort. Furthermore, the indication for which each echocardiogram was performed was not available, and as a result, we could not assess the correlation of clinical indication with the prevalence of specific echocardiographic parameters.

Nevertheless, we report new information about a unique patient population that can be used to further investigate the association of echocardiographic parameters with adverse outcomes or modifiable risk factors in ICU patients receiving CRRT.

Conclusions

We assessed a large cohort of ICU patients who received CRRT and noted an increased prevalence of pulmonary hypertension, diastolic dysfunction, and RV dysfunction. Patients in the cardiac ICU had higher prevalence rates for most echocardiographic abnormalities compared with patients admitted to noncardiac ICUs. Patients with AKI had a higher prevalence of pulmonary hypertension compared with patients with ESRD. Future studies that aim to predict adverse outcomes with echocardiographic parameters in this patient population can lead to the identification of modifiable risk factors and eventually improve patient care. These relationships must then be validated in prospective studies.

Supporting information

S1 File. De-identified dataset used for the analyses of this study.

https://doi.org/10.1371/journal.pone.0209994.s001

(XLSX)

References

  1. 1. Zimmerman JE, Kramer AA, Knaus WA. Changes in hospital mortality for United States intensive care unit admissions from 1988 to 2012. Crit Care. 2013;17(2):R81. Epub 2013/04/30. pmid:23622086; PubMed Central PMCID: PMCPMC4057290.
  2. 2. Bellomo R, Ronco C, Mehta RL, Asfar P, Boisrame-Helms J, Darmon M, et al. Acute kidney injury in the ICU: from injury to recovery: reports from the 5th Paris International Conference. Ann Intensive Care. 2017;7(1):49. Epub 2017/05/06. pmid:28474317; PubMed Central PMCID: PMCPMC5418176.
  3. 3. Hoste EA, Bagshaw SM, Bellomo R, Cely CM, Colman R, Cruz DN, et al. Epidemiology of acute kidney injury in critically ill patients: the multinational AKI-EPI study. Intensive care medicine. 2015;41(8):1411–23. Epub 2015/07/15. pmid:26162677.
  4. 4. Kellum JA, Sileanu FE, Murugan R, Lucko N, Shaw AD, Clermont G. Classifying AKI by Urine Output versus Serum Creatinine Level. J Am Soc Nephrol. 2015;26(9):2231–8. Epub 2015/01/09. pmid:25568178; PubMed Central PMCID: PMCPMC4552117.
  5. 5. Bouchard J, Acharya A, Cerda J, Maccariello ER, Madarasu RC, Tolwani AJ, et al. A Prospective International Multicenter Study of AKI in the Intensive Care Unit. Clin J Am Soc Nephrol. 2015;10(8):1324–31. Epub 2015/07/22. pmid:26195505; PubMed Central PMCID: PMCPMC4527019.
  6. 6. Mehta RL, Cerda J, Burdmann EA, Tonelli M, Garcia-Garcia G, Jha V, et al. International Society of Nephrology's 0by25 initiative for acute kidney injury (zero preventable deaths by 2025): a human rights case for nephrology. Lancet. 2015;385(9987):2616–43. Epub 2015/03/18. pmid:25777661.
  7. 7. Uchino S, Kellum JA, Bellomo R, Doig GS, Morimatsu H, Morgera S, et al. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA. 2005;294(7):813–8. Epub 2005/08/18. pmid:16106006.
  8. 8. Metcalfe W, Simpson M, Khan IH, Prescott GJ, Simpson K, Smith WC, et al. Acute renal failure requiring renal replacement therapy: incidence and outcome. QJM. 2002;95(9):579–83. Epub 2002/09/03. pmid:12205335.
  9. 9. Ronco C, Ricci Z. Renal replacement therapies: physiological review. Intensive care medicine. 2008;34(12):2139–46. Epub 2008/09/16. pmid:18791697.
  10. 10. Villa G, Ricci Z, Ronco C. Renal Replacement Therapy. Critical care clinics. 2015;31(4):839–48. Epub 2015/09/28. pmid:26410148.
  11. 11. Ostermann M, Joannidis M, Pani A, Floris M, De Rosa S, Kellum JA, et al. Patient Selection and Timing of Continuous Renal Replacement Therapy. Blood purification. 2016;42(3):224–37. Epub 2016/08/27. pmid:27561956.
  12. 12. Vinsonneau C, Camus C, Combes A, Costa de Beauregard MA, Klouche K, Boulain T, et al. Continuous venovenous haemodiafiltration versus intermittent haemodialysis for acute renal failure in patients with multiple-organ dysfunction syndrome: a multicentre randomised trial. Lancet. 2006;368(9533):379–85. Epub 2006/08/01. pmid:16876666.
  13. 13. Rabindranath K, Adams J, Macleod AM, Muirhead N. Intermittent versus continuous renal replacement therapy for acute renal failure in adults. Cochrane database of systematic reviews (Online). 2007;(3):CD003773. Epub 2007/07/20. pmid:17636735.
  14. 14. Khwaja A. KDIGO clinical practice guidelines for acute kidney injury. Nephron. 2012;120(4):c179–84. Epub 2012/08/15. pmid:22890468.
  15. 15. Husain-Syed F, McCullough PA, Birk HW, Renker M, Brocca A, Seeger W, et al. Cardio-Pulmonary-Renal Interactions: A Multidisciplinary Approach. Journal of the American College of Cardiology. 2015;65(22):2433–48. Epub 2015/06/06. pmid:26046738.
  16. 16. Kanji HD, McCallum J, Sirounis D, MacRedmond R, Moss R, Boyd JH. Limited echocardiography-guided therapy in subacute shock is associated with change in management and improved outcomes. J Crit Care. 2014;29(5):700–5. Epub 2014/05/27. pmid:24857642.
  17. 17. See KC, Ng J, Siow WT, Ong V, Phua J. Frequency and prognostic impact of basic critical care echocardiography abnormalities in patients with acute respiratory distress syndrome. Ann Intensive Care. 2017;7(1):120. Epub 2017/12/21. pmid:29260440; PubMed Central PMCID: PMCPMC5736519.
  18. 18. Stamm JA, McVerry BJ, Mathier MA, Donahoe MP, Saul MI, Gladwin MT. Doppler-defined pulmonary hypertension in medical intensive care unit patients: Retrospective investigation of risk factors and impact on mortality. Pulm Circ. 2011;1(1):95–102. Epub 2011/10/29. pmid:22034595; PubMed Central PMCID: PMCPMC3198625.
  19. 19. Vallabhajosyula S, Gillespie SM, Barbara DW, Anavekar NS, Pulido JN. Impact of New-Onset Left Ventricular Dysfunction on Outcomes in Mechanically Ventilated Patients With Severe Sepsis and Septic Shock. J Intensive Care Med. 2016:885066616684774. Epub 2016/01/01. pmid:28553776.
  20. 20. Hickson LJ, Negrotto SM, Onuigbo M, Scott CG, Rule AD, Norby SM, et al. Echocardiography Criteria for Structural Heart Disease in Patients With End-Stage Renal Disease Initiating Hemodialysis. J Am Coll Cardiol. 2016;67(10):1173–82. Epub 2016/03/12. pmid:26965538; PubMed Central PMCID: PMCPMC4788810.
  21. 21. Tang M, Batty JA, Lin C, Fan X, Chan KE, Kalim S. Pulmonary Hypertension, Mortality, and Cardiovascular Disease in CKD and ESRD Patients: A Systematic Review and Meta-analysis. Am J Kidney Dis. 2018;72(1):75–83. Epub 2018/02/13. pmid:29429751.
  22. 22. Santosh S, Chu C, Mwangi J, Narayan M, Mosman A, Nayak R, et al. Changes in pulmonary artery systolic pressure and right ventricular function in patients with end-stage renal disease on maintenance dialysis. Nephrology (Carlton). 2017. Epub 2017/10/21. pmid:29053201.
  23. 23. National Kidney F. KDOQI Clinical Practice Guideline for Diabetes and CKD: 2012 Update. Am J Kidney Dis. 2012;60(5):850–86. Epub 2012/10/17. pmid:23067652.
  24. 24. Alsara A, Warner DO, Li G, Herasevich V, Gajic O, Kor DJ. Derivation and validation of automated electronic search strategies to identify pertinent risk factors for postoperative acute lung injury. Mayo Clin Proc. 2011;86(5):382–8. Epub 2011/05/03. pmid:21531881; PubMed Central PMCID: PMCPMC3084640.
  25. 25. Herasevich V, Pickering BW, Dong Y, Peters SG, Gajic O. Informatics infrastructure for syndrome surveillance, decision support, reporting, and modeling of critical illness. Mayo Clin Proc. 2010;85(3):247–54. Epub 2010/03/03. pmid:20194152; PubMed Central PMCID: PMCPMC2843116.
  26. 26. Singh B, Singh A, Ahmed A, Wilson GA, Pickering BW, Herasevich V, et al. Derivation and validation of automated electronic search strategies to extract Charlson comorbidities from electronic medical records. Mayo Clin Proc. 2012;87(9):817–24. Epub 2012/09/11. pmid:22958988; PubMed Central PMCID: PMCPMC3538495.
  27. 27. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, et al. Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005;18(12):1440–63. Epub 2005/12/27. pmid:16376782.
  28. 28. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr. 2009;22(2):107–33. Epub 2009/02/04. pmid:19187853.
  29. 29. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, et al. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr. 2010;23(7):685–713; quiz 86–8. Epub 2010/07/14. pmid:20620859.
  30. 30. Klein AL, Abbara S, Agler DA, Appleton CP, Asher CR, Hoit B, et al. American Society of Echocardiography clinical recommendations for multimodality cardiovascular imaging of patients with pericardial disease: endorsed by the Society for Cardiovascular Magnetic Resonance and Society of Cardiovascular Computed Tomography. J Am Soc Echocardiogr. 2013;26(9):965–1012 e15. Epub 2013/09/04. pmid:23998693.
  31. 31. Zoghbi WA, Enriquez-Sarano M, Foster E, Grayburn PA, Kraft CD, Levine RA, et al. Recommendations for evaluation of the severity of native valvular regurgitation with two-dimensional and Doppler echocardiography. J Am Soc Echocardiogr. 2003;16(7):777–802. Epub 2003/07/02. pmid:12835667.
  32. 32. Baumgartner H, Hung J, Bermejo J, Chambers JB, Evangelista A, Griffin BP, et al. Echocardiographic assessment of valve stenosis: EAE/ASE recommendations for clinical practice. J Am Soc Echocardiogr. 2009;22(1):1–23; quiz 101–2. Epub 2009/01/10. pmid:19130998.
  33. 33. Vallabhajosyula S, Jentzer JC, Geske JB, Kumar M, Sakhuja A, Singhal A, et al. New-Onset Heart Failure and Mortality in Hospital Survivors of Sepsis-Related Left Ventricular Dysfunction. Shock (Augusta, Ga. 2018;49(2):144–9. Epub 2017/07/21. pmid:28727607; PubMed Central PMCID: PMCPMC5766383.
  34. 34. Vallabhajosyula S, Kumar M, Pandompatam G, Sakhuja A, Kashyap R, Kashani K, et al. Prognostic impact of isolated right ventricular dysfunction in sepsis and septic shock: an 8-year historical cohort study. Ann Intensive Care. 2017;7(1):94. Epub 2017/09/09. pmid:28884343; PubMed Central PMCID: PMCPMC5589718.
  35. 35. Sanfilippo F, Corredor C, Fletcher N, Landesberg G, Benedetto U, Foex P, et al. Diastolic dysfunction and mortality in septic patients: a systematic review and meta-analysis. Intensive care medicine. 2015;41(6):1004–13. Epub 2015/03/25. pmid:25800584.
  36. 36. Etchecopar-Chevreuil C, Francois B, Clavel M, Pichon N, Gastinne H, Vignon P. Cardiac morphological and functional changes during early septic shock: a transesophageal echocardiographic study. Intensive Care Med. 2008;34(2):250–6. Epub 2007/11/16. pmid:18004543.
  37. 37. Sturgess DJ, Marwick TH, Joyce C, Jenkins C, Jones M, Masci P, et al. Prediction of hospital outcome in septic shock: a prospective comparison of tissue Doppler and cardiac biomarkers. Crit Care. 2010;14(2):R44. Epub 2010/03/25. pmid:20331902; PubMed Central PMCID: PMCPMC2887156.
  38. 38. Pulido JN, Afessa B, Masaki M, Yuasa T, Gillespie S, Herasevich V, et al. Clinical spectrum, frequency, and significance of myocardial dysfunction in severe sepsis and septic shock. Mayo Clin Proc. 2012;87(7):620–8. Epub 2012/06/12. pmid:22683055; PubMed Central PMCID: PMCPMC3538477.
  39. 39. Jentzer JC, Mathier MA. Pulmonary Hypertension in the Intensive Care Unit. J Intensive Care Med. 2016;31(6):369–85. Epub 2015/05/07. pmid:25944777.
  40. 40. Haji K, Haji D, Canty DJ, Royse AG, Tharmaraj D, Azraee M, et al. The Feasibility and Impact of Routine Combined Limited Transthoracic Echocardiography and Lung Ultrasound on Diagnosis and Management of Patients Admitted to ICU: A Prospective Observational Study. J Cardiothorac Vasc Anesth. 2018;32(1):354–60. Epub 2017/11/12. pmid:29126689.
  41. 41. Mutlak D, Lessick J, Reisner SA, Aronson D, Dabbah S, Agmon Y. Echocardiography-based spectrum of severe tricuspid regurgitation: the frequency of apparently idiopathic tricuspid regurgitation. J Am Soc Echocardiogr. 2007;20(4):405–8. Epub 2007/04/03. pmid:17400120.
  42. 42. Sagie A, Schwammenthal E, Padial LR, Vazquez de Prada JA, Weyman AE, Levine RA. Determinants of functional tricuspid regurgitation in incomplete tricuspid valve closure: Doppler color flow study of 109 patients. J Am Coll Cardiol. 1994;24(2):446–53. Epub 1994/08/01. pmid:8034882.
  43. 43. Jue J, Chung W, Schiller NB. Does inferior vena cava size predict right atrial pressures in patients receiving mechanical ventilation? J Am Soc Echocardiogr. 1992;5(6):613–9. Epub 1992/11/01. pmid:1466886.
  44. 44. Chen KP, Cavender S, Lee J, Feng M, Mark RG, Celi LA, et al. Peripheral Edema, Central Venous Pressure, and Risk of AKI in Critical Illness. Clin J Am Soc Nephrol. 2016;11(4):602–8. Epub 2016/01/21. pmid:26787777; PubMed Central PMCID: PMCPMC4822669.
  45. 45. Wong BT, Chan MJ, Glassford NJ, Martensson J, Bion V, Chai SY, et al. Mean arterial pressure and mean perfusion pressure deficit in septic acute kidney injury. J Crit Care. 2015;30(5):975–81. Epub 2015/05/28. pmid:26015150.
  46. 46. Harnett JD, Foley RN, Kent GM, Barre PE, Murray D, Parfrey PS. Congestive heart failure in dialysis patients: prevalence, incidence, prognosis and risk factors. Kidney Int. 1995;47(3):884–90. Epub 1995/03/01. pmid:7752588.
  47. 47. Roberts MA, Polkinghorne KR, McDonald SP, Ierino FL. Secular trends in cardiovascular mortality rates of patients receiving dialysis compared with the general population. Am J Kidney Dis. 2011;58(1):64–72. Epub 2011/04/05. pmid:21458896.
  48. 48. Ronco C, Cicoira M, McCullough PA. Cardiorenal syndrome type 1: pathophysiological crosstalk leading to combined heart and kidney dysfunction in the setting of acutely decompensated heart failure. J Am Coll Cardiol. 2012;60(12):1031–42. Epub 2012/07/31. pmid:22840531.
  49. 49. Schrier RW, Bansal S. Pulmonary hypertension, right ventricular failure, and kidney: different from left ventricular failure? Clin J Am Soc Nephrol. 2008;3(5):1232–7. Epub 2008/07/11. pmid:18614776; PubMed Central PMCID: PMCPMC4571151.