Hemodynamic Insights From Simultaneous Common Carotid and Internal Jugular Doppler Ultrasonography in a Patient With Hypoxemia and Multiple Organ Dysfunction

A 68-year-old man was admitted to the ICU for shock, acute kidney injury that required continuous venovenous hemofiltration (CVVH), and hypoxemia after right-sided chest tube placement for unilateral hydrothorax. His medical history was notable for ischemic cardiomyopathy with biventricular dysfunction, congestive heart failure, and atrial flutter. He was admitted to the ICU and intubated for hypoxemia and increased work of breathing on the general medical floor. In the ICU, arterial blood gas analysis revealed a pH of 7.42, Paco2 of 47 mm Hg, and Pao2 of 57 mm Hg on 60% Fio2. He was receiving assist-control ventilation with a tidal volume of 6 mL/kg and a positive end-expiratory pressure of 5 cm H2O; he was fully passive with the ventilator. Furthermore, the patient was in rapid atrial flutter at a rate of 120 beats per minute; his BP was 125/75 mm Hg, and he was not receiving vasoactive medications. Nevertheless, he manifested hypoperfusion with elevated arterial lactate (4.0 mM), creatinine level prior to initiation of CVVH (5.6 mg/dL), and capillary refill time (> 3 s). To better understand the patient’s hemodynamics, thermodilution-calibrated pulse contour analysis was obtained by placement of a PiCCO catheter (Pulsion Medical, Munich, Germany) in the femoral artery and the use of the Philips M1012A continuous cardiac output monitor (Philips Healthcare, Best, The Netherlands, and Andover, MA). After PiCCO calibration, the patient was given a rapid fluid challenge of 0.9% saline solution at 100 mL/min for roughly 3 minutes to test for fluid responsiveness. Additionally, a wireless, wearable, continuous wave Doppler ultrasound device (Flosonics Medical, Sudbury, Canada) (Fig 1) was adhered over the patient’s left common carotid and internal jugular vein to continuously monitor carotid artery and internal jugular vein Doppler signals. Doppler spectrograms were recorded during the three cold saline solution flushes that are required for PiCCO calibration (Fig 2A and C ) (Video 1), for 1 minute prior to the fluid challenge, and for the entirety of its infusion (Fig 2B).Figure 2Results from the critically ill patient. A, Baseline carotid artery and internal jugular Doppler spectrograms. In the jugular spectrogram, the maximum d-wave velocity is 44 cm/sec, and the minimum is 16 cm/sec, with a calculated respiratory variation of 93%. B, Doppler spectrograms after the rapid fluid challenge. The maximum and minimum d-wave velocities have fallen to 32 cm/s and 15 cm/s, respectively. with a respiratory variation of 72%. Note that the carotid spectrogram at the 337-s mark also reveals a bubble artifact. C, Doppler spectrograms immediately after a thermodilution calibration injection of cold saline solution into the right atrium. Arrows identify air bubble artifacts; these were observed with each calibration injection. D, The relative change of SV from the PiCCO device vs ccFT and VTI. The dotted horizontal line represents the threshold for fluid responsiveness from the PiCCO device (ie, 10%). ccFT = corrected flow time of the carotid artery; CVP = central venous pressure; SV = stroke volume; VTI = carotid velocity time integral.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Question 1: What explains the morphologic condition of the initial jugular venous trace and can this be used to infer right atrial pressure qualitatively? Question 2: What are the artifacts seen during the calibration flushes and can this partly explain the patient’s hypoxemia? Question 3: Does the change in jugular and carotid Doppler signals throughout the rapid fluid challenge give any insight into whether the patient is fluid responsive? Answer 1: The characteristics of venous Doppler have been elucidated in numerous large veins, which include the superior and inferior vena cavae1Reynolds T. Appleton C.P. Doppler flow velocity patterns of the superior vena cava, inferior vena cava, hepatic vein, coronary sinus, and atrial septal defect: a guide for the echocardiographer.J Am Soc Echocardiogr. 1991; 4: 503-512Abstract Full Text PDF PubMed Google Scholar and the hepatic,1Reynolds T. Appleton C.P. Doppler flow velocity patterns of the superior vena cava, inferior vena cava, hepatic vein, coronary sinus, and atrial septal defect: a guide for the echocardiographer.J Am Soc Echocardiogr. 1991; 4: 503-512Abstract Full Text PDF PubMed Google Scholar the intrarenal,2Iida N. Seo Y. Sai S. et al.Clinical implications of intrarenal hemodynamic evaluation by Doppler ultrasonography in heart failure.JACC: Heart Failure. 2016; 4: 674-682Crossref PubMed Scopus (0) Google Scholar femoral,3Abu-Yousef M.M. Kakish M. Mufid M. Pulsatile venous Doppler flow in lower limbs: highly indicative of elevated right atrium pressure.AJR. Am J Roentgenol. 1996; 167: 977-980Crossref Scopus (45) Google Scholar and internal jugular veins.4Sivaciyan V. Ranganathan N. Transcutaneous doppler jugular venous flow velocity recording.Circulation. 1978; 57: 930-939Crossref Scopus (71) Google Scholar The physiologic conditions that create the venous Doppler morphologic conditions are largely interchangeable for each of these great veins.5Kenny J.-E.S. Assessing fluid intolerance with Doppler ultrasonography: a physiological framework.Med Sci. 2022; 10: 12Google Scholar When the pressure outside of the vein supersedes the pressure inside, the vein collapses into an ellipsoid shape, and the venous Doppler ultrasound assumes relatively high velocity based on Bernoulli’s principle with minimal respiratory undulation; this is the normal jugular venous morphologic condition in healthy individuals in the semirecumbent position6Kenny J.-E.S. Prager R. Rola P. McCulloch G. Eibl J.K. Haycock K. The effect of gravity-induced preload change on the venous excess ultrasound (VExUS) score and internal jugular vein Doppler in healthy volunteers.Intensive Care Med Exp. 2023; 11: 19Crossref Scopus (6) Google Scholar (Fig 1A). As the pressure within the vein rises and its cross-sectional area increases, Doppler ultrasound velocity falls (ie, which indicates the reduction in pressure gradient) and becomes pulsatile, which reflects the change in right atrial pressure during a cardiac cycle (Fig 1B). Normally, at the end of diastole, atrial kick raises right atrial pressure (ie, the a-wave) that diminishes venous velocity. Thereafter, systolic tricuspid excursion and atrial relaxation reduce right atrial pressure (ie, the x-descent), which enhances venous velocity (ie, the systolic s-wave). Return of the tricuspid annulus towards the cardiac base, coupled with ongoing venous blood ingress, increases right atrial pressure (ie, the v-wave) that diminishes great vein blood velocity. Then, when the tricuspid valve opens during mechanical diastole, pressure falls again (ie, the y-descent) that augments venous velocity that causes the diastolic d-wave. In this patient, prior to the fluid challenge, we observed a prominent diastolic d-wave (ie, consistent with a pronounced y-descent) and minimal s-wave (which intimates poor tricuspid systolic excursion and/or impaired atrial relaxation) depicted in Figures 2A and B.4Sivaciyan V. Ranganathan N. Transcutaneous doppler jugular venous flow velocity recording.Circulation. 1978; 57: 930-939Crossref Scopus (71) Google Scholar, 5Kenny J.-E.S. Assessing fluid intolerance with Doppler ultrasonography: a physiological framework.Med Sci. 2022; 10: 12Google Scholar, 6Kenny J.-E.S. Prager R. Rola P. McCulloch G. Eibl J.K. Haycock K. The effect of gravity-induced preload change on the venous excess ultrasound (VExUS) score and internal jugular vein Doppler in healthy volunteers.Intensive Care Med Exp. 2023; 11: 19Crossref Scopus (6) Google Scholar Within the intrarenal vein, this pattern is most consistent with a “monophasic d-wave” and associated with an elevated right atrial pressure (ie, > 15 mm Hg).2Iida N. Seo Y. Sai S. et al.Clinical implications of intrarenal hemodynamic evaluation by Doppler ultrasonography in heart failure.JACC: Heart Failure. 2016; 4: 674-682Crossref PubMed Scopus (0) Google Scholar The patient’s recorded central venous pressure at the time of the Doppler signal was 14 mm Hg. Prior to fluids, this patient had notable respiratory variation in the d-wave (ie, y-descent) and diastolic venous filling velocity merged into systolic venous filling. The fusion of the d-waves and s-waves occurs primarily because of the rapid heart rate (Fig 2A and B). When the heart rate is normal, there is ample time during diastole for right atrial pressure to rise, given ongoing venous return; the rise in right atrial pressure as diastole progresses is manifested as decreased venous velocity (Fig 1B). In addition, there is normally atrial kick at the very end of diastole, which raises right atrial pressure further, just prior to the onset of systole. In this patient, the very rapid rate, in conjunction with loss of coordinated atrial activity, caused the venous d-waves and s-waves to merge. Answer 2: The high-intensity, sporadic, stochastic velocity signals following each PiCCO calibration are air bubbles consistent with right-to-left cardiac shunting (Fig 2C) (Video 1). It is known that Doppler ultrasound of the carotid artery can make this diagnosis.7Censori B. Partziguian T. Poloni M. Common carotid artery duplex for the bubble test to detect right-to-left shunt.Ultrasound Med Biol. 2010; 36: 566-570Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar The rapidity of the thermodilution calibration injection likely led to the generation of small air bubbles in the 0.9% sodium chloride solution and their delivery directly into the right atrium via the central venous catheter. Presence of these artifacts in the carotid artery within a few cardiac cycles after each calibration injection strongly suggests intracardiac shunt. Indeed, earlier in the day, the patient underwent echocardiography with a bubble study and was found to have a patent foramen ovale. High right atrial pressure likely exacerbated right-to-left atrial shunting, which is a certain contributor to the patient’s hypoxemia. Answer 3: At the end of the rapid fluid challenge, continuous venous-arterial Doppler (CVAD) revealed diminished respiratory variation and velocity in the jugular venous d-wave and minimal change in the carotid corrected flow time (Fig 2A, B, and D).8Barjaktarevic I. Toppen W.E. Hu S. et al.Ultrasound assessment of the change in carotid corrected flow time in fluid responsiveness in undifferentiated shock.Crit Care Med. 2018; 46: 1040-1046Crossref Scopus (66) Google Scholar These findings imply that the fluid challenge increased right atrial pressure (as described earlier) but that it had minimal effect on stroke volume, respectively. Raw flow time is the duration of systole in milliseconds; flow time is measured in the common carotid artery as the time from the systolic upstroke to the dicrotic notch (Fig 1A). Flow time is determined predominantly by heart rate, stroke volume, afterload, and contractility. By applying the formula of Wodey,8Barjaktarevic I. Toppen W.E. Hu S. et al.Ultrasound assessment of the change in carotid corrected flow time in fluid responsiveness in undifferentiated shock.Crit Care Med. 2018; 46: 1040-1046Crossref Scopus (66) Google Scholar the effect of heart rate is controlled for mathematically and changes in the resultant “corrected flow time” reflect change in stroke volume, afterload, and contractility. The corrected flow time generally is increased by stroke volume and decreased by contractility; the effect of afterload can increase or decrease the duration of systole depending on the magnitude of afterload. If an intervention is performed where afterload and contractility are presumed constant, then changes in corrected flow time reflect changes in stroke volume. In summary, in this patient during the rapid fluid challenge, CVAD implied rising right atrial pressure and lack of stroke volume augmentation. These findings were confirmed as his right atrial pressure increased to 17 mm Hg and stroke volume index did not increase as measured simultaneously by the PiCCO device. Basic point-of-care ultrasonography in the ICU usually focuses on B-mode imaging for both diagnostic and management decisions with relatively less emphasis on quantitative Doppler findings.5Kenny J.-E.S. Assessing fluid intolerance with Doppler ultrasonography: a physiological framework.Med Sci. 2022; 10: 12Google Scholar Further, even if Doppler ultrasonography is deployed at the bedside, it often is limited to measurement of a few cardiac cycles during directed assessments and subject to human sampling variability. These ultrasonographic “snap-shots” might miss insights otherwise gleaned from more protracted measures, especially throughout an entire hemodynamic assessment. On the other hand, invasive monitoring better tracks the trend of an intervention, over several minutes or even hours, which is not typically feasible for point-of-care ultrasonography. The drawbacks to invasive monitors are the cost, time, and complications associated with indwelling venous and arterial catheters. Barjaktarevic et al9Barjaktarevic I. Kenny J.-É.S. Berlin D. Cannesson M. The evolution of ultrasound in critical care: from procedural guidance to hemodynamic monitor.J Ultrasound Med. 2021; 40: 401Crossref Scopus (18) Google Scholar have suggested that technologic advancements could shape new paradigms in Doppler ultrasonography; that is, an approach that marries the benefits of both point-of-care ultrasonography and invasive catheters during a functional hemodynamic assessment (eg, fluid challenge, passive leg raise). To illustrate this concept, a wearable, continuous wave, Doppler ultrasound transducer that transmits wirelessly to an iOS device (Apple Inc) was placed on a critically ill, hypoperfused patient. With this hands-free Doppler ultrasound, CVAD revealed numerous features of hemodynamic interest. First, the patient’s venous filling pressure was elevated initially, which suggested impaired right heart systolic function. Though high venous pressure makes the probability of being fluid responsive low, this patient had been receiving CVVH; therefore, the hemodynamic benefit of additional preload was uncertain. Also, there was notable respiratory variation in his jugular venous d-wave (ie, y-descent) that hinted that the right heart was not preload limited (Fig 2A). Second, with all three thermodilution calibrations, bubble artifacts were discerned in the carotid artery Doppler spectrogram (Fig 2C), which is consistent with intracardiac shunt. This observation provided an explanation for his persistent hypoxemia and represents the first known report by wireless Doppler ultrasonography. Third, after a rapid infusion of approximately 250 to 300 mL, the jugular venous d-wave reduced its absolute velocity and respiratory variation, both compatible with rising right atrial pressure (Fig 2A and B). Simultaneously, neither the carotid artery velocity time integral nor the carotid corrected flow time surpassed thresholds for detecting a 10% stroke volume augmentation as reported in healthy volunteers who endured central hypovolemia with simulated blood transfusion10Kenny J.-É.S. Barjaktarevic I. Mackenzie D.C. et al.Carotid Doppler ultrasonography correlates with stroke volume in a human model of hypovolaemia and resuscitation: analysis of 48 570 cardiac cycles.Br J Anaesth. 2021; 127: e60-e63Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar and in critically ill patients with undifferentiated shock (Fig 2D).8Barjaktarevic I. Toppen W.E. Hu S. et al.Ultrasound assessment of the change in carotid corrected flow time in fluid responsiveness in undifferentiated shock.Crit Care Med. 2018; 46: 1040-1046Crossref Scopus (66) Google Scholar As discussed in a recent physiologic framework,5Kenny J.-E.S. Assessing fluid intolerance with Doppler ultrasonography: a physiological framework.Med Sci. 2022; 10: 12Google Scholar contemporaneous Doppler measures of both cardiac filling (eg, venous Doppler ultrasonography) and output (eg, arterial Doppler ultrasonography) recapitulate the Frank-Starling curve in real time.5Kenny J.-E.S. Assessing fluid intolerance with Doppler ultrasonography: a physiological framework.Med Sci. 2022; 10: 12Google Scholar More concretely, that this patient augmented right atrial pressure, but not stroke volume, strongly suggested that he was on the “plateau” of his cardiac function curve. Importantly, each of the aforementioned findings were corroborated with invasive measures and an echocardiographic bubble study. We have no doubt that CVAD ultrasonography cannot, and should not, replace advanced echocardiography in the ICU, nor can it supplant invasive hemodynamic monitors. Nevertheless, given that it is noninvasive and comparatively simple, acquisition and interpretation of CVAD ultrasound evaluation could facilitate decision-making earlier in care, such as in the ambulance, the ED, and the general medical floor. Though the CVAD paradigm requires further validation, its font of hemodynamic information make it of interest to any clinician at the intersection of ultrasonography, physiology, and resuscitation. 1.The shape of the internal jugular vein Doppler spectrogram, like other great veins, characterizes right atrial pressure and its change.2.Air emboli in the common carotid artery following rapid venous injection of saline suggests intracardiac shunting as a cause of hypoxemia.3.Changes (or lack thereof) in common carotid artery Doppler velocity and systolic time can be used to infer stroke volume change (or lack thereof).4.Simultaneous venous and arterial Doppler during a hemodynamic intervention might be used to build a real-time Frank-Starling curve. The authors have reported to CHEST the following: J. E. S. K. and J. K. E. are co-founders and C. H. is an employee of Flosonics Medical. None declared (D. A., F. B., V. F., A. V., A. G., S. P.). Other contributions: CHEST worked with the authors to ensure that the Journal policies on patient consent to report information were met. Additional information: Videos for this case are available under "Supplementary Data." eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiJkYWE5NzJkOWMzMTEzMzFmNTFlMmQ0NmQ1NGU3NjYwNiIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNzEyNjU2NDM0fQ.MgBI9G9uthEo28GV3qHL6qq203uCwoj27lJilNBtoDefCA1TXtKx9da5ZrRvUqe20J7NVYIBRrZZ9UNb_Q2ckGFfBZf9YsDGAw2gftbxj9OYXb2HmJOHk9rFa2-3Kbr4ixGgbi3g2X8Pzv8KsSAs6FxWYYW8tsRnY0IPe_WD5Sjx94Fz40aPf0okubELp_yUZqYdQfTIiEhUx6iBseuT-4B4MDrgYFm6UHMPWFCMg2KPOTLuVA71elt6zSH9Wj2X7ftCh-vIXP2gzxX-SsKKrLj_ToaFGJTs2X3dmP8aBHBDlLctwGsdmEsjG9mu3QRHPOAIntNUy59G7Zxl_a6ADg Download .mp4 (18.48 MB) Help with .mp4 files Video 1

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