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Review Article
Keywords: The main objective of fluid therapy is to increase cardiac output (CO). Large, rapidly administered
cardiac output
volumes of fluids are the cornerstone of treating patients in shock to restore circulating volume and
cardiac index
improve tissue perfusion. However, determining exactly how much fluid a given patient requires can be
pulse contour analysis
central venous pressure challenging. If enough fluid is not given, poor tissue perfusion can lead to ischemia, anaerobic
lithium dilution metabolism, and ultimately cell and patient death. Conversely, increased morbidity and mortality
ultrasound associated with excessive intravenous fluid administration has been reported in the human literature in
a wide variety of conditions. This review focuses on types of available CO monitoring, their application in
veterinary medicine as well as current research trends in noninvasive evaluation of CO.
Department of Veterinary Clinical Sciences,
Purdue University College of Veterinary & 2016 Elsevier Inc. All rights reserved.
Medicine, West Lafayette, IN, USA
n
Address reprint requests to: Kristen
Marshall, DVM, Purdue University College
of Veterinary Medicine, 625 Harrison St,
West Lafayette, IN, USA.
E-mail: marsha80@purdue.edu
(K. Marshall)
Administration of intravenous fluids is a critical, life-saving ther- Determining when a patient has gotten to the point where
apy for both human and animal patients. Large, rapidly adminis- further fluids would not improve CO is the clinical problem that
tered volumes of fluids are the cornerstone of initial stabilization directs CO monitoring has been designed to address. A clinician
in most types of shock; the goal is to restore circulating volume wants to give enough fluids to maximize CO and avoid the
and improve tissue perfusion.1 An alternative way of thinking development of ischemia, anaerobic metabolism, and ultimately
about treating these patients is to consider improving the cardiac cell and patient death,5 but not to give such a large volume of fluid
output (CO). that there is increased morbidity and mortality from excessive
Cardiac output is defined as the volume of blood that is intravenous fluid administration.6-9
transferred from the left ventricle to systemic circulation over Knowing that an unstable patient is no longer fluid responsive
time. This is measured in ml/kg/min in veterinary medicine. might also lead a clinician to seek alternate therapies to improve
Normal CO in the dog or cat is 120-200 mL/kg/min. Another way perfusion (inotropes, pressors, blood products, etc.). Several
to think about CO in species of variable size such as dogs and cats methods of assessing fluid responsiveness have been investigated
is to divide the CO by the animal’s body surface area. This is in veterinary medicine.
known as the cardiac index (CI). Surface area is used in this
equation as it is thought to correlate better with the animal’s
metabolic rate than the weight. Cardiac index is measured in Estimation of Preload1
L/min/m2 (Table 1).2
The importance of determining the CO and understanding the Central Venous Pressure
variables involved helps to demonstrate the fact that not every
animal in shock or showing evidence of hypoperfusion requires Although not a direct measure of CO, central venous pressure
fluid therapy. Previous research in human medicine has shown has been used to guide fluid therapy, to assess a patient’s volume
that approximately 50% of critically ill patients are fluid responsive.3 status, and to measure the response to fluid administration in
Fluid responsiveness can be explained by the Frank-Starling (FS) human and veterinary medicine for several decades. Because
principle and curve (Fig 1). central venous pressure is equivalent to the pressure within the
The FS principle states that stroke volume increases as cardiac intrathoracic vena cava, it would approximate right atrial pressure.
end-diastolic volume increases (i.e., as the ventricles fill with more The pressure in the right atrium and vena cava is directly related to
blood, more blood is ejected from the heart). This relationship is the volume of blood in these locations.
built on the fact that more blood means increased stretching of the Blood in the vena cava and right atrium is largely representa-
cardiac myofibrils, which improves contractility.4 However, as the tive of the venous return (blood returning from the peripheral
myofibrils have a maximal amount that they can physically vascular beds into the central venous compartment). This systemic
stretch, this creates a plateau on the curve (Fig 1). As the patient blood presented to the heart is also known as the preload. The
moves toward the flat part of the FS curve, the myofibrils become preload arriving at the right atrium should completely empty into
maximally stretched and CO does not increase, no matter how the right ventricle, thus creating the right ventricular end-diastolic
much more fluid is presented to the heart. volume. Therefore, right ventricular end-diastolic volume is
http://dx.doi.org/10.1053/j.tcam.2016.08.006
1527-3369/ & 2016 Topics in Companion Animal Medicine. Published by Elsevier Inc.
K. Marshall et al. / Topics in Companion An Med 31 (2016) 100–108 101
Table 1
RAP RV
Comparision of formulas for CO and CI. CVP RAV volume
CO ¼ HR SV CO HR SV
CI ¼ ¼
BSA BSA
LV LA
volume volume
Preload dependent
Fig. 1. The Frank-Starling curve. On the steep portion of the Frank-Starling curve,
stroke volume increases as the preload increases (i.e., as the cardiac end-diastolic
volume increases). In other words, as there is increased ventricular filling, more
blood is ejected from the heart. When the cardiac myofibrils reach maximal
stretch, the ventricles cannot fill any further and no additional blood can be ejected
from the heart. This is depicted by the flat part of the curve. When patients are in
the preload dependent part of the curve, they would likely be fluid responsive. Fig. 3. Correct placement of the jugular catheter for central venous pressure
However, when patients are on the plateau part of the curve (preload independent measurement. Note: The tip of the jugular catheter is immediately cranial to the
portion), they would not be responsive to fluid administration. right atrium.
102 K. Marshall et al. / Topics in Companion An Med 31 (2016) 100–108
Fig. 4. Central venous pressure (CVP) measurement. This picture shows a dog
having his central venous pressure measured. Note, that we are using a manometer
attached to a jugular catheter to evaluate the pressure reading.
Table 2
A comparison of Central Venous Pressure (CVP) Monitoring With Serial Examinations
Patient 1: 3-year-old male castrated Golden Retriever Patient 2: 5-year-old female spayed000 Yorkshire Terrier
8AM: QAR, HR ¼ 120, RR ¼ 12, mm-pink, CRT o2, good pulse quality, 8AM: Obtunded, HR ¼ 180, RR ¼ 36, mm-pale, CRT 4 2, weak femoral pulses,
CVP ¼ 0, and Doppler BP ¼ 90 CVP ¼ 1, and Doppler blood pressure ¼ 40
Fluid bolus given Fluid bolus given
12AM: QAR, HR ¼ 90, RR ¼ 12, mm-pink, CRT o2, good pulse quality, 12PM Obtunded, HR ¼ 160, RR ¼ 24, mm-pale, CRT 2 s, weak femoral pulses,
CVP ¼ 2, and Doppler blood pressure ¼ 120 CVP ¼ 2, and Doppler blood pressure ¼ 70
Fluid bolus given
4PM: BAR, HR ¼ 70, RR ¼ 12, mm-pink, CRT o2, good pulse quality, 4PM: QAR, HR ¼ 160, RR ¼ 16, mm-light pink, CRT o 2 s, weak femoral pulses,
CVP ¼ 5, and Doppler blood pressure ¼ 110 CVP ¼ 2, and Doppler blood pressure ¼ 90
Fluid bolus given
8PM: BAR, HR ¼ 60, RR ¼ 10, mm-pink, CRT o 2 s, good pulse quality 8PM: QAR, HR ¼ 100, RR ¼ 12, mm-light pink, CRT o 2 s, improved femoral pulses,
CVP ¼ 0, and Doppler blood pressure ¼ 120 CVP ¼ 5, and Doppler blood pressure ¼ 100
Both patients presented with a 2-day history of severe watery diarrhea, vomiting, and lethargy. Note, that patient 1 has persistently low CVP values; however, the remainder
of his physical examination parameters are improving over time. In this case, it is unlikely that CVP measurements accurately reflect volume status in this clinically stable
patient. In contrast, patient 2 appears to be in shock based on her physical examination findings. Her CVP numbers are suggestive of hypovolemia. The CVP values used along
with her examination findings suggest that fluid therapy may be beneficial to this patient. BAR, bright, alert, and responsive; QAR, quiet, alert, and responsive; CRT, capillary
refill time; mm, mucous membrane color; HR, heart rate; RR, respiratory rate.
over approximately a 3-minute period (Fig 6) An arterial blood thermodilution. In transpulmonary thermodilution, a patient
sample can be compared with a mixed arteriovenous (usually receives an injection of a predetermined amount of an indicator
from the pulmonary artery) blood sample as an alternative to the (dye, lithium, or cold saline) into the bloodstream (usually the
respiratory gas analysis.2 jugular vein), and this indicator is sampled and measured in blood
Although the Fick’s method was considered the original downstream from the original injection site (usually the femoral
gold standard for CO monitoring, it has several disadvantages artery). The amount of the indicator found in the downstream
that prevent it from being clinically useful. First, it is not a blood is used to generate a time-dilution curve that in turn can be
real-time measurement of CO, because the respiratory gases and used to derive CO (Fig 8). However, in pulmonary artery thermo-
arterial blood gases require laboratory analysis, which takes time dilution, a pulmonary artery catheter is placed and a predeter-
before acquiring results. It also requires that the patient be mined amount of indicator is injected into the catheter and is
intubated to obtain accurate collection of inhaled and exhaled detected by a thermistor located in the pulmonary artery. Inter-
respiratory gases. Finally, this method can only be used in a mittent transpulmonary thermodilution has acceptable agreement
patient who is hemodynamically stable because the results are with pulmonary artery thermodilution but is not as accurate in
less accurate if shunting of blood is occurring in an unstable monitoring trends.25
patient.21 These 2 methods have recently been compared in patients with
fluid overload and were found to show good agreement and an
accurate assessment of CO.26
Noninvasive CO Monitoring
Noninvasive CO monitoring is a method that calculates CO by
carbon dioxide (CO2) rebreathing using a modified Fick’s equation.
An intubated patient is connected to a proprietary rebreathing
system that contains CO2 and flow sensors. A rebreathing exercise
using a “rebreathing loop” is performed to assess CO. (Fig 7). The
comparative value of the CO2 concentration can be used to
calculate CO.
When CO is low, the exhaled CO2 is similar to inhaled CO2
because less blood is traveling to tissues and bringing waste CO2
from the tissues back to the lungs to be exhaled. When the CO is
high, more blood is circulating through the tissues and bringing
CO2 back to the lungs, so the exhaled CO2 is significantly higher
than inhaled CO2. The change in CO2 after the rebreathing circuit
is activated for a predefined period of time and is used to
estimate CO.
This method of CO monitoring is less invasive than the Fick’s
method and has been found to work well in dogs and foals.22,23
Limitations include the need for an intubated and preferably
ventilated patient, which is not always practical in a clinical
setting.
Fig. 7. Noninvasive Cardiac Output (NICO). This diagram shows the setup for using NICO. The NICO device analyzes the CO2 exhaled by the patient through an endotracheal
tube. Typically, this is done during a rebreathing exercise. During the rebreathing exercise, a rebreathing valve (pictured earlier) is opened and the patient breathes in their
own exhaled gases. This exercise increases the concentration of inhaled CO2. Then when the rebreathing loop is closed, the CO2 sensor measures the patient's inhaled CO2
concentration and compares it with the exhaled CO2. The rebreathing loop is simply used to increase the magnitude of CO2 delivered to the patient for ease of measurement.
(Adapted with permission from http://frca.mikrocom.co.uk/Anaesthetics/Presentations/CardiacOutput/index.php).
Indicator dilution methods have replaced Fick’s method as the rupture, pulmonary thrombosis, and arrhythmias making them
current gold standard of CO monitoring because of their high level less practical for clinical patients.
of accuracy and ease of use. However, most indicator dilution
methods are relatively invasive, requiring a pulmonary artery Pulse Contour Analysis
catheter, central venous catheterization, or central arterial cathe-
terization or all of these. Pulmonary artery catheters have been More recently, the dilution methods described earlier have
associated with serious side effects such as pulmonary artery been combined with pulse contour analysis. In addition to
Fig. 8. Indicator dilution method for cardiac output monitoring. This method of cardiac output monitoring involves injecting an indicator, usually lithium, room temperature
saline, or a dye into the venous side of circulation. A known concentration of indicator is typically injected into the jugular vein. Blood samples are then removed from the
arterial side of circulation, and the difference in concentration of the indicator is measured and used to calculate cardiac output in a method similar to the Fick's method.
RAEDV, right atrial end-diastolic volume; LAEDV, left atrial end-diastolic volume; PBV, Pulmonary blood volume; LAEDV, left atrial end-diastolic volume; LVEDV, left
ventricular end-diastolic volume. (Image adapted with permission from derangedphysiology.com).
K. Marshall et al. / Topics in Companion An Med 31 (2016) 100–108 105
Ultrasonographic Methods
Temperature
Transthoracic Echocardiography
Low cardiac output Transthoracic echocardiography has long been used to estimate
CO. Stroke volume is calculated from echocardiographic measure-
Time
ments of the velocity of blood flow in the left ventricular outflow
multiplied by the cross-sectional area of the left ventricular
Temperature
outflow tract. This product equals stroke volume, and CO is then
calculated by multiplying the stroke volume by the patient’s heart
rate.29
This method is noninvasive, requiring only the use of an
High cardiac output ultrasound probe to perform the echocardiogram. However, it is
Time technically difficult to get the correct measurements, typically
requiring a trained cardiologist. Additionally, this method cannot
continuously report the CO, and any arrhythmias would affect the
Temperature
accuracy.
Fig. 9. Time vs. indicator curves created during PiCCO (thermodilution) or LiDCO
Esophageal Doppler
(lithium dilution) pulse contour analysis techniques. Curve 1 represents the curve
seen with normal cardiac output. In low cardiac output states, such as depicted in Esophageal Doppler (ED) is used to measure blood flow
curve 2, the curve is taller and wider because it takes a longer time to detect the velocity in the descending aorta. The Doppler probe is placed
dye or temperature change in low cardiac output states. The opposite is true for orally into the esophagus and inserted to the level of the
curve 3—the high output cardiac state—where the indicator is detected sooner. descending aorta. Aortic flow velocity combined with aortic
This is represented by a smaller and steeper curve. The cardiac output is measured
by the area under the curve. In PiCCO annd LiDCO methods, the computer used to
diameter is used to calculate stroke volume and then CO (Fig 11).
measure these images is initially calibrated by comparing its measured CO with the This method is minimally invasive. However, correct
CO measured by thermodilution or lithium techniques, respectively. probe placement is essential to obtain accurate measurements.
106 K. Marshall et al. / Topics in Companion An Med 31 (2016) 100–108
Fig. 11. Diagram of esophageal Doppler technique for cardiac output monitoring. The Doppler probe is inserted through the mouth to the level of the descending aorta. The
probe has 2 parts, a transmission crystal and a receiving crystal. The ultrasound waveform detects the velocity and peak flow of blood through the descending aorta through
the crystals and uses this information to calculate the stroke volume, which in turn is used to calculate cardiac output (i.e., by multiplying it by heart rate).
Additionally, to tolerate the placement of the probe, general a current encounters as it travels through a circuit; in this
anesthesia is required. ED has been evaluated in dogs, cats, and case, the circuit is the thorax. The impedance of the curr-
horses with variable results. Specifically, ED was not accurate in ent varies in relation to the amount of fluid within the thorax
measuring CO in dogs33,34 but may be useful to monitor trends in and specifically owing to changes in blood flow within the aorta.
cats.35 In horses, ED was found to give accurate CO data but was This method is noninvasive and requires the application of
difficult and time consuming to use.36 sensor pads to the thorax that detect changes of the amplitude of
the electric current as it passes through the thorax. In both human
and veterinary medicine, TEB has had variable correlation com-
Ultrasound CO Monitor pared with thermodilution methods of CO monitoring, making it
Ultrasound CO monitor (USCOM) is a noninvasive ultrasound unreliable to predict CO.41,42 Another potential drawback of TEB in
monitor that uses transaortic or transpulmonary blood flow veterinary medicine is its decreased accuracy in awake, moving
tracings to calculate CO and stroke volume (Fig 12). The USCOM patients and loud environments, reducing its use in an ICU setting
machine uses a proprietary mathematical formula to calculate on awake patients.
stroke volume from the waveform tracings. Bioreactance (NICOM) is similar to TEB in that an electric
However, as a standard aortic diameter measurement is pre- current of a known frequency is applied across the thorax
loaded into the machine for adult and pediatric human patients for (Fig 13). However, in bioreactance, the frequency or phase shift
stroke volume calculation, this presents a problem in veterinary of the electric current is measured. A delay in phase shift (i.e., a
medicine given the wide variety of patient sizes encountered. decrease in frequency of the electric current) is associated with an
Therefore, before using the USCOM, an echocardiogram would increase in stroke volume.
need to be performed to determine aortic diameter and incorpo- Bioreactance is noninvasive and only requires the application
rate this into the machine’s software. Only then would there be a of adhesive sensor pads to the thorax. Unlike bioimpedance,
chance for appropriate calculation of the animal’s CO with this bioreactance has been shown to correlate well with thermodilu-
method. tion methods of CO monitoring in a variety of human patients.43,44
Although USCOM is noninvasive, it has had mixed results Bioreactance has been evaluated experimentally in dogs and had
compared with thermodilution in animals and is not a continuous an excellent correlation with thermodilution but has not been
monitoring device.37 Recent human studies have shown that used clinically.45
USCOM can detect decreases in stroke volume because of blood
loss in conscious patients, making USCOM potentially useful
in an emergency setting to assess human patients with Conclusions
hypovolemia.38 USCOM has been found to be accurate in sheep
and beagles39,40; however, it is has not been used clinically in Direct CO monitoring is the most ideal way to assess fluid
veterinary patients. responsiveness and to guide fluid therapy in critically ill patients.
However, there is no one good way to measure CO in veterinary
medicine. Many methods used to evaluate CO are invasive, poorly
Bioimpedance and Bioreactance researched in veterinary medicine, or impractical to use clinically.
Additionally, the most commonly used objective clinical estimate
Thoracic bioimpedance (TEB) applies a high-frequency elect- of volume status—central venous pressure—does not reliably
ric current of known amplitude and frequency across the thorax correlate with preload in the heart and is a poor predictor of fluid
(Fig 13). Impedance is defined as the amount of resistance responsiveness.
K. Marshall et al. / Topics in Companion An Med 31 (2016) 100–108 107
Fig. 12. USCOM. This image shows proper placement of the ultrasound probe and typical waveform on the USCOM display.
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