ICU Management & Practice, Volume 16 - Issue 3, 2016

Monitoring Peripheral Circulation

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Even though systemic haemodynamic variables may be normalised, ‏there could be regions with inadequate regional oxygenation at the tissue ‏level. The most recent developments of noninvasive monitoring of the ‏peripheral circulation have helped physicians to early identify patients ‏at high risk for tissue hypoperfusion, organ failure and poor outcome. ‏


Why Might Clinical Assessment of Peripheral Circulation be Helpful?


Examination of peripheral circulation is easily ‏done by touching the skin, measuring capillary ‏refill time (CRT) or even by observing the ‏skin mottling pattern. The cutaneous vascular ‏bed plays an important role in thermoregulation ‏of the body, and this process can result ‏in skin circulation alterations that have direct ‏effects on skin temperature and colour, i.e., a ‏cold, clammy, white and mottled skin. There ‏are different methods to clinically assess the ‏peripheral perfusion.


Mottle Score


Pallor, mottling and cyanosis are key visual indicators ‏of reduced skin circulation, which can ‏be scored by just looking at the skin. Mottling ‏is the result of heterogenic small vessel vasoconstriction ‏and is thought to reflect abnormal ‏skin perfusion. It is defined as a bluish skin ‏discolouration that typically manifests near the ‏elbows or knees and has a distinct patchy pattern. ‏

Capillary Refill Time


Capillary refill time (CRT) is defined as the time ‏required for a distal capillary bed (e.g. nail bed, ‏forehead or knee) to regain its colour after pressure ‏has been applied to cause blanching. Over ‏the past 30 years, the definition of a delayed ‏CRT has been debated in the literature. Very ‏few studies have addressed the CRT normal ‏range in adults and its relation to body site, ‏effect of ambient or skin temperature, and ‏its reliability among examiners. Compelling ‏recent studies have demonstrated that the interrater ‏reliability for CRT measurement between ‏examiners showed substantial agreement for ‏the strategy of subjective CRT evaluation at the ‏bedside (Ait-Oufella et al. 2014; van Genderen ‏et al. 2014b). Assuming normal core temperature, ‏decreased skin blood flow as the cause of ‏delayed CRT can be estimated by measuring ‏skin temperature, since cold extremities reflect ‏constriction of cutaneous vessels that ultimately ‏decreases the amount of blood volume within ‏peripheral vasculature. By contrast, peripheral ‏vasodilation has the opposite effect. Inducing ‏peripheral vasodilation with nitroglycerin infusion ‏in patients with shock after haemodynamic ‏stabilisation and with much delayed CRT resulted ‏in significant decrease in CRT by 51% toward ‏normal compared with baseline values (Lima ‏et al. 2014).

Skin temperature

One should pay attention to how to evaluate skin ‏temperature. A temperature gradient can better ‏reflect changes in cutaneous blood flow than ‏the absolute skin temperature itself. As peripheral ‏temperature may be influenced by ambient ‏temperature, a gradient between forearm and ‏finger temperature may be a more reliable ‏measurement, as the two skin temperatures ‏are exposed to the same ambient temperature. ‏Assessing skin temperature by touching the ‏extremities or measuring a body temperature ‏gradient can assist the physician to recognise a ‏clinically acceptable CRT, which is more predictive ‏in warm extremities conditions. Because ‏of a conditional effect, cold extremities will ‏often be related to a delayed CRT. Therefore, if ‏the extremities are cold, one should expect a ‏delayed CRT and CRT will not be much help ‏for the clinician. On the other hand, warm ‏extremities indicate adequate cutaneous blood ‏flow and one should expect a normal CRT, and ‏a delayed CRT in this condition suggests cutaneous ‏microcirculatory derangement (Lima et ‏al. 2011).

See Also: Study: Hyperoxia Alters Microcirculation in Healthy Volunteers 

Minimally Invasive Technologies to Assess 
Peripheral Circulation

Despite all the technological innovation in monitoring ‏peripheral circulation, there has been little ‏success in incorporating these technologies in ‏clinical practice. Many factors contribute to this, ‏but their clinical use still faces some hurdles ‏for adoption. The signal from these devices is ‏accessible at regional level and is often unfamiliar ‏to the doctor, who is unable to contextualise ‏its use in order to influence critical care. This ‏is a barrier against their acceptance, as is the ‏high cost of these devices. To be successful, the ‏technique should be feasible for routine use at ‏the bedside, robust, easy to use and to integrate ‏into care. Minimally invasive technologies that ‏cover some of those criteria include optical ‏monitoring devices and transcutaneous measure- ment of oxygen tension (Table 1) (Lima and ‏Bakker 2005). Optical monitoring utilises the ‏optical properties of haemoglobin to measure ‏partial pressure of oxygen and haemoglobin ‏saturation. Commonly used optical methods ‏in the clinical setting that are able to monitor ‏tissue oxygenation at the bedside include nearinfrared ‏spectroscopy and direct visualisation ‏of the sublingual microcirculation. Continuous ‏transcutaneous measurement of oxygen tension ‏is based on the electrochemical properties of ‏noble metals to measure the oxygen content ‏of the tissue.


Near-Infrared Spectroscopy (NIRS)


The utility of NIRS for managing critically ill ‏patients remains a matter of debate (Macdonald ‏and Brown 2015). A new trend for the NIRSderived ‏StO2 application is in predicting complications ‏and early identification of septic patients ‏at high risk for microcirculatory failure during ‏specific haemodynamic therapeutic interventions, ‏such as vasopressor and blood transfusion ‏therapy (Conrad et al. 2015; Damiani et al. ‏2015). These studies outline the new trend of ‏the clinical application of NIRS as a potential ‏candidate to evaluate tissue monitoring during ‏clinical treatment of those diseases that impact ‏microvascular function, such as sepsis and hypovolaemia. ‏However, there are some drawbacks of ‏NIRS technology that still have to be addressed ‏in future studies. Changes in StO2 values may ‏be confounded by factors other than the true ‏marker of thenar muscle oxygenation, and StO2 ‏values may mislead the bedside clinician to ‏assume that tissue hypoxia is present, when this ‏change may merely reflect low blood flow to the ‏superficial layers above the muscle capillary beds. ‏In addition, the technique for using vascular ‏occlusion test (VOT) has not been standardised. ‏Currently, various types and degrees of deflation ‏thresholds (StO2 of 10% or 40%; duration of ‏3 or 5 minutes) are used and no supporting ‏evidence in the literature shows which of the ‏methods is superior and more reliable to assess ‏the VOT-derived StO2 slopes. These highlight a ‏necessary further step in evaluating the NIRS ‏clinical utility and its possible use in predicting ‏complications and early identification of patients ‏at risk for microcirculatory failure.


Direct Visualisation of the Sublingual Microcirculation


Due to rapid advances in technology, microcirculation ‏evaluation has been dynamic work, and ‏new devices have been introduced that improve ‏microcirculatory image acquisition. Recently, ‏a more advanced version of handheld microscopes ‏(CytoCam, Braedius Medical, Naarden, ‏The Netherlands), based on Incident Dark Field ‏(IDF), has been introduced to overcome persistent ‏limitations of the earlier devices (Hutchings ‏et al. 2015). The main technological improvements ‏of IDF include higher optical resolution, ‏lower weight of the device and digital signal ‏allowing more vessels to be observed with larger ‏detail. In addition, recording of videos and image ‏frames are directly computer analysed automatically ‏at the bedside. Whether IDF measurements ‏can reproduce and confirm similar microcirculatory ‏patterns in shock from the previous studies ‏with SDF needs to be confirmed. Nevertheless, ‏some studies have compared SDF imaging and ‏CytoCam IDF imaging in healthy subjects and ‏neonates with promising results (Aykut et al. ‏2015; Gilbert-Kawai et al. 2016; van Elteren et ‏al. 2015). Other studies have focused on the ‏feasibility of monitoring and analysing sublingual ‏microcirculation by nurses at the bedside ‏using the Cytocam IDF (Tanaka et al. 2015). ‏Bringing to the bedside the complete package ‏of microcirculation analysis is an initial step ‏towards the incorporation of physicians and ‏nurses into the measurement and interpretation ‏of microcirculation status at the bedside ‏(Lima et al. 2015). ‏


Continuous PtcO2 transcutaneous measurement


Oxygen sensors for transcutaneous electrochemical ‏measurements are based on polarography: ‏a typical amperometric transducer ‏in which the rate of a chemical reaction is ‏detected by the current drained through an ‏electrode. The sensor heats the skin to 43-45ºC, ‏and as a result the skin surface oxygen tension ‏is increased. These transcutaneous sensors ‏enable us to directly estimate arterial oxygen ‏pressure (PaO2). However, in adults the skin ‏is thick, and differences in the skin cause the be lower than PaO2. The correlation between ‏PtcO2 and PaO2 also depends on the adequacy ‏of blood flow. The low blood flow caused by ‏vasoconstriction during shock overcomes the ‏vasodilatory effect of PtcO2 sensor. This causes ‏a mild tissue hypoxia beneath the PtcO2 sensor. ‏The lack of the PtcO2 ability to accurately reflect ‏the PaO2 in low flow shock enables us to estimate ‏cutaneous blood flow through the relationship ‏between the two variables. The PtcO2 and PaO2 ‏values are almost equal when the blood flow ‏is adequate. During low flow shock, however, ‏the PtcO2 will drop and becomes dependent on ‏the PaO2 value. Some studies have suggested the ‏use of an oxygen challenge test, which refers ‏to the lack of PtcO2 rise in response to high ‏oxygen inspired fraction in patients with normal ‏lung function, and has shown good predictive ‏value for unfavourable outcome of septic shock ‏patients (Mari et al. 2014; Schlager et al. 2014). ‏Some technical aspects should be considered ‏when performing the oxygen challenge test, ‏such as microcirculatory modifications due to ‏heat-induced vasodilation by the electrode, and ‏altered cutaneous vasomotor reactivity due to ‏the transient hyperoxia. Altered lung function ‏might have an influence on PtcO2 and thus affect ‏the oxygen challenge test. For example, a PaO2 ‏at 100% inspired oxygen fraction can remain ‏low with no subsequent increase of PtcO2 during ‏the oxygen challenge test (Mari et al. 2014).


Clinical Implications


Recent advances in diagnostic and monitoring ‏technologies have helped intensivists to better ‏understand the complex pathophysiology of ‏acute circulatory failure. The power and objectivity ‏provided by these new technologies ‏might cause us to think that peripheral circulation ‏examination in the intensive care setting ‏has become obsolete. Much emphasis is given ‏to the global variables of perfusion, whereas ‏relatively little is said about less vital organs, ‏like skin and/or muscle. One may argue about ‏the clinical significance of monitoring circulation ‏of these non-vital organs in which blood ‏flow is not crucial for the immediate survival. ‏Abnormalities in peripheral circulation may still ‏persist although systemic haemodynamic stability ‏has been reached. Moreover, the persistence of ‏these alterations has been associated with worse ‏outcomes (Chien et al. 2007; Poeze et al. 2005). ‏Therefore, some argue that following normalisation ‏of circulation parameters, global systemic ‏parameters are of less importance (Dunser et al. ‏2013). In fact physicians often lose sight of this ‏important point, placing too much emphasis on ‏systemic haemodynamic variables while failing ‏to take the time to perform a simple physical ‏examination of peripheral circulation. The absence ‏of cold extremities, delayed CRT or mottled skin ‏after initial resuscitation identifies patients with a ‏more favourable outcome (Ait-Oufella et al. 2011, ‏Lima and Takala, 2014). One next logical step, ‏therefore, would be incorporating therapeutic ‏strategies into resuscitation protocols that aim at ‏normalising (peripheral) circulation parameters ‏to investigate the impact of peripheral circulation ‏target resuscitation in the survival of critically ill ‏patients (van Genderen et al. 2014a). Thoughtfully ‏integrated with the new technology, the clinical ‏assessment of peripheral circulation should and ‏will continue to be central to intensive care clinical ‏practice.


Conflict of Interest


Alexandre Lima declares that he has no conflict ‏of interest. Michel van Genderen declares that ‏he has no conflict of interest.




CRT capillary refill time

NIRS near infrared spectroscopy

VOT vascular occlusion test

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Damiani E, Adrario E, Luchetti MM et al. (2015) Plasma free hemoglobin and microcirculatory response to fresh or old blood transfusions in sepsis. PLoS One, 10(5): e0122655.



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Lima A, López A, Van Genderen ME et al. (2015) Interrater reliability and diagnostic performance of subjective evaluation of sublingual microcirculation images by physicians and nurses: a multicenter observational study. Shock, 44(3): 239-44.



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Lima A, Van Genderen ME, Van Bommel J et al. (2014) Nitroglycerin reverts clinical manifestations of poor peripheral perfusion in patients with circulatory shock. Crit Care, 18(3): R126.



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Schlager O, Gschwandtner ME, Willfort-Ehringer A et al. (2014) Transcutaneous oxygen tension monitoring in critically ill patients receiving packed red blood cells. J Crit Care, 29(6): 1057-62.



Tanaka S, Harrois A, Nicolaï C et al. (2015) Qualitative real-time analysis by nurses of sublingual microcirculation in intensive care unit: the MICRONURSE study. Crit Care, 19: 388. doi: 10.1186/s13054-015-1106-3.



Van Elteren HA, Ince C, Tibboel D et al. (2015) Cutaneous microcirculation in preterm neonates: comparison between sidestream dark field (SDF) and incident dark field (IDF) imaging. J Clin Monit Comput, 29(5): 543-8.



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van Genderen ME, Paauwe J, de Jonge J et al. (2014b) Clinical assessment of peripheral perfusion to predict postoperative complications after major abdominal surgery early: a prospective observational study in adults. Crit Care, 18(3): R114.


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