Alterations in tissue oxygen saturation measured by near-infrared spectroscopy in trauma patients after initial resuscitation are associated with occult shock

Trauma is the most frequent cause of death among people aged between 5 and 29 years old worldwide [1], and in trauma patients, hemorrhagic shock is the first cause of preventable death [2, 3]. To increase the chances of survival, efforts must be made to rapidly detect and resuscitate patients from shock [2, 4, 5]. The classical definition of shock is the alteration of vital signs, but, after normalization of these parameters, up to 85% of severely injured trauma patients still have persistent hypoperfusion and ongoing tissue acidosis, also known as occult shock, which may lead to organ dysfunction and death [4, 6]. Traditional markers such as blood pressure, heart rate, urine output, and mental status are still commonly used to guide resuscitation in trauma patients [7, 8] but they are non-specific [9, 10]. Other markers such as arterial lactate or base deficit (BD) are accurate and objective but require invasive monitoring or intermittent blood sampling, and may still fail to detect regional hypoperfusion [9]. To improve the ability to detect ongoing hypoperfusion, monitoring of regional “non-vital” areas, such as the splanchnic area or peripheral skeletal muscle, has been proposed [11, 12]. It has been suggested that regional hypoperfusion should be evaluated at the end of conventional resuscitation, when “global” hypoperfusion markers have been corrected [11]. On the whole, even though several markers of resuscitation have been described, to date, no gold standard has been identified [4].

During hemorrhagic shock, the activation of the sympathetic nervous system causes a redistribution of the blood flow from the periphery to the central compartment, to maintain optimal perfusion of the vital organs [13]. Near-infrared spectroscopy (NIRS) provides a rapid, noninvasive, and continuous estimate of local tissue oximetry, also known as regional tissue oxygen saturation (rSO₂), and it is generally used in peripheral areas such as the skeletal muscle [9, 14, 15]. Real-time measurements of rSO₂ allow dynamic assessment of the patient’s response to resuscitation, and additional data can be obtained from a vascular occlusion test (VOT), a regional stress test that has repeatedly demonstrated its value in the assessment of hemodynamic alterations in several scenarios [10, 14].

The objective of this study was to establish whether NIRS-derived muscle rSO₂, and the response to a VOT, were associated with occult shock once conventional global resuscitation was considered to be complete. To this end, other commonly used markers of shock were compared, including vital signs, Shock Index, ROPE index, hemoglobin, natriuretic atrial peptide, arterial BD, serum lactate concentration, and coagulopathy, defined according to rotational thromboelastography (ROTEM^®).

Our data suggest that, after 8 h of active treatment, alterations in rSO₂-related parameters may help to detect apparently hemodynamically stable patients who are still under-resuscitated. These findings are relevant, since alterations in NIRS parameters can provide clinicians with important information regarding the evaluation of otherwise clinically stable patients.

Occult shock, defined as persistent hypoperfusion with normal vital signs, remains a controversial entity [5], and its definition has evolved along with the appearance of new metabolic and perfusion parameters. In recent years, regional parameters have demonstrated their additional value compared with global metabolic parameters [5, 12, 19, 20] such as lactate, thus further stressing the importance of the concept of occult shock. In the present study, occult shock was defined as the need for additional blood cell transfusion, use of vasopressors or need for surgery or angioembolization in trauma patients, whose vital signs were normal, between the 8th and 48th hour of hospital admission. Our results suggest that regional tissue oxygenation parameters play a key role in the detection of occult shock and in the need for further resuscitation interventions.

Our findings are consistent with previous data on NIRS monitoring, and are based on a strong pathophysiological rationale. We observed that, in apparently stable patients, higher rates of desaturation following a VOT were associated with the need for further resuscitation interventions to control bleeding in the following 48 h. These higher rSO₂ desaturation rates can only be attributed to two underlying mechanisms, or a combination of them: (a) diminished local blood flow, and (b) increased local metabolic rate. In situations of hypovolemia, blood flow is diverted from the periphery to the central compartment, causing a “stealing effect” of blood from these peripheral or non-vital areas. This compensatory mechanism is mainly driven by the activation of the sympathetic system, which also increases the metabolic rate, as a result of the effect of the release of catecholamines [13]. Regrettably, our study does not allow us to separate these two phenomena, but our results are consistent with those of other authors who have shown that alterations in VOT-derived parameters are associated with the redistribution of the blood flow towards the central compartment and sympathetic activation [19, 20]. Interestingly, VOT-derived parameters are useful in situations where the compensatory mechanisms are subclinical and are not detected by the standard hemodynamic monitoring tools.

Previous studies have already described NIRS technology as a useful tool for detecting tissue hypoperfusion in trauma patients [4, 14, 15, 21, 22]. The results of our study coincide with those of Guyette et al. [10] which obtained a prehospital absolute rSO₂ and performed a VOT in 150 trauma patients, and concluded that, even though rSO₂ had prognostic value for mortality and multiple organ failure, it did not identify occult shock states. This was considered an inherent limitation of the technology, insofar as peripheral vasoconstriction associated with compensated shock states may be accompanied by a reduction in regional tissue oxygen demand and compromised supply. However, stressing the system by producing a vascular occlusion yielded parameters such as the rSO₂ de-saturation and re-saturation slopes, which distinguished between patients requiring bleeding control maneuvers and those that did not. Additionally, the analysis of lactate and SBP found no statistical relationship for these variables, and the authors concluded that VOT-derived variables were capable of detecting occult shock when vital signs and lactate were normal. NIRS technology has also been recommended in AHD patients before starting resuscitation maneuvers [15] or when “global” resuscitation maneuvers have finished, to identify patients with persistent microcirculatory hypoperfusion [14, 21]. The second case coincides with the moment when occult shock was evaluated in this study, after 8 h of hospital admission. Conversely, Crookes et al. [9] found a statistically significant relationship only between absolute rSO₂ and severe shock, and not with mild or moderate shock. It should be stressed that no VOT was performed; therefore, in situations of severe shock absolute rSO₂ is altered, but in states of moderate or occult shock it remains normal while VOT-derived variables are altered. In general, we can infer that absolute rSO₂ values may be capable of detecting overt shock, and that VOT-derived parameters are useful in situations where the hemodynamic status is apparently compensated and provide additional help in the detection of tissue hypoperfusion. When analyzing the HDU group, one would expect HDU patients to show lower regional oxygenation parameters. However, the lack of differences might derive from our definition of HDU, including those patients who were hypotensive, tachycardic, and/or requiring vasopressors. In fact, 27 patients were classified as HDU because they were on vasopressors. Therefore, although we considered those patients to be HDU, they were probably resuscitated, with normalized tissue perfusion/oxygenation, despite requiring vasopressors to achieve that normalization. Our study adds to the current evidence and underlines the value of regional tissue oxygenation as part of the monitoring tool kit for the hemodynamic resuscitation of trauma patients.

The predictive power of non-NIRS-related variables was very limited except for lactate and BD, two parameters that have classically been related to occult shock detection [4‐6, 23‐26]. However, some publications such as James et al. [27] reject the relationship between tissue acidosis and lactate, considering that lactate elevation is related to the catecholaminergic response to trauma. Other authors such as Pal et al. [23] and Petrosoniak et al. [5] have associated persistent elevation of lactate with occult shock; Abramson et al. [24] considered that patients with pathologic lactate and normalized vital signs needed more aggressive monitoring. Brohi et al. [25] stated that lactate and BD can be considered equivalent and that lactate alteration is an indicator of hypoperfusion, while Guyette et al. [26] recommend prehospital lactate evaluation to identify occult shock in patients with normalized vital signs.

Blow et al. [6] defined occult shock as the presence of lactate > 25 mg/dL in patients with SBP > 100 mmHg, HR < 120 mmHg and diuresis > 1 ml/kg/h. Patients who met the inclusion criteria received intensive resuscitation to normalize lactate values during the first 24 h of hospital stay, and showed reduced mortality when normalization was achieved.

In contrast, our study did not detect a statistically significant relationship between lactate or BD and occult shock. This absence of a statistical relation might be attributable, on the one hand, to the small sample size, as we compared 12 THD patients with five OS patients. On the other hand, most authors associate lactate and BD with mortality [4, 6, 24, 25, 28] and multiple organ failure [4, 6, 25, 28] considering it to be secondary to tissue hypoperfusion; however, in our study, NIRS VOT-derived variables showed a higher capacity to detect microcirculation alterations, even though the sample of patients analyzed was small.

A previous study by our group considered the Shock Index (SI) as a marker of occult shock when it was ≥ 0.8 [29] because patients subsequently needed maneuvers to control surgical bleeding or activation of a massive transfusion protocol. It has also been considered as an occult shock marker with scores ≥ 0.9 [30, 31], in relation to multiple organ failure or mortality in patients with previously normal vital signs.

In contrast, our study did not find a statistically significant relationship between the SI and occult shock. This may have been due to the moment in time when the SI was evaluated. Generally, the studies that associate the SI with bleeding control maneuvers use it during prehospital care [31, 32] or at hospital admission [29, 31, 33, 34]; no studies have evaluated the SI after the first hour of hospital admission.

The main limitation of our study is the small sample of trauma patients analyzed. However, and though the number of patients is small, VOT-derived variables presented statistically significant relationships with occult shock, while the other variables did not.

After 8 h of hospital care, NIRS evaluation with an occlusion test might be helpful for identifying occult shock in otherwise apparently hemodynamically stable trauma patients. In this study, no other resuscitation marker analyzed showed a statistically significant association with occult shock detection. Therefore, VOT-derived parameters may be a relevant screening tool for detecting patients at risk of hemodynamic deterioration. Further and larger prospective study would be needed to confirm our findings.