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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 2  |  Issue : 3  |  Page : 25-33

Republication: Correlations between venous collapsibility and common hemodynamic and ventilatory parameters: A multivariable assessment


1 Department of Anesthesiology, The Ohio State University College of Medicine, Columbus, OH, USA
2 Departments of Anesthesiology; Surgery, The Ohio State University College of Medicine, Columbus, OH, USA
3 Department of Emergency Medicine, The Ohio State University College of Medicine, Columbus, OH, USA
4 Department of Research and Innovation, St. Luke's University Health Network, Bethlehem, PA, USA

Date of Submission17-Apr-2016
Date of Acceptance08-May-2016
Date of Web Publication19-Aug-2016

Correspondence Address:
Stanislaw P Stawicki
St. Luke's University Health Network, 801 Ostrum Street, Bethlehem, PA 18015
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2455-5568.188738

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  Abstract 

Introduction: Although the venous collapsibility index (VCI) and central venous pressure (CVP) have been shown to correlate reasonably well, little has been reported on the relationships between VCI and other commonly used hemodynamic variables (i.e., HR, blood pressure). This is a retrospective, post hoc analysis of data from a recently completed 3-year prospective study of VCI in critically ill and injured patients.
Materials and Methods: A total of 267 previously recorded data pairs in a group of 82 adults (≥18 to <90 years) patients were included in this analysis. Subsequent correlations were performed between VCI and the following clinical parameters: (a) Heart rate (HR), (b) systolic blood pressure (SBP), (c) diastolic blood pressure (DBP), (d) mean arterial pressure (MAP), (e) pulse pressure, (f) abdominal perfusion pressure (APP or MAP-CVP), (g) positive end-expiratory pressure (PEEP), head-of-bed elevation, and (h) HR-blood pressure index (i.e., HR minus MAP). In addition, correlations between inferior vena cava (IVC) maximum diameter (cm) and demographic variables (age, gender) were performed.
Results: Male patients had significantly greater maximum IVC diameters (2.12 ± 0.89 cm) than female patients (1.81 ± 0.61 cm,P< 0.01). We also observed a statistically significant increase in maximum IVC diameter with increasing age, where patients ages 18–44 had mean maximum IVC diameters of 1.81 ± 0.67 and patients ages 45–90 had mean maximum IVC diameters of 2.04 ± 0.78 (P < 0.05). Statistically significant correlations were found between VCI and DBP (R = 0.217,P< 0.03), PEEP (−0.25,P< 0.01), APP (R = 0.23,P< 0.01), and CVP (R = −0.395,P< 0.01). In addition, in patients who were noted to have clinically and/or hemodynamically “discrepant” VCI and CVP measurements, a high VCI (>50%) more accurately correlated to expected SBP and DBP behavior.
Conclusions: These preliminary results suggest that DBP may correlate with volume status-based VCI behavior than either SBP or MAP and that VCI may be more accurate in patients experiencing intravascular volume depletion. While these findings are not entirely surprising, further studies are warranted to improve our understanding of the clinical implications and relevance of these findings.
The following core competencies are addressed in this article: Medical knowledge, Patient care.
Republished with permission from: Patil P, Kelly N, Papadimos TJ, Bahner DP, Stawicki SP. Correlations between venous collapsibility and common hemodynamic and ventilatory parameters: A multi-variable assessment. OPUS 12 Scientist 2014;8(1):1-5.

Keywords: Clinical correlations, hand-carried ultrasound, hemodynamic assessment, intensivist bedside ultrasonography, venous collapsibility


How to cite this article:
Patil P, Kelly N, Papadimos TJ, Bahner DP, Stawicki SP. Republication: Correlations between venous collapsibility and common hemodynamic and ventilatory parameters: A multivariable assessment. Int J Acad Med 2016;2, Suppl S1:25-33

How to cite this URL:
Patil P, Kelly N, Papadimos TJ, Bahner DP, Stawicki SP. Republication: Correlations between venous collapsibility and common hemodynamic and ventilatory parameters: A multivariable assessment. Int J Acad Med [serial online] 2016 [cited 2019 Jul 23];2, Suppl S1:25-33. Available from: http://www.ijam-web.org/text.asp?2016/2/3/25/188738


  Introduction Top


Traditional hemodynamic assessment of the critically ill and injured patients continues to present a significant challenge to the intensivist due to its propensities for inaccuracy and/or misinterpretation.[1],[2] It is not uncommon for a patient with “normal” vital signs to be in compensated shock state, nor is it atypical for an occasional patient in no acute distress to appear clinically “hypotensive” or “dehydrated.“[3],[4]

Sonologist-performed intravascular volume assessment using venous collapsibility index (VCI) has been introduced to provide bedside clinicians with new, previously inaccessible options for assessing intravascular volume status without resorting to more invasive techniques of hemodynamic assessment (i.e., central venous pressure [CVP] or pulmonary artery catheter).[5],[6] One of the more widely used bedside sonographic parameters for estimation of intravascular volume status is the VCI.[7]

Invasively-placed central venous catheters (CVCs) have long been associated with a variety of potential complications.[8] As a consequence, increasing the number of minimally- and non-invasive hemodynamic monitoring techniques have been introduced.[9],[10],[11],[12],[13],[14],[15],[16] Although a significant amount of research has been published on correlations between VCI and invasively-placed CVCs (pulmonary artery catheter parameters),[14],[17] relatively little literature exists regarding similar correlations with traditional vital signs (i.e. blood pressure, heart rate [HR]). The object of the current investigation is to provide descriptive information regarding the relationships observed between VCI and a variety of traditional “vital signs” as well as a number of related variables that may correlate with observed clinical hemodynamic patterns.


  Materials and Methods Top


After the Institutional Review Board approval, prospective data collection of simultaneously measured sonographic (VCI) and traditional (i.e., HR, blood pressure, CVP) hemodynamic and intravascular volume status variables was performed in 82 adult (ages ≥18 and ≤90 years) patients between June 1, 2011, and May 30, 2014, at a tertiary academic medical center. Consenting patients underwent serial, concurrently performed evaluations of VCI, HR, blood pressure (systolic blood pressure [SBP], diastolic blood pressure [DBP], and mean), CVP (when available), head-of-bed (HOB) elevation, and positive end-expiratory pressure (PEEP). Additional, secondary variables derived from the primary data included the “heart rate-blood pressure index“ (HRBPI) or (HR minus mean arterial blood pressure [MAP]) and the “systemic perfusion pressure” or (MAP minus CVP).

Descriptive and correlative analyses were carried out using Minitab 16 Statistics (Minitab, Inc., State College, Pennsylvania, USA) software package. Normally distributed continuous data were analyzed using Student's t-test and ANOVA while nonnormally distributed variables were analyzed using Mann–Whitney U-test and Kruskal–Wallis testing. Categorical variables were analyzed using Chi-square and Fisher's exact test as appropriate. Correlative analyses were performed using the coefficient of determination. Data are reported as mean ± standard deviation or median with interquartile range as appropriate. Statistical significance was set at alpha = 0.05.

Details of our ultrasound scanning procedures and protocols have been outlined elsewhere 5–7 and will be omitted in this manuscript to avoid duplicate and/or redundant publication. Venous collapsibility was computed, based on the minimum and maximum venous diameters, and determined by M-mode sonography of the vein wall as outlined in our previous work.[5],[6],[7] For the purposes of this study, inferior vena cava collapsibility index (IVC-CI) and subclavian vein CI were considered interchangeable and are being referred to collectively as “venous collapsibility index” as per previously described procedures, techniques, and correlation-based rationale.[5],[6],[7]


  Results Top


Maximum IVC diameter: Demographic determinants.

We observed a statistically significant difference in maximum IVC diameter between male patients (2.12 ± 0.89 cm) and female patients (1.81 ± 0.61 cm, P < 0.01). We also observed a significant difference in maximum IVC diameters between patients <45 years (1.81 ± 0.67) and >45 years of age (2.04 ± 0.78, P < 0.05). Graphical representations of these findings are shown in [Figure 1].
Figure 1: Graphical representation of the relationship between maximum inferior vena cava diameter, patient age (left) and patient gender (right). Males and older patients (≥45 years) had significantly greater maximum measured inferior vena cava diameters

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Heart rate

The correlation between HR and VCI was very poor and not statistically significant (R = 0.069, P = 0.31). Graphical representation of the relationship is shown in [Figure 2].
Figure 2: Relationship between heart rate and venous collapsibility index among patients in this study (R = 0.069, P= 0.310, n = 256 data pairs)

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Systolic blood pressure

The correlation between SBP and VCI was very poor and not statistically significant (R = 0.050, P = 0.61). Graphical representation of the relationship between these variables is shown in [Figure 3].
Figure 3: Relationship between systolic blood pressure and venous collapsibility index for the study group (R = 0.050, P= 0.61, n = 256 measurement pairs)

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Diastolic blood pressure

The correlation between DBP and VCI was poor (R = 0.217) although stronger than that between SBP and VCI. It was statistically significant (P < 0.03). Graphical representation of the correlation between VCI and DBP can be seen in [Figure 4].
Figure 4: Relationship between diastolic blood pressure and venous collapsibility index in the current study (R = 0.217, P< 0.03, n = 256 data pairs)

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Mean blood pressure

The correlation between MAP and VCI was also poor (R = 0.130). The relationship did near statistical significance (P = 0.06). Graphical depiction of the correlation between MAP and VCI is shown in [Figure 5].
Figure 5: Relationship between mean blood pressure and venous collapsibility index measurements for the study group (R = 0.130, P= 0.06, n = 256 data points)

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Pulse pressure

The correlation between pulse pressure (SBP–DBP) and VCI was very poor and not statistically significant. The graph depicting the above relationship is presented in [Figure 6].
Figure 6: Relationship between pulse pressure and venous collapsibility index measurements of patients in the current study. No significant correlation was seen between the variables

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Heart rate-blood pressure index

This variable or a difference between measured HR and the mean blood pressure represents an attempt at quantifying the degree of hemodynamic dysfunction. For example, a patient who is tachycardic and hypotensive is expected to have a higher HRBPI than a patient who is normocardic and normotensive. The correlation between the HRBPI and VCI was very poor and not statistically significant [Figure 7].
Figure 7: Relationship between heart rate-blood pressure index and venous collapsibility index measurements of patients at a tertiary care medical center. The heart rate-blood pressure index is the difference between heart rate and mean arterial blood pressure. It is used to quantify hemodynamic dysfunction

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Central venous pressure

The correlation between CVP and VCI was weak but relatively stronger than any other correlations above. The two variables were inversely proportional with R = −0.395 (P< 0.01). [Figure 8] demonstrates this relationship.
Figure 8: Relationship between central venous pressure and venous collapsibility index measurements in this study (R = −0.395, P< 0.01, n = 256 data points)

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Systemic (abdominal) perfusion pressure

There was a significant but weak relationship between VCI and the abdominal perfusion pressure (APP) (R = 0.230, P < 0.01). The relationship between VCI and APP is depicted in [Figure 9].
Figure 9: Graphical depiction of the relationship between abdominal perfusion pressure and venous collapsibility in the study group (R = 0.230, P< 0.01, n = 256 measurements)

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Positive end-expiratory pressure

There was a weak but significant relationship between the level of PEEP and the venous collapsibility (R = −0.25, P < 0.01). Details of the correlation are shown in [Figure 10].
Figure 10: Relationship between positive end-expiratory pressure and venous collapsibility index in the current study (R = 0–0.250, P< 0.01, n = 256 data points)

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Head-of-bed elevation

The correlation between VCI and HOB elevation was very weak and not statistically significant (R = 0.010, P = 0.94). [Figure 11] depicts this relationship.
Figure 11: Relationship between head-of-bed elevation and venous collapsibility index in the study group (R = 0.010, P = 0.94, n = 256 measurement pairs)

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Range-based venous collapsibility index relationships

An examination of relationships between each of the above variables and previously published, clinically-relevant VCI ranges (0–24, 25–49, 50–74, 75+) is shown in [Table 1]. Among the variables examined, statistically significant relationships were found in CVP, DBP, and systemic (abdominal) perfusion pressures (all, P < 0.05).
Table 1: Relationship between venous collapsibility index ranges (0-24, 25-49, 50-74, 75+) and selected hemodynamic parameters

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Analyses of clinically discrepant venous collapsibility index-central venous pressure ranges

To better define the utility of vital signs as a tie-breaker variable in situ ations where VCI-CVP measurements are discrepant, we performed an analysis of vital signs in two such specific scenarios. In the first scenario, the combination of high CVP (i.e., >13) and high VCI (i.e., >50%) results in a potentially contradictory hemodynamic assessment. In this scenario, no difference in HR or MAP has been observed (both, P > 0.05). However, the SBP (139 mmHg vs. 104 mmHg) and DBP (85 mmHg vs. 61 mmHg) are both statistically higher for the lower VCI group (i.e., <50%). In the second scenario, low CVP (i.e., <7) is superimposed on a low VCI (i.e., <50%). In this case, no statistically significant differences in HR, SBP, DBP, or MAP have been noted (all, P > 0.05).


  Discussion Top


Hemodynamic monitoring of the critically ill and injured patients continues to pose a significant challenge. As our understanding of the complex hemodynamic relationships involving intravascular volume, pressure, and blood flow evolve, the understanding of hemodynamic assessment methods and their benefits and limitations becomes increasingly important. This is especially important when one considers the rapidly expanding array of hemodynamic devices and methods available to the modern practitioner.[9],[18],[19],[20] The correlation between CVP and VCI, previously demonstrated in a number of independent patient samples,[5],[14] was confirmed in the current analysis. Not surprisingly, venous collapsibility showed the strongest correlation to VCI when compared to the other variables under study.

Our data demonstrate that there is also weak, but significant relationship between PEEP and VCI. Likewise, the increased intrathoracic pressure that results from elevations in PEEP reduces left ventricular stroke volume, causing the expected inverse relationship between PEEP and VCI.[7],[21] Consequently, the clinical applicability of both CVP and VCI may be limited in patients requiring levels of PEEP >10 and appropriate corrections in interpretations of CVP and VCI should be considered.[7]

Traditionally, IVC sonographic findings and vital signs have been observed to have a poor correlation.[5],[14],[22] As significant changes in blood pressure do not occur until the late stages of shock, it is not surprising that the VCI did not have a significant correlation with either MAP or SBP in this analysis. It is interesting to note that DBP seems to correlate better with VCI than the other traditional “vital signs.” Conversely, it is surprising that HR, the initial compensatory response to hypovolemia, exhibited a very poor correlation to VCI. Therefore, during the early shock stage, VCI may be a more reliable marker of “low volume state” than blood pressure or HR.

It is important to note that systemic perfusion pressure showed a direct relationship with VCI in our analysis. The idea that significant elevations in intravascular volume could impede organ perfusion due to “flow stasis” has previously been demonstrated and outlined.[23],[24] The physiology involved here has significant implications in the setting of intra-abdominal hypertension and abdominal compartment syndrome and may be valuable as an early diagnostic indicator.[24] A similar principle may also be applicable with respect to the behavior of cerebral perfusion pressure in relation to intrathoracic and intra-abdominal pressures as well as the CVP.[25],[26],[27]

Finally, in situ ations, where the VCI and CVP do not exhibit an otherwise expected correlation, VCI was noted to have a better correlation both SBP and DBP when elevated (i.e., >50% collapsibility), but not when reduced (<50% collapsibility). As discussed earlier, this continues to highlight the shortcomings of vital signs in assessing early compensated hypovolemia.

Limitations of this study include a relatively small sample of paired hemodynamic measurements, the fact that repeated measurements were not controlled for a number of patient-related factors (i.e., HOB elevation, PEEP level) and the post hoc character of the current analysis. Strengths of the current project include its comprehensive character, high quality of the clinical hemodynamic data collected, and the prospective character of data acquisition.


  Conclusion Top


Sonologic assessment of intravascular volume status allows the bedside practitioner to directly visualize the anatomic and physiologic interrelationships associated with hemodynamic interventions. The current study corroborates the contention that vital signs correlate poorly with markers of “centrally measured” intravascular volume status such as VCI and CVP. Further studies need to be done to further refine our understanding of the above findings and their applicability to various clinical scenarios.

Acknowledgement

Justifications for re-publishing this scholarly content include: (a) The phasing out of the original publication after a formal merger of OPUS 12 Scientist with the International Journal of Academic Medicine and (b) Wider dissemination of the research outcome(s) and the associated scientific knowledge.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Carr BG, Dean AJ, Everett WW, Ku BS, Mark DG, Okusanya O, et al. Intensivist bedside ultrasound (INBU) for volume assessment in the intensive care unit: A pilot study. J Trauma 2007;63:495-500.  Back to cited text no. 1
    
2.
Birkhahn RH, Gaeta TJ, Van Deusen SK, Tloczkowski J. The ability of traditional vital signs and shock index to identify ruptured ectopic pregnancy. Am J Obstet Gynecol 2003;189:1293-6.  Back to cited text no. 2
    
3.
Batchinsky AI, Salinas J, Jones JA, Necsoiu C, Cancio LC. Predicting the need to perform life-saving interventions in trauma patients by using new vital signs and artificial neural networks. In: Artificial Intelligence in Medicine. Berlin Heidelberg: Springer; 2009. p. 390-4.  Back to cited text no. 3
    
4.
Martin JT, Alkhoury F, O'Connor JA, Kyriakides TC, Bonadies JA. 'Normal' vital signs belie occult hypoperfusion in geriatric trauma patients. Am Surg 2010;76:65-9.  Back to cited text no. 4
    
5.
Dries DJ, Waxman K. Adequate resuscitation of burn patients may not be measured by urine output and vital signs. Crit Care Med 1991;19:327-9.  Back to cited text no. 5
    
6.
Stawicki SP, Braslow BM, Panebianco NL, Kirkpatrick JN, Gracias VH, Hayden GE, et al. Intensivist use of hand-carried ultrasonography to measure IVC collapsibility in estimating intravascular volume status: Correlations with CVP. J Am Coll Surg 2009;209:55-61.  Back to cited text no. 6
    
7.
Kent A, Bahner DP, Boulger CT, Eiferman DS, Adkins EJ, Evans DC, et al. Sonographic evaluation of intravascular volume status in the surgical intensive care unit: A prospective comparison of subclavian vein and inferior vena cava collapsibility index. J Surg Res 2013;184:561-6.  Back to cited text no. 7
    
8.
Stawicki SP, Adkins EJ, Eiferman DS, Evans DC, Ali NA, Njoku C, et al. Prospective evaluation of intravascular volume status in critically ill patients: Does inferior vena cava collapsibility correlate with central venous pressure? J Trauma Acute Care Surg 2014;76:956-63.  Back to cited text no. 8
    
9.
Evans DC, Doraiswamy VA, Prosciak MP, Silviera M, Seamon MJ, Rodriguez Funes V, et al. Complications associated with pulmonary artery catheters: A comprehensive clinical review. Scand J Surg 2009;98:199-208.  Back to cited text no. 9
    
10.
Stawicki PS, Braslow B, Gracias VH. Exploring measurement biases associated with esophageal Doppler monitoring in critically ill patients in intensive care unit. Ann Thorac Med 2007;2:148-53.  Back to cited text no. 10
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11.
Cipolla J, Stawicki S, Spatz D. Hemodynamic monitoring of organ donors: A novel use of the esophageal echo-Doppler probe. Am Surg 2006;72:500-4.  Back to cited text no. 11
    
12.
Stawicki SP, Hoff WS, Cipolla J, Hoey BA. Esophageal Doppler monitoring during organ donor resuscitation: New benefits of existing technology. Prog Transplant 2006;16:10.  Back to cited text no. 12
    
13.
Stawicki SP, Hoff WS, Cipolla J, deQuevedo R. Use of non-invasive esophageal echo-Doppler system in the ICU: A practical experience. J Trauma 2005;59:506-7.  Back to cited text no. 13
    
14.
Eiferman DS, Davido HT, Howard JM, Gerckens J, Evans DC, Cook CH, et al. Two methods of hemodynamic and volume status assessment in critically Ill patients: A study of disagreement. J Intensive Care Med 2016;31:113-7.  Back to cited text no. 14
    
15.
Stawicki SP, Bahner DP. Evidence tables: Inferior vena cava collapsibility index (IVCCI). OPUS 12 Scientist 2012;6:3-5.  Back to cited text no. 15
    
16.
Stawicki SP, Seamon MJ, Meredith DM, Chovanes J, Paszczuk A, Kim PK, et al. Transthoracic echocardiography for suspected pulmonary embolism in the intensive care unit: Unjustly underused or rightfully ignored? J Clin Ultrasound 2008;36:291-302.  Back to cited text no. 16
    
17.
Stawicki SP, Seamon MJ, Kim PK, Meredith DM, Chovanes J, Schwab CW, et al. Transthoracic echocardiography for pulmonary embolism in the ICU: Finding the “right” findings. J Am Coll Surg 2008;206:42-7.  Back to cited text no. 17
    
18.
Stawicki SP, Panebianco NL, Kirkpatrick J, Gracias VH, Hayden G, Dean AJ. Intensivist use of hand-carried ultrasound to measure E/e' and IVC collapsibility in estimating volume status: Correlations with pulmonary artery and central venous pressures. South Med J 2008;101:861.  Back to cited text no. 18
    
19.
Fischer MO, Pelissier A, Bohadana D, Gérard JL, Hanouz JL, Fellahi JL. Prediction of responsiveness to an intravenous fluid challenge in patients after cardiac surgery with cardiopulmonary bypass: A comparison between arterial pulse pressure variation and digital plethysmographic variability index. J Cardiothorac Vasc Anesth 2013;27:1087-93.  Back to cited text no. 19
    
20.
Critoph CH, Patel V, Mist B, Thomas MD, Elliott PM. Non-invasive assessment of cardiac output at rest and during exercise by finger plethysmography. Clin Physiol Funct Imaging 2013;33:338-43.  Back to cited text no. 20
    
21.
Porter JM, Swain ID. Measurement of cardiac output by electrical impedance plethysmography. J Biomed Eng 1987;9:222-31.  Back to cited text no. 21
    
22.
Luecke T, Pelosi P. Clinical review: Positive end-expiratory pressure and cardiac output. Crit Care 2005;9:607-21.  Back to cited text no. 22
    
23.
Stawicki SP, Howard JM, Pryor JP, Bahner DP, Whitmill ML, Dean AJ. Portable ultrasonography in mass casualty incidents: The CAVEAT examination. World J Orthop 2010;1:10-9.  Back to cited text no. 23
    
24.
Guazzi M, Gatto P, Giusti G, Pizzamiglio F, Previtali I, Vignati C, et al. Pathophysiology of cardiorenal syndrome in decompensated heart failure: Role of lung-right heart-kidney interaction. Int J Cardiol 2013;169:379-84.  Back to cited text no. 24
    
25.
Stawicki SP, Prosciak MP. The pulmonary artery catheter in 2008 – A (finally) maturing modality? OPUS 12 Scientist 2008;2:5-9.  Back to cited text no. 25
    
26.
Bloomfield GL, Ridings PC, Blocher CR, Marmarou A, Sugerman HJ. A proposed relationship between increased intra-abdominal, intrathoracic, and intracranial pressure. Crit Care Med 1997;25:496-503.  Back to cited text no. 26
    
27.
Bloomfield GL, Dalton JM, Sugerman HJ, Ridings PC, DeMaria EJ, Bullock R. Treatment of increasing intracranial pressure secondary to the acute abdominal compartment syndrome in a patient with combined abdominal and head trauma. J Trauma 1995;39:1168-70.  Back to cited text no. 27
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11]
 
 
    Tables

  [Table 1]


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[Pubmed] | [DOI]



 

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