REVIEW ARTICLE

Clinical studies on intra-abdominal hypertension and abdominal compartment syndrome Jasper J. Atema, MD, Jesse M. van Buijtenen, MD, Bas Lamme, MD, PhD, and Marja A. Boermeester, MD, PhD, Amsterdam, The Netherlands

A

n elevation in intra-abdominal pressure (IAP) may result in intra-abdominal hypertension (IAH) or even abdominal compartment syndrome and occurs in a wide variety of critically ill patients.1 Although recent international consensus definitions and recommendations have helped to define, characterize, and raise awareness of abdominal compartment syndrome, multiple aspects of the diagnosis and treatment remain a subject of discussion.2,3 The association between IAP and organ function was described as early as 1876 when the German Wendt4 reported the association between a high IAP and oliguria. Thereafter, several reports on the effect of increased IAP on different organ systems were made.5,6 It was only until 1984 that Kron et al.7 measured the IAP as a criterion for abdominal decompression. This group was also the first to use the term abdominal compartment syndrome (ACS). Thereafter, the number of publications related to IAH, IAP, and ACS seem to have increased exponentially. This study aimed to analyze the increasing number of publications on the ACS in number, origin, and type of the study and to categorize and discuss the topics and findings of the main clinical studies.

PATIENTS AND METHODS Search For the period 1947 to April 2012, PubMed was searched using the three terms abdominal compartment syndrome, intraabdominal hypertension, and intra-abdominal pressure. All study abstracts were searched for appropriateness of the search term(s) and had to contain at least one of the three search terms. When the abstract was inconclusive or missing, the complete article was retrieved. Two authors independently performed the search and discrepancies were solved by group discussion. No language limits were applied. In addition to the PubMed search, we incorporated missing articles from the online World Society of the Abdominal Compartment Syndrome (WSACS) database.8

Submitted: April 29, 2013, Revised: July 22, 2013, Accepted: July 23, 2013. From the Department of Surgery (J.J.A., M.A.B.), Academic Medical Center; Department of Surgery (J.M.V.B.), VU University Medical Center; and Department of Surgery (B.L.), Albert Schweitzer Hospital, Dordrecht, the Netherlands. Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal’s Web site (www.jtrauma.com). Address for reprints: Marja A. Boermeester, MD, PhD, Department of Surgery (G4132.1), Academic Medical Center, PB 22660, 10100 DD Amsterdam, the Netherlands; email: [email protected]. DOI: 10.1097/TA.0b013e3182a85f59

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Articles retrieved using the previously mentioned search terms related to compartment syndromes of extremities were excluded.

Definitions For this study, the definitions are used as put forward at the 2007 World Congress of the Abdominal Compartment Syndrome (WCACS) consensus meeting.2,3 Intra-abdominal pressure was defined as the pressure within the abdominal cavity, expressed in milliliters of mercury and measured at end expiration in the complete supine position. Normal IAP is approximately 5 mm Hg to 7 mm Hg in critically ill adults. IAH was defined as a sustained or repeated pathologic elevation in IAP of 12 mm Hg or greater measured in a standardized manner at three occasions separated by 4-hour to 6-hour interval. The ACS was defined as IAP greater than 20 mm Hg (with or without abdominal perfusion pressure of G50 mm Hg; calculated as mean arterial pressure minus IAP) measured in a standardized manner at three occasions separated by 1-hour to 6-hour interval. This must coincide with single- or multiple-organ failure that was not previously present as measured by the Sequential Organ Failure Assessment (SOFA) score.9

Data Collection and Analysis Data concerning the articles’ first author, country and continent of origin, journal name, year of publication, language, and type of publication were collected. In case of multiple contributing nationalities or international studies, the country of origin of the study’s first author was decisive. Furthermore, 5-year impact factors (as defined by Journal Citation Reports [JCR] in 2012) of the journals were added to the database.10,11 The estimated population numbers of the various countries and continents have been retrieved using the GeoHive Global Statistics online database.12 The articles were categorized into four types of publications, according to the type of the study the article described; clinical, animal, in vitro (including cadaver studies), or other. The clinical studies were subdivided into four groups according to study design; randomized controlled trials, cohort studies, casecontrol studies, and case reports and series (as defined by the Centre for Evidence-Based Medicine).13 Data analysis was performed using IBM SPSS version 19.0 (IBM Corp., Armonk, NY).

RESULTS On April 30, 2012, the latest update of the PubMed search was performed. We screened a total of 5,245 abstracts. A search using the term abdominal compartment syndrome resulted in J Trauma Acute Care Surg Volume 76, Number 1

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Atema et al.

Figure 1. The number of annually published articles on ACS, IAH, and IAP in the last 65 years (n = 1,211).

1,354 articles, whereas intra abdominal hypertension resulted in 949, and intra abdominal pressure resulted in 2,942 articles. Besides these PubMed results, we incorporated 487 articles from the online WSACS literature database.8 After eliminating overlap and articles not fulfilling inclusion criteria, 1,211 individual articles were included in the present review. Of these included articles, 87.4% were published in English. The number of yearly published articles in the last six decades has increased exponentially, as shown in Figure 1. TABLE 1. Total Number of Publications on IAP, IAH, and ACS per Country, and Number of Publications per Country Corrected for Number of Inhabitants (n = 1,211)

Country United States Germany Belgium United Kingdom China Italy Turkey Australia Canada France Greece Spain Israel Japan Sweden Switzerland Russia The Netherlands Finland Brazil

Publications (Percentage of Total) 431 74 72 56 52 50 49 40 31 31 25 24 23 22 21 16 15 14 13 12

(35.6) (6.1) (5.9) (4.6) (4.2) (4.1) (4.0) (3.3) (2.6) (2.6) (2.1) (2.0) (1.9) (1.8) (1.7) (1.3) (1.2) (1.2) (1.1) (1.0)

Per 106 Inhabitants (Ranking) 1.36 0.90 6.67 0.89 0.04 0.82 0.66 1.75 0.89 0.49 2.19 0.51 2.99 0.17 2.21 2.07 0.11 0.84 2.41 0.06

(8) (9) (1) (11) (20) (13) (14) (7) (10) (16) (5) (15) (2) (17) (4) (6) (18) (12) (3) (19)

Of the included articles, 39.8% were retrieved using the search term abdominal compartment syndrome alone, whereas the single search term intra abdominal hypertension accounted for 0.9%, and intra abdominal pressure accounted for 17.8%. In 9.9%, both terms, abdominal compartment syndrome and intra abdominal pressure were found. In 21.7%, the combination of all three search terms was found.

Categorizing All Publications by Country, Journal, Study Type, and Patient/Disease Category The 20 countries listed in Table 1 account for 88.4% of all included articles. When corrected for the number of inhabitants, Belgium was leading with 6.67 publications per 106 inhabitants, followed by Israel (2.99) and Finland (2.41). The United States contributed the largest absolute number of articles (n = 431), accounting for 35.6% of the articles, followed by Germany (n = 74, 6.1%) and Belgium (n = 72, 5.9%). Table 2 shows the number of publications per continent. Europe tops the list (n = 471, 38.9%), followed by North America (n = 462, 38.2%) and Asia (n = 204, 16.8%). The top 10 journals publishing on ACS, IAH and IAP are shown in Table 3. The Journal of Trauma published most articles (n = 99, 8.2%) followed by Critical Care Medicine (n = 53, 4.4%), the American Surgeon (n= 51, 4.2%) and TABLE 2. Number of Publications on IAP, IAH and ACS Per Continent (n = 1,211) Continent Europe North America Asia Oceania South America Africa

n

Percentage

471 462 204 41 25 8

38.9 38.2 16.8 3.4 2.1 0.7

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TABLE 3. Top 10 Journals Regarding Number of Publications on IAP, IAH, and ACS Journal J Trauma Acute Care Surg* Crit Care Med Intensive Care Med Am Surg Acta Clin Belg World J Surg Am J Surg Crit Care Arch Surg J Surg Res

n (%)

JCR 5-Year Impact Factor 201211

99 (8.2) 53 (4.4) 51 (4.2) 51 (4.2) 34 (2.8) 22 (1.8) 21 (1.7) 20 (1.7) 18 (1.5) 18 (1.5)

2.942 6.401 5.036 1.165 0.724 2.751 2.727 5.248 4.750 2.123

TABLE 4. Articles on IAP, IAH, and ACS Subdivided Into Type of Study (n = 1,211)

236

N

Percentage

16 281 10 294 3

2.6 46.5 1.7 48.7 0.5

*Categorized references (case reports and case series excluded) in Appendix 1 (Supplemental Digital Content 1, http://links.lww.com/TA/A326).

Intensive Care Medicine (n= 51, 4.2%).. A supplement of the Acta Clinica Belgica in 2007 was a special edition in honorary of the third World Congress on Abdominal Compartment and accounted for 28 articles (2.3%). The American Surgeon published a supplement in 2011 on the occasion of the fifth World Congress, containing 15 articles on IAH and ACS (1.2%). The top 10 journals together published 38.9% of the included articles. The median 5-year impact factor calculated from this top 10 is 2.846 (range, 0.724Y6.401), and the highest impact factor is 6.401 by Critical Care Medicine. From all 1,211 articles, the journal’s 5-year impact factors of 947 articles (78.2%) were collected from the JCR database, and the median impact factor was 1.946 (range, 0.238Y36.427). Considering the top 20 contributing first authors, 11 are member of the 2012 WSACS Executive Committee, and 8 authors contributed to the WCACS consensus publications.2,3 The type of publication is reflected in Table 4. The majority of studies consisted of clinical studies (n = 604, 49.9%), and 14.9% were animal studies. Only 12 studies (1.0%) seemed to be in vitro studies. Seven articles could not be allocated to any of the groups because of language problems or the inability to retrieve the full article. The other 407 publications consisted of 277 reviews, of which 28 (10.1%) were considered systematic, 103 commentaries, 13 surveys, 10 technical reports, 3 consensus definitions and recommendations, and 1 trial protocol proposal. Table 5 shows the included clinical studies (n = 604) grouped according to the type of study design. The majority were case reports and case series (n = 294, 48.7%). Excluding case reports and case series, we found 307 clinical studies on the topic (references categorized by type of study in Appendix 1 Supplemental

Clinical study Animal study In vitro study Other (mostly reviews) Unknown

Type of Study Design Randomized controlled trial Cohort study Case-control study Case reports and case series Unknown

*Previously titled The Journal of Trauma and The Journal of Trauma, Injury, Infection, and Critical Care.

Type of Publication

TABLE 5. Frequency of Types of Clinical Studies on IAP, IAH and ACS (n = 604)*

n

Percentage

604 181 12 407 7

49.9 14.9 1.0 33.6 0.6

Digital Content 1, http://links.lww.com/TA/A326). A total of 281 (46.5%) were identified as cohort studies, of which 180 (64.1%) were prospective. In three articles, the type of study design could not be determined because of language problems.

Topics and Main Findings of the Clinical Studies The main topics of the clinical studies, case reports, and case series excluded are discussed later in light of knowledge gained on ACS as well as the proportion of studies on subtopics of ACS and management (n = 307). Key to IAH and the ACS is the measurement of IAP. Of the 307 clinical studies, 53 (17.3%) have reported on different aspects and techniques of IAP measurements, for example, the effect of body positioning or instillation volume on pressure measurements (Table 6; references categorized by subtopic in Appendix 3, Supplemental Digital Content 3, http://links.lww.com/TA/A328).14,15 The standardized method for determining IAP was described by Malbrain et al.3 in 2006 and is performed at end expiration in the supine position with a maximal instillation volume of 25-mL sterile saline and the transducer zeroed at the level of the midaxillary line. Normal IAP ranges from 5 mm Hg to 7 mm Hg in critically ill adults, but various conditions such as obesity have been TABLE 6. Clinical Studies (Case Reports and Case Series Excluded) on IAP, IAH, and ACS Subdivided Based on Disease or Patient Category and Subtopic (n = 307)* Patient Category

n

Percentage

Medical/surgical ICU patients Trauma Open abdomen (for various indications) Severe acute pancreatitis Paediatric Abdominal aorta aneurysm Burn Miscellaneous Subtopic Intra-abdominal pressure measurement Incidence, prevalence, and risk factors Clinical outcomes Prevention and treatment Miscellaneous

57 44 34 32 18 16 14 92 N 53 48 82 89 35

18.6 14.3 11.1 10.4 5.9 5.2 4.6 30.0 17.3 15.6 26.7 29.0 11.4

*Categorized references in Appendices 2 (Supplemental Digital Content 2, http:// links.lww.com/TA/A327) and 3 (Supplemental Digital Content 3, http://links.lww.com/ TA/A328).

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associated with a chronic increase of IAP.3,16 Pressure levels in children are reported to be lower.17 There is no consensus in which patients and when IAP should be measured. While IAH and ACS were originally considered to be a disease of the traumatically injured patients, IAH and ACS have now been recognized to occur in all critically ill patient populations. Table 6 gives an overview of the 307 clinical studies categorized by disease or patient category (categorized references in Appendix 2 Supplemental Digital Content 2, http:// links.lww.com/TA/A327). Given the multiple underlying pathologies, ACS can be classified in three types.3 Primary ACS is caused by the presence of an intra-abdominal or retroperitoneal pathology or process, such as an abdominal trauma,18 a strangulated hernia19 or elective abdominal surgery,20 whereas secondary ACS develops in the absence of primary abdominal pathology, usually seen in the postresuscitation phase for septic or hemorrhagic shock or burn injuries.21,22 Tertiary or recurrent ACS develops after the surgical or medical treatment of either primary or secondary ACS.23 Most clinical studies on IAP, IAH, and ACS have included an unselected and mixed (medical and surgical) intensive care unit (ICU) population (Table 6, 57 studies; 18.6%). Prevalence rates of IAH on ICU admission vary from 20% to 30%, and incidence rates vary from 30% to 55%.24Y29 Several risk factors for the development of ACS in critically ill adult patients have been described, namely, massive fluid resuscitation,24,30,31 multiple transfusions,32 hypothermia,30 acidosis,30 body mass index,25,33 sepsis,33 mechanical ventilation,26 abdominal trauma,34 and abdominal surgery.24 Forty-eight clinical articles (15.6%) studied the incidence or prevalence rates and risk factors for ACS (categorized references in Appendix 3, Supplemental Digital Content 3, http://links.lww.com/TA/A328). Mortality rates of 50% have been described in critically ill adult and pediatric patients, and early recognition and treatment have proven to reduce mortality.30,35 Several subpopulations are associated with a higher incidence rate of IAH/ACS compared with the general critically ill patients. Patients with severe acute pancreatitis (SAP) were included in 10.4% of the clinical studies (Table 6; all references in Appendix 2, Supplemental Digital Content 2, http://links.lww.com/ TA/A327). IAH has a reported incidence of approximately 60%; ACS is reported to develop in 12% to 56%36Y38 Several risk factors for the development of IAH in patients with SAP have been identified, and IAH is associated with an increased morbidity and mortality.38,39 Nonsurgical interventions, such as percutaneous drainage of intraperitoneal fluid40 and continuous hemodiafiltration,41 have been suggested to decrease IAP in patients with acute pancreatitis. Furthermore, a conservative protocol-based approach of patients with SAP, including monitoring of the IAP, has proven to be a rational and effective treatment strategy.42 Surgical decompression seems the most effective way to decrease IAP in patients with acute pancreatitis.43 Burn patients are another subpopulation frequently associated with IAH, although only 1% of all burn patients develop IAH (all references in Appendix 2, Supplemental Digital Content 2, http://links.lww.com/TA/A327).44,45 Incidence is positively correlated with burn size. Rates of IAH of 36% and ACS of 17% have been reported in patients with burn areas of greater than 40% and greater than 30% of total body surface area, respectively.45Y47

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Despite various treatment strategies, including lower fluid resuscitation volumes,48 escharotomy,49 and burn resuscitation protocols,50 mortality rates in burn patients with ACS remain high.44,51 Abdominal compartment syndrome is also a frequently recognized complication following open and endovascular repair of ruptured abdominal aortic aneurysms.52,53 The open abdomen, both as prophylaxis or after decompressive laparotomy, has been described in patients after undergoing ruptured abdominal aortic aneurysms repair (Table 6; Appendix 2, Supplemental Digital Content 2, http://links.lww.com/TA/A327).54,55 With the increase of IAP and the development of IAH, several organ systems are affected. Impaired cardiovascular, respiratory, renal, gastrointestinal, hepatic, and neurologic functioning has been described in IAH/ACS.56Y58 The influence of elevated IAP and ACS on different clinical outcomes, for example, specific organ dysfunction, morbidity or mortality, was the subject of 82 articles (26.7%; references categorized by subtopic of ACS in Appendix 3, Supplemental Digital Content 3, http:// links.lww.com/TA/A328). Regarding the clinical studies, the most frequent subject was the prevention or treatment of ACS (89 studies, 29.0%; references in Appendix 3, Supplemental Digital Content 3, http:// links.lww.com/TA/A328). Several nonoperative strategies to reduce IAP have been described such as sedation,59 percutaneous drainage of free intraperitoneal fluid or blood,40,60 adequate fluid resuscitation,48,61 continuous hemofiltration,41 and negative extraabdominal pressure.62 Surgical decompression by laparotomy remains the only definitive treatment of ACS and can successfully reduce IAP.43,63 With the increased interest and awareness of IAH/ACS, the open abdomen has become an accepted treatment strategy. It has been described both as prophylaxis and as treatment of ACS. Furthermore, several different methods for temporary abdominal closure have been studied.64Y67 Thirty-four studies included patients with an open abdomen for various indications, including ACS. The characteristics and main findings of the 16 randomized controlled trials are listed in Table 7. Seven studied the effect of different IAP levels during laparoscopic cholecystectomy on various parameters and postoperative outcomes. Five studies evaluated the effect of resuscitation protocols, traditional Chinese medicine, or indwelling catheter drainage on IAP in SAP patients. Two trials included patients undergoing emergency laparotomy and studied temporary abdominal closure techniques and suture techniques. One trial studied the effect of traditional Chinese medicine on IAP in ICU patients with multiorgan failure, and one trial evaluated the effect of type of resuscitation fluid on IAP in burn patients.

DISCUSSION This study presents a descriptive review of publications on IAH, IAP, and ACS during the last 65 years. Since its first description, the number of publications has grown exponentially in the last six decades, suggesting increased interest and awareness. Most articles consist of low-level evidence (especially case reports and expert opinions). To date, many questions concerning ACS have not been answered yet. However, considering the exponential rise in number of published articles, knowledge is

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237

238

2009

2009

2010

2010

Mao et al.74

Yang et al.**75

Celik et al.76

Chen et al.**77

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0

6

1

NA

2

NA

0

6

3

15

Patients undergoing elective laparoscopic cholecystectomy Patients undergoing elective laparoscopic cholecystectomy

Study Population

Turkey

China

India

China

Turkey

China

China

India

Turkey

Patients undergoing elective laparoscopic cholecystectomy

Severe acute pancreatitis patients

Patients undergoing elective laparoscopic cholecystectomy ICU patients with multiorgan failure Patients undergoing emergency laparotomy

Severe acute pancreatitis patients

Severe acute pancreatitis patients

Patients undergoing elective laparoscopic cholecystectomy Patients undergoing elective laparoscopic cholecystectomy

United States Patients undergoing emergency laparotomy requiring temporary abdominal closure Turkey Patients undergoing elective laparoscopic cholecystectomy China Severe acute pancreatitis patients

United States Burn patients (Q25% TBS with inhalation injury or Q40% TBS without) China Severe acute pancreatitis patients

Turkey

Turkey

Country

60

41

190

60

60

120

76

26

52

80

45

51

110

31

22

100

No. Patients

Mesh closure

Routine conservative treatment

Crystalloid resuscitation

High IAP level (14Y15 mm Hg)

NA

Control

3 different IAP levels; 10, 13, and 16 mm Hg

Hydroxyethyl starch resuscitation

Reinforced tension line sutures

Colloid plus crystalloid resuscitation 3 different IAP levels; 8, 12 and 14 mm Hg Tongfu Granule†

Controlled fluid resuscitation

Similar effects on pulmonary function test results Lower IAP levels in intervention group

No effect of IAP levels on gastric intramucosal pH Less depression of immune function (expressed as interleukin 2 and 6) in the low IAP group Less increase in IAP and less volume requirement in plasma-resuscitated patients Lower mortality, lower APACHE II scores after 5 d and shorter hospitalization times in intervention group No signification differences in delayed fascial closure or fistula rate

Main Conclusion

NA

Ringer’s lactate resuscitation

Continuous suturing

No difference in IAP but increased incidence of fascial dehiscence in continuous suture group Lower incidence of IAH and reduced use of mechanical ventilation in intervention group No differences on thromboelastography

More pronounced effect of high IAP on QT dispersion Decrease in postoperative pain and hospital stay, and preservation of lung function in low pressure level group Rapid fluid resuscitation Lower incidence of ACS in controlled fluid resuscitation group (i.a.) Crystalloid resuscitation Decline of IAP was significant higher in crystalloid plus colloid group NA No effect of IAP level on postoperative pain Placebo Decreased IAP in intervention group

3 different IAP levels; 8, 12, NA and 15 mm Hg Da-Cheng-Qi decoction enema+ Normal saline enema and sodium sulphate orally Low IAP level (7 mm Hg) High IAP level (15 mm Hg) Low IAP level (8 mm Hg) High IAP level (12 mm Hg)

Vacuum-assisted closure

Routine conservative treatment combined with indwelling catheter drainage

Plasma resuscitation

5 different IAP levels; 8, 10, 12, 14, and 16 mm Hg Low IAP level (10 mm Hg)

Intervention

*Web of Science (accessed July 2013). **Article in Chinese (English abstract). †Traditional Chinese medicines. APACHE, Acute Physiology And Chronic Health Evaluation; i.a., among other outcomes; NA, not applicable/available; TBS, Total body surface area.

2011

2009

Joshipura et al.73

Topal et al.79

2009

Ekici et al.72

2011

2008

Zhang et al.71

Du et al.61

9

Karagulle et al.70 2008

2011

1

2008

Bee et al.67

Agarwal et al.78

59

2006

Sun et al.40

92

2005

4

3

O’Mara et al.48

2004

2004

68

No. Year Citations

Basgul et al.69

Celik et al.

Reference

TABLE 7. Characteristics of the 16 Randomized Controlled Trials on IAP, IAH, and ACS

Atema et al. J Trauma Acute Care Surg Volume 76, Number 1

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increasing. Sixteen randomized trials and 180 prospective cohort studies on various aspects of ACS have been published and are categorized and discussed in this review. The authors are aware that scoring abstract heuristics only, information about the type of article, and study design might have been erroneous. Furthermore, determining the quality of the articles’ content based on the journal’s impact factor is an oversimplification. Moreover, for 248 articles, no impact factor was available (yet) from the online JCR database. Because nonEnglish publications produced by Asian countries, which are not available in PubMed, were not included, this could have underestimated the overall number of articles and the share of the Asian continent. The exponential increase in number of published articles indicates the clinical awareness and interest in ACS. Hopefully, future research will outline a high-quality evidence-based approach to patients with increased IAP, IAH, and ACS. Studies should focus on the value of IAH monitoring in relation to patient outcome and the type and timing of interventions for ACS to improve patient survival. AUTHORSHIP J.J.A. contributed in the literature search, data collection, data analysis, data interpretation, and writing. J.M.V.B. contributed in the literature search, data collection, data analysis, data interpretation, and writing. B.L. contributed in the study design, data interpretation, and critical revision. M.A.B. contributed in the supervision, study design, data interpretation, and critical revision.

DISCLOSURE The authors declare no conflicts of interest.

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