A systematic review of the management of acute superior mesenteric vein thrombosis in adults : Journal of Pancreatology

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A systematic review of the management of acute superior mesenteric vein thrombosis in adults

Phoenix, Eimear MB BCh BAOa; Beck, Jonathan MB BCh BAO, BScb; Patterson, Timothy J. MB BCh BAO, BSca,∗; Spence, Robert A.J. MB BCh BAO, MEda; Taylor, Mark A. MB BCh BAO, PhDb; Spence, Gary M. MB BCh BAO, MDa

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Journal of Pancreatology 3(3):p 111-120, September 2020. | DOI: 10.1097/JP9.0000000000000051

Abstract

Introduction

First described in 1894, acute thrombosis of the superior mesenteric vein (SMV) is a rare (incidence: 1.8 per 100,000 person years) but potentially catastrophic condition.[1,2]

The SMV provides the venous drainage for the embryological midgut and merges with the splenic vein to form the portal vein. Thrombotic occlusion of the SMV leads to insufficient perfusion pressure secondary to increased resistance in the mesenteric venous bed. With stagnating flow, increased venous pressure results in significant edema of the bowel wall. A cascade of submucosal hemorrhage, ischemia, and eventually total infarction of the bowel may result. Consequences are determined by thrombotic location as well as the extent of the occlusion.[3]

Various risk factors for thrombotic occlusion of the SMV have been identified; obesity, intra-abdominal inflammatory conditions such as pancreatitis, appendicitis, diverticulitis, as well as both acquired and inherited thrombophilia. Importantly, SMV thrombosis can occur more commonly following certain procedures such as laparoscopic sleeve gastrectomy, pancreatitic, and splenic surgery.[4,5]

Patients with SMV thrombosis may present with typical signs of acute bowel ischemia—nausea, vomiting, diarrhea, and pain out of proportion to physical findings. However, symptoms are often less severe than those associated with acute arterial mesenteric ischemia. In a Mayo Clinic series, 9% of patients with acute SMV thrombosis had symptoms of less than 24-h duration, with the majority having experienced symptoms for over 48 h.[6] Arbitrarily if symptoms are present for >30 days, or a portal cavernoma is present on imaging, then SMV thrombosis is considered chronic.

The multinational registry referenced previously reported anti-coagulation as the mainstay of initial treatment (76.7% of patients), with thrombolysis and surgery also being reported.[7] The European society for vascular surgery (ESVS) Clinical Practice guidelines (2017) are available and these summarize and it is readily acknowledged that the evidence basis of the management of SMV thrombosis is poor.[8]

Aim

The aim of this systematic review was to critically analyze current evidence regarding management options of acute SMV thrombosis in adults. This evaluated conservative, medical, interventional, and surgical management.

Methods

The systematic review was conducted in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement.[9] A review protocol was registered with the PROSPERO systematic review database on November 28, 2018; registration number: CRD42018116825.

Eligibility criteria

To be eligible for this systematic review a study must have reported the management of SMV thrombosis in an adult (18 years and above) population. Reporting characteristics for inclusion were studies published in peer-reviewed journals to ensure methodological and reporting reliability. Case series (arbitrability >5 patients) were included. The study period was from January 1, 2000 until January 31, 2019. No studies were excluded based on language.

Information sources and search

Four databases: PubMed, Ovid EMBASE, SCOPUS, and Cochrane Library were searched. In addition to these 4 trial registries: ClinicalTrials.gov, European Clinical Trials Register, ISRCTN Register, Cochrane Clinical Trials Database, and the International Clinical Trials Registry Platform were searched.

For PubMed, the search was conducted using both MeSH terms and the advanced search option. The MeSH terms ‘mesenteric vein’ AND ‘embolism and thrombosis’ were used. In addition to this an advanced search was conducted using the terms ‘mesenteric vein’ AND ‘thrombosis’.

Ovid Embase and SCOPUS were also searched with the same terms as the PubMed advanced search terms. The Cochrane Library and trial registries were all searched using the term “mesenteric vein”. Trial registries were all searched using the term “mesenteric vein”. The literature search was performed from January 1, 2000 to December 1, 2018. This was updated on January 31, 2019.

Study selection and data collection process

Two independent reviewers, authors 1 and 2, reviewed all titles and then abstracts, placing any screened citations into a database. After this, duplicates were then eliminated and if possible using the abstracts available a decision was made on its inclusion. The full text was then assessed and disagreements between reviewers were resolved by consensus, or if necessary arbitration by a senior author. The .pdf files of the selected studies were then exported to Mendeley reference manager. Once each author had completed data extraction, the data files were electronically compared and discrepancies in data entry were investigated and resolved.

Data items and summary measures

Author, year of publication, and country of publication were recorded. Details of management used were recorded along with any technical details such as dose, duration, or site. Numbers of patients in each treatment group were also recorded. Outcome data type from individual studies was expected to be heterogenous so the authors simply had a data collection section for outcomes. Due to this expected heterogeneity, summary measures were not specified by the authors at the stage of the initial search.

Risk of bias in individual studies and across all studies

Assessment of potential bias would be assessed using the Cochrane Collaboration (for randomized controlled trials [RCTs]) and ROBINS-I (for observational studies) risk of bias tools and tabulated.[10,11] Due to lack of RCTs found during this study the Cochrane Collaboration tool was not used.

Results

Study selection

In total 16,199 studies were screened, of which 103 were assessed for eligibility. Of the 19 studies included in the review, all were retrospective observational. These search results are displayed in Figure 1.

F1
Figure 1:
A PRISMA flow diagram of study selection, resulting in 19 studies being selected for qualitative synthesis.

Study characteristics

Table 1 demonstrates the characteristics of included studies. The 19 studies comprised of 472 patients with 445 patients treated solely medically, and 148 patients undergoing surgical intervention.[1,11–29] Eleven studies reported on anti-coagulation, 1 reported on anti-coagulation in conjunction with endovascular thrombectomy, 9 reported on thrombolysis, and 10 reported on surgery. Gender, age, location, size, and follow-up characteristics are included in Table 1, individual study details are presented in online Appendix 1, https://links.lww.com/JP9/A5.

T1
Table 1:
Study characteristics of included studies, including location, study type, groups, numbers and genders of participants, mean age and follow-up.

In addition, the authors found 2 studies in trial registries which are yet to begin, ongoing, or yet to be published. These are both non-randomized, single arm studies, examining anti-coagulation using heparin (followed by warfarin) and rivaroxaban respectively.[30,31] These studies are presented in Table 2.

T2
Table 2:
Studies found in trial registries which are yet to be published, both examining systemic anti-coagulation.

Results of individual studies

Mortality data were reported by 16 of the 19 studies and postintervention morbidity by 12 studies. Studies reported baseline management received by all patients and gave details of long-term treatment. The summarized results of each study are presented in Table 3  , details of each individual study are presented in online Appendix 2, https://links.lww.com/JP9/A5. Mortality and morbidity data were, in the majority of studies, not presented as separate entities, limiting comparison, and reporting.

T3
Table 3:
Mortality, morbidity, and risk factors presented by each study.
T4
Table 3 (Continued):
Mortality, morbidity, and risk factors presented by each study.
T5
Table 3 (Continued):
Mortality, morbidity, and risk factors presented by each study.

Details of each treatment intervention, as presented in the original studies, and presumed etiology of each SMV thrombosis are given in online Appendix 3, https://links.lww.com/JP9/A5.

Risk of bias within and across studies

Risk of bias was assessed using the ROBINS-I risk of bias tool. A low risk of bias overall was found in 1 study, a moderate risk in 8 studies, a serious risk in 5 studies, with none having a critical risk. Due to access restrictions or information not being specified in the original manuscript, there were 5 studies that overall risk of bias could not be described. The domains which overall had the lowest risk of bias were due to missing data, bias in the measurement of outcomes, and bias in the selection of the reported result. We found that the domain: bias due to confounding, overall had the highest risk of bias. The risk of bias assessment is presented in Table 4.

T6
Table 4:
Risk of bias in each study as assessed using the ROBINS-I risk of bias tool.

Discussion

To date, this is the first systematic review of the management of SMV thrombosis. The results of this study demonstrate that in patients with SMV thrombosis, without signs of peritonism or perforation, then systemic anti-coagulation with heparin or local thrombolysis is a widely accepted therapeutic strategy. Yet, the evidence reported in the literature for these strategies is limited with a shortage of RCTs both past and forthcoming. In addition, the current available publications highlight continued uncertainty regarding definitive management.

In light of current evidence, optimal management is still unclear and clinical judgment is frequently a major factor in patient management. Subsequently, there is recognized difficulty in determining optimal and definitive management for patients with SMV thrombosis and further evidence is required.

Primary treatment goals for any thrombosis or embolism is recanalization, limiting its extension, and long-term prevention. If irreversible ischemia of end-organ tissue is caused then bowel resection may be required with SMV thrombosis. Anti-coagulation for treating other sites of thrombosis such as pulmonary has a large evidence base with a commonly recognized pathway for investigation, risk stratification, and treatment.[32] This relies on early anti-coagulation, with a specific marker (hemodynamic compromise) to instigate thrombolysis with surgical intervention rarely appropriate. Similarly, a well-defined structure for the treatment of cardiac and cranial thrombosis, and embolism exists.[33,34] No such pathway exists for visceral venous embolism, leading to subsequent difficulty, and widening discretion regarding appropriate management.

In the majority of studies, low molecular weight heparin was administered immediately following diagnosis, followed by long-term anti-coagulation of varying duration. Oral warfarin was used in 16 studies as long-term anti-coagulation of choice, varying between 3 months to lifelong.[1,12–23,25–29] Data reported by these studies is limited due to small population sizes. The largest study (77 patients) which examined anti-coagulation reported a 1 year pathology specific mortality of 0.9%.[20] One study utilized sub-cutaneous (SC) heparin as an extended treatment.[22] However, long-term mortality data were not reported.[22] A current trial, NCT02627053, is being conducted which is examining the safety of Rivaroxaban in SMV (and other intraabdominal) thrombosis—with the trial follow-up finishing in December 2019.[30]

Thrombolysis was reported by 9 studies with systemic, trans-hepatic, trans-jugular, trans-femoral, trans-radial, and direct intraoperative (via Fogarty catheter) routes all being reported.[14–19,24–26] The largest study (46 patients) examining thrombolysis reported on the use of transcatheter lysis via various routes.[19] At a mean of 22 months there was 2.2% pathology specific mortality.[19] Except for systemic and direction intraoperative thrombolysis, these delivery methods all require interventional radiology or vascular surgery capacity—which may not be present in all centers.

Ten studies reported surgery as a distinct or semidistinct intervention group.[1,12,13,15,21–23,26–29] In one of these, laparotomy, with subsequent resection of small bowel or colon if required, had been the primary method of both diagnosis and treatment of SMV thrombosis until computerised tomography (CT) diagnosis had allowed some patients to be managed medically.[26] This selection into treatment groups, based on the timeframe the patient attended hospital, instead of by randomization, adds a confounding bias to the interpretation of any results. For patients in the other 9 studies, the decision to proceed to laparotomy was based on peritonism, perforation, septic shock, or non-enhancing bowel visualized on CT angiogram. The mortality reported after surgery was heterogenous, ranging from 0% to 39% at 2 years. The largest study (15 patients) to specifically report on the mortality of a surgical population showed a 10% 30-day mortality.[12] Another study, which combined medically managed and surgically managed groups showed that at both 30 days and 5 years short bowel syndrome (SBS) (defined as <100 cm of small bowel remaining) was, on multivariate analysis, associated with increased mortality.[22] The authors of this study stated at 30 days, colonic involvement in the infracted segment was predictive for increased mortality.[22]

A significant complication to be considered following bowel resection is SBS. SBS is the most common cause of SMV thrombosis specific mortality, with 10 of 105 patients undergoing laparotomy and subsequent resection identified during this study developing SBS.[1,12,13,15,21–23,26–29] Given the morbidity and increased mortality associated with lifelong total parenteral nutrition, SBS is a major consequence to be considered. Survival of patients who develop SBS is dependent on the degree of adaption of remaining bowel with the support of pharmacological and nutritional therapies, with 30% 5 year mortality being reported.[35] The advent of small bowel transplantation, currently only being conducted in 4 specialist centers in the United Kingdom, does provide a treatment option for an increasing group of patients.[36]

Overall, 30-day SMV thrombosis specific mortality rates varied from 0%[21,23] to 24%[15] and was extremely heterogenous. Similarly, 1 year surgical mortality (39.0%–76.9%) and 2-year medical therapy mortality (0.7%–4.0%) displayed the same heterogeneity. With medical management having significantly less mortality, accurate identification of patients of high risk of ischemia and perforation must be undertaken, to justify surgical intervention. This can be established in the setting of peritonitis, with the aid of CT imaging. Subsequently these patients are often self-selected due to unstable clinical picture.

Similarly to thrombosis and embolism at other sites, pre-disposing factors are recognized and may change management. Thirteen of the 19 studies reported patients with either hematology pathology or a hypercoagulable state.[1,12–15,18,19,21,24–27,29] In addition to these recent surgery and know intra-abdominal malignancy were also reported by 9 and 5 studies respectively.[1,12–15,21,24–27,29] Data regarding etiology were provided heterogeneously so the authors of this study were unable to link etiological and outcome data. In addition to this, data regarding size of thrombosis and area of the vascular tree affected was not provided so the authors are unable to comment on outcomes related to these factors.

Although these may not affect initial management, secondary prevention will be affected. In the pregnant patient, a multidisciplinary team approach must be used in conjunction with obstetrics due to poor fetal outcomes associated with SMV thrombosis.[37] To date there have been 15 reported cases in the literature, summarized in a 2018 review.[37] Four were idiopathic and 11 had precipitating factors. These resulted in 8 fetal deaths and 1 maternal death.[37] These were all treated with parenteral low-molecular weight heparin initially, with surgery being employed if there were signs of perforation or peritonism.

Limitations

The authors of this review recognize that these data, other than giving a brief overview of current practice worldwide, does not assist the evidenced-based practitioner. This same lack of evidence is acknowledged in British Journal of Haematology guidelines for the investigation and management of venous thrombo-embolism at unusual sites. It recommends that in the case of SMV thrombosis, surgery should be reserved for peritonitic patients; otherwise anti-coagulation should be the treatment of choice. In addition, the guidelines recommends long-term anti-coagulation for those found to have thrombophilia, but admits this is not based on evidence.[38]

There is both a lack of RCTs within the current published literature and upcoming trials. None of the observational studies were from prospectively collected databases. The bias assessment conducted by the authors demonstrated that bias due to risk of confounding factors was the greatest overall risk. The confounding factor was, for many studies, these patients’ clinical state on presentation—with sicker patients self-selecting into interventional or surgical groups.

Although the authors acknowledge that the diagnostic lag associated with SMV thrombosis would be a factor limiting the feasibility of RCTs—there is scope for RCTs comparing anti-coagulation regimens. These must employ an intention to treat analysis, allowing for change in a patients clinical condition. This would enable the investigator to maintain control of confounding factors and conduct an intention to treat analysis which would reduce bias.

As highlighted above, national guidelines are lacking in the United Kingdom. The ESVS 2017 guidelines on the management of the diseases of mesenteric arteries and veins described 11 recommendations for the management of mesenteric vein thrombosis.[8] They recommended that patients with mesenteric vein thrombosis should be investigated for other comorbidities including abdominal malignancy and thrombophilia. They illustrate a diagnostic and management algorithm with recommendations in the radiology literature and includes both surgical and medical management.[39] They recommend joint CT imaging (both arterial and portal phases) and diagnostic work-up for malignancy, and distinguish between acute and chronic mesenteric vein ischemia. Anti-coagulation with heparin is recommended globally for patients with acute ischemia—citing evidence which analyzed both mesenteric and portal vein thrombosis patients. In addition, angiography is recommended if a patient clinically deteriorates—preceding endovascular or surgical intervention. Similarly to UK pulmonary embolism guidelines, they recommend that SMV thrombosis judged to be from a reversible cause be anti-coagulated for between 3 and 6 months, with lifelong anti-coagulation for patients with recurrent thrombosis or proven thrombophilia.[32]

The authors propose the most appropriate response to this would be the instigation of a regional database reporting current investigation and treatment strategies and follow up arrangement. Using the results of this a prospective national database, RCT planning and guideline commissioning could be best actioned.

An alternative strategy for improving outcomes may involve increasing clinician awareness or investigation strategies. Data not presented by any of the reported studies was time from presentation to diagnosis or instigation of treatment—we do acknowledge that CT imaging has become ubiquitous and was used as a diagnostic tool in all of the included studies.

Conclusion

Acute superior mesenteric venous thrombosis is an important but rare cause of intestinal ischemia. The limited available evidence presented in this review shows that anti-coagulation appears to have an acceptable efficacy and safety profile with convention to commence this early after diagnosis. Surgical intervention is now reserved for the peritonitic or perforated patient.

The systematic review has highlighted the limited evidence base for the management of SMV thrombosis. There is a requirement for further studies in this area to form firm evidence-based conclusions.

Acknowledgments

The systematic review was conducted in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement.[9] A review protocol was registered with the PROSPERO systematic review database on November 28, 2018; registration number: CRD42018116825.

Author contributions

None.

Financial support

The study received nil funding.

Conflicts of interest

The authors declare no conflicts of interest.

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Keywords:

Acute mesenteric ischemia; Mesenteric vein; Thrombus

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