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Pediatric Radiology

https://doi.org/10.1007/s00247-018-4284-8

ORIGINAL ARTICLE

MR angiography and 2-D phase-contrast imaging for evaluation


of meso-rex bypass function
Heather A. Stefek 1,2 & Cynthia K. Rigsby 2,3 & Haben Berhane 2 & Andrada R. Popescu 2 & Shankar Rajeswaran 2 &
Riccardo A. Superina 4,5

Received: 30 June 2018 / Revised: 3 September 2018 / Accepted: 5 October 2018


# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Background The meso-Rex bypass restores blood flow to the liver in patients with extrahepatic portal vein thrombosis. Stenosis
occurs in some cases, causing the reappearance of portal hypertension. Complications such as thrombocytopenia present on a
spectrum and there are currently no guidelines regarding a threshold for endovascular intervention. While Doppler ultrasound
(US) is common for routine evaluation, magnetic resonance (MR) angiography with two-dimensional phase-contrast MRI (2-D
PC-MRI) may improve the assessment of meso-Rex bypass function.
Objectives To determine the feasibility and utility of MR angiography with 2-D PC-MRI in evaluating children with meso-Rex
bypass and to correlate meso-Rex bypass blood flow to markers of portal hypertension.
Materials and methods MR angiography and 2-D PC-MRI in meso-Rex bypass patients were retrospectively analyzed.
Minimum bypass diameter was measured on MR angiography and used to calculate cross-sectional area. Meso-Rex bypass
blood flow was measured using 2-D PC-MRI and divided by ascending aortic flow to quantify bypass flow relative to systemic
circulation. Platelet and white blood cell counts were recorded. Correlation was performed between minimum bypass area, blood
flow and clinical data.
Results Twenty-five children (median age: 9.5 years) with meso-Rex bypass underwent MR angiography and 2-D PC-MRI. The
majority of patients were referred to imaging given clinical concern for complications. Eighteen of the 25 patients demonstrated
>50% narrowing of the bypass cross-sectional area. The mean platelet count in 19 patients was 127 K/μL. There was a significant
correlation between minimum cross-sectional bypass area and bypass flow (rho=0.469, P=0.018) and between bypass flow and
platelet counts (r=0.525, P=0.021).
Conclusion Two-dimensional PC-MRI can quantify meso-Rex bypass blood flow relative to total systemic flow. In a cohort of 25
children, bypass flow correlated to minimum bypass area and platelet count. Two-dimensional PC-MRI may be valuable
alongside MR angiography to assess bypass integrity.

Keywords Children . Magnetic resonance imaging . Meso-Rex bypass . Magnetic resonance angiography . Two-dimensional
phase-contrast

Electronic supplementary material The online version of this article


(https://doi.org/10.1007/s00247-018-4284-8) contains supplementary
material, which is available to authorized users.

* Heather A. Stefek 3
Department of Radiology, Northwestern Memorial Hospital,
heather.stefek@northwestern.edu Chicago, IL, USA
4
Department of Surgery, Northwestern Memorial Hospital,
1
Northwestern University Feinberg School of Medicine, Chicago, IL, USA
420 E. Superior St., Chicago, IL 60611, USA 5
Division of Transplant Surgery,
2
Medical Imaging, Ann & Robert H. Lurie Children’s Hospital of Chicago,
Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, USA
Chicago, IL, USA
Pediatr Radiol

Introduction stenosis. Unfortunately, complications are often unpredictable


and multifactorial, making it difficult to establish definitive
The meso-Rex bypass is considered the intervention of choice criteria of when intervention should be pursued. There are
in managing extrahepatic portal vein thrombosis [1]. Initially no guidelines regarding corrective intervention for complica-
described by de Ville de Goyet [2] in 1992, the procedure tions related to a meso-Rex bypass; decisions are based on
utilizes an autologous vein graft, most commonly the internal clinical data and imaging studies.
jugular vein, to redirect blood from the superior mesenteric Follow-up evaluation of the meso-Rex bypass typically
vein to the left portal vein (Fig. 1) [3]. Compared to prior involves serial Doppler ultrasound (US) studies to assess for
treatment options for portal vein obstruction, including adequate blood flow and presence of stenoses [6]. However,
portosystemic shunts and variceal banding, the meso-Rex by- accuracy of flow quantification may be limited by tortuosity
pass offers the advantage of restoring physiological blood of the bypass, which can preclude adequate views for mea-
flow to the liver. This allows for more significant normaliza- surement. In patients with clinical evidence or US findings
tion of liver function following surgery, including improve- suggestive of bypass stenosis, additional evaluation is often
ment in platelet count, international normalized ratio (INR) performed with magnetic resonance imaging (MRI). MR an-
and blood ammonia [4, 5]. In addition, patients who undergo giography provides detailed visualization of the meso-Rex
meso-Rex bypass have improved postsurgical weight-for-age bypass and abdominal vessels, which allows for more precise
compared to those with splenorenal shunts, highlighting the measurements and intervention planning. Two-dimensional
importance of adequate liver function in normal pediatric phase-contrast MRI (2-D PC-MRI) has been successful in
growth and development [4]. quantifying portal venous flow in normal subjects and may
While the majority of bypasses remain patent for years, 10– likewise prove valuable in assessing meso-Rex bypass blood
17% develop stenosis [1, 6]. Stenosis most commonly occurs flow [7]. The purpose of this study is to determine the utility of
near the left portal vein anastomosis and can occur months to MR angiography with 2-D PC-MRI in evaluating children
years after surgery [6]. The sequelae of bypass narrowing are with meso-Rex bypasses and to compare blood flow through
portal hypertension and hepatic dysfunction, including varice- the bypass with clinical markers of portal hypertension.
al bleeding, hypersplenism and hyperammonemia [3].
Hypersplenism leads to increased sequestration of platelets
and white blood cells and can cause significant splenomegaly. Materials and methods
Endovascular intervention such as angioplasty and/or stent
placement is the mainstay of treatment for meso-Rex bypass Patient population and clinical data

The retrospective study is institutional review board (IRB)


approved and HIPAA compliant. Informed consent was
waived by the IRB. A retrospective PACS search identified
all children with a meso-Rex bypass with clinically indicated
abdominal MR angiography with 2-D PC-MRI was per-
formed at Ann and Robert H. Lurie Children’s Hospital
(Lurie Children’s) Hospital between 2013 and 2017. Meso-
Rex bypass and aortic blood flow have been a part of the
clinically indicated MR imaging protocol since 2013. Patient
age, height and weight were recorded on the same day as the
MRI. Platelet count, white blood cell count and blood ammo-
nia level were recorded from the same day as MRI when
available. Relevant clinical history including time from sur-
gery to imaging, complications and study indication were re-
corded from the electronic medical record (Epic, Verona, WI).

Imaging protocol

MR angiography
Fig. 1 Diagram of the meso-Rex bypass: inferior vena cava (IVC),
superior mesenteric vein (SMV), inferior mesenteric vein (IMV),
splenic vein (SV), cavernous transformation of the portal vein (CTPV),
Abdominal MR angiography was performed at 1.5 T using a
right portal vein (RPV), left portal vein (LPV). (Reprinted with 3-D T1 gradient echo sequence with respiratory navigator
permission [3]) triggering at end-expiration and electrocardiography (ECG)
Pediatr Radiol

gating in diastole (T1 fast low angle shot [FLASH], Aera; Phase-contrast imaging data analysis
Siemens Healthineers, Malvern, PA). Patients fasted for at
least 4 h before the study. General anesthesia was used in 18 Two-dimensional PC-MRI meso-Rex bypass and aortic root
patients, and the remaining 7 patients were imaged awake. blood flow sequences were post-processed in Qflow (Medis,
MR angiography parameters included: field of view (FOV) The Netherlands) by an imaging technologist with >5 years of
300 × 280 mm, slice thickness reconstructed at 1.3 mm, repe- experience. Data were reviewed by one of two attending pe-
tition time (TR) 3.3 ms and echo time (TE) 1.27 ms. All diatric radiologists (C.K.R. with 18 years of experience and
examinations were performed following contrast: 20 patients A.P. with 10 years of experience). Meso-Rex bypass flow was
received 0.03 mmol/kg gadofosveset trisodium (Ablavar; divided by flow in the aortic root to obtain a ratio of bypass-to-
Lantheus Medical Imaging, North Billerica, MA), two re- systemic blood flow, representing the percentage of systemic
ceived 2.5 mg/kg ferumoxytol (Feraheme; AMAG blood flow being transported by the meso-Rex bypass. Meso-
Pharmaceuticals, Waltham, MA), two received 0.1 mmol/kg Rex bypass flow was compared to normal portal vein flow
Gadavist (Bayer HealthCare, Whippany, NJ) and one received using published data for fasting healthy children [9].
0.1 mmol/kg Dotarem (Guerbet, France). For exams using a
blood pool contrast, images were acquired in the steady state Statistical methods
following contrast administration. For those performed with
extracellular gadolinium-based contrast agents, our protocol Regression analysis was performed in SPSS (IBM, Armonk,
consists of an initial bolus injection followed by a slow con- NY) to correlate the minimum cross-sectional area of the
tinuous contrast infusion. meso-Rex bypass, blood flow and clinical data including
platelet and white blood cell (WBC) count. Pearson’s coeffi-
cient was calculated for variables with a normal data distribu-
MR angiography image analysis tion; Spearman’s rho was calculated for variables with abnor-
mal data distribution. P<0.05 was considered statistically
Minimum diameter of the meso-Rex bypass was measured in significant.
two orthogonal planes on MR angiography using Vitrea (Vital
Images, Minnetonka, MN). Minimum cross-sectional area
(π x r1 x r2) was calculated and normalized to body sur- Results
face area (BSA). This area was compared to the cross-
sectional area of the mid-bypass to quantify the extent Demographics
of narrowing as a percentage. Vitrea software was used
to generate 3-D reconstructions of the MR angiography to The final cohort included 25 patients (12 female, 13 male)
aid visualization of the bypass. Spleen lengths were re- with a median age of 9.5 years (interquartile range [IQR]:
corded from the MR angiography images and compared 8.0–12.6 years). Imaging was performed at a median of
to normative values [8]. 53 months (IQR: 19–64 months) following meso-Rex bypass
surgery, with all patients imaged 9 or more months following
surgery (Table 1). An additional patient was not included in
Phase-contrast imaging this final cohort as imaging had been performed in the imme-
diate postoperative period to evaluate for postsurgical compli-
Retrospectively ECG-gated 2-D PC-MRI was acquired cations. Original meso-Rex bypass was constructed using an
perpendicular to the long axis of the bypass in the mid internal jugular vein autograft in 22 of 25 patients. In the
portion of the meso-Rex bypass with plane placement to remaining three patients, the inferior mesenteric vein was used
avoid any stenosis. The following parameters were used to form the bypass as preoperative evaluation demonstrated
for meso-Rex bypass 2-D PC-MRI: repetition time inadequate or absent internal jugular vein. Two patients addi-
TR 5.8 ms, TE 3.5 ms, velocity encoding of 40–80 cm/s tionally required incorporation of a Gore-tex (Gore Medical,
and a spatial resolution of at least 4 pixels across the Flagstaff, AZ) graft in either initial or revision surgery.
meso-Rex bypass diameter. Blood flow in the aortic root MRI was performed as part of routine follow-up in asymp-
was also quantified to report meso-Rex bypass flow as a tomatic patients in 11 of 25 studies. In these cases, MRI was
percentage of total systemic arterial flow. For the aortic 2- used to assess the function of the meso-Rex bypass both 1 year
D PC-MRI sequence, retrospectively ECG-gated 2-D PC- following placement as well as 5 years later, in order to deter-
MRI was obtained perpendicular to the long axis of the mine discharge from routine follow-up at Lurie Children’s.
aortic root with the following parameters: TR 5.7–5.8 ms, Fourteen patients had additional indications for the MRI, in-
TE 2.1–4.4 ms and velocity encoding of 150–200 cm/s to cluding elevated ammonia (n=1), worsening thrombocytope-
avoid aliasing. nia and/or progression of splenomegaly (n=6), history of
Pediatr Radiol

Table 1 Demographics and


clinical data for the final study Number n=25 patients
cohort
Age Median: 9.5 years (range: 2.5–19 years)
Gender 12 female, 13 male
Time between surgery and MRI Median: 53 months (range: 9–109 months)
Platelet count Mean: 127×103/μL (normal: 150–450×103/μL)
White blood cell count Mean: 4.8×103/μL (normal: 4.5–10×103/μL)

previous stenosis, angioplasty or modification (n=6) and as- of 25 patients had splenomegaly; 1 patient was post-
sessment of stenosis identification on US (n=1). Eleven pa- splenectomy.
tients in the cohort had more than one MRI examination per- Three cases are selected to highlight the range of outcomes
formed; the most recent study was used in each case. encountered in meso-Rex bypasses. The first was a 7-year-old
boy seen 5 years after surgery. Imaging demonstrated a patent
Clinical data bypass transporting 21% of systemic circulation, reassuring
for continued adequacy of function (Fig. 3). Another patient
Nineteen patients had laboratory data evaluated on the day of in the cohort, also a 7-year-old boy, underwent MRI 19 months
MRI with measurement of platelets, WBC count and ammo- after surgery due to signs of compromised portal flow, with
nia levels. In this group, the mean platelet count was 127,000 thrombocytopenia to 74 K/μL and elevated ammonia at
per microliter (K/μL) (±56 K/μL) with 14 children below the 94 μmol/L. While imaging confirmed bypass patency, only
normal range of 150-450 K/μL. Mean WBC count was 4.8 K/ 5% of the systemic circulation was being transported by the
μL (±1.7 K/μL) with 6 children below the normal range of bypass. This compromised forward flow likely contributed to
4.5-10 K/μL. Median ammonia was 33 μmol per liter the formation of varices (Fig. 4). A third patient, a 14-year-old
(μmol/L) (IQR: 23–43 μmol/L), with 9 children above the girl, was found to have a stenosis near the left portal vein
normal level of 11–35 μmol/L. anastomosis (Fig. 5). She underwent angioplasty and follow-
up MR angiography demonstrated improvement in patency as
MR angiography and phase-contrast MRI well as increased blood flow from 10 to 19% of systemic
circulation (Fig. 5).
Median indexed minimum cross-sectional area of the bypass
was 22 mm2/m2 with values ranging from 1 to 62 mm2/m2 Regression analysis
(IQR: 10–37 mm2/m2). In comparing the narrowest bypass
segment to the patent mid-bypass, 7 patients had <50% de- Indexed minimum cross-sectional bypass area was signifi-
crease in cross-sectional area, 10 patients had 50–80% de- cantly correlated to blood flow through the bypass, with a
crease in area and 8 patients had >80% decrease in cross- larger area corresponding to higher flow (Spearman
sectional area. Stenosis occurred near the upstream of the left rho=0.469, P=0.018, Fig. 6). In addition, in the 19 patients
portal vein anastomosis in all but one patient, who demonstrat-
ed a narrowing of the mid-bypass. Two patients in the group
had severe stenosis measuring less than 1 mm with exact mea-
surements difficult to discern due to the small diameter and
spatial resolution of the MR study. They were assigned a min-
imum diameter of 1×1 mm for the purposes of this study.
Of 26 patients initially imaged, phase-contrast MRI suc-
cessfully measured aortic root and meso-Rex bypass flow in
all but 1 patient (96%) A single case was excluded from the
final cohort for technically inadequate ascending aortic flow
sequence. On average, phase-contrast imaging of the bypass
lasted 103 s (±56 s) and that of the ascending aorta lasted 98 s
(±49 s). In the final cohort, mean blood flow through the
meso-Rex bypass was 13% (±5.9%) of systemic blood flow
with values ranging from 1.2% to 25%. Notably, in 20 of 25
patients, the bypass transported less than 18.3% of systemic Fig. 2 Meso-Rex bypass flow with each bar representing one patient. The
flow (Fig. 2). Eighteen percent of systemic flow represents dashed line marks 18.3% of systemic flow, which is the normal calculated
normal portal vein flow in healthy children [9]. Twenty-one ratio of portal vein (PV) to total systemic blood flow [9]
Pediatr Radiol

Fig. 3 Three-dimensional MR angiography reconstruction in a 7-year-


old boy with meso-Rex bypass placed at the age of 2 years. There is
minimal narrowing of the patent meso-Rex bypass near the left portal
vein anastomosis (arrow). By 2-D phase-contrast MRI, the bypass
transported 21% of the systemic blood flow. These findings were Fig. 4 Three-dimensional MR angiography reconstruction in a 7-year-
reassuring of continued adequacy of function old boy presenting 19 months after meso-Rex bypass surgery with
clinical signs of compromised portal flow. MR angiography
demonstrates a patent meso-Rex bypass (short arrow) transporting 5%
with laboratory data, flow significantly correlated to the plate-
of the systemic blood flow. A dominant gastric varix (long arrow) was
let count with lower flow corresponding to a lower platelet visualized originating from the portal vein and leading to a network of
count (r=0.525, P=0.021, Fig. 7). There was a trend toward varices, likely secondary to decreased forward flow through the bypass
lower WBC count in patients with decreased blood flow, but
the correlation was not statistically significant (r=0.380, transported through the meso-Rex bypass is important in
P=0.109). assessing bypass function. Flow through a well-functioning
meso-Rex bypass should be the equivalent of flow within a
normal portal vein. Based on reported values for blood flow in
Discussion healthy children, the portal vein transports 18.3% of systemic
blood flow [9]. Compromised portal venous flow leads to
In this study, 2-D PC-MRI successfully quantified blood flow complications such as portal hypertension and hepatic
through the meso-Rex bypass and ascending aorta in 96% of dysfunction, and restoring adequate flow to the liver
patients, a promising success rate that suggests future larger- ameliorates these complications. For example, thrombo-
scale application. Two-dimensional PC-MRI has several ad- cytopenia in patients with portal vein stenosis or cirrho-
vantages over Doppler US in measuring flow. Obtaining sis improves following treatment with angioplasty or
views for accurate flow measurement is less technically chal- liver transplant, respectively [10, 11]. Similar improve-
lenging with 2-D PC-MRI than with Doppler US, especially ment is seen after endovascular correction of meso-Rex
in tortuous bypasses. In addition, MRI avoids the limi- bypass stenosis [6]. However, the threshold to intervene
tations of bowel gas artifact and technologist variability can be unclear, especially in patients with comorbidities
that can impact US studies. Furthermore, MR angiogra- or history of recurrent stenosis. Further characterizing
phy provides 3-D visualization of the bypass that can be the relationship between bypass blood flow and clinical
valuable in assessing intervention feasibility. Inclusion complications may clarify the need for intervention.
of phase-contrast imaging adds little time to MR exams; Following placement of a meso-Rex bypass, routine
on average, measurement of ascending aortic and bypass follow-up includes physical examination and a complete
flow requires less than 2 min each. blood count as well as serial Doppler US studies, typically
By quantifying meso-Rex bypass and ascending aortic performed at 1, 3, 6 and 12 months after surgery [6]. In
flow volumes in the same exam, flow through the meso-Rex addition, MRI is often routinely performed 1 year after
bypass can be quantified relative to total cardiac output. This surgery as well as 5 years after surgery, at which point
provides a means of “normalizing” flow volumes to the pa- successful cases are transitioned to less frequent follow-
tient’s own blood volume. The fraction of systemic circulation up. Patients are also referred for MRI if there are US
Pediatr Radiol

Fig. 5 A 14-year-old girl imaged


9 months after surgery was noted
to have a stenosis of the meso-
Rex bypass (a) near the left portal
vein anastomosis (arrow). Two-
dimensional PC-MRI quantified
the meso-Rex bypass transporting
10% of the systemic blood flow. b
The patient subsequently
underwent angioplasty and
follow-up imaging demonstrates
improvement of patency (arrow)
and increased blood flow to 19%

findings suggestive of stenosis and/or symptoms of portal hy- initially present due to extrahepatic portal vein thrombo-
pertension. Greater than 50% bypass narrowing was present in sis, which may not completely normalize following by-
18 of 25 patients, with 8 of these patients demonstrating >80% pass. Furthermore, the degree of stenosis noted on imag-
bypass narrowing. This rate of stenosis was much higher than ing may be disparate from the clinical picture. No objec-
the incidence of bypass stenosis in all meso-Rex patients, tive guidelines dictate the threshold for intervention and
which is reported to be 10–17% [1, 6]. At our institution, decisions are based on clinical trends and imaging [3].
US is preferred for routine bypass surveillance and many of At our institution, the decision to intervene is made when
the patients in our cohort underwent MRI to assess complica- there is radiographic evidence of bypass stenosis as well
tions initially suspected on US imaging. This composition of as an overall decline in the clinical picture, including
our cohort was reflected in phase-contrast imaging, with 80% sequelae of hypersplenism such as splenomegaly and
of the cohort calculated to transport less blood flow through thrombocytopenia. However, we lack definitive guide-
the meso-Rex bypass than through a normal portal vein. lines and cutoffs to define adequate bypass function
Clinical data in the cohort mirrored phase-contrast findings, and decisions are made on a case-by-case basis. In our
with 14 patients displaying clinical thrombocytopenia, 6 with cohort, decreased blood flow measured by phase-contrast
leukopenia and 9 with elevated blood ammonia at the time of imaging was significantly correlated to worsening throm-
the MRI study. bocytopenia and trended to lower WBC counts. For this
Smaller minimum indexed area of the bypass was sig- reason, it may be valuable to consider blood flow as a
nificantly correlated to decreased blood flow, affirming biomarker when assessing function of the bypass and
that stenoses impact flow. However, deciding when to intervention threshold.
intervene on stenoses can be difficult in clinical practice. The utility of 2-D PC-MRI in clinical care was further
Clinical complications are multifactorial and mirror those made evident in the consideration of individual patients in

Fig. 6 A scatterplot shows the relationship between the minimum cross-


sectional meso-Rex bypass area and blood flow by 2-D phase-contrast Fig. 7 A scatterplot shows the relationship between the bypass flow by 2-
MRI D phase-contrast MRI and platelet count
Pediatr Radiol

the cohort. Imaging can be valuable to track long-term Compliance with ethical standards
function of the meso-Rex bypass and may, in turn, help
characterize predictors of positive outcomes. It can clarify Conflicts of interest None
the etiology of bypass failure and, as discussed above,
play a role in optimizing the timing of interventions for
bypass stenoses. Future research avenues should aim to References
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Acknowledgements A special thanks to 3-D analyst Brian Reilly from portal venous stenosis before and after treatment in pediatric liver
Ann & Robert H. Lurie Children’s Hospital of Chicago for his contribu- transplantation: evaluation with Doppler ultrasound. Transplant
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