Gadolinium-enhanced magnetic resonance angiography for hepatomesenteric vascular evaluation: single and double doses comparison in schistosomiasis patients

Abstracts

OBJETIVO: Determinar a freqüência de visualização dos segmentos da circulação hepatomesentérica pela angiografia por ressonância magnética (angio-RM) com contraste e comparar o valor do método, utilizando-se duas diferentes dosagens de gadolínio (doses simples e dupla). MATERIAIS E MÉTODOS: Estudo prospectivo de 36 pacientes esquistossomóticos submetidos a angio-RM. Os exames foram realizados em equipamento de RM de 1,5 T, usando-se bobina de corpo e bomba injetora para a administração endovenosa do contraste. Foram utilizadas, de maneira randomizada, dose dupla do contraste paramagnético (0,2 mmol/kg de Gd-DTPA) em 21 pacientes e dose simples (0,1 mmol/kg) em outros 15 pacientes. Os exames foram interpretados por dois observadores em consenso, que classificaram o grau de visualização de 25 segmentos vasculares estabelecidos para análise, sem conhecimento da dose de gadolínio utilizada. RESULTADOS: Os segmentos vasculares proximais e de maior calibre foram as estruturas com melhor grau de visualização na maioria da amostra em estudo. O tronco celíaco, a artéria hepática comum, a artéria esplênica, a croça e terço médio da artéria mesentérica superior, a veia porta, a veia esplênica e a veia mesentérica superior apresentaram grau 2 de visualização em mais de 70% da amostra. Quanto à comparação das diferentes dosagens, não houve diferença significante (p < 0,05) no grau de visualização das diversas estruturas analisadas entre os grupos dose simples e dose dupla, com uma exceção isolada: na avaliação da artéria hepática direita (p = 0,008), o grupo dose simples apresentou maior freqüência de visualização grau 2, com valor significante. CONCLUSÃO: O grau de visualização dos segmentos vasculares hepatomesentéricos pela angio-RM com contraste é elevado, sendo maior nos segmentos proximais e de maior calibre. A comparação entre os grupos que utilizaram dose simples e dupla de contraste demonstrou resultados semelhantes.

Angiografia por ressonância magnética; Esquistossomose; Gadolínio

ORIGINAL ARTICLE

Gadolinium-enhanced magnetic resonance angiography for hepatomesenteric vascular evaluation: single and double doses comparison in schistosomiasis patients^*

Rogério Pedreschi Caldana^I; Alexandre Sérgio de Araújo Bezerra^II; Giuseppe D'Ippolito^III; Jacob Szejnfeld^IV

^IDoctorate by Department of Diagnostic Imaging, Universidade Federal de São Paulo-Escola Paulista de Medicina

^IIPost-graduation at Department of Diagnostic Imaging, Universidade Federal de São Paulo-Escola Paulista de Medicina

^IIIAdjunct Professor at Department of Diagnostic Imaging, Universidade Federal de São Paulo-Escola Paulista de Medicina

^IVFull Professor at Department of Diagnostic Imaging, Universidade Federal de São Paulo-Escola Paulista de Medicina

^{Mailing address}

ABSTRACT

OBJECTIVE: To evaluate the visibility of hepatomesenteric vascular segments by 3D gadolinium-enhanced magnetic resonance (MR) angiography and to compare the method effectiveness between two different gadolinium doses (single and double doses).

MATERIALS AND METHODS: A prospective study was performed with 36 schistosomiasis patients who were submitted to 3D contrast-enhanced MR angiography. Scans were performed in a high-field equipment (1.5 T), with body coil and power injector for intravenous contrast administration. Contrast double doses (Gd-DTPA 0.2 mmol/kg) and single doses (0.1 mmol/kg) were randomly used respectively in 21 and 15 patients. Studies were interpreted by consensus between two observers who have rated the visualization degree of 25 proximal vascular segments without knowing the dose used.

RESULTS: Proximal and calibrous vascular segments have presented higher visualization degree in the greatest part of the sample studied. The celiac trunk, common hepatic artery, splenic artery, proximal and medium third of superior mesenteric artery, portal vein, splenic vein and superior mesenteric vein have presented grade 2 visualization in more than 70% of the sample studied. As regards comparison between different doses, there was no significant difference (p < 0.05) in the visualization degree of several structures evaluated, between double dose and single dose groups, except for an isolate case of evaluation of right hepatic artery (p = 0.008) in which the single dose group has presented a higher frequency of grade 2 visualization with statistical significance.

CONCLUSION: The visualization degree of hepatomesenteric vascular segments by 3D gadolinium-enhanced MR angiography is high, especially in the proximal and calibrous segments. The comparison between groups using single and double contrast doses has demonstrated similar results.

Keywords: Magnetic resonance angiography; Schistosomiasis; Gadolinium.

INTRODUCTION

Starting from 1994, the introduction of the gadolinium-enhanced magnetic resonance (MR) angiography has made available a new and promising method of vascular study^(1,2). Through a methodology based on ultra-fast sequences associated with high contrast-enhancement provided by the first vascular passage of gadolinium, one has found a mean for studying blood vessels with a quality comparable to the conventional angiography image, with the advantages of minimal invasiveness and non-utilization of potentially allergenic and nephrotoxic iodine contrast agent. For these reasons, the MR angiography has rapidly gained room in literature and in the diagnostic practice, becoming one of the main subject-matters of study in the MRI field during the latest decade.

Initially, countless studies sought to validate this new procedure, comparing it with the arteriography that is considered as a reference method for vascular evaluation since its introduction early in the fifties. Thus, the gadolinium-enhanced MR angiography has presented a diagnostic efficacy comparable to arteriography for identifying the grade and localization of stenosis in aortoiliac^(3–6) and renal territories⁽⁷⁾ and in supra-aortic branches^(8,9).

The utilization of gadolinium-enhanced MR angiography in the mesenteric vascular territory was demonstrated in 2000 by Ernst et al.⁽¹⁰⁾, in a comparative study on arteriography and MR angiography in 33 patients. The concordance resulting was higher than 60% for the majority of vascular segments, excepting intrahepatic and superior mesenteric arteries which have been better evaluated by arteriography. Results presented were consistent due its prospective nature and standardized methodology. Notwithstanding, the authors have utilized a single dose instead of double dose of paramagnetic contrast agent, a factor yet without enough support in literature as to visibility results in comparison with double dose in the mesenteric territory.

As a matter of fact, the gadolinium dose is one of the most controversial variables in MR angiography and reason for several recent researches. Aiming at maximizing the vascular enhancement, the first studies have utilized a contrast agent double dose (0.2 mmol/kg), which has become a standard in studies of the different vascular segments^(1,2). Also, one has demonstrated that a three-time increase in the usual dose (0,3 mmol/kg), despite its safety, does not bring significant benefit to the image quality in comparison to double dose⁽¹¹⁾.

On the other hand, with the increasing development of technical resources and resulting gain in temporal and spatial resolution of examination sequences, one has started investigating the contrast single dose effectiveness compared with the double dose in MR angiography, principally considering the economies related to the high cost of paramagnetic contrast agent⁽¹²⁾. For this purpose, several studies were performed in some arterial territories with good results with gadolinium single dose, like in the abdominal aorta^(12,13), renal arteries^(14–16) and carotid arteries evaluation⁽¹⁷⁾.

The main argument in favor of double dose is related to the larger contrast bolus extent, which would allow larger error margin in examination temporal planning and may contribute to the better quality of image in studies impaired by other variables. Additionally, the higher vascular enhancement peak resulting from the double dose could eventually correlate with higher conspicuousness in low caliber vessels evaluation, a factor of relevance in the mesenteric territory. However, the recent technological gains have increased the speed of data acquisition^(18,19), besides improving the image contrast and detailing. This has reduced the value assigned to the contrast agent double dose and, consequently, a revaluation has become necessary.

Based on these considerations and on results presented by literature, there is some question about the capability of the gadolinium double dose to offer a better visualization of hepatic and mesenteric circulation or a better reproducibility when compared with the contrast agent single dose. On the other hand, in case of similarity between double and single doses results, a reduction of the contrast dose in hepatomesenteric territory MR angiography will be feasible, with cost reduction without affecting the method efficacy.

With the purpose of evaluating the hepatic and mesenteric vascularization through MR angiography, we have tried to form a homogeneous group of patients capable of providing the research with a consistent basis. Also, it is important to note that this study would bring diagnostic benefits to the patients involved. For these reasons, we have opted to study a group of schistosomiasis patients.

It is important to test the variables related to the examination technique also in this group as an additional step towards MR angiography consolidation as a diagnostic methodology of technical refinement and practical applicability.

Therefore, we have planned this study with the objectives of: a) determining the frequency of visualization of hepatomesenteric circulation segments by means of contrast-enhanced MR angiography; b) establishing the method value by comparing paramagnetic contrast agent single and double doses.

MATERIALS AND METHODS

Between June/2000 and June/2002, we performed a double-blind prospective study analyzing the hepatomesenteric circulation of 36 ambulatory patients with schistosomiasis by means of gadolinium-enhanced 3D MR angiography. The criteria for inclusion in this study were: conscious and cooperative > 18 year old patients with diagnosis of schistosomiasis mansoni proved by rectal biopsy or strong laboratory, clinical or epidemiological evidence (patients coming from endemic areas presenting imaging findings compatible with periportal fibrosis and positive stool test). The following exclusion criteria were taken into consideration: MR contraindications (cardiac pacemaker, cerebral aneurysm clips, coclear implants, claustrophobia), alcoholism history (> 160 g/day ethanol ingestion), positive serology for hepatitis B or C virus, proved history of autoimmune disease (due to the risk of associated autoimmune hepatitis) and known use of hepatotoxic drugs.

The studied group was constituted of 19 male and 17 female patients, ages between 28 and 71 years (median 43, mean 44.6). Ten of these patients had been previously submitted to splenectomy and the other 26 experienced some degree of splenomegaly during the period of study (splenic index > 800) and had not any history of portosystemic bypass.

Examinations were performed in a high field (1.5 T) ACS/NT model Philips MR equipment with 15 mT/m gradient. A body coil was employed as signal transmitter and receiver. A Spectris (Medrad) MR injector was employed in the first 14 cases of the sample and an Injektron 82 MRT (Medtron) in the 22 remaining cases.

The TSE and FFE techniques were applied for abdominal study, through T1-weighted sequences in phase and phase opposition modes, T2-weighted sequences at two different echo times (90 and 160 ms) and T1-weighted axial sequence after paramagnetic contrast agent injection. The MR angiography was performed with FFE (echo-gradient) sequence in three consecutive phases under apnea: non-enhanced, arterial and portal venous. The 3D acquisition volume was planned in coronal plane, positioned anteriorly to the aorta, including its lumen and following its course.

Contrast agent injection was made through a mechanical pump at constant 3 ml/s, followed by 15 to 20 ml of physiological solution.

The time interval for starting the arterial phase of dynamic sequence was calculated by the test-dose method, utilizing 1 ml contrast followed by 15 ml physiological solution. In the group studied, this time ranged between 9 and 21 seconds after the injection starting. The venous phase was initiated 60 seconds after concluding the arterial phase acquisition.

We have utilized paramagnetic contrast agent double dose (0.2 mmol/kg, equivalent to 0.4 ml/kg Gd-DTPA) in 21 patients, and single dose (0.1 mmol/kg, equivalent to 0.2 ml/kg) in the other 15 patients. The decision by the dose of contrast injected has been randomly made to avoid possible sampling errors^(20,21), the dosing sequence to be applied in this study also being randomly established.

Images have been reconstructed by means of MIP technique for obtaining 3D images in 16 different projections. The studies analysis has been based both on original images recorded in two post-subtraction dynamic phases (arterial and portal) and images deriving from reconstruction using MIP technique (Figure 1).

Images were consensually interpreted by two experienced radiologists working for more than four years with magnetic resonance imaging.

Twenty-five hepatomesenteric circulation vascular segments were selected for visualization grade analysis: celiac trunk, common hepatic artery, proper hepatic artery, left gastric artery, splenic artery, gastroduodenal artery, right gastric artery, right hepatic artery, left hepatic artery, middle hepatic artery, arch, middle third and distal third of the superior mesenteric artery, jejunal and ileal arteries, middle colic artery, right colic artery, ileocolic artery, inferior pancreaticoduodenal artery, inferior mesenteric artery, portal vein, right and left portal branches, splenic vein, superior and inferior mesenteric veins.

The structures identified were rated in a subjective way with grades 0 to 2, according to their visualization grade provided by intravenous contrast: grade 0 was assigned to unidenfied structures, grade 1 was assigned to partially visualized structures and grade 2 to clearly visualized structures.

Figures 2 to 13 depict the visualization of some of the main vascular segments being studied.

Statistical analysis

The comparative analysis between single and double doses was performed by means of the Fisher test. The significance level determined was 5% (p < 0.05). In order to allow the test application and easy results interpretation, tables were reduced to only two categories of visualization grades, gathering grades 0 and 1 together into a single group. This group included the cases where the grade of visualization did not reach enough quality for diagnosis purposes.

RESULTS

Frequency of visualization of vascular branches

Proximal and high caliber vascular segments have been the structures bearing higher grades of visualization in the greatest part of the sample studied. Celiac trunk, common hepatic artery, splenic artery, arch and middle third of the superior mesenteric artery, portal vein, splenic vein and superior mesenteric vein have presented visualization grade 2 in more than 70% of the sample. On the other hand, the right gastric artery, middle hepatic artery and inferior pancreaticoduodenal artery have been the structures with lowest grades of visualization and have not been identified in more than 93% of the sample by both investigators. Tables 1 and 2 show the frequency of visualization of vascular segments by both investigators in the contrast agent single dose and double dose groups.

In the sample studied, seven cases of portal vein cavernous transformation were identified, presenting ill-defined outline associated with tortuous venous structures along the portal bed (Figures 14 and 15).

Except for one vascular segment (right hepatic artery), all the other segments studied have presented similar visualization grades between different dosing groups (no statistically significant difference). This may be observed in Figures 16 and 17. Only the right hepatic artery had higher frequency of visualization grade 2 with single dose. However, only five cases were discordant.

DISCUSSION

Our purpose in this study was not correlating diagnosis methods, since the comparison between mesenteric MR angiography and digital arteriography for the territory studied has already been made⁽¹⁰⁾. However, the findings of this study are complementary to the conclusions of the study developed by Ernst et al.⁽¹⁰⁾, where there was a good correlation between those methods in the evaluation of the proximal portions of mesenteric arteries with an adequate visualization of distal ramifications achieved only with arteriography⁽¹⁰⁾.

One of the main factors deserving consideration is the sample being studied. The fact of evaluating a group of schistosomiasis patients brings the advantage of anticipating parameters for the patients themselves who may benefit from the diagnosis methodology studied. Besides the diagnostic information obtained in each case, the examinations performed in this study constituted a response to the already existent demand for the schistosomiasis patients evaluation method.

Sample randomization was adopted to remove any non-controlled influence that could unintentionally distort the cases distribution⁽²²⁾. The asymmetry in both groups dimensions was originated by the randomization process, but this has not posed a problem for the statistical method employed.

The MR angiography sensitivity can be increased resulting in a better vascular detailing through splanchnic vasodilatation. Hany et al., in 1998, proved that the caloric stimulus resulting from a 475 kcal meal 15 minutes before examination can improve the detection of mesenteric arterial ramifications⁽²³⁾. This was not possible in our study because the MR cholangiopancreatography was performed in a same period of examination for part of the patients. Therefore, we opted not to include this technical refinement for the purposes of sample homogenization.

In spite of recent publications supporting the use of synergy coils^(24–26) instead of body coils, in a comparative study developed with the same equipment utilized in our study, the sequences using synergy coils presented a similar quality and lower signal/noise ratio in relation to the sequences performed with body coils⁽²⁷⁾.

The quality of a contrast-enhanced MR angiography study is highly dependent on an appropriate dynamic phase temporal planning, as well as on the injection technique. The early data acquisition results in an insufficient arterial contrast enhancement and the delayed data acquisition causes undesirable venous contrast effect and enhancement of parenchymal structures. In this study, the utilization of the test-dose technique has assured an adequate calculation of the time interval for the start of dynamic sequence, minimizing errors resulting from technical failure in temporal planning. A power injector was utilized due to the advantage of providing constant injection speed, resulting in a higher arterial signal intensity than the one resulting from manual injection⁽²⁸⁾.

Frequency of visualization of vascular segments

Based on the analysis of results related to grade of vascular branches visualization, it is possible to identify three different vascular groups: a group of clearly visualized segments, characterized by the high frequency of grade 2 visualization; a group of intermediary visualization segments with distribution of results among the three grades established, and a third group including unsatisfactorily visualized segments, characterized by the high frequency of grade 0 visualization.

The first group of vascular segments (clearly visualized) includes celiac trunk, common hepatic artery, splenic artery, arch and middle third of superior mesenteric artery, portal vein, splenic vein and superior mesenteric vein. The second group (intermediary visualization) includes the following segments: right and left proper hepatic arteries, left gastric artery, gastroduodenal artery, distal third of the superior mesenteric artery, jejunal and ileal arteries, middle and right colic arteries, ileocolic artery, Inferior mesenteric artery, left and right portal branches and inferior mesenteric vein. The third group (unsatisfactory visualization) includes the right gastric artery, middle hepatic artery and inferior pancreaticoduodenal artery.

Thus, we have observed that the appropriate visualization of vascular segments presented correlation with their caliber and proximity. Generally and according to expectations the proximal and higher caliber segments were more clearly identified than distal ramifications. These findings are in concordance with updated literature references, with studies demonstrating a good quality imaging by MR angiography for celiac trunk and mesenteric arterial trunk evaluation, but poor quality for intra-hepatic arteries and mesenteric ramifications⁽¹⁰⁾. It is our understanding that low caliber, anatomical variability and MR angiography grade of spatial resolution are determinant of unsatisfactory visualization of distal vascular segments by this method.

If the evaluation of a low caliber arterial territory has resulted unsatisfactory, on the other hand, an adequate visualization of the two proximal thirds of the superior mesenteric artery is an excellent indicator of this method diagnostic potentiality, since the greatest part of atherosclerotic lesions (the main disease affecting the mesenteric arterial bed) occur exactly on the proximal portions of this artery⁽²⁹⁾.

Similarly, a clear visualization of the largest extent of the portomesenteric venous bed (portal, splenic and superior mesenteric veins), a segment usually involved by this region venous diseases, is a good indicator of this method potential effectiveness, also for the venous territory.

Specifically regarding the portal vein, it is valid to observe that the presence of cavernous transformation in some cases of the sample may justify its partial or non-visualization. In these cases, the lower visibility of this vascular segment has not occurred due technical limitation, but rather due anatomical variation.

Results also illustrate a particularity of this patients group: the high frequency of portal thrombosis with cavernous transformation identified in seven cases (19.4%) from the whole sample (36 patients). The morphological aspect of the portal vein cavernous transformation has already been clearly established both by MR⁽³⁰⁾ and MR angiography⁽³¹⁾, and its identification in our sample is an additional indicator of this method usefulness for this purpose.

Comparison between gadolinium single and double doses in MR angiography

Results have shown an excellent equivalence between both gadolinium doses (single and double doses). There was no significant difference in the visualization grade for the different structures analyzed between the single-dose group and the double-dose group, except in the evaluation of the right hepatic artery where the single-dose group presented significantly higher frequency of visualization grade 2.

According to expectations and similarly to results observed in other vascular territories, the utilization of gadolinium single or double doses presented similar results in the evaluation of the mesenteric vascular territory. Therefore, the utilization of gadolinium double dose does not seem to be a determining factor for higher vascular visibility, indicating that results presented by Ernst et al.⁽¹⁰⁾ with contrast agent single dose are representative of an adequate methodology for the mesenteric MR angiography. In our study, notwithstanding the application of the test-dose technique, we have not achieved better visualization indices in relation to those of Ernst et al., who have utilized multiple sequences at previously established time intervals, suggesting that both methods are useful and adequate for temporal planning.

Our results also reinforce the results of studies published on MR angiography with contrast agent single dose in other vascular territories^(14,15,17).

Therefore, it is reasonable to admit that it is possible to utilize gadolinium single dose for evaluation of hepatomesenteric circulation by MR angiography, with results comparable to those obtained with the usual contrast agent double dose.

The results of the present study reinforce the value of MR angiography for evaluation of hepatomesenteric circulation as a safe, easy-to-perform, increasingly available method, presenting a high frequency of vascular visualization and useful, principally in the investigation of the proximal bed, the site most frequently affected by pathological alterations of such vessels.

Specifically regarding the schistosomiasis patient, the MR angiography may play a fundamental role in hepatomesenteric circulation reevaluations, especially with post-surgical follow-up purposes. In a recent publication, Lopes Filho and Haddad comment the relevance of evolutionary studies for evaluation of surgical anastomosis patency in schistosomiasis patients⁽³²⁾. Therefore, the utilization of MR angiography is one of the different means of increasing the benefits of such a promising method.

CONCLUSIONS

The analysis of results from hepatomesenteric circulation evaluation by means of contrast-enhanced MR angiography of 36 schistosomiasis patients has allowed us to conclude that:

1. The frequency of visualization for hepatomesenteric bed vascular segments is high, principally on proximal and high caliber vessels.

2. The frequency of visualization for hepatomesenteric circulation segments is similar with both the use of single dose and use of double dose of paramagnetic contrast agent.

REFERENCES

Received August 1st, 2005.

Accepted after revision October 3, 2005.

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*

Study developed at Department of Diagnostic Imaging, Universidade Federal de São Paulo-Escola Paulista de Medicina, São Paulo, SP, Brazil.

Publication Dates

• Publication in this collection
  26 Sept 2006
• Date of issue
  Aug 2006

History

• Accepted
  03 Oct 2005
• Received
  01 Aug 2005