Original Research
Neuroradiology/Head and Neck Imaging
December 23, 2015

Signal Change in the Dentate Nucleus on T1-Weighted MR Images After Multiple Administrations of Gadopentetate Dimeglumine Versus Gadobutrol

Abstract

OBJECTIVE. The objective of this study was to evaluate signal changes in the dentate nucleus on unenhanced T1-weighted MR images after multiple administrations of gadopentetate dimeglumine versus gadobutrol.
MATERIALS AND METHODS. Two study groups were identified, each of which included 25 consecutive patients. Each group received six or more administrations of either gadobutrol only or gadopentetate dimeglumine only, without having had exposure to any other gadolinium-based contrast agent (GBCA). The mean signal intensity (SI) in the dentate nucleus on unenhanced T1-weighted MR images was measured, with the use of the pons and the cerebellar peduncle as references to calculate the DNP SI ratio (i.e., the ratio of the SI in the dentate nucleus to the SI in the pons) and the DCP SI ratio (i.e., the ratio of the SI in the dentate nucleus to the SI in the cerebellar peduncle).
RESULTS. After six administrations of gadopentetate dimeglumine, the SI in the dentate nucleus on unenhanced T1-weighted MR images increased from a DCP SI ratio of 0.997 before administration to 1.034 after the last of six administrations (p = 0.0007) and then to 1.063 after all administrations (p = 0.0004). No statistically significant increase was noted in association with administration of gadobutrol, for which the DCP SI ratio was 0.995 before administration, 1.009 after the last of six administrations (p = 0.1172), and 0.992 after all administrations (p = 0.7592). The change in the DCP SI ratio after administration of gadopentetate dimeglumine correlated with the number of administrations the patient received (p < 0.0001).
CONCLUSION. Unenhanced T1 signal hyperintensity was observed in the dentate nucleus after multiple administrations of gadopentetate dimeglumine, a linear ionic agent, but not after multiple administrations of gadobutrol, a macrocyclic GBCA.
Increased signal in the dentate nucleus and the globus pallidus has been noted on unenhanced T1-weighted MR images [15] after multiple administrations of linear gadolinium-based contrast agents (GBCAs), specifically gadopentetate dimeglumine (Magnevist, Bayer HealthCare), gadobenate dimeglumine (MultiHance, Bracco), and gadodiamide (Omniscan, GE Healthcare), but not after multiple administrations of gadoteridol (ProHance, Bracco) or gadoterate meglumine (Dotarem, Guerbet), which are macrocyclic agents [6, 7]
Gadobutrol (Gadavist, Bayer HealthCare) is a third macrocyclic GBCA that is nonionic and that also has high in vitro stability, compared with the linear GBCAs gadopentetate dimeglumine and gadodiamide. Thus, we would expect gadobutrol to behave similarly to other macro cyclic GBCAs. However, in a study performed with no control population, Stojanov et al. [8] reported increased signal intensity (SI) in the dentate nucleus and the globus pallidus after gadobutrol was administered four to six times to patients with relapsing remitting multiple sclerosis.
Since January 2013, our institution has switched from using gadopentetate dimeglumine to gadobutrol as our primary GBCA in contrast-enhanced MRI examinations. Using gadobutrol provides us with the opportunity to investigate the SI in the dentate nucleus in two groups of patients who received either gadobutrol exclusively or gadopentetate dimeglumine exclusively (i.e., a positive control group), to determine whether multiple administrations of gadobutrol are also associated with T1 signal hyperintensity in the dentate nucleus of patients with a variety of brain diseases.

Materials and Methods

This HIPAA-compliant retrospective review of existing patient data and images was approved by the institutional review board at Weill Medical College. The requirement for informed consent was waived.

Patients

Radiology records were searched to identify two groups of adult patients who had all undergone six or more GBCA-enhanced MRI examinations that included an initial brain MRI study in which T1-weighted images were acquired before the first administration of GBCA plus a final brain MRI study performed after gadolinium had been administered six or more times. Patients were excluded from the study if they had undergone GBCA-enhanced MRI studies at an institution other than the study institution, if they had a history of undergoing neurosurgical procedures that likely involved MRI examinations performed somewhere other than at the study institution, if MR images of the basal ganglia or cerebellum were unsatisfactory because of artifacts or pathologic findings, or if there was a lack of unenhanced T1-weighted MR images. Group 1 consisted of 25 consecutive patients for whom every instance of contrast agent administration exclusively involved gadobutrol, whereas group 2 consisted of 25 consecutive patients for whom every instance of contrast agent administration exclusively involved gadopentetate dimeglumine.
Demographic data and information about diagnoses, treatments, and medications were obtained from the electronic medical records of the patients. These electronic medical records were also searched for information about MRI scans performed at institutions other than the study institution, and any patient with evidence of having had gadolinium administered at an institution other than the study institution was excluded. Data on imaging details, including imaging parameters and gadolinium administration, were obtained from the PACS at our institution.

MRI Protocol

All patients underwent imaging performed using either a 1.5- or 3-T MRI system and standardized protocols, which included acquisition of 2D axial spin-echo T1-weighted images with the use of a TR/TE of 500/14 (adjusted, as necessary, for the number of slices needed to cover the brain) and a slice thickness of 5 mm. For all patients, the GBCA dose received was 0.1 mmol/kg of body weight.

Imaging and Data Analysis

Quantitative analysis was performed in a manner similar to that reported in previous studies [1, 2]. Oval ROIs were positioned on the right dentate nucleus, the central pons, and the right cerebellar peduncle on unenhanced T1-weighted images. ROIs were placed on the left side if ROIs placed on the right side could not be measured as a result of the presence of artifacts or observation of brain pathologic findings. T2-weighted images were used to guide ROI placement. One radiologist measured SIs twice on 100 studies, to assess intraobserver reproducibility. A second radiologist also measured the SIs on the same 100 studies, to assess interobserver agreement. To ascertain the effect of the number of injections of contrast medium, such measurements were performed by the first radiologist after each administration of GBCA, when unenhanced T1-weighted images of the brain were available.
The DNP SI ratio (i.e., the ratio of SI in the dentate nucleus to the SI in the pons) was calculated by dividing the SI in the dentate nucleus by the SI in the pons. The relative percentage change in the DNP SI ratio (Rchange) after any number (x) of injections of GBCA was calculated using the following equation: Rchange = 100 × (DNPx − DNP0) / DNP0, where 0 indicated that the DNP SI ratio was determined before the first administration of GBCA. Because accumulation of gadolinium in the pons has been reported in an autopsy series, and because some of the observed effect was related to field differences and signal inhomogeneity occurring over the distance between the dentate and pons, we also measured the SI in the cerebellar peduncle. A DCP SI ratio (i.e., the ratio of the SI in the dentate nucleus to the SI in the cerebellar peduncle) was calculated by dividing the SI in the dentate nucleus by the SI in the cerebellar peduncle. The relative percentage change in the DCP SI ratio after any number (x) of injections of GBCA were calculated using the following equation: Rchange = 100 × (DCPx − DCP0) / DCP0, where 0 indicated that the DCP SI ratio was determined before the first administration of GBCA.

Statistical Analysis

Data on categoric variables were presented in terms of the number of patients, and data on continuous variables were presented as the mean (± SD) value and range. A one-sample t test was applied to evaluate whether the percentage change in the SI ratio in the dentate nucleus after injections of GBCA was different from zero. Variability in the DNP SI ratio and the DCP SI ratio was calculated to determine which ratio was more suitable for use in the statistical analyses. To assess interobserver reproducibility, intraclass correlation coefficients were calculated for the 100 studies in which ROIs were measured by two radiologists. To assess intraobserver reproducibility, intraclass correlation coefficients were calculated for the 100 studies in which ROIs were measured twice by the same observer. For the groups administered gadobutrol only and gadopentetate dimeglumine only, the following linear mixed model was applied to detect how the DCP SI ratio varied on the basis of the number of administrations: DCPx SI ratio = slope × number of administrations + intercept. Administrations of contrast medium were considered a fixed effect, and patients were considered a random effect.

Results

Demographic data for the two groups of patients who were administered a GBCA are presented in Table 1. The following characteristics were similar among patients in both groups: mean age; sex distribution; use of radiation therapy, chemotherapy, or both; renal function; indications of liver dysfunction; and history of neurosurgery. However, the group administered gadobutrol exclusively had a lower mean number of administrations of contrast agent per patient, compared with the group administered gadopentetate dimeglumine exclusively; this finding reflects the fact that gadobutrol was used for fewer years than was gadopentetate dimeglumine at our institution. Accordingly, a comparison of the two contrast agents was performed on the basis of measurements obtained after six administrations and on the basis of measurements obtained after all administrations.
TABLE 1: Demographic and Clinical Characteristics of 50 Patients in the Study Sample
ParameterPatients Administered Gadobutrol Exclusively (n = 25)Patients Administered Gadopentetate Dimeglumine Exclusively (n = 25)
Age at last MRI examination (y), mean ± SD (range)54 ± 16 (26-87)53 ± 14 (24-87)
Sex  
 Male1515
 Female1010
No. of GBCA administrations, mean ± SD (range)7.8 ± 2.4 (6-16)12.1 ± 5.2 (6-23)
Time between initial and final GBCA administration (d), mean ± SD (range)205±152(22-558)849 ± 634 (74-2399)
Time between final GBCA administration and measurement (d), mean ± SD (range)64 ± 65 (1-208)101 ± 80 (1-270)
Primary indication for brain MRI  
 Primary brain tumor1318
 Brain metastasis33
 Demyelination22
 Infection62
 CNS vasculitis10
Underwent neurosurgerya1922
Received chemotherapyb1825
Received radiation therapyb  
 Whole brain20
 Tumor selective1414
Abnormal liver function1712
Estimated GFR (mL/min/1.73 m2)  
 > 9046
 60-901013
 30-5996
 < 3020

Note—Except where otherwise indicated, data are the number of patients. GBCA = gadolinium-based contrast agent, GFR = glomerular filtration rate.

a
Neurosurgery was performed between the times when the first and final enhanced MRI examinations were performed.
b
Chemotherapy or radiation therapy or both were received between the times when the first and final enhanced MRI examinations were performed.
Table 2 provides a comparison of the change in the DCP and DNP SI ratios after both six administrations and all administrations of gadopentetate dimeglumine versus gadobutrol. The increase in the signal noted on T1-weighted MR images after administration of gadopentetate dimeglumine was highly statistically significant (p = 0.0007, for both the DCP and DNP SI ratios after six administrations; p = 0.0004, for the DCP SI ratio after all administrations; and p = 0.0011, for the DNP SI ratio after all administrations). However, the change in signal noted after administration of gadobutrol was not statistically significantly different (p = 0.1172, for the DCP SI ratio after six administrations; p = 0.0877, for the DNP SI ratio after six administrations; p = 0.7592, for the DCP SI ratio after all administrations; and p = 0.1400, for the DNP SI ratio after all administrations).
TABLE 2: Comparison of Changes in the DCP SI Ratio (the Ratio of the Signal Intensity [SI] in the Dentate Nucleus to the SI in the Cerebellar Peduncle) and the DNP SI Ratio (the Ratio of the SI in the Dentate Nucleus to the SI in the Pons) After Administrations of Gadopentetate Dimeglumine Versus Gadobutrol
Ratio and Contrast AgentBefore GBCA AdministrationsAfter Six GBCA AdministrationsAfter All GBCA Administrations
DCP SI RatioRchange (%)pDCP SI RatioRchange (%)p
DCP SI ratio       
 Gadopentetate dimeglumine0.997 ± 0.0281.034 ± 0.0483.759 ± 4.7680.00071.063 ± 0.0726.758 ± 9.1220.0004
 Gadobutrol0.995 ± 0.0301.009 ± 0.0341.442 ± 4.3460.11720.992 ± 0.045−0.312 ± 4.9310.7592
DNP SI ratio       
 Gadopentetate dimeglumine0.981 ± 0.0451.048 ± 0.0786.874 ± 6.9650.00071.063 ± 0.1058.508 ± 12.2730.0011
 Gadobutrol0.999 ± 0.0611.029 ± 0.0563.197 ± 6.8910.08770.972 ± 0.065−2.400 ± 8.2460.1400

Note—GBCA = gadolinium-based contrast agent; Rchange = 100 × (DCPx − DCP0) / DCP0 or (DNPx − DNP0) / DNP0, where x denotes the number of administrations of GBCA.

The DCP SI ratio, in which the cerebellar peduncle was used as the reference, showed less variability and a substantially lower SD. Accordingly, all further analyses used the DCP SI ratio as the measure of signal accumulation in the dentate nucleus. For the 100 MRI examinations measured by two different observers, there was excellent agreement (intraclass correlation coefficient, 0.99). For the 100 MRI studies measured twice by the same observer, there was similarly excellent agreement (intraclass correlation coefficient, 0.99).
For the group of patients who received gadopentetate dimeglumine exclusively, the linear mixed model showed that the slope (Fig. 1A) had a statistically significant increase from zero (p < 0.0001). The between-patient variance component was 0.0015, whereas the within-family patient variance component was less than 0.0005. Thus, 76% of variability came from differences between individual patients. Figure 2 shows the unenhanced T1-weighted image of a patient who was administered gadopentetate dimeglumine exclusively, with increased SI noted in the dentate nucleus. For the group of patients who were administered gadobutrol exclusively, the linear mixed model showed that the slope (Fig. 1B) was not statistically significantly increased from zero (p = 0.36). Figure 3 shows the unenhanced T1-weighted image of a typical patient who was administered gadobutrol exclusively, with no increased SI noted in the dentate nucleus.
Fig. 1A —Effect of number of administrations of gadolinium-based contrast agent on DCP SI ratio (i.e., ratio of signal intensity [SI] in dentate nucleus to SI in cerebellar peduncle).
A, Scatterplot shows that slope corresponds to increase in DCP SI ratio of 0.0041 multiplied by number of administrations + 1.008. This finding is statistically significantly different from zero (p < 0.0001), indicating that there is increased change in SI in dentate nucleus on T1-weighted MR images after gadopentetate dimeglumine administrations.
Fig. 1B —Effect of number of administrations of gadolinium-based contrast agent on DCP SI ratio (i.e., ratio of signal intensity [SI] in dentate nucleus to SI in cerebellar peduncle).
B, Scatterplot shows slope corresponds to increase in DCP SI ratio of −0.0007 × number of administrations + 1.0009. This finding is not statistically significantly different from zero (p = 0.36), indicating that there is no significant change in SI in dentate nucleus on T1-weighted MR images after gadobutrol administrations.
Fig. 2A —61-year-old woman with glioblastoma multiforme.
A, Unenhanced T1-weighted spin-echo MR images acquired before (A) and after (B) 22 administrations of gadopentetate dimeglumine show increased signal intensity (arrows, B) in dentate nucleus relative to rest of cerebellum.
Fig. 2B —61-year-old woman with glioblastoma multiforme.
B, Unenhanced T1-weighted spin-echo MR images acquired before (A) and after (B) 22 administrations of gadopentetate dimeglumine show increased signal intensity (arrows, B) in dentate nucleus relative to rest of cerebellum.
Fig. 3A —29-year-old man with acute myeloid leukemia and fungal infection.
A, Unenhanced T1-weighted spin-echo MR images acquired before (A) and after (B) nine administrations of gadobutrol show no increased signal intensity in dentate nucleus relative to rest of cerebellum.
Fig. 3B —29-year-old man with acute myeloid leukemia and fungal infection.
B, Unenhanced T1-weighted spin-echo MR images acquired before (A) and after (B) nine administrations of gadobutrol show no increased signal intensity in dentate nucleus relative to rest of cerebellum.

Discussion

Increased SI in the dentate nucleus on unenhanced T1-weighted images after multiple exposures to a linear GBCA likely reflects residual or progressive accumulation of GBCA at that location, as has been confirmed both at autopsy [9, 10] and in animal studies [11]. However, the present study shows that after six or more exposures to gadobutrol, which is a nonionic macrocyclic agent, no appreciable mean increase in SI was seen in the dentate nucleus. This finding is consistent with the reports of Kanda et al. [6], who noted a lower SI in the dentate nucleus after patient exposures to gadoteridol, a nonionic macrocyclic GBCA, compared with exposures to the linear agents gadopentetate dimeglumine and gadodiamide. It is also consistent with the findings of Radbruch et al. [7], who found a lower SI in the dentate nucleus after administration of gadoterate meglumine, an ionic macro-cyclic GBCA, than after administration of gadopentetate dimeglumine. Showing that all three commercially available macrocyclic GBCAs (gadoteridol, gadoterate meglumine, and gadobutrol) produce less of an increase in signal in the dentate nucleus on T1-weighted images, compared with the linear agents, supports the possibility that the high stability of GBCA mitigates this effect.
These results may appear different from those of Stojanov et al. [8], who reported an increased SI in the dentate nucleus relative to the pons after four to six administrations of gadobutrol to patients with relapsing remitting multiple sclerosis. However in that study, there was no control group (e.g., patients who were administered a linear contrast agent, for comparison); the correlation of findings with the number of administrations was of borderline statistical significance (p = 0.046); there was no correlation with the total gadobutrol dose received; the increase in signal in the dentate nucleus was small; and the characteristic pattern of an increase in signal in the dentate nucleus, which we observed in the present study after administration of gadopentetate dimeglumine (Fig. 2), was not apparent on their images. Stojanov and colleagues exclusively analyzed patients with relapsing remitting multiple sclerosis, to make this observation. In the present study, we analyzed patients who had a greater spectrum of diseases; in fact, only two patients had multiple sclerosis. Furthermore, the increased SI in the dentate nucleus that was observed by Stojanov et al. was greatest in the short intervals between MRI examinations, but the SI was reduced when there was a long interval between MRI examinations, thereby raising the possibility of washout, which we also observed anecdotally.
Although the present study evaluated a lower total number of subjects than did the studies by Kanda et al. [6], Errante et al. [2], and Radbruch et al. [7], all 50 subjects received at least six injections of GBCA; on the basis of our experience, it is after six injections when the effect of gadopentetate dimeglumine begins to be noticeable. The other studies that investigated macrocyclic agents included only four patients (Kanda et al.), 22 patients (Errante et al.), or nine patients (Stojanov et al. [8]) who received six or more administrations of GBCA. Although Radbruch and colleagues made sure that all their subjects had received six administrations of contrast agent, they did not require exclusive exposure to a single contrast agent. Eliminating patients who received fewer than six administrations while also requiring all injections to involve use of the same GBCA increased the power of our study and enabled us to directly compare GBCAs after an identical number of administrations of each agent. This approach also made it easier to identify the dentate nucleus for placement of ROIs on the MR images of patients who were administered gadopentetate dimeglumine, because it showed an increase in signal relative to the surrounding brain (Fig. 2).
Macrocyclic agents are more stable than linear agents because the rigid macro cyclic ring system requires substantial energy to dissociate gadolinium from the macrocycle. This leads to a lower propensity for gadolinium dissociation or transmetallation, as has been seen in multiple in vitro studies [1214]. Frenzel et al. [15] showed that the release of gadolinium ions in human serum at 37°C was below the quantification limit of 0.1% for macrocyclic GBCAs, including gadobutrol, compared with the quantification limit of 20–21% for linear GBCAs. This crucial difference in stability between GBCAs favors the theory that dissociation of gadolinium ion from the chelator is part of the mechanism for this effect. However, because gadolinium bound to phosphates may not be expected to produce any signal enhancement on T1-weighted images, the anion to which the dissociated gadolinium would bind is unclear. It is possibly that gadolinium ions could bind to citrates, neuromelanin chelators [16, 17] that are known to be present in the brain, or to other large proteins that could both maintain solubility and reduce the rotation correlation to maximize the T1 enhancement effect.
Limitations of the present study include the small sample size and the absence of signal changes in the dentate nucleus in one-half of the patients evaluated, which precluded us from investigating correlations with diagnosis, renal function, treatments, or other clinical factors. Gadobutrol is a relatively new GBCA in the United States. Although our institution has used gadobutrol for contrast-enhanced MRI examinations since January 2013, many of the patients underwent prior MRI studies performed with nongadobutrol agents, resulting in a much smaller sample size of patients who were exposed exclusively to gadobutrol. Also, we did not investigate the globus pallidus. We found the observation of increased SI in the globus pallidus to be less reliable and more difficult to localize, compared with the SI in the dentate nucleus, and we also found that increased SI is influenced by a wide spectrum of diagnoses [2].
In conclusion, our study found no measurable increase in the SI in the dentate nucleus on T1-weighted MR images of patients who were exposed to gadobutrol only.

Acknowledgments

We thank Ashley Giambrone (Weill Cornell Medical Center) and Dan Haverstock and Shuxin Yin (both from Bayer Pharmaceuticals) for engaging in helpful discussions on statistics.

Footnote

M. R. Prince has patent agreements with Bayer Pharmaceuticals.

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 414 - 419
PubMed: 26700156

History

Submitted: July 27, 2015
Accepted: October 5, 2015
Version of record online: December 23, 2015

Keywords

  1. contrast agents
  2. dentate nucleus
  3. gadobutrol
  4. gadolinium
  5. gadopentetate dimeglumine
  6. globus pallidus
  7. MRI
  8. safety

Authors

Affiliations

Yan Cao
Department of Radiology, Weill Medical College, 416 E 55th St, New York, NY 10021.
Daisy Q. Huang
Department of Radiology, Weill Medical College, 416 E 55th St, New York, NY 10021.
George Shih
Department of Radiology, Weill Medical College, 416 E 55th St, New York, NY 10021.
Martin R. Prince
Department of Radiology, Weill Medical College, 416 E 55th St, New York, NY 10021.

Notes

Address correspondence to M. R. Prince ([email protected]).

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