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Anaphylaxis to Gadolinium Radiocontrast a Case Report and Review of the Literature

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Introduction

The extraordinarily low incidence of agin reactions to gadolinium-based contrast agents (GBCAsouthward)has frustrated efforts to compare their relative safety, because hundreds of thousands of administrations may be necessary to detect differences at these low rates. Ionic and nonionic iodine-based dissimilarity agents are known to take dissimilar firsthand reaction rates. GBCA agin reactions occur less frequently merely may as well have differences related to chemic construction, ionicity, and affinity for serum proteins (1–5).

Information on firsthand reactions to GBCAs have been reported in large case series (2–15). We hypothesized that there are differences in rates of immediate allergic reactions to ionic versus nonionic, linear versus macrocyclic, and protein-binding versus non–poly peptide-bounden GBCAs that may exist detectable when data from multiple large case series are combined. The purpose of this systematic review and meta-analysis was to determine if there are differences in rates of firsthand allergic events among types of GBCAs.

Materials and Methods

Search Strategy

This meta-analysis was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, or PRISMA (16). A search of the PubMed and Google Scholar databases for all published studies through February 2017 was conducted independently by ii radiology research fellows (B.A.H. and Z.F., with 10 and 3 years of experience, respectively). The following key words were used: "GBCA" or "gadolinium" combined with "adverse result," "agin event," or "allergic reaction." Reference lists of the retrieved articles were screened, and additional manual citation searching was performed for each article that met inclusion criteria, with removal of duplicate articles. There were no language limitations. Then, titles and abstracts were reviewed, and comments, letters, reviews, and articles in which rates of immediate adverse reactions to specific GBCAs were non reported were excluded. On the ground of full-text review of the remaining manufactures, six studies were excluded considering reactions to GBCAs were reported generically instead of being attributed to a specific GBCA. Two articles were excluded because they overlapped with subsequent, updated manufactures on the topic from the aforementioned institutions. Finally, we excluded articles in which the authors did non utilize the American Higher of Radiology (ACR) Manual on Contrast Media Nomenclature system for dividing astute reactions into three categories (mild, moderate, and severe) (17–twenty). Since the ACR Manual on Contrast Media evolved during the past 10 years, with a separation of allergic-similar and physiologic reactions in the more recent versions (xix,20), we contacted authors of articles for farther information, when necessary, to exclude physiologic reactions (as divers in the ACR Manual on Dissimilarity Media pages 103–104 [twenty]) from the data on mild, moderate, and severe allergic-like reactions. We assessed risk of bias in the 9 last studies by using A Cochrane Risk of Bias Assessment Tool for Non-Randomized Studies of Interventions, or ACROBAT-NRSI (21).

Data Extraction

Two authors (B.A.H.and Z.F.) independently read each article that met inclusion and exclusion criteria and extracted the number of administrations; the numbers of balmy, moderate, and astringent reactions; and the number of deaths for each GBCA. For articles in which both firsthand and delayed reactions were reported, data on the delayed reactions were excluded. All discrepancies in the data extractions between the two observers were resolved in consensus with a third reviewer (M.R.P., with 30 years of radiology research experience).

Classification of Agin Events

All selected articles included apply of the ACR Manual on Contrast Media system for classification of astute reactions as mild, moderate, or severe (17–20). Balmy allergic-like reactions were cocky-limited, without prove of progression and included limited urticaria, pruritus, limited cutaneous edema, express itching or "scratchy" throat, nasal congestion, sneezing, conjunctivitis, and rhinorrhea. Moderate reactions were more pronounced, commonly required medical treatment, and included lengthened urticaria and/or puritis, diffuse erythema with stable vital signs, facial edema without dyspnea, pharynx tightness or hoarseness without dyspnea, wheezing, and mild bronchospasm without hypoxia. Severe reactions were potentially life-threatening, with risk of permanent morbidity or expiry if non treated accordingly, and included lengthened edema or facial edema with dyspnea, diffuse erythema with hypotension, laryngeal edema with stridor and/or hypoxia, wheezing and/or bronchospasm, substantial hypoxia, and anaphylactic shock (17–twenty).

Classification of GBCA Type

GBCAs were grouped according to their chemic construction and properties (Table one) (22–28). Each GBCA was either macrocyclic (gadoterate, gadobutrol, and gadoteridol) or linear (all of the rest). GBCAdue south likewise were grouped according to ionicity. There were data on a unmarried nonionic linear GBCA (gadodiamide), which was compared with iv ionic linear GBCAdue south to appraise the effect of ionicity. Three of the ionic linear GBCAs had moieties that transiently bound serum proteins (eg, albumin) that conferred high relaxivity and claret pool distribution (gadofosveset), loftier relaxivity and 50% hepatobiliary excretion (gadoxetate), and high relaxivity and 4% hepatobiliary excretion (gadobenate dimeglumine) (28). These three GBCAs were grouped together as ionic linear GBCAs with protein bounden. To assess the event of ionicity in a linear GBCA without the misreckoning effect of protein binding, nosotros compared the linear nonionic GBCA (gadodiamide) with a linear ionic GBCA without protein binding (gadopentetate dimeglumine). To assess the issue of protein binding in linear GBCAdue south without the confounding effect of ionicity, nosotros compared the linear ionic protein-bounden GBCAs to the linear ionic not–protein-binding GBCA. To compare linear agents to macrocyclic agents without confounding from the property of protein bounden, a group of linear GBCAdue south without protein binding (gadodiamide and gadopentetate dimeglumine) was compared with the macrocyclic group, none of which had protein bounden. For further comparison of linear and macrocyclic GBCAs, with elimination of confounding effects of both protein bounden and ionicity, a comparison of a nonionic linear (gadodiamide) GBCA with nonionic macrocyclic (gadobutrol and gadoteridol)GBCAs was performed.

Table 1 Characteristics of GBCAs

Table 1

Statistical Methods

The mild, moderate, severe or fatal, and overall reaction rates; astringent or fatal reaction rates; and moderate or severe or fatal reaction rates were compared among different GBCA groups as we take described. For each comparing, we merely used information from the articles in which both types of GBCAs were investigated. Relative risk was estimated by using the Mantel-Haenszel blazon method of Rothman and Boice (29), and an x2 test was performed with the hypothesis that relative run a risk would equal 1. We considered a type I mistake of .05 as indicative of a significant divergence (P , .05). We also conducted additional meta-analyses by comparing overall reaction rates between the GBCA with the lowest reaction rate and each of the other agents. For all meta-analyses, nosotros performed heterogeneity cess by using both the Cochran Q and I 2 statistics. A moderate heterogeneity among studies was adamant equally a P value of the Cochran Q less than 0.i and an I 2 greater than 50%, and severe heterogeneity was considered with a P value of the Cochran Q less than .05 or an I 2 greater than 75%. Random furnishings were added when severe heterogeneity was detected (30,31). For all statistical calculations, we used software (StatsDirect statistical software version 3.0.198; StatsDirect, Altrincham, England).

Results

Nine articles met the criteria and included a total of 716 978 GBCA administrations (Tabular array 2, ,Fig one), with 983 administrations reported to have resulted in immediate agin reactions. Three articles reported only allergic-like reactions (seven,10,14). The other half dozen manufactures reported both allergic and physiologic reactions. In i of these (9), all physiologic reactions could be excluded without contacting the authors. In the remaining five manufactures (ii,11–thirteen,15) in which both allergic-like and physiologic reactions were reported, authors were contacted for clarification. In this manner, 321 physiologic reactions were eliminated, leaving 662 allergic-similar reactions (Table two).

Tabular array two Nine Articles in which Immediate Reactions to GBCAs Were Reported

Table 2

Figure 1:

Figure 1: Flowchart shows the article search process. AE = adverse event

The overall rate of patients who had immediate allergic-similar reactions was nine.2 per ten 000 administrations and the overall rate of severe immediate allergic-like reactions was 0.52 per ten 000 administrations. Breakdowns according to individual GBCA appear in Table 1 and Figure 2, and co-ordinate to chemical construction in Tables 3 and 4. In this cohort, 81% (539 of 662) of reactions were mild, 13% (86 of 662) were moderate, and 6% (37 of 662) were severe.

Figure 2:

Figure ii: Graph shows rates of immediate balmy, moderate, and severe allergic-like reactions to GBCA, combining data from all nine articles. Horizontal lines indicate 95% CIs.

Table three Comparison of Immediate, Allergic-like Reactions to GBCAs Categorized according to Chelate Molecular Construction

Table 3

Tabular array 4 Moderate Plus Severe (Including Fatal) Immediate Allergic-like Reactions to GBCAsouth

Table 4

The nonionic linear GBCA, gadodiamide, had the everyman overall rate of immediate adverse reactions, at 1.5 per ten 000 administrations, which was significantly less than that for linear ionic GBCAs, at 8.3 per x 000 administrations (relative risk, 0.19; P < .00001) (Fig 3a) and less than that for nonionic macrocyclic agents, at 16 per 10 000 administrations (relative hazard, 0.12; P < .001) (Fig 3d). These data and CIs are included in Table 3.

Figure 3a:

Figure 3a: Woods plots bear witness relative chance for immediate, allergic-like reactions to GBCAsouth. (a) Plot shows data for four articles in which total allergic-similar reactions to linear ionic and linear nonionic GBCAs were were compared. (b) Plot shows information from eight articles in which linear ionic with protein bounden and linear ionic without protein binding GBCAs were compared. (c) Plot shows data from 7 manufactures in which linear without poly peptide binding and macrocyclic (besides without protein binding) GBCAs were compared. (d) Plot shows data from four articles in which linear nonionic and macrocyclic nonionic GBCAs were compared. Size of squares indicates relative weighting of studies. Horizontal lines indicate 95% CIsouthward.
Figure 3b:

Figure 3b: Forest plots show relative chance for immediate, allergic-like reactions to GBCAdue south. (a) Plot shows data for four articles in which total allergic-similar reactions to linear ionic and linear nonionic GBCAdue south were were compared. (b) Plot shows data from viii articles in which linear ionic with poly peptide bounden and linear ionic without protein binding GBCAs were compared. (c) Plot shows data from vii articles in which linear without protein binding and macrocyclic (likewise without protein binding) GBCAsouthward were compared. (d) Plot shows data from four articles in which linear nonionic and macrocyclic nonionic GBCAsouthward were compared. Size of squares indicates relative weighting of studies. Horizontal lines betoken 95% CIdue south.
Figure 3c:

Figure 3c: Forest plots show relative risk for immediate, allergic-like reactions to GBCAsouth. (a) Plot shows data for four articles in which total allergic-like reactions to linear ionic and linear nonionic GBCAsouth were were compared. (b) Plot shows data from 8 articles in which linear ionic with poly peptide binding and linear ionic without poly peptide binding GBCAs were compared. (c) Plot shows data from seven articles in which linear without poly peptide binding and macrocyclic (also without protein binding) GBCAsouth were compared. (d) Plot shows data from four articles in which linear nonionic and macrocyclic nonionic GBCAsouth were compared. Size of squares indicates relative weighting of studies. Horizontal lines indicate 95% CIs.
Figure 3d:

Figure 3d: Forest plots show relative risk for immediate, allergic-like reactions to GBCAdue south. (a) Plot shows data for four manufactures in which full allergic-like reactions to linear ionic and linear nonionic GBCAs were were compared. (b) Plot shows data from eight articles in which linear ionic with poly peptide binding and linear ionic without poly peptide binding GBCAs were compared. (c) Plot shows information from seven manufactures in which linear without protein binding and macrocyclic (also without protein binding) GBCAdue south were compared. (d) Plot shows data from four articles in which linear nonionic and macrocyclic nonionic GBCAsouth were compared. Size of squares indicates relative weighting of studies. Horizontal lines betoken 95% CIs.

The nonionic linear GBCA besides had the lowest rate of moderate and severe (including fatal) agin reactions, at 0.38, compared with linear ionic GBCAs, at ane.9 per x 000 administrations (relative take a chance, 0.2; P = .017) (Table iv, Fig 4a). In the comparison of gadodiamide with each of the other GBCAs individually, on the footing of the relative risk of reaction, utilize of gadodiamide resulted in fewer total reactions, at 1.5 per x 000 injections, than did utilise of gadopentetate dimeglumine, at 5.2 per 10 000 injections (relative risk, 0.27 [95% CI: 0.xiv, 0.55]; P = .0002) gadobenate at 17 (relative risk, 0.1 [95% CI: 0.05, 0.20]; P < .0001); gadoterate at nine (relative risk, 0.sixteen [95% CI: 0.05, 0.54]; P = .003); gadobutrol at 16 (relative risk, 0.16 [95% CI: 0.05, 0.54]; P = .003); and gadoteridol at sixteen (relative risk, 0.07 [95% CI: 0.02, 0.18]; P < .0001) reactions per 10 000 injections (Fig 2). A comparing to gadofosveset and gadoxetate with gadodiamide could non be performed because of the lack of articles in which gadodiamide was used with those GBCAs. Although gadofosveset had the highest overall rate of firsthand allergic-similar reactions at 91 (95% CI: 37, 168) per 10 000 injections, information technology had the lowest number of administrations (only 797) and did not have any astringent reactions (Tabular array 1). Linear agents without protein binding had a lower reaction rate, at 4.4 (95% CI: 3.8, 5.1) per x 000 injections, compared with macrocyclics (likewise without poly peptide bounden), at xiv per x 000 injections (relative take a chance, 0.46; P = .01) (Table 3, Fig 3c). This comparison had moderate heterogeneity (Cochran Q, fifteen; P , .02; I 2, 61%) and was the only comparison that required the random effects model to mitigate heterogeneity, although the statistical significance of the difference did not change compared with that of the fixed effects model. Furthermore, a comparison in which nosotros controlled for both ionicity and poly peptide binding showed that nonionic linear GBCA had a lower relative take a chance compared with nonionic macrocyclic GBCAdue south for all reactions (0.12 [95% CI: 0.05, 0.31]; P < .0001) and for moderate and severe reactions (0.19 [95% CI: 0.05, 0.66], P = .009) (Fig 3d). The comparison of ionic linear GBCA without protein binding (gadopentetate dimeglumine) to ionic macrocyclic GBCA (gadoterate) involved a smaller number of injections and did not testify a significant difference. We as well did non find a departure between ionic macrocyclic and nonionic macrocyclic GBCAsouth.

Figure 4a:

Figure 4a: Forest plots evidence relative adventure for immediate, allergic-like reactions to GBCA that were moderate or severe (including fatal). (a) Plot shows data from 4 articles in which total allergic-like reactions to linear ionic and linear nonionic GBCAsouthward were compared. (b) Plot shows information from eight manufactures in which linear ionic with poly peptide binding and linear ionic GBCAs without protein binding were compared. (c) Plot shows data from iv articles in which linear nonionic and macrocyclic nonionic GBCAsouth were compared. Size of squares indicates relative weighting of studies. Horizontal lines indicate 95% CIs.
Figure 4b:

Figure 4b: Forest plots prove relative risk for immediate, allergic-similar reactions to GBCA that were moderate or severe (including fatal). (a) Plot shows data from four articles in which total allergic-like reactions to linear ionic and linear nonionic GBCAs were compared. (b) Plot shows data from eight articles in which linear ionic with poly peptide binding and linear ionic GBCAs without protein binding were compared. (c) Plot shows data from four manufactures in which linear nonionic and macrocyclic nonionic GBCAdue south were compared. Size of squares indicates relative weighting of studies. Horizontal lines indicate 95% CIdue south.
Figure 4c:

Figure 4c: Forest plots show relative take chances for immediate, allergic-like reactions to GBCA that were moderate or severe (including fatal). (a) Plot shows data from iv articles in which total allergic-like reactions to linear ionic and linear nonionic GBCAs were compared. (b) Plot shows information from eight articles in which linear ionic with poly peptide bounden and linear ionic GBCAs without protein binding were compared. (c) Plot shows information from four manufactures in which linear nonionic and macrocyclic nonionic GBCAs were compared. Size of squares indicates relative weighting of studies. Horizontal lines indicate 95% CIs.

All GBCAs with protein binding (gadoxetate, gadofosveset, and gadobenate) were linear ionic GBCAs. Protein bounden was associated with a greater rate of reactions, at 17 (95% CI: 15, xx) per 10 000 injections compared with gadopentetate dimeglumine, the 1 ionic linear agent without poly peptide binding, at 5.2 (95% CI: four.5, 6.0) per ten 000 injections (relative hazard, three.1 [95% CI: 2.4, iii.8]; P < .0001) (Fig 3b). Moreover, the rate of severe or fatal reactions was greater for protein bounden (gadoxetate, gadofosveset, and gadobenate) linear ionic GBCAdue south, at ane.23 (95% CI: 0.7, i.nine) per x 000 injections, compared with a non–poly peptide-binding linear ionic GBCA (gadopentetate dimeglumine), at 0.21 (95% CI: 0.09, 0.04) per 10 000 injections (relative risk, 6.3 [95% CI: 2, twenty]; P = .0021) (Figs 3d, 4b).

There were two deaths caused by severe reactions to GBCAs, with a rate of ii.7 per ane million administrations. An ionic GBCA with protein binding, gadobenate dimeglumine acquired one death, and the other death was related to a macrocyclic GBCA, gadobutrol.

By using ACROBAT-NRSI (21), we plant a moderate risk of bias due to missing data in six articles. In ii articles (12,xiv), data were missing on the type of GBCA that induced reactions. In five articles (2,eleven–13,15), data on physiologic and allergic reactions were initially pooled. Authors were contacted to resolve these biases. In 1 commodity (10), investigators reported information collection partially funded by manufacture. None of the other studies reported manufacture agreements related to the study, but eight of 67 authors reported manufacture agreements unrelated to the study. In seven manufactures, moderate bias due to confounding was present (eg, use of gadoxetate for liver MR imaging and unlike GBCAs for other indications). All nine studies had a low chance of bias in selection of cases into the report in the reported results, in measurement of outcomes, and finally a moderate adventure of overall bias (Table 5).

Tabular array 5 Risk of Bias in the Included Studies

Table 5

Discussion

The extraordinarily depression rate of immediate reactions to GBCAs and the rare incidence of fatal reactions has led to a generalization that all GBCAs are safety, especially compared with iodine-based contrast media (one–v). Differences in reaction rates between GBCAdue south have been hypothesized only are difficult to bear witness due to the large number of patients needed to prove statistically pregnant differences for such rare events (2,vii,9–15,32). These data combined from nine well-designed studies (ii,7,9–xv) including 716 978 GBCA administrations show a college rate of reactions associated with the properties of ionicity, poly peptide binding, and cyclic construction.

Ionic agents automatically split into fragments, ane positively charged and one negatively charged when they are injected into the claret stream, which doubles the number of particles in solution, doubling the osmolality and raising the viscosity, which may contribute to a higher reaction rate (33–35). Thus, it is not surprising that the GBCA with the lowest rate of immediate allergic-similar reactions was nonionic, and this property is well established as conferring a lower rate of reactions for iodine-based dissimilarity agents (1,36–42). No outcome of ionicity was observed for macrocyclic agents, although there are fewer data on macrocyclic GBCAs.

The favorable low reaction rate for nonionic linear GBCAs stands in dissimilarity to their worrisome lower kinetic stability, which is idea to increase the risk of nephrogenic systemic fibrosis and gadolinium retentiveness in the brain (22,43–45). Because take a chance of development of nephrogenic systemic fibrosis can be decreased past screening renal function before administration, nonionic linear agents may be considered for patients with normal renal function who are at increased risk of allergic reactions. This may include patients with asthma, astringent allergies, or a history of prior reaction to other GBCAdue south. It may likewise be considered at centers that lack an immediately bachelor code team to help treat astringent reactions (eg, outpatient imaging centers), which can be beyond the ability of a single radiologist to handle.

Protein binding may confer the favorable qualities of higher GBCA relaxivity, hepatobiliary excretion, or sequestration inside the blood pool (28). Our ascertainment of a higher rate of reactions for GBCAsouth with protein binding is also consistent with those of prior reports (46).

Macrocyclic GBCAs had a greater rate of reactions compared with linear GBCAsouthward, which was confirmed in a comparison of nonionic linear to nonionic macrocyclic GBCAs that was controlled for ionicity and protein-binding effects. This greater rate of allergic-like reactions must exist considered with other aspects of safety including the favorable stability of macrocyclic agents that reduces adventure of nephrogenic systemic fibrosis and gadolinium retention in the brain (43,47,48). An overall cess of condom should not focus on a unmarried GBCA property.

The two deaths reported in these nine publications correspond to a rate of 2.eight per ane million administrations. Both deaths involved GBCAdue south with factors contributing to college adventure (2,7). Gadobenate is ionic and protein binding. Gadobutrol is macrocyclic. It is besides important to consider that decease due to an agin reaction is a multifactorial event. Information technology depends on the skills of the hospital staff in differentiating the symptoms of anaphylaxis from other differential diagnoses such as a vasovagal reaction or panic assail and in responding quickly before the reaction becomes life threatening (6,49–54). The use of ability injection may be a take a chance cistron if it delays recognition and handling of reactions. In at to the lowest degree one of these deaths, the patient received GBCA by means of ability injection (2), which contributed to a filibuster in diagnosis. Data on the method of injection for the other death were not available (7). When a power injector is used, the close-proximity patient monitoring that automatically occurs with manus injections should not be allowed to lapse.

Limitations of this meta-analysis included the retrospective analysis of data, which may accept created a selection bias, and a dependence on meticulous tape keeping for information accuracy. It was not possible to control for temporal biases, such equally the Weber effect (10,55), because data on when each GBCA was used at each establishment were not available. However, combining data from countries with unlike GBCA introduction dates (Korea, Japan, European countries, and the U.s.a.) with data collections spanning from 2000 to 2016 was expected to minimize temporal biases that might have been nowadays.

Not all of the GBCAsouthward were used by all of the authors, and then differences in how each middle reported events could have biased the results. We mitigated this risk by requiring that all articles involved the use of the ACR classification system for contrast material reactions, and we contacted authors to eliminate physiologic reactions. Eliminating physiologic reactions reduced heterogeneity. The limitation of study heterogeneity was too mitigated by using a random effects model when Cochran heterogeneity was high. Only one comparing required use of the random effects model due to loftier heterogeneity, and when we also used a fixed effects model for that comparison, the significance did non alter. There was a variation in the number of subjects per report, ranging from x 608 to 194 400, which could take overweighted the outcome of larger studies. Finally, in spite of the large number of GBCA administrations, the very low incidence of moderate and astringent reactions limited the statistical ability for their evaluation.

In conclusion, by combining data from 9 studies of immediate reactions to GBCA we showed that poly peptide binding, macrocyclic structure, and ionicity are associated with higher rates of allergic-like adverse events.

Advances in Knowledge

  • ■ In a systematic review of nine studies of immediate reactions to gadolinium-based dissimilarity agents (GBCAs), 1.5 immediate allergic-like agin events per 10 000 administrations of nonionic linear GBCA were reported (P < .00001), which was less than the 8.iii and sixteen reactions per 10 000 administrations reported for ionic linear GBCA and nonionic macrocyclic GBCA, respectively (P < .001).

  • ■ Ionic linear GBCAs known to have poly peptide bounden were associated with a higher rate of immediate allergic-similar reactions, (17 per ten 000 administrations) compared with the same ionic linear chelate classification without poly peptide bounden (5.two per 10 000 administrations, P < .0001).

  • ■ Linear GBCAs without protein bounden had a lower rate of immediate allergic-like reactions (4.4 per x 000 administrations) compared with macrocyclic GBCAs without protein binding (fourteen per 10 000 administrations, P = .01).

Implication for Patient Care

  • ■ When patients with glomerular filtration rates greater than 30 mL/min per 1.73 mtwo and for whom at that place is clinical business organization for allergic reactions crave contrast cloth–enhanced MR imaging, information technology is reasonable to consider the bug of ionicity, protein binding, and macrocyclic versus linear chelate structure when selecting a GBCA.

Disclosures of Conflicts of Interest: B.A.H. disclosed no relevant relationships. Y.Z. disclosed no relevant relationships. Z.F. disclosed no relevant relationships. K.R.P. Activities related to the nowadays article: disclosed no relevant relationships. Activities non related to the present commodity: consultancy for Bayer, Bracco, and GE Healthcare; patents with Bayer, Bracco, GE Healthcare, Lantheus and Mallinkrodt/Guerbet. Other relationships: disclosed no relevant relationships.

Author Contributions

Author contributions: Guarantors of integrity of unabridged study, A.H.B., Y.Z., M.R.P.; study concepts/report blueprint or data conquering or data assay/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content,D all authors; blessing of final version of submitted manuscript, all authors; agrees to ensure whatever questions related to the work are appropriately resolved, all authors; literature inquiry, all authors; clinical studies, Y.Z.; experimental studies, Y.Z.; statistical analysis, Y.Z., M.R.P.; and manuscript editing, all authors

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Received December ane, 2016; revision requested February 1, 2017; revision received April eight; accepted May 8; final version accepted June 8.
Published online: Aug 25 2017
Published in print: Feb 2018

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Source: https://pubs.rsna.org/doi/full/10.1148/radiol.2017162740

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