mri ct-scan sinusitis

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Computed Tomography vs. Magnetic ResonanceImaging of Acute Bacterial Sinusitis:A Rabbit Model

Joseph E. Kerschn er, M D,* M ich ael J. Cruz, M D,* Davi d J. Beste, MD ,*

Kath leen M . Donah ue, PhD ,†and Karen Sue Kehl , PhD ‡

Purpose: Computed topography (CT) and magnetic resonance imaging (MRI) are important,both clinically and in a research setting, in assessing bacterial sinusitis (BS). The use of CTscanning to evaluate sinus opacification in a reversible model of rabbit acute sinusitis hasbeen reported. MRI offers the potential for better visualization of soft tissue and fluid changeswithin the paranasal sinuses. MRI has potential as a research tool in animal models ofsinusitis. This article compares the use of CT and MRI in measuring maxillary sinusopacification in rabbits during experimental, reversible BS.Materials and Methods: In 2 independent trials, New Zealand White rabbits were imaged forbaseline anatomy, and BS was generated by sinus inoculation with Staphylococcus aureus.

Serial imaging was performed as a measure of the progression and resolution of BS during thetrials. Two experienced, independent reviewers then scored each CT and MRI for percentopacification of the maxillary sinus. These scores were analyzed to assess the degree ofagreement between the reviewers.Results: The correlation coefficients for CT and MRI were 0.6816 and 0.3584, respectively.The Z-statistic comparing these correlation coefficients was significant (P Ͻ .0001), indicatingthat CT is a more precise measure of reversible BS in this rabbit model. Differences in meanscan time and cost per scan were also significantly different (P Ͻ .0001), with CT being bothquicker and less expensive.Conclusions: Greater interobserver consistency of scan interpretation, with less time andcost, make CT the preferred tool for measuring BS in this rabbit model. Attributes of MRI suchas better resolution of fluid-tissue interfaces and custom surface coil design for visualization ofspecific anatomic structures are discussed as they may increase the effectiveness of MRI asan imaging modality in future sinusitis research.(Am J Otolaryngol 2000;21:298-305. Copyright 2000 by W.B. Saunders Company)

Various techniques are used in experimen-tal sinusitis research. Dependingon theparam-eters of the study, sinus cultures, histology,cil iary activity, computed tomography (CT),and magnetic resonance i maging (M RI) haveall been valuable experimental tools and mea-sures of sinusitis.1-4 Image modality improve-

ments, clinical avail abili ty, and their use in

experimental protocols has contributed to the

expansion of our knowledge of anatomy and

thepathophysiology of sinusitis.5 CT provides

excellent delineation of sinus anatomy and

the abil ity to assess progression of sinusitis in

anoninvasivemanner.5,6 With increasingavail -

abili ty, MRI has also become a viable research

tool. Similar to CT, MRI all ows for repeated

evaluations in a noninvasivemanner. MRI has

provided an additional modality for i maging

sinus mucosal inflammatory responses and

also provides high resolution with theeli mina-tion of the biological risks associated with

ionizing radiation.7,8 Drawbacks of MRI in-

clude longer scan time, greater cost, and lossof detail regarding bone anatomy. T he poten-

tial for deli neation of tissue-fluid or fluid-

fluid interfaces has also been proposed and

From the *Department of Otolaryngology and Commu-

nication Science, and the †Department of Radiology andBiophysics, Medical College of Wisconsin, 9000 WWisconsin Ave, Milwaukee, WI; and the ‡Department ofPathology, Children’s Hospital of Wisconsin, 9000 WWisconsin Ave, Milwaukee, WI.

Presented at the American Rhinologic Society AnnualMeeting, San Antonio, TX, September 12, 1998.

Address reprint requests to Joseph E. Kerschner, MD,Children’s Hospital of Wisconsin, 9000 W WisconsinAve, Milwaukee, WI 53226.

Copyright 2000 by W.B. Saunders Company0196-0709/00/2105-0003$10.00/0doi:10.1053/ajot.2000.9874

298 American Journal of Otolaryngology, Vol 21, No 5 (September-October), 2000: pp 298-305



investigated as an advantage in MRI.9,10 Differ-ing opinions exist regarding thevalue of these2 modali ties in animal models, and no previ-ous study has compared the techniques of CTand MRI as instruments in animal model

sinusitis research. This study evaluates theprecision of CT and M RI image modali ties bycomparinginterobserver variability when scor-ing sinusitis progression. Efficiency of the 2imaging modali ties was also compared byevaluatingthe cost and time required for the 2techniques.

MATERIALS AND METHODS

CT Imaging Technique

Animal subjects included 9 female Pasteu-rell a-free New Zealand white rabbits 1.5 to 2.0kg. Scans were performed on a General Elec-tric HiSpeed Advanced System #UCT3, Model9800(Fairfield, CT). Standard head placementwas obtained with a styrofoam support toobtain coronal views of themaxillary sinuses.Contiguous 2-mm sections were imaged, with18 to 21 sections obtained per animal. Base-li ne CT scans were obtained before to sinus ormaxillary ostium manipulation. CT scans andsubsequent procedures were done under ket-amine anesthesia (35mg/kg).

MRI Technique

Animal subjects included 16 Pasteurell a-free New Zealand white rabbits 1.5 to 2.0 kg.MRI was done on a 3.0 Tesla (3T) BrukerBiospec System (Bruker Medical, Ettlinger,Germany) fitted with a custom-buil t 8.5-inlocal 3-axis gradient coil and a quadraturetransmit-receive birdcage RF coil. Spin-echoimage sequence (TR/TEϭ 2,000/24 ms, ma-trix 256ϫ 256, FOV ϭ 10 cm, 4 averages for a

total acquisition timeϭ

17 min) was used toobtain 13 contiguous 2-mm coronal sections.Standard head placement was obtained with astyrofoam support. Scan times were recordedas acquisition time plus additional time re-quired for system set-up and technical adjust-ments. Baseli ne MRI scans were obtained be-fore sinus or maxillary ostium manipulation.MRI scans and subsequent procedures weredone under ketamine anesthesia (35mg/kg).

Bacterial Sinusitis

Reversible bacterial sinusitis was estab-lished as previously described in our labora-tory.6 Briefly, animals in both imaging trials

underwent bilateral partial removal of themaxil lary bone to all ow direct access to themaxillary sinus ostia for reversible occlusion. The maxill ary ostia wereoccluded with Mero-cel plugs (Merccel, Mystic, CT). Direct micro-scopic visuali zation was used to confirm cor-rect placement of the pl ug. Five days afterocclusion, animals underwent bilateral maxil -lary sinus cultures, as well as a second imag-ing study. A cefazoli n-sensitive Staphylococ-

cus aureus wasobtained fromcli nical samplesin the microbiology lab of Children’s Hospitalof Wisconsin in Mil waukee. A suspension of

108 CFU/ mL was prepared in sterile sali neafter overnight growth on tryptic soy bloodagar at 37°C. Maxil lary sinus inoculation with0.5 mL of S. aureus (108 CFU/mL) was doneatthis time.

Follow-up Imaging

On day 7 after inoculation, an additionalimaging study was done in both trials toevaluate the progression of sinusitis beforeremoval of the ostial plugs. All foll ow-upscans were done in the same coronal plane

and with the same specifi cations as the base-li ne imaging previously described. The ostialplugs were then removed and additional serialscans were done to evaluate sinusitis resolu-tion. In theCT trial, scans wereobtained every3 days after ostial plug removal until thesinusitis resolved. The MRI group received afoll ow-up scan on a daily basis, to generatemoredata regarding sinusitis resolution for anadditional study, resulting in a greater numberof follow-up scans. Some animals resolvedtheir sinusitis more quickly than others andfurther scans were not obtained once themax-

il lary sinus returned to normal. Animals werefoll owed for a maximum of 21 days afterinoculation. A total of 27 follow-up CT and 89follow-up MRI scans wereobtainedpostinocu-lation.

CT and MRI Sinus Opacification Scoring

Two of the authors (JK and MC) indepen-dently scored each imaging study. The inde-

CT VERSUS MRI OF ACUTE BACTERIAL SINUSITIS 299



pendent reviewers estimated percent opacifi-cation of the maxillary sinus for each of thecontiguousscans. Theaverage opacifi cation of theentire maxillary sinus was then calculatedand given a score based on the percentage of

opacification. These authors then graded left and right

maxillary sinuses for percent opacificationwith 1 for less than 10% opacification, 2 for10% to 19% opacifi cation, 3 for 20% to 29%opacification, 4 for 30% to 39% opacification,5 for 40% to 49% opacification, 6 for 50% to59% opacification,7 for 60% to69% opacifica-tion, 8 for 70% to 79% opacification, 9 for80% to 89% opacification, and 10 for 90% orgreater opacification. Thi s produced a scale of 1 to 10 for sinusitis scores.

Statistical Methods

Cohen’s kappa correlation for agreementwas used for indi vidual CT reviewer and MRIreviewer agreement of sinusitis scoring. AZ-score was then used to test for interobserver

differences between kappa correlations. Meanscan times were calculated for CT and MRI,and a standard t test was used to analyzedifferences between means. Wi th 95% confi-dence intervals used for scan times, cost per

scan comparisons were made between imag-ing techniques based on $140/hr for CT, and$75/hr for MRI. These rates for scanner usewereinstitutional research charges.

RESULTS

Figures 1 and 2 show selected radiologicviews that are representative images of therabbit paranasal sinuses before ostial occlu-sion and inoculation. Figures 3 and 4 show CTand MR images of sinus opacification afterostial occlusion and sinus inoculation.

As shown in Table 1, the Cohen’s kappacorrelation coefficient for agreement betweenthe 2 CT reviewers was 0.6816 and for MRI,0.3584. TheZ-scorecomparing thekappacoef-ficientswas statistically signifi cant (P Ͻ .0001)indicatinggreater interobserveragreement wi th

Fig 1. (A) CT scan of anterior maxillary sinus (arrow)—preinoculation. (B) MRI scan of anterior maxillary sinus(arrow)—preinoculation.

KERSCHNER ET AL300



CT imaging in the interpretation and subse-

quent scoring of sinusitis progression.Mean scan times and 95% confidenceinter-

vals for CT and MRI are shown in Table 2.Mean scan time for CT was 2.5028 minutesand 29.0567 minutes for M RI. Scan time 95%confidence intervals for CT and MRI tech-niques were 2.2352 to 2.7704 minutes, and26.7441to 29.4463minutes, respectively.Thus,approximately 25 additional minutes wererequired to obtain M RI versus CT images peranimal per scan. A t test for unequal variancesfound mean scan times to be signifi cantlydifferent (P Ͻ .0001). By using these intervals

combined with cost per hour of each tech-nique, cost per scan ranged from $5.21 to$6.46 and $33.43 to $36.81 for CT and MRItechni ques, respectively.

DISCUSSION

The rabbit model of BS was first proposedby Hilding in 1941.11 It has since been usedeffectively as a method for in vivo analysis of

BS. With this model, investigators have de-

scribed histologic changes in sinus mucosa,bacterial virulence, mucociliary flow character-istics, and surgical healing associated withexperimentally induced BS.1-4,12 This institu-tion recently reported successful CT imagingof reversible sinus inflammation i n the rabbitmodel after temporary maxillary ostial occlu-sion and bacterial inoculation.6 Critical re-view of peer-review grant proposals with thistechnique generated conflicting opini ons re-garding the value of CT and M RI in sinusitisresearch. The paucity of published data com-paring these2 techniques prompted this inves-

tigation. The 2 imaging methods were com-pared by using identical protocols forproducing reversible, experimental BS. Com-parison of methods involved analysis of scanreviewer agreement (precision), and the costand time (efficiency) associated with eachmethod.

CT deli neates, in true anatomic cross-sections, the intricate anatomical bony frame-work of the sinuses and allows assessment of

Fig 2. (A) CT scan of posterior maxillary sinus (short arrow), and ethmoid sinus (long arrow)—preinoculation. (B)MRI scan of posterior maxillary sinus (short arrow), and ethmoid sinus (long arrow)—preinoculation.




thesubtleair-boneor tissue-boneinterfaces.13-15

In the case of the paranasal sinuses, it is idealfor visuali zing complex areas such as theosteomeatal complex ethmoid sinuses.16 Thesecharacteristics, along with an increased avail-ability and reduced cost, have made CT themodali ty of choice for analyzingtheparanasalsinuses in most clini cal situations.

These same quali ties have also made CTvaluable for sinusitis research. A s a noninva-sive tool, it all ows for repeated measures of sinus inflammation progression or resolutionwithout disturbing the experimentally estab-lished sinus cavity environment. The rabbit

model has paranasal sinus anatomy that issomewhat more complex than in humans inthat the superior and posterior portions of themaxillary sinuscan be difficult to differentiatefrom the ethmoid sinuses. CT permits theseareas to be precisely assessed wi th regard todegree of sinus opacifi cation.

A clinical disadvantage of CT is ionizingradiation exposure. Thi s factor is notof signifi -

cant concern in thecurrent model of rabbit BS,

but could havei mplicationsi n clinicall y basedhuman studies or i n animal studies designedfor long-term survival.17 CT also provides li m-ited tissue-fluid discrimination. Although thereare inherently different attenuation values fortissue and fluid, there is considerable overlapin these values with mucoid secretions andinflamed tissue mucosa. This overlap makesfor imprecise image margins when these pro-cesses occur i n close proximity.7,8 This studyevaluated overall maxil lary sinus opacifi ca-tion, which encompasses both fluid and soft-tissue (mucosal) components.

MRI also all ows for true anatomic cross-section assessment of theparanasal sinuses. Incontrast with CT, MRI technology offers thepotential advantage of improved tissue-fluidinterface discrimination. Thi s difference i spossible by specifi c evaluation and detectionof bonded hydrogen molecules within sub-stances, as well as their relaxation times (T1

and T2) in response to various magnetic pulse

Fig 3. (A) CT scan of opacified anterior maxillary sinus (arrow)—postinoculation. (B) MRI scan of opacifiedanterior maxillary sinus (arrow)—postinoculation.

KERSCHNER ET AL302



sequences.7 This possibili ty has led to some

investigations that used MRI to delineate thecomponents of sinusitis including mucosaltissue changes and fluid secretion.18

A custom surfacecoil with specific configu-ration was constructed for this study and TR/T E settings were used to maximize signalto noiseratio. Reviewersfound that differentia-tion could not be made between mucosalinflammation and secreted mucous or fluid inthis study. Theimagespin echo sequenceusedwas predominantly T2-weighted in order to

minimize susceptibil ity effects; however, it is

unclear as to how much of an effect the fieldstrength influenced image contrast. Future

studies are warranted with this model to fur-ther assess the abili ty to deli neate tissue-fluid

interfaces as differentiation between mucosalthickening and secretions could provide addi-tional data for understanding of the patho-physiology of BS.

Because of the difficulty in defining boneanatomy and maxil lary sinus detail with M Rimages, there was poorer agreement betweenreviewers in scoring sinus opacification com-pared with CT (Table 1). Thi s made MR less

precise i n evaluating sinus opacifi cation, asone measure of a tool’s precision is interob-server consistency in makingmeasurements.19

In addition, signifi cantly more scan time wasrequired as compared with CT (Table 2). Fromthe standpoint of investigative protocols, thisadditional time to obtain MR images posesgreater anesthesia-related risksfor animal mod-els. Perhaps of even greater signifi cance, the

Fig 4. (A) CT scan of opacified posterior maxillary sinus (short arrow), and ethmoid sinus (long arrow)—postinoculation. (B) MRI scan of opacified posterior maxillary sinus (short arrow), and ethmoid sinus (longarrow)—postinoculation.

TABLE 1. CT and MRI Reviewer Agreement

Cohen’s

Kappa ()Correlation

Coefficient

Standard

Error Z-score*

CT scan (N ϭ 72) 0.68 .0693

4.13†MRI scan (N ϭ 210) 0.36 .0384

*Test for equality of Kappa statistics.†P Ͻ .0001.




increased time adversely effects experimentaldesign and feasibility in the research setting,as protocols often require multipl e subjectsreceiving multiple scans. Measurements thatrequire significantly longer timeto obtain maynot be able to be incorporated in trials requir-ing repeat measurements on a large number of

animals.Cost of any experimental tool is also asignificant consideration for any investigator.Even with theuse of fast spin-echo sequences,it would be unlikely that faster image acquisi-tion time would offset the expense of theinstrument. Justifi cation of increased timeandexpense for MRI would bereasonable if futureinvestigations provide clear advantages in mea-sures of sinusitis or understanding of experi-mental pathophysiology.

CONCLUSION

CT and M R imaging are noninvasive meth-ods of monitoring theprogression, resolution,or anatomical variations associated with para-nasal sinusitis and can besuccessfully used inthis animal model of sinusitis. This studyshows the usefulness of the New Zealandwhite rabbit as an in vivo model for thecomparison of CT versus MR image modali tiesduring the course of experimental sinusitis.For experienced sinus image reviewers, CTwas found to be both more precise and moreefficient than M R i maging for in vivo parana-

sal sinus i maging. Changing technology suchas the use of spiral CT, functional contrast-enhanced, or improved customization of MRIdesign may improve the value of theseinstru-ments as measures of sinusitis in the future.However, with the current study design, CT isa more effective tool asa noninvasive measureto assessthe complex eventsinvolved in sinus-itis progression and resolution.

ACKNOWLEDGMENTS

The authors thank Deborah L. Donahoe,

LATG, Otolaryngology Surgery, and BrianSpar-land, Department of Biophysicswithout whose

assistance this study could not have been

completed.

REFERENCES

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TABLE 2. Mean Scan Times Associated and Costs per Scan

MeanMinutes

StandardError t Test*

Scan Time 95%Confidence Interval

Cost per Scan (FromConfidence Interval)

CT scan (N ϭ 36) 2.58 0.1318 2.2352-2.7704 $5.21-$6.46Ϫ36.8794†

MRI scan (N ϭ 105) 28.09 0.6812 26.7441-29.463 $33.43-$36.81

*t test for difference in mean scan time (unequal variances).

†P Ͻ .0001.

KERSCHNER ET AL304



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