the prevalence of incidental findings on magnetic resonance ... · web viewword count: 2461...

Incidental findings on head MRI in patients with cognitive symptoms

Incidental findings identified on head MRI for investigation of cognitive impairment: a retrospective review

Stella Andrea Glasmacher1, Hannah Sam Thomas1, Lucy Stirland2, Tim Wilkinson3,4, Jane Lumsden3, Gavin Langlands3, Briony Waddell5, Guy Holloway6,7, Gerard Thompson3, Suvankar Pal3,7*

1) College of Medicine and Veterinary MedicineUniversity of Edinburgh47 Little France CrescentEdinburgh, United Kingdom

2) Division of Psychiatry, University of EdinburghKennedy TowerRoyal Edinburgh HospitalMorningside TerraceEdinburgh, United Kingdom

3) Centre for Clinical Brain SciencesChancellor’s Building49 Little France CrescentEdinburgh, United Kingdom

4) Usher Institute of Population Health Sciences and InformaticsUniversity of Edinburgh9 Little France RoadEdinburgh, United Kingdom

5) Department of NeurologyNinewells HospitalDundee, United Kingdom

6) Department of Old Age Psychiatry NHS LothianMorningside Royal Edinburgh HospitalEdinburgh, United Kingdom

7) Anne Rowling Regenerative Neurology ClinicRoyal Infirmary of Edinburgh49 Little France CrescentEdinburgh, United Kingdom

*Corresponding authorSenior Clinical Lecturer in Neurology & Honorary Consultant Neurologist, Centre for Clinical Brain Sciences, Chancellor’s Building, 49 Little France Crescent, EdinburghEdinburgh Email: [email protected] Phone: 0044 7940 230846

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mailto:[email protected]


Abstract

Introduction: Incidental findings are common in presumed healthy volunteers but are infrequently

studied in patients in a clinical context.

Objective: To determine the prevalence, nature, and management implications of incidental findings

on head MRI in patients presenting with cognitive symptoms, and to quantify and describe

unexpected MRI abnormalities that are of uncertain relevance to the patient’s cognitive symptoms.

Methods: A single-centre retrospective review of patients attending a regional early-onset cognitive

disorders clinic between March 2012 and October 2018. Medical records of consecutive patients who

underwent head MRI were reviewed. Unexpected MRI findings were classified according to their

severity and likelihood of being incidental. Markers of small vessel disease and cerebral atrophy were

excluded.

Results: Records of 694 patients were reviewed (median age 60 years, 49.9% female), of whom 514

(74.1%) underwent head MRI. 54% of patients received a diagnosis of a neurodegenerative disorder.

Overall 111 incidental findings were identified in 100 patients of whom 18 patients (3.5%, 95%CI

2.2%, 5.6%) had 18 incidental findings classified as requiring additional medical evaluation. 82

patients (16%, 95%CI 13.0%, 19.5%) had 93 incidental findings without clearly defined diagnostic

consequences. 17 patients (3.3%) underwent further investigations, 14 patients (2.7%) were referred

to another specialist clinic and three patients (0.6%) were treated surgically. Two patients had MRI

findings of uncertain relevance to their cognitive symptoms, necessitating prolonged clinic follow-up.

Conclusion: Incidental findings are common in patients with cognitive impairment from this large

clinic-based series; however, few required additional medical evaluation. These data could help

inform discussions between clinicians and people with cognitive symptoms regarding the likelihood

and potential implications of incidental imaging findings.

Keywords: incidental findings, magnetic resonance imaging, cognitive impairment, early-onset

dementia, brain, Alzheimer’s dementia

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Introduction

Incidental findings are previously unrecognised abnormalities with potential clinical relevance that are

detected by chance, and are not related to the reason for the examination [1]. They are common in

presumed healthy research participants undergoing head magnetic resonance imaging (MRI) [2-11];

however, there is paucity of prevalence data on patients in clinical settings. In contrast to presumed

healthy volunteers attending research imaging, patients undergoing MRI in a clinical context are

systematically assessed for relevant symptoms, allowing investigators to judge the extent to which an

imaging finding is likely to be incidental. Recent qualitative research suggests that some presumed

healthy volunteers view imaging research as a “health check” to investigate undeclared but potentially

relevant physical symptoms [12]. It is thus possible that, in the absence of contextual information,

imaging findings related to underlying symptoms could be misinterpreted as representing incidental

findings in presumed healthy volunteers. Research on incidental findings in patients in a defined

clinical context could thus complement the growing body of imaging literature on presumed healthy

volunteers. To date, the prevalence of incidental findings has not been examined in patients presenting

with symptoms suggestive of dementia, for whom head MRI is a recommended investigation [13].

The use of MRI is especially valuable in the identification and quantification of global and regional

cerebral atrophy, vascular burden, and exclusion of mass lesions. Data on incidental findings in this

population could inform discussions between patients and clinicians prior to MRI. The aims of this

study are to investigate the prevalence, nature, and management implications of incidental findings

identified on head MRI in patients presenting with cognitive symptoms, and to quantify and describe

unexpected MRI abnormalities that are of uncertain relevance to the patient’s cognitive symptoms.

Methods

The Anne Rowling Regenerative Neurology cognitive disorders clinic is an interdisciplinary tertiary

referral centre for specialist evaluation of patients with suspected early-onset or atypical dementias

residing in South East Scotland. Data were extracted from electronic patient records of consecutive

patients who attended the clinic over a six-year period between March 2012 and October 2018.

Patients underwent 1.5 T head MRI on various standard clinical systems within the NHS in South

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East Scotland. Sequence protocols varied by local practice and over time, but all included a T1-

weighted image (axial or sagittal spin echo or SPGR volumetric), an axial T2w spin echo image, an

axial echo planar diffusion weighted image, and an axial spin echo or volumetric FLAIR image. In a

proportion of cases, gradient echo imaging was acquired. MR images were interpreted by consultant

radiologists. The following imaging findings were specified a priori as not being incidental in our

study population due to their frequent association with cognitive impairment: global or regional

cerebral atrophy, ventricular enlargement, white matter hyperintensities suggesting small vessel

disease, microbleeds, silent infarcts, and gliosis. The classification system by Hegenscheid [14],

Bamberg [15] and Langner [16] was used to categorise incidental findings according to severity as

follows: category I/non-reportable (normal anatomical variations or incidental findings without

clearly defined diagnostic consequences); category II/reportable (incidental findings requiring

additional medical clarification); category III/actionable (incidental findings requiring urgent medical

clarification). Abnormalities considered to represent a finding requiring additional medical

clarification were classified as category II/reportable even if subsequent imaging did not confirm the

initial suspicion. Findings were classified according to their likelihood of being incidental as follows:

A: finding is most likely to be incidental; B: finding is more likely to be incidental but contribution to

cognitive symptoms cannot be excluded; C: finding is equally likely to be incidental or related to the

cognitive symptoms experienced by the patient. Data were extracted from electronic records by one

author (SAG); data on patients with incidental findings and MRI reports on all patients were

independently extracted by a second author (HST). Inter-rater reliability between independent data

extractors was calculated using the kappa statistic. A two-tailed Chi-square test was used for

significance testing of proportions. The “two-step” cluster analysis method was used to gauge

whether, statistically, patients with category II/reportable incidental findings represent a “cluster” that

differed from the remaining patient population with regards to the following variables: reporting

radiologist, age, sex and the presence of a neurodegenerative condition. The log-likelihood method

was used for distance measure. The relative importance of the presence of a category II/reportable

incidental finding in estimating a model using the above variables was reported using the predictor

importance criterion. Values can range between 0 and 1 where a value of 1 indicates high predictor

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importance. A p-value <0.05 was considered statistically significant. All data are reported as effect

estimate with 95% confidence intervals (CI). Data were analysed using GraphPad Prism® version 8

and IBM® SPSS® version 24.

Results

The median age of the study population was 60.5 years (IQR 64-53) and 346 patients (346/694,

49.9%) were female. Records of 694 patients were reviewed, of whom 514 (74.1%) underwent head

MRI. Of those who underwent head MRI, 280 patients (280/514, 54.5%) had a neurodegenerative

disorder. 109 patients (109/514, 21.2%) had conditions such as functional disorders, subjective

cognitive impairment, depression, anxiety, multifactorial cognitive impairment, or medication-related

cognitive impairment. There were 111 incidental findings in 100 patients; no patient had more than

two incidental findings. Eighteen patients (18/514, 3.5%, 95%CI 2.2%, 5.6%) had 18 category

II/reportable findings and 82 patients (82/514, 16.0%, 95%CI 13.0%, 19.5%) had 93 category I/non-

reportable findings. No patient had a category III/actionable finding. The prevalence of category II

incidental findings is summarised in Table 1. There were no statistically significant differences in age

(p=0.75) or sex (p=0.56) between patients without incidental findings or category I findings, patients

with category II findings, and patients who did not undergo MRI. Similarly, the predictor importance

of the presence of a category II/reportable incidental finding was 0, indicating that patients with

category II/reportable incidental findings did not substantially differ from the remaining patient

population with regards to reporting radiologist, age, sex and the presence of a neurodegenerative

disorder. 180 patients lacked MRI data because imaging was not clinically indicated (143/694,

20.6%), the patient declined MRI (14/694, 2.0%), the patient was claustrophobic (8/694, 1.1%), MRI

was contra-indicated (7/694, 1.0%), or performed externally and the imaging information was

unavailable (3/694, 0.4%). In five patients (5/694, 0.7%) the reason was unclear. Among those who

did not undergo MRI, 122 patients (122/180, 67.8%) had previously undergone head computed

tomography (CT), of whom 27 patients (27/122, 24.1%) were identified with 28 incidental findings.

Of these, five were category II/reportable findings (3 cerebral aneurysms, 1 colloid cyst, 1 pituitary

adenoma). This figure does not differ significantly to the prevalence of category II/reportable

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incidental findings on head MRI (p=0.75). The inter-rater reliability between the two independent

data extractors was excellent at 0.95 (0.94, 0.96).

Referral and clinical management of incidental findings

Seventeen patients (17/514, 3.3%) underwent additional investigations, of whom 15 (15/514, 2.9%)

had a category II/reportable incidental findings. Each patient had a mean of 2.4 (SD 2.3)

investigations, equalling a total of 40 further investigations. Fourteen patients (14/514, 2.7%) were

referred for consultation with another specialist, four (4/514, 0.78%) were discussed with another

specialist and one was advised to consult a dentist. The most common specialties for onward referral

were Neurosurgery (n=6), Otolaryngology (n=4), Endocrinology (n=3), Ophthalmology (n=2) and

Maxillofacial surgery (n=1); all referrals were non-urgent. Follow up duration varied between one

consultation and 48 months and patients who were referred attended a mean of 2.9 (SD 3.5) specialty

appointments. In eight patients (8/514, 1.6%) an incidental finding resulted in prolonged follow-up in

the cognitive clinic. Three patients (3/514, 0.58%) received surgical treatment for an incidental

finding: one patient underwent stenting and embolisation of an unruptured cerebral aneurysm and one

patient underwent a thyroidectomy for a mixed solid/cystic thyroid nodule. One patient underwent

nasal septoplasty for a category I/non-reportable finding but later admitted to symptoms of nasal

obstruction. There were no surgical complications. A dementia diagnosis was the reason for the

adoption of a more conservative management strategy in two patients. Both patients were discharged

from clinic follow up and did not undergo additional investigations which would normally be offered

for their incidental finding (Warthin’s tumour and retro-bulbar orbital mass).

Imaging findings of uncertain significance to the patient’s cognitive symptoms

Two findings were classified as category B and the remainder as category A. One patient presented

with fluctuating short-term memory problems and mild problems in judgement. They were diagnosed

with multifactorial cognitive impairment due to a combination of medication effects, anxiety, and

depression. MRI revealed a right frontal low-grade glioma. This finding was disclosed to the patient

in a clinic consultation by the responsible consultant and is managed with clinical surveillance and

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interval scanning under Neurosurgery. They were followed up in the cognitive clinic for 29 months

following disclosure of the incidental glioma, during which time there was evidence of worsening

mood and memory associated with a drop in their Addenbrooke’s III Cognitive Examination score by

eleven points. The impression was that this deterioration in cognitive function was multifactorial in

nature, with anxiety resulting from the disclosure of the glioma being a contributing factor; however,

it is not possible to exclude an effect of the glioma on their cognitive function. It was considered that

the glioma was unlikely to explain the above constellation of symptoms, in particular, the day-by-day

fluctuation in their cognition but it may account for their mild problems in judgement. Another patient

presented with an 8-year history of difficulties in both short- and long-term memory, speech

disturbance and low mood, in keeping with mild cognitive impairment. MRI showed multiple foci of

elevated T2 and reduced T1 signal involving the periventricular, subcortical, and juxta-cortical white

matter in keeping with demyelination. Repeat imaging showed static appearances; however, on

follow-up in the clinic they reported a band-like sensory disturbance across their thoracic wall. They

consequently underwent MRI of the cervical and thoracic spine, which showed no convincing

evidence of demyelinating cord plaques and no cord compression or myelopathy. In the absence of

motor symptoms and signs, a diagnosis of a radiologically isolated syndrome of central nervous

system demyelination was considered more likely than an isolated slowly evolving cognitive

presentation of multiple sclerosis but this could not be excluded with absolute confidence and the

individual remains under ongoing follow up.

Discussion

We have investigated the prevalence, nature, and management implications of incidental findings on

head MRI in patients presenting to an inter-disciplinary regional cognitive disorders clinic. Our study

population comprised consecutive and unselected outpatients who were heterogeneous in clinical

demographics and diagnosis. The prevalence of category II/reportable findings we report (3.5%) is

higher than the prevalence of potentially serious incidental findings reported in a recent

comprehensive meta-analysis on presumed healthy volunteers (1.3%) [2]. Of note, we also included

incidental findings on high cervical sections (1/18; 5.6%) in our prevalence estimate; further, several

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category II/reportable incidental findings were not regarded as potentially serious (7/18; 38.9%).

Accounting for the above factors, the difference in the prevalence of incidental findings is likely to be

due to chance. Nonetheless, non-serious findings that require further clarification may result in

additional anxiety for patients and costs to the healthcare system. Several previous studies included

markers of small vessel disease such as white matter hyperintensities, microbleeds and silent infarcts

in the definition of incidental findings [5,9,10]. We decided a priori to exclude markers of small

vessel disease and atrophy, which are commonly related to memory impairment [17] and therefore

difficult to refute in terms of causality. The prevalence of incidental findings in our study was

considerably lower compared to previous studies on patients in a clinical context, which often

regarded incidental finding as any “abnormal” MRI report [18-20]; conversely, we have taken a more

pragmatic approach to the classification of incidental findings. Given the relative rarity of individual

incidental findings we are not able to comment on whether their prevalence is more or less common in

people with cognitive impairment compared to the general population.

Two patients were identified with MRI findings that were most likely to be incidental but where a

contribution to the cognitive symptoms by the finding could not be excluded. These cases illustrate

the uncertainty that can result from such findings, necessitating prolonged follow up in the cognitive

clinic. Several patients underwent CT rather than MRI for diagnosis of dementia; often, these were

comparatively older patients with severe dementia [21]. The ethical aspects of managing incidental

findings should be considered carefully in patients with dementia, where prognosis is likely to be

limited. This is especially problematic in patients with severe dementia who do not have capacity to

decide on management; in many cases, a more conservative strategy is appropriate.

Limitations

Our imaging protocols were heterogenous and several different MRI scanners were used, images were

reviewed by different radiologists and findings were retrospectively extracted from non-structured

radiology reports. However, spatial resolution was the same for all patients (1.5T) and there was no

evidence of a clustering effect with regards to the radiologist reporting on category II/reportable

incidental findings. Some radiologists may not have included category I/non-reportable findings in

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their report [22] where there was potential for such findings to be misinterpreted by the referring

clinical team. Further, the process of classifying the severity and nature of MRI findings is inherently

subjective and there is no universally accepted classification system. All the above factors may have

resulted in underreporting of incidental findings; however, the prevalence of incidental findings in our

study was in keeping with previous studies on presumed healthy volunteers.

Our study conditions are representative of those encountered by practising clinicians across most

Western countries. It should, however, be noted that our study population comprises comparatively

younger patients [4,6,10,23] attending a tertiary referral centre; thus, our results cannot readily be

extrapolated to older adults.

Implications for practice

Head MRI is recommended by clinical guidelines for the investigation of patients presenting with

symptoms of dementia [13]. However, a substantial proportion of patients attending cognitive clinics,

including ours, have a suspected diagnosis of subjective cognitive impairment or a psychiatric

disorder. Here, the risk-benefit ratio of head MRI is uncertain, and our data can be used to weigh up

the risks and benefits of head MRI in this context. Further, our data can be used to support discussions

with patients on the risk of incidental findings and the attendant necessity for further investigations

and treatment regardless of the presumed cognitive diagnosis.

Conclusion

Incidental findings on head MRI are common in patients presenting with cognitive symptoms

although only a small proportion of findings (3.5%) were classified as requiring additional medical

clarification. Our findings could help clinicians in discussing incidental findings with patients prior to

MRI. Additionally, our data could be used to weigh up the risks and benefits of head MRI in patients

with a suspected diagnosis of subjective cognitive impairment or a psychiatric disorder where the

risk-benefit ratio of head MRI is uncertain.

Acknowledgements

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None

Statement of Ethics

All procedures performed in studies involving human participants were in accordance with the ethical

standards of the institutional and/or national research committee and with the 1964 Helsinki

declaration and its later amendments or comparable ethical standards. Ethics approval was obtained

for the Rowling Care database from which patients were drawn and for which patients gave written

consent (South East Scotland Research Ethics Committee reference 16/SS/0156).

Disclosure Statement

Lucy Stirland is funded by the Medical Research Foundation (MRF) and Medical Research Council

(MRC) through the PsySTAR, Psychiatry: Scottish Training in Academic Research programme, grant

number MR/J000914/1. Tim Wilkinson is funded by an MRC Clinical Research Training Fellowship

(MR/P001823/1). The remaining authors report no conflicts of interest.

Funding Sources

No funding was obtained for this study.

Author contributions

SAG, GT and SP designed the study; LS, TW, GL, BW, JL and GH contributed to data acquisition;

SAG and HST extracted data from electronic records; SAG, HST, GT and SP analysed the data; SP

supervised the project; SAG drafted the manuscript; all authors reviewed the manuscript for important

intellectual content and approved the final version.

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Table 1. Prevalence and type of category II/reportable incidental findings

N (%/514)

95% CIs Referred (n)

FurtherInvestigated (n)

Treated (n) Likelihood of finding being incidental

Vascular abnormalities (total)Cerebral aneurysm (berry/fusiform) 2/1 (0.58) 0.15, 1.8 1 1 1 ACavernomas (multiple, no haemorrhage) 1 (0.19) 0.01, 1.3 1 A

CystsRathke’s cleft cyst 1 (0.19) 0.01, 1.3 1 1 A

Neoplasms Low grade glioma 1 (0.19) 0.01, 1.3 1 1 BMeningioma* 1 (0.19) 0.01, 1.3 1 1 AVestibular Schwannoma 1 (0.19) 0.01, 1.3 1 1 ADysembryoplastic neuroepithelial tumour (DNET)

1 (0.19) 0.01, 1.3 ** 1 A

Pituitary abnormality (haemorrhagic adenoma or haemorrhagic cyst)

1 (0.19) 0.01, 1.3 1 1 A

Retro-bulbar orbital mass 1 (0.19) 0.01, 1.3 1 AWarthin’s tumour 1 (0.19) 0.01, 1.3 1 1 A

Other intracranial abnormalitiesPossible demyelination 2 (0.39) 0.07, 1.6 2 A/BEncephalomalacia (initially unable to exclude DNET)

1 (0.19) 0.01, 1.3 1 A

Cerebellar abnormality*** 1 (0.19) 0.01, 1.3 1 AExtracranial

Periapical cyst 1 (0.19) 0.01, 1.3 AMixed solid and cystic thyroid cyst 1 (0.19) 0.01, 1.3 1 1 1 A

Total 18 (3.5) 2.2, 5.6 9 13 2Table 1 Prevalence and type of category II/reportable incidental findings. *A further patient had a meningioma which was heavily calcified and therefore classified as category I/non-reportable. **Already under regular Neurology follow- up. ***peripheral symmetrical band of T2 and FLAIR hyperintensity of unclear aetiology

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