Months backward test A review of its use in clinical studies

Copyright Information of the Article Published OnlineTITLE Months backward test: A review of its use in clinical studies AUTHORs James Meagher, Maeve Leonard, Laura Donoghue, Niamh O’Reg

Copyright Information of the Article Published Online

TITLE Months backward test: A review of its use in clinical studies

AUTHOR(s)

James Meagher, Maeve Leonard, Laura Donoghue, Niamh O’Regan, Suzanne Timmons, Chris Exton, Walter Cullen, Colum Dunne, Dimitrios Adamis, Alasdair J Maclullich, David Meagher

CITATION

Meagher J, Leonard M, Donoghue L, O’Regan N, Timmons S, Exton C, Cullen W, Dunne C, Adamis D, Maclullich AJ, Meagher D Months backward test: A review of its use in clinical studies World J Psychiatr 2015; 5(3): 305-314

different terms, provided the original work is properly cited and the use is non-commercial See:

http://creativecommons.org/licenses/by-nc/4.0/

that is commonly used in clinical practice It provides a convenient test of central proce-ssing speed and both focused and sustained attention This review of studies reporting its use

in clinical popu-lations identified many different approaches to administration and interpretation of the test Overall, cognitively intact adults can complete the test within 60 s without omission

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errors, such that failure to achieve this is strongly suggestive of cognitive dysfunction The sensitivity for neurocognitive disturbance in hospitalised patients is 83%-93% and repeated testing can identify deteriorating cognitive function over time.

Dementia

g Group Inc All rights reserved.

Months backward test: A review of its use in clinical studie s

James Meagher, Maeve Leonard, Laura Donoghue, Niamh O’Regan, Suzanne Timmons, Chris Exton, Walte

r Cullen, Colum Dunne, Dimitrios Adamis, Alasdair J Maclullich, David Meagher

James Meagher, Cognitive Impairment Research Group, Graduate Entry Medical School, University of Limerick, Limerick, Ireland Maeve Leonard, Laura Donoghue, Walter Cullen, Colum Dunne, Dimitrios Adamis, David Meagher, University of Limerick

Medical School, Limerick, Ireland

Maeve Leonard, Colum Dunne, Dimitrios Adamis, David Meagher, Cognitive Impairment Research Group, Centre for

Interventions in Infection, Inflammation and Immunity (4i), Graduate Entry Medical School, University of Limerick, Limerick,Ireland

Niamh O’Regan, Suzanne Timmons, Centre for Gerontology and Rehabilitation, St Finbarr’s Hospital, Cork, Ireland

Chris Exton, Department of Computer Sciences, University of Limerick, Limerick, Ireland

Walter Cullen, School of Medicine and Medical Science, University College Dublin, Dublin, Ireland

Dimitrios Adamis, Sligo Mental Health Services, Sligo, Ireland

Alasdair J Maclullich, Edinburgh Delirium Research Group, University of Edinburgh, Edinburgh EH8 9XD, United KingdomDavid Meagher, Department of Psychiatry, University Hospital Limerick, Limerick, Ireland

Author contributions: All authors contributed to this paper

Correspondence to: David Meagher, Professor, Cognitive Impairment Research Group, Centre for Interventions in Infection,

Inflammation and Immunity (4i), Graduate Entry Medical School, University of Limerick, Castletroy, Limerick, Ireland.david.meagher@ul.ie

Telephone: +353-61-202700

Received: March 5, 2015 Revised: June 9, 2015 Accepted: June 30, 2015

Published online: September 22, 2015

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AIM: To review the use of the Months Backwards Test (MBT) in clinical and research contexts

METHODS: We conducted a systematic review of reports relating to the MBT based upon a search of PsychINFOand MEDLINE between January 1980 and December 2014 Only reports that specifically described findings pertaining

to the MBT were included Findings were considered in terms of rating procedures, testing performance, psychometricproperties, neuropsychological studies and use in clinical populations

RESULTS: We identified 22 data reports The MBT is administered and rated in a variety of ways with very littleconsistency across studies It has been used to assess various cognitive functions including focused and sustainedattention as well as central processing speed Performance can be assessed in terms of the ability to accuratelycomplete the test without errors (“MB accuracy”), and time taken to complete the test (“MB duration”) Completiontime in cognitively intact subjects is usually < 20 s with upper limits of 60-90 s typically applied in studies Themajority of cognitively intact adults can complete the test without error such that any errors of omission arestrongly suggestive of cognitive dysfunction Coverage of clinical populations, including those with significantcognitive difficulties is high with the majority of subjects able to engage with MBT procedures Performancecorrelates highly with other cognitive tests, especially of attention, including the digit span backwards, trailmakingtest B, serial threes and sevens, tests of simple and complex choice reaction time, delayed story recall andstandardized list learning measures Test-retest and inter-rater reliability are high (both > 0.90) Functionalmagnetic resonance imaging studies comparing the months forward test and MBT indicate greater involvement ofmore complex networks (bilateral middle and inferior frontal gyri, the posterior parietal cortex and the left anteriorcingulate gyrus) for backwards cognitive processing The MBT has been usefully applied to the study of a variety

of clinical presentations, for both cognitive and functional assessment In addition to the assessment of majorneuropsychiatric conditions such as delirium, dementia and Mild Cognitive Impairment, the MBT has been used inthe assessment of concussion, profiling of neurocognitive impairments in organic brain disorders and Parkinson’sdisease, prediction of delirium risk in surgical patients and medication compliance in diabetes The reportedsensitivity for acute neurocognitive disturbance/delirium in hospitalised patients is estimated at 83%-93%.Repeated testing can be used to identify deteriorating cognitive function over time

CONCLUSION: The MBT is a simple, versatile tool that is sensitive to significant cognitive impairment.Performance can be assessed according to accuracy and speed of performance However, greater consistency inadministration and rating is needed We suggest two approaches to assessing performance - a simple (pass/fail)method as well as a ten point scale for rating test performance (467).

Key words: Cognition; Assessment; Months backward test; Delirium; Dementia

© The Author(s) 2015 Published by Baishideng Publishing Group Inc All rights reserved.

Core tip: The months backward test is a brief test of cognitive function that is commonly used in clinical practice It

provides a convenient test of central processing speed and both focused and sustained attention This review ofstudies reporting its use in clinical populations identified many different approaches to administration andinterpretation of the test Overall, cognitively intact adults can complete the test within 60 s without omissionerrors, such that failure to achieve this is strongly suggestive of cognitive dysfunction The sensitivity forneurocognitive disturbance in hospitalised patients is 83%-93% and repeated testing can identify deterioratingcognitive function over time

Meagher J, Leonard M, Donoghue L, O’Regan N, Timmons S, Exton C, Cullen W, Dunne C, Adamis D, Maclullich AJ, Meagher D

Months backward test: A review of its use in clinical studies World J Psychiatr 2015; 5(3): 305-314 Available from: URL:

http://www.wjgnet.com/2220-3206/full/v5/i3/305.htm DOI: http://dx.doi.org/10.5498/wjp.v5.i3.305

INTRODUCTION

The months backwards test (MBT), also known as the months of the year in reverse order (MOYR) test is a rapid(< 2 min) and simple to administer test of cognitive function that is widely used at the bedside It has beendescribed as primarily a test of attention[1-3], as well as a test of concentration[4], working memory, executivefunction[5,6], cognitive flexibility[7] and central processing speed[8] The MBT has been applied to study cognitivefunction in Parkinson’s disease[9], to stage dementia[10-12], assess concussion in sports[13-15], predict medicationadherence in patients with diabetes[6], and predict delirium risk[5] The MBT has particular utility in screening for

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delirium and related disorders in hospitalised patients[16-18]

We conducted a review of the test to determine: (1) the ways in which is administered and rated; (2) itspsychometric properties, including comparison with other simple bedside tests of cognition; and (3) findings fromits use in clinical and research studies

MATERIALS AND METHODS

We searched PsychINFO and MEDLINE for papers reporting the use and characteristics of the MBT, searching from

1980 onwards using the search terms “Months reverse” or “months backward” and “test”, with human and Englishlanguage limits Because the MBT is a component of several composite test batteries, the review was limited toreports where the MBT was described separately, so that its application and findings could be individually reported

“Months reverse” or “months backward” and “test” with English language limits identified 502 articles of which

17 were relevant to the review Additional articles (n = 5) were identified by reviewing the references of these

reports and checking for similar work by the authors and subsequent citations (Figure 1)

RESULTS

The 22 articles identified included descriptions of various ways that the test has been applied (including testingprocedures and interpretation of test performance), psychometric properties, and findings in a variety of differentpopulations

Testing procedures

The test requests the subject to recite the months of the year in reverse order starting with December, thenNovember, then October and so on, until the subject reaches January or cannot continue Some variants require

the patient to reach a particular month (e.g., July) rather than recite all twelve The test is often preceded by

asking the patient to recite the months forwards, indicating their capacity to engage and understand simple

commands (i.e., basic contextual awareness) In the reviewed papers, the MBT was mostly conducted at the bedside or in other routine clinical patient contacts (e.g., outpatient/memory clinic) It can be also be administered

by telephone (Ball et al[8], 1999) and versions are available in several languages

The test requires minimal formal training but must be explained clearly and logically to the subject (see Table 1for an example of test introduction and procedures) Basic training for testers usually includes an explanation ofprocedures, followed by observing the test being performed, and then being observed conducting it, to ensureclarity of explanation and consistent administration and interpretation However, training procedures are notaddressed in most reports

Where the test is timed, the patient is often asked to recite the months as quickly as possible[19] The taskcommences after the participant has confirmed that they have understood the instructions and are ready to start.There is less consistency as to how to respond to the patient who is struggling with the test in respect ofprompting or re-orientating them to the test Similarly, the number of discrete trials allowable to assess (best)performance is not consistently defined It is common for the rater to record the participant’s responses month bymonth to include omissions and commissions, as well as pauses (denoted by an underscore that corresponds withthe duration of delay)

The test typically takes 1-2 min, with cognitively intact patients usually completing the test within 20 s[19] Cut offtimes for completion of 60[20], 75[8], and 90 s[21] have been suggested to define an upper limit above which patientscannot successfully complete the test

Rating of performance

Table 2 details the approaches to MBT scoring adopted in the studies included in this review Performance can beassessed in two ways: (1) ability to accurately complete the test without errors (“MB accuracy”); and (2) timetaken to complete the test (“MB duration”) Most subjects under 65 years of age can readily complete the testwithout error[14,19,20], and therefore the duration to complete the test is more useful (measuring central processingspeed) in younger populations

“MB accuracy” assesses the capacity to complete the test, and how far subjects can reach without error and

with/without prompting Errors include: (1) omissions; (2) perseverations or stuttered responses (e.g.,

“September… September…August, July”); and (3) Commissions such as false positive errors (i.e., words that are

relevant to the task but incorrect such as July where June should be) and intrusion errors involving words orphrases that are not related to the task[22]

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In many cases, test performance is dichotimised into a positive or negative result according to specific criteriasuch as correctly reciting all months with minimal prompting (if under age 65 years) or reciting until July (if aged

65 or older)[16], completing either 7 consecutive correct iterations or 11 correct with no more than one mistake[20],omission of two or more months[21], or a total of two or more errors of any kind[7] In other testing procedures, anordinal scale of accuracy performance (ranging from 0-2) is used[9,23,24], while a continuous scale of accuracyperformance can be established according to the total number of errors[19] Lamar et al[25] used the Accuracy Index{= [1 - (false positive + misses)/(number of possible correct)] × 100} This algorithm yields a percentage scorewhereby patients obtaining a score of 100% correctly identified all targets without commissions or omissions

“MB duration” assessment varies considerably across studies and reflects the impact of factors such as age,gender and educational level on performance[13,19] The Wechsler Memory Scale - third edition (WMS-III)[23]

identifies four levels of performance - 0 (> 17 s), 1 (12-16 s), 2 (10-11 s), and 3 (1-9 s) Weintraub[26] suggests a

performance cut off of 16 s while Ball et al[8] rated performance on a time continuum up to a predetermined limit

of 75 s, with those unable to complete the sequence allocated a score of 75 s and no consideration given to errors

In other work, time limits of 60 s[20] and 90 s[21] have been applied

Other work has combined accuracy (1 point for > 1 error of any kind) and speed of completion (1 point ifcompletion time > 24 s) to rate performance on an ordinal scale (0, 1, 2)[27]

Performance in different populations

Studies have explored MBT performance in various populations, including examining the impact of age, genderand educational level upon results Typically, the MBT takes twice as long as reciting the MF in cognitively intactpersons, although this distinction is increased in subjects with mild cognitive impairment or establisheddementia[11] Halstead[28] in a seminal paper cited the discrepancy between forwards and backwards testperformance as evidence of “senile inelasticity” and a reduced capacity to inhibit the impulse to recite wellestablished patterns in their (usual) forwards manner In general, the MBT is a simple test that most participantscan complete without error, so that being unable to perform the task is unusual in younger adults and in thesepopulations is a sensitive indicator of impairment Indeed, as response accuracy is so high, the MBT has primarilybeen used to test processing speed test in cognitively intact individuals

Successful completion rates for the MBT have been reported for a range of populations Young et al[20] found

89% of high school student athletes could successfully complete the test Östberg et al[19] found 95% of logically intact adults completed the task without error, while the majority of the remaining participants made a

neuro-single error, with more than one error occurring in less than 1% of those tested Shehata et al[14] found that 92%

of university-level athletes could complete the MBT without error Ettlin et al[27] found that 8/70 patients withorganic brain lesions made errors (of any type) while all 48 neurologically intact subjects completed the test

without error Conversely, Jinguji et al[13] reported that one third of high school athletes could not complete thetest, with better completion rates in females and those aged 16-19 years compared with 13-15 years

The completion time for the MBT differs across reports In a community dwelling population aged over 65

years, Ball et al[8] found the MBT duration was 17 ± 10 s, increasing at four-year follow up to 25 ± 21 s Ettlin et

al[27] reported task completion times of 12.1 ± 11.4 in 48 neurologically intact individuals (mean age 40.4 ± 13.8)with much slower completion times for patients with frontal (33.1 ± 40.8) and non-frontal (21.6 ± 12.4) lesions

Ostberg et al[11] reported completion times of 9.6 ± 3.1 s in 66 elderly memory clinic attenders without identifiable

objective cognitive impairment Östberg et al[19] studied 216 neurologically intact adults and found a mean timefor completion of 11.6 ± 5.6 s Durations varied according to age and educational level from 9.0 ± 2.2 in the 30-

60 age category with greater (third level) educational exposure to 16.3 ± 8.1 in over 60 years old who had lowereducational attainments

Numerous studies have identified how MBT performance varies with age Östberg et al[19] found that peak

performance (MB duration) occurred in 30-60 year olds compared with younger and older age bands Ball et al[8]

found an exponential relationship between advancing age and MB duration, both cross-sectionally and

longitudinally Jinguji et al[13] found greater completion rates amongst 16-19 years old compared to 13-15 years

old Ostberg et al[11] found a weak association between age and MBT but not MFT performance in elderly memoryclinic attenders Although some work suggests a trend towards better test performance in females[13,14], otherstudies suggest similar MB accuracy[20] and MB duration[11,19] for otherwise similar male and female subjects

Psychometric properties

A key advantage of the MBT is that the universal nature of the content allows for excellent coverage, and

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performance can be studied in most patients from a variety of populations, including those with significantcognitive impairments[11,16] Because most normal elderly (typically > 95% in studies) can complete the testwithout difficulty[19,16], poor performance is very suggestive of abnormality Moreover, the lack of reliance on motor

or visual abilities reduces the impact of disturbances to these functions on performance Ostberg et al[11] foundthat only 6 of 234 memory clinic attendees could not be assessed with the MBT

The MBT has high concordance with many other cognitive tests, including the digit span backwards[13,29],trailmaking test B[29], serial threes and sevens[20], delayed story recall (WMS-R) and standardized list learningmeasures[29] In addition, concurrent validity with the MBT has been described for other cognitive tests including

culture fair Intelligence Quotient (r = 0.31; P < 0.02)[24], short-blessed test (r = 0.5)[8], trailmaking test B (r =

0.45)[8], and tests of simple (r = 0.52) and complex choice (r = 0.51) reaction time[8]

Test-retest reliability has been examined for both “MB accuracy” and “MB duration” Ball et al[8] found MBduration had excellent test-retest reliability (0.90) amongst 120 elderly community residents reassessed 1 wk to

10 d later, suggesting that it is an operationally stable measure Of note, at four-year follow-up, the time taken forthe MBT had increased considerably (as above) emphasising that it can also capture deteriorating cognitive

function over time Marinus et al[9] examined test-retest reliability (K = 0.44) for MB accuracy in 30 patients with

Parkinson’s disease after a 6 wk interval Östberg et al[19] found test-retest reliability of 0.82 for duration and 0.97for accuracy in 40 neurologically intact adults aged 18-80 assessed by periods separated by three weeks Theinter-rater reliability of the MBT between a neuropsychologist and a postdoctoral research fellow in patients with

traumatic brain injury was high (r = 0.95)[29]

Neuropsychological studies

The MBT engages a range of cognitive and perceptual faculties including hearing, speech, basic comprehension,the ability to focus and sustain attention, working memory and executive function The information involved is anautomatic word sequence that is non-novel and relatively universal - few patients have difficulties with theinformation content as it reflects culturally acquired factual knowledge The basic ability to recite MF can be used totest the ability to generate automatic speech in patients with dysphasia[30], while the MBT requires mental controland sustained attention in order to inhibit the impulse to recite the months in a forwards direction

The cognitive processes of attention and working memory are often conceptualised within a tripartite model[31]

where a central executive component controls a phonological loop (allowing subvocal rehearsal) and a visuospatialsketchpad (facilitating mental visualisation) Forwards processing is linked to procedural memory, while backwardsprocessing has greater engagement of working memory In addition, backwards processing has greaterinvolvement of visuospatial mechanisms[32] thought to reflect the role of visual imagery in transforming material intoreverse order by, for example, visualising the calendar and reading from bottom to top Neuroimaging studies offocal brain lesions and positron emission tomography studies of the neural elements that appear involved in

forwards vs backwards processing (using the digit span tests) indicate that backwards processing is linked to

greater activation of the dorsolateral prefrontal cortex bilaterally and recruitment of Broca’s area[33] The degree ofactivation increases with increasing task difficulty Increased activation of areas contributing to speech motor per-formance occurs during reverse rather than forwards recitation even though both tasks comprise the same wordsand behavioural data Moreover, there is typically a much higher volume of word production under forward testing.This indicates that engagement of these areas depends on the degree of automatization rather than on productionspeed of verbal utterances, and demonstrates the contribution of Broca’s area to the silent rehearsal process underreverse testing[34] However, other work[32] emphasises individual variability in the relative reliance upon visuospatial

vs subvocal mechanisms in task performance, including backwards tests.

Wildgruber et al[34] compared the response of neural networks during MF vs MBT using functional magnetic

resonance imaging Both tests were associated with activation of the left motor cortex, supplementary motor areaand temporo-parietal junction, while the MBT was associated with greater activation of the bilateral middle andinferior frontal gyri, the posterior parietal cortex and the left anterior cingulate gyrus These studies indicatinggreater involvement of more complex networks for backwards cognitive processing are further supported byevidence that tasks involving backwards processing are more susceptible to the effects of ageing[11,25]

Use of the MBT in clinical populations

The simplicity and convenience of the MBT has allowed its use in a range of clinical scenarios, including some whichrequire speed and portability of assessment procedures The MBT has demonstrated utility as a single or independentmeasure and as part of composite testing tools These studies include the use of the MBT in the assessment of

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