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Multiple Sclerosis Journal 26(9)

1026 journals.sagepub.com/home/msj

4. McDonald WI, Miller DH and Thompson AJ. Are magnetic resonance findings predictive of clinical outcome in therapeutic trials in multiple sclerosis? The dilemma of interferon-beta. Ann Neurol 1994; 36(1): 14–18.

5. Majumder S, Mondal T and Deen MJ. Wearable sensors for remote health monitoring. Sensors 2017; 17: 130. 6. Evenson KR, Goto MM and Furberg RD. Systematic

review of the validity and reliability of consumer-wearable activity trackers. Int J Behav Nutr Phys Act 2015; 12: 159.

7. Akhbardeh A, Arjona JK, Krysko KM, et al. Novel MS vital sign: multi-sensor captures upper and lower limb dysfunction. Ann Clin Transl Neurol. Epub ahead of print 26 February 2020. DOI: 10.1002/acn3.50988.

8. Midaglia L, Mulero P, Montalban X, et al. Adherence and satisfaction of smartphone- and smartwatch-based remote active testing and passive monitoring in people with multiple sclerosis: nonrandomized interventional feasibility study. J Med Internet Res 2019; 21: e14863.

9. Bove R, White CC, Giovannoni G, et al. Evaluating more naturalistic outcome measures: A 1-year smartphone study in multiple sclerosis. Neurol

Neuroimmunol Neuroinflamm 2015; 2(6): e162.

10. Block VJ, Bove R, Zhao C, et al. Association of continuous assessment of step count by remote monitoring with disability progression among adults with multiple sclerosis. JAMA Netw Open 2019; 2(3): e190570.

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SAGE journals

We should monitor our patients with wearable

technology instead of neurological examination

– No

Uğur Uygunoğlu and Aksel Siva

While the incidence of chronic neurological diseases remained stable over time, the prevalence increased particularly in the past 15 years and shifted to older ages. The main reason for this is the decline of mortal-ity which is apparent in the general population as well.1 The increased prevalence of neurological

dis-eases inevitably resulted in huge economic impacts for the health care system and, when considering the increased disability by aging this economic impact is relevant for patients and their caregivers as well. Therefore, in an effort to reduce the admittance and examination of patients, sophisticated technological devices have been developed in recent years. We increasingly see wearable devices in the form of smartphones, smartwatches, or smartrings, measuring our heart rhythm, blood pressure, sleep patterns, and other vital functions for popular use while enhancing awareness of what is going on in an individual’s body! Should we monitor our patients with wearable tech-nology instead of neurological examination? Should new technology replace the good old neurological examination? Should artificial intelligence replace the good old neurologist?

These are relevant questions that were raised and have been discussed a great deal in recent years! In our opinions, one of us being an older scholar and the

other one from the younger generation, our view is “no!”, at least not yet! So, why do we think as such? It is true that through 24 (or longer) hours of heart rhythm and blood pressure monitoring cardiologists can evaluate the cardiological status of their patients and make treatment decisions based on these find-ings. There are suggested wireless wearable sensors to monitor motor fluctuations in Parkinson’s disease patients that provide reliable quantitative information to be used for clinical decision making.2 In a number

of emerging studies, it was shown that wearable tech-nology may be used in monitoring gait, reveal gait compensations, unstable walking patterns, and fatigue in people with multiple sclerosis (MS).3,4 These

tech-nological advances enable objective and standardized patient assessments in the clinic and now are sug-gested to be used for out-of-clinic setting as well! Then how come we think that the neurological exam should remain our priority today?

First, while the three-dimensional motion analysis system seems to be the accurate system for evaluating the patients outside of the examination room, the widespread adoption of this system as a routine clini-cal tool is inconvenient due to the high cost, long preparation time, and requiring a specialist staff for operating these systems.5 Furthermore, these devices Multiple Sclerosis Journal

2020, Vol. 26(9) 1026 –1028 DOI: 10.1177/

1352458520908769 © The Author(s), 2020. Article reuse guidelines: sagepub.com/journals-permissions

Correspondence to:

A Siva

Department of Neurology, School of Medicine, Istanbul University-Cerrahpaşa, 34098 Istanbul, Turkey. akselsiva@gmail.com Uğur Uygunoğlu Aksel Siva Department of Neurology, School of Medicine, Istanbul University-Cerrahpaşa, Istanbul, Turkey

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journals.sagepub.com/home/msj 1027

are yet uncomfortable and impractical for long-term wear, and patients with cognitive impairment may not have the ability to fully understand the importance of these devices and how to use them properly.

Second, as the studies in MS mainly focused on the pace collected free-living data rather than gait varia-bility, the validity and reliability of these devices still need to be proven with comparative studies in large populations to determine within-person standard deviation, reproducibility, and predictive values. The reliability of devices varies with the degree of disabil-ity, and the findings may be insensitive to subtle changes early in the disease.6

A recent study that recruited relapsing-remitting mul-tiple sclerosis (RRMS) patients having Expanded Disability Status Scale (EDSS) score ⩽3.0 and with-out clinical evidence of gait deterioration revealed that gait and balance performance had progressively declined even in the absence of both acute clinical relapse and change in clinical status. However, as the authors had concluded, the follow-up duration of 12 months was too short and magnetic resonance imaging (MRI) data were lacking which may reveal active inflammation in patients who deteriorated over this period.7 Moreover, this deterioration might be

related to factors such as physical and psychological. Third, the following clinical situations clearly reveal two other areas where face-to-face evaluation is supe-rior to wearable technology:

1. Pseudo-relapse. A detailed history may reveal that a number of physical (i.e. too much work), psychological (i.e. mood changes), and biolog-ical (i.e. infections or metabolic changes) con-ditions may cause fluctuations on the functions of the person with multiple sclerosis (PwMS). For an experienced neurologist, many times the patient’s words will be sufficient and replace advanced technology which is still costly these days and at times may be misleading as this technology monitor changes independently from the underlying causes.

2. Pseudo-worsening. PwMS will let you know that she or he may not walk the same long dis-tance that they could a year before, and it is likely that this may not be detected on the neu-rological exam. Such a statement may be either due to an insidious progression of the disease or due to “pseudo-progression” or both. The term “pseudo-progression” is used to describe accu-mulating insidious disability due to factors indi-rectly related or unrelated to MS.8 For example,

hip-related issues such as osteoarthritis and avascular necrosis are not uncommon among MS patients, and usually seen in the ages that the progressive phase of MS starts, delay of neurological examination may cause the wors-ening of symptoms that is basically associated with the hip problems, and more importantly these symptoms may be misinterpreted as MS progression. Degenerative vertebral disc dis-eases may also mimic MS symptoms and worsen ambulation and may even result in acute myelopathy. However, the underlying reason causing pseudo-progression should be clarified by clinicians along with neurological examina-tion in order to preclude unnecessary treatment changes in MS. Moreover, spasticity and neuro-pathic pain are other symptoms disturbing walking and as the devices are not specifically designed for evaluating spasticity and pain this may result in symptomatic treatment delays. Recently, a study conducted with body-worn sensors was published supporting our concerns regarding wearable technologies in case of pseudo-progression.9 They found greater

varia-tion in between-visit performance than did the less disabled MS when they divided patients in two subgroups based on their initial EDSS ((0– 3.5) as MS-mild, and EDSS (4–5.5) as MS-moderate), and they concluded that this variation may be a key indicator of worsening gait and balance disability in MS. However, this variation might be related, in part, to pseudo-progression that is particularly observed in pro-gressive MS.

Of course, when compared to wearable technologies, clinical assessments have some limitations as well. One of the main limitations of clinical assessments is that they provide information at a single time-point and do not take into consideration real-world condi-tions outside the examination room.10 However, do

we need these sophisticated technologies in our clini-cal evaluation and decision making? We believe that it is still equally and even more important to listen to what the patient says and what our neurological exam reveals, and wearable technologies need to evolve to be less invasive and more comfortable to wear for long durations in free-living environments and to employ smart strategies that enable the inclusion of additional data modalities. The other point is that cur-rently few wearable devices are focused on upper extremity functions such as hand dexterity and tremor. The PwMS will clearly describe the minor changes in performing skill-requiring hand movements and

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Multiple Sclerosis Journal 26(9)

1028 journals.sagepub.com/home/msj

although that such changes may not be detected on the neuro-exam and even on the nine-hole peg test, for an experienced neurologist this would be a significant note to write down on the patient’s chart. Tremor is another disabling symptom in MS easily detected on the neuro-exam.

Currently, to our knowledge, there are no studies comparing treatment decisions made on findings based on wearable technology versus neurological examination. Until such studies are carried out and show superiority of these devices over neurological exam, we have to rely on what we learn directly from our patients, what our exam discloses, what imaging or other laboratory studies reveal, and what we con-clude from our traditional way of evaluating our patients with everything. Wearable technologies are likely to develop further but even by then, they may be only an assistive device to support the neurological exam along with the imaging and other biomarkers but not to replace them.

Acknowledgements

We thank Professor Daniel Pelletier (University of Southern California in Los Angeles) for his valuable suggestions.

Declaration of Conflicting Interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/ or publication of this article: Honoraria or consultancy fees received (U.U.) from F Hoffman-La Roche Ltd, Sanovel, Bayer, Merck-Serono, Novartis, Teva, and Biogen Idec/Gen Pharma of Turkey, and (A.S.) from F Hoffman-La Roche Ltd, Sanofi-Genzyme, Bayer, Merck-Serono, Novartis, Teva, and Biogen Idec/Gen Pharma of Turkey. None are related to this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

References

1. Rotstein DL, Chen H, Wilton AS, et al. Temporal trends in multiple sclerosis prevalence and incidence in a large population. Neurology 2018; 90(16): e1435–e1441.

2. Patel S, Chen BR, Buckley T, et al. Home monitoring of patients with Parkinson’s disease via wearable technology and a web-based application. Conf Proc

IEEE Eng Med Biol Soc 2010; 2010: 4411–4414.

3. Motl RW, Sandroff BM and Sosnoff JJ. Commercially available accelerometry as an ecologically valid measure of ambulation in individuals with multiple sclerosis. Expert Rev

Neurother 2012; 12(9): 1079–1088.

4. Block VAJ, Pitsch E, Tahir P, et al. Physical activity monitoring in neurological disease: A systematic review. PLoS ONE 2016; 11(4): e0154335.

5. Lord S, Galna B and Rochester L. Moving forward on gait measurement: Toward a more refined approach.

Mov Disord 2013; 28(11): 1534–1543.

6. Shanahan CJ, Boonstra FMC, Cofré Lizama LE, et al. Technologies for advanced gait and balance assessments in people with multiple sclerosis. Front

Neurol 2018; 8: 708.

7. Galea MP, Cofré Lizama LE, Butzkueven H, et al. Gait and balance deterioration over a 12-month period in multiple sclerosis patients with EDSS scores ⩽ 3.0. Neurorehabilitation 2017; 40(2): 277–284.

8. Kantarci OH. Phases and phenotypes of multiple sclerosis. Continuum 2019; 25(3): 636–654. 9. Spain RI, Mancini M, Horak FB, et al. Body-worn

sensors capture variability, but not decline, of gait and balance measures in multiple sclerosis over 18 months. Gait Posture 2014; 39(3): 958–964. 10. Frechette ML, Meyer BM, Tulipani LJ, et al. Next

steps in wearable technology and community ambulation in multiple sclerosis. Curr Neurol

Neurosci Rep 2019; 19(10): 80.

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SAGE journals

We should monitor our patients with

wearable technology instead of neurological

examination – Commentary

Giampaolo Brichetto Multiple Sclerosis Journal

2020, Vol. 26(9) 1028 –1030 DOI: 10.1177/

1352458520930985 © The Author(s), 2020. Article reuse guidelines: sagepub.com/journals-permissions

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