Assessing Cranial Nerves in Physical Therapy Practice: Findings from a Cross-Sectional Survey and Implication for Clinical Practice

Background and objective: Serious pathologies of the neck can potentially result in cranial nerve palsy. Knowledge about cranial nerve examination (CNE) seems sparse, and its use is still unknown. We aim to investigate the knowledge, skills, and utilization of CNE of Italian physiotherapists. Materials and Methods: An online cross-sectional survey. Results: 396 completed the survey, reaching the required sample size. Although Italian physiotherapists consider CNE relevant (mean ± SD = 7.6/10 ± 2.0), over half of all responders (n = 229 (57.8%)) were not trained in the fundamentals and around a third did not use it in their daily practice (n = 138 (34.8%)). Additionally, participants were unconfident and insecure in conducting (n = 152 (38.4%) and n = 147 (37.1%)), interpreting (n = 140 (35.4%) and n = 164 (41.4%)), and managing the CNE (n = 141 (35.6%) and n = 154 (38.9%)). Possessing a musculoskeletal specialization was associated with an increased value attributed to clinical practice guidelines and reduced the lack of confidence in conducting, interpreting, and managing the CNE (respectively, n = 35 (25.5%), p = 0.0001; n = 32 (23.4%) p = 0.0002; n = 32 (23.4%) p = 0.0002). Working in a direct access setting significantly increased the considered relevance of guidelines and the concerns about arterial (p = 0.004) and other serious pathologies (p = 0.021). Pain and visual disturbances were considered the main indicators to CNE, demonstrating limited knowledge of signs and symptoms’ indicating CNE. Participants considered specific training in CNE as relevant (mean ± SD = 7.6/10 = 2.1). Conclusions: a substantial proportion of Italian physiotherapists are not schooled in the fundamentals of cranial nerve examination. Given the number of physiotherapists who work in first contact roles, this is a professional concern.


Introduction
Neck pain and associated disorders (NAD) are common complex biopsychosocial disorders with a high physical, psychosocial, and economic impact, leading to increased healthcare utilization [1][2][3]. The Neck Pain Task Force recommends a four-grade classification system of neck pain severity that is intended to help patients, researchers, clinicians, and policy makers in framing their questions and decisions [4].
Clinical practice guidelines recommend ruling out signs or symptoms of major structural pathologies (i.e., NAD IV)-such as congenital craniovertebral anomalies, cervical vascular pathologies, anatomical instabilities, and autonomic disorders-masquerading as neck pain before providing any evidence-based intervention [1,5,6]. The screening for the referral process in case of serious pathologies in physiotherapy-especially in a direct access setting-is a professional challenge. The incidence of delayed diagnosis of serious pathologies ranges from 5% to 20% in the cervical region [7], leading to a lack of recognition that may result in life-threatening consequences [8]. Red flags are signs and symptoms that should alert physiotherapists to consider carefully if the patient is within their scope of practice [1,9,10] and whether they need appropriate medical referral [1,[11][12][13]. Commonly, patients with NAD IV present subtle transient antecedent neurological signs and symptoms or risk factors (i.e., acute onset of unusual headache or neck pain, recent trauma to the head or neck, and/or ischemic signs and symptoms, in younger people under 50 years) [14,15]. Clinicians should identify these during the subjective patient history and further verify during the neurological testing [8,[16][17][18][19], especially by the use of cranial nerve examination (CNE) because serious pathologies of the neck can potentially result in cranial nerve (CN) palsy (especially CNs V, VI, VIII, IX, X, and XII) [11,[20][21][22]. Physiotherapists therefore require skills in a wide range of neurological examination procedures required to screen all potential NAD IV clinical presentations [23].
Only 5% of clinicians routinely screen for red flags during initial assessment [6,8]. However, screening for serious pathology is a priority [1,5,6] and requires expertise in that field and a systematic approach [24]. In addition, information about physiotherapists' knowledge of CNE is sparse and its use by physiotherapists is still unknown. Our survey aims to investigate the knowledge, skills, and utilization of CNE in a sample of Italian physiotherapists. This study aims to contribute to the knowledge base and discussion regarding potential future directions for the screening for referral process of NAD IV.

Methods
An online cross-sectional questionnaire survey was developed using the online platform Survey Monkey (SVMK Inc., San Mateo, USA) for Italian physiotherapists. The study is reported in line with the Checklist for Reporting Results of Internet Surveys (CHER-RIES) [25] and the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [26].

Survey Development
With the permission of the authors, to develop our version, we translated, modified the contents of, and culturally adapted into the Italian setting an unpublished recent survey conducted in the U.K. [27]. The survey was revised and adapted by two authors (native English and Italian specialized musculoskeletal physiotherapists with experience in education and research; FMo and AF). Then, the survey was piloted by six experienced Italian physiotherapists and physicians (AP, EG, FC, FMa, MG, and FP) for additional feedback on wording, response logic, and the fulfillment duration. The use of the original U.K. survey and the feedback provided by the pilot stage, respectively, strengthened the content and the face validity.
The survey was structured in three sections: the first section investigated demographic information, practice settings, and the education level; the second investigated the knowledge, skills, and clinical impact of CNE; the last section investigated education and personal opinions.
The survey consisted of 36 questions with a combination of close-ended (few of them with multiple selection) and Likert-scale questions. Only one question was an openended question (Supplement 1). All questions were presented at the same order and were mandatory to complete the survey.

Setting and Recruitment
A web-link to the survey was distributed via a mailing list of the Italian Physiotherapists Association on 23 March 2020. To take advantage of the forced period due to the COVID-19 pandemic and to maximize the response rate, invitations to participate were frequently re-published once per week via social media networks (Facebook, Twitter, LinkedIn, and Instagram). The survey was open for one month, and the closing date was 26 April 2020. For pragmatic purposes and in line with previous internationally published surveys, we adopted this methodological approach with the aim to collect the maximum number of answers within a specific period as most responses occur early after posting [28][29][30][31][32][33][34][35]. A priori, a sample size was calculated using the e-survey Dillman's formula [36] with a 95% confidence level and a 5% of margin of error. At the time of the survey, the number of physiotherapists registered to the Italian Physiotherapists Association was 7398; therefore, the required sample size for this study was 366 [37]. The questionnaire could be completed on any electronic device with internet access; as Survey Monkey was used without collecting respondents' IP addresses, the recruitment was anonymous and voluntary; in addition, the same IP was not allowed to access to the survey more than one time. Completion took approximately 10-15 min. No compensation or reimbursement were offered.

Data Processing and Analysis
Data from the survey platform were transferred to, and stored in, an encrypted computer for the purposes of data analysis, and access was allowed only to researchers involved in the data analysis. Incomplete surveys were not collected nor analyzed. We analyzed the open-ended questions by coding and categorizing the answers, adopting a bottom-up mixed approach [38].
Descriptive statistics was computed to describe the collected variables. A Chi-squared independent test was run to study any difference between responses provided by sample subgroups (i.e., Orthopedic Manipulative Physical Therapist (OMPT) specialization, physiotherapy access regimen, and experience years) to the categorical questions; in case the Chi-squared revealed significant differences (p < 0.05), adjusted standardized residuals [39] with their Bonferroni-corrected p-value were calculated for each cell to identify which cells of the contingency tables were accountable for the significant effect [40,41]. Moreover, to study any differences between responses provided by sample subgroups to the ordinal (i.e., Likert) questions, an independent t-test or an univariate ANOVA with Bonferroni-corrected post-hoc comparisons was run for answers to two categories (i.e., OMPT specialization and physical therapy access regimen) or to five categories (i.e., experience years).
All statistical analyses were performed with SPSS software (SPSS. Version 20 for Windows; SPSS Inc., Chicago, IL, USA, 2004), and the level was set at p-value < 0.05 for all comparisons.

Ethics
This study was approved by the Human Subjects Committee of the Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos of Madrid, with approval letter URJC-DPTO 55-2019. The authors followed the principles outlined in the Declaration of Helsinki for this study [42].

Responses
A total of 420 physiotherapists provided the consent and completed the survey. Of those, 24 were excluded as they did not work in Italy and were not included in the final analysis with the purpose to avoid any bias affecting our findings [43]. A final number of 396 physiotherapists was included. Although available for a very short period, our sample was in line with previous Italian surveys and reached the required sample size [44,45].  Table 1.

Knowledge and Education
Although Italian physiotherapists attribute a moderate importance to guidelines for assessing NAD (mean = 7.5/10 points; SD = 2.1), most of them were not familiar with the utilization (n = 256, 64.6%; 95%CI 59.9-69.4). A significant difference was found in possessing an OMPT specialization and working in a direct setting in attributing importance to guidelines (p = 0.003). Notably, a moderate percentage declares to manage 1 to 5 patients per month with potentially concerning clinical presentations such as headache (n = 175, 44   However, the majority of the respondents (n = 229, 57.8%; 95%CI 53.0-62.7) have not been sufficiently trained in CNE, primarily because of a lack of musculoskeletal focus during their undergraduate programs (n = 146, 63.8%; 95%CI 57.5-70.0). Interestingly, 71 (31.0%; 95%CI 25.0-37.0) did not feel the need to be educated in CNE because it was not considered relevant for their clinical practice (Table 3). Table 3. Knowledge, education, and confidence with regard to cranial nerve examination.

Mean (SD) N (%) 95%CI
How valuable do you consider guidelines for the management of cervical disorders? Likert scale (0-10) 7.   A significant difference was found in the confidence in conducting CNE among participants (p < 0.001). Post hoc tests illustrated the differences between those with an OMPT qualification and the reduction of lack of confidence in the ability of conducting (n = 35, 25.5%; p = 0.0001), interpreting the findings (n = 32, 23.4%; p = 0.0002), and managing the abnormal findings (n = 32, 23.4%; p = 0.0002) ( Table 2). Additionally, post hoc tests illustrated that those with 0-5 years of experience are significantly less sure in interpreting the findings (n = 11, 11.3%; p = 0.002) ( Table 4). When abnormal findings were detected during the CNE, one-third (n = 128, 32.3%; 95%CI 27.7-36.9) of all respondents did not feel the need to refer to a physician in case of a positive finding during CNE, suggesting an underestimate of its clinical relevance.
Generally, manual therapy-especially spinal thrust manipulation-was not considered directly linked or the direct cause of cervical arterial dissection (mean = 4.0/10 points; SD = 2.9). A significant difference was found in considering manual therapy to the neck causing adverse events in those with >20 years of experience (5.31 ± 3.15; p = 0.001) and in those which not possess a OMPT specialization (4.41 ± 2.96; p = 0.0003). However, more than half of the physiotherapists felt discouraged from using manual therapy to the neck region because of a perceived fear of causing adverse events (n = 267, 67.4%; 95%CI 62.8-72.0); that is, participants were highly concerned about vascular pathologies (mean = 7.7/10 points; SD = 2.2) and instability of the cranio-cervical junction (mean = 7.6/10 points; SD = 2.4). A significant difference was found in the perceived safety and working in a direct access setting for both vascular pathologies (7.97 ± 2.09; p = 0.004) and cervical instability (7.84 ± 2.33; p = 0.021) ( Table 5). Although the majority of the respondents were aware of the lack of a causal link, they still had concerns mainly for spinal thrust manipulations (n = 270, 68.2%; 95%CI 63.6-72.8) or mobilizations (n = 110, 27.8%; 95%CI 23.4-32.2) compared to exercises (n = 21, 5.3%; 95%CI 3.1-7.5).

Key Findings
This is the first published study to investigate physiotherapists' knowledge, understanding, and skills in the use of CNE, providing indications on future physiotherapy education, research, and practice. Our results highlight that CNE is considered relevant to be implemented in the screening of cervicocranial presentations and as part of the triage process. However, Italian physiotherapists reported not being sufficiently trained for an appropriate utilization in clinical practice. Interestingly, 57.8% of respondents stated that they had not received a specific training in CNE and linked this to omissions from the university's core undergraduate curriculum programs (63.8%). A total of 31.0% of the not-trained did not consider CNE a relevant skill for their clinical practice. The most recent guidelines for the management of NAD recommend priority screening to rule out major pathologies mimicking musculoskeletal conditions [1,6,18,46]. Furthermore, it is the physiotherapists' responsibility to screen if the patient's presenting symptoms are within their scope of practice and appropriate for physiotherapy management. However, our findings show that although a large proportion of respondents worked in a direct (41.4%) access setting, most of them (64.6%) were not aware of guidelines when assessing patients with NAD with potential serious pathologies [1,5,21,47,48].
Clinicians should raise their index of suspicion of serious pathologies (i.e., congenital craniovertebral anomalies, cervical arterial pathologies, anatomical instabilities, autonomic disorders, etc.) during the subjective patient history taking. The identification of any red flags should be explored in detail with specific questioning as patients often did not think to mention them spontaneously [18]. It has been suggested that advanced clinical reasoning incorporating detailed knowledge of potential pathologies, combined with appropriate clinical testing (e.g., neurological signs or function examination), may be required to make the best informed judgement [23]. As clinicians cannot rely on valid and reliable screening tests that may help in identifying NAD IV patients [11], the neurological examination (i.e., cranial nerves, peripheral nerves, and upper motor neuron examination) is a key part of the triage process and may assist in evaluating the potential for serious conditions. Although Italian physiotherapists occasionally encounter patients with potential concerning clinical presentations, such as headache, whiplash, neck or head trauma, dizziness, or visual disturbances, a relevant number (34.8%) of respondents did not routinely include CNE in their assessment, even when potentially required based on the patient's history. Moreover, the majority suggested that they were not confident or secure (respectively, 38.4% and 37.1%) in conducting CN assessment, identifying pathognomonic signs and symptoms (respectively, 35.4% and 41.4%), or interpreting and managing the findings of the examination (respectively, 35.6% and 38.9%). Interestingly, those that had less clinical experience (<5 years) use the CNE significantly rarely and showed lesser confidence in interpreting the assessment finding. On the other hand, those possessing an OMPT specialization showed more confidence in conducting a CNE, interpreting the findings, and managing the examination results. This observation may be related to a significantly better understanding of the relevance of guidelines for the participants possessing an OMPT specialization. Although an increasing number of primary studies suggest the importance of CNE when examining the neck region to inform pattern recognition of sinister clinical conditions [13,47,[49][50][51][52][53][54][55][56][57][58][59][60][61][62][63], our findings may reflect the lack of high-quality evidence for CN involvement in NAD IV. To the best of the authors' knowledge, no specific data are available to support the diagnostic accuracy of a complete CNE. However, although peripheral neurological examination (e.g., sensory, motor, and reflex testing) has been shown to possess low sensitivity, moderate specificity, and limited diagnostic accuracy [49], the examination of isolated CN injury for focal impairment shows poor sensitivity (0.22) but high specificity (0.95) and is predictable for advanced diagnostic imaging [50], and raising the index of suspicion of serious pathologies. Therefore, it is suggested to contextualize the physical examination, including the neurological examination, with the clinical presentation and subjective patient history and to combine more tests in order to strengthen their clinical relevance [51].
Our study highlights the need for further education and research for an appropriate clinical utilization and diagnosis [51].

Recommendations for Clinical Practice
The results of our study show that Italian physiotherapists do not conduct an adequate screening for referral and systems review procedures. The lack of expertise and updated education in that field may explain the reported increased fear of manual therapy delivery to the neck because of perceived potential risk of adverse events (n = 267, 67.4%). That is, those without an OMPT specialization (p = 0.0003) and with more than 20 years of clinical experience (p = 0.001) showed a significant increase in belief that manual therapy to the neck can cause adverse events. It is important to note that the first IFOMPT Master's program was started in 2004 (i.e., <20 years) [59], and physiotherapists that typically attend postgraduate programs are younger and have less experience than 20 years [60]. This observation may reflect the suspicion that many colleagues still based their clinical practice on continually propagated dogmatic knowledge instead of scientific clinical studies [61][62][63]. Therefore, we strongly encourage institutions and policymakers to use the findings of our study as a starting point to introduce appropriate screening for referral competencies into the Italian physiotherapy core curriculum and invite other research group to collaborate for further generalize our result in other countries.
Although there is no convincing evidence to support a causal link between spinal thrust manipulation and cervical artery dissection or anatomical instability [64], in addition to the notion that mobilization and manipulation have been shown to possess the same adverse events' risk [65], the majority of Italian physiotherapists are more discouraged from using spinal thrust manipulation (68.2%) compared to mobilizations (27.8%) in patients with NAD. These anecdotal beliefs strongly influence physiotherapists' clinical practice [65][66][67][68]. Therefore, we advise updating the knowledge of physiotherapists concerning adverse events. Furthermore, although cervical arterial dissection has been documented related to a wide variety exercises [18,[69][70][71], physiotherapists are not accustomed to evaluating cardiovascular parameters [72][73][74], and only 5.3% of the respondents are concerned about the exercises' related risk: considering that 62% of physiotherapists' patients potentially have a history or suffer of cardiac disease, the risk of acute myocardial infarction during exercise is seven times higher than that of sudden cardiac death [75][76][77][78]. Therefore, we advise physiotherapists to consider risk factors and more specific cardiovascular parameters, in their clinical reasoning. To guide physiotherapists in their daily practice, we created an infographic decision tool for early identification of potential vascular/neurological pathologies of the neck for public use (Supplement 2). Moreover, an extensive description of the CNE is available elsewhere [79].

Strengths and Limitations
A key strength is the high response rate, which permitted a required sample size calculation, confirming the willingness of physiotherapists to participate in this study. Moreover, authors have adopted a previous local online survey to understand the opinion of the target population. The methodological choice was previously used in surveys representing a valid tool aimed to capture the perspective of a large sample of healthcare providers [80]. That is, although we do not send personal invitations, the publication of several reminders helped to recruit a number of Italian physiotherapists in line with previous surveys [44,45]. However, the number of responders could have been influenced by the detailed and specific questions that were employed. Additionally, there is also high potential for responder bias, as those with stronger positive or negative interest in the topic may be more likely to respond or to give more detail to the survey. The recruitment methodology may potentially lead to a selection bias.

Conclusions
Our study exposed a concerning number of Italian physiotherapists who work as first-line practitioners who had not been trained in the fundamentals of CNE. Many of those who had been trained reported a lack of knowledge or confidence about exactly when and how to implement CN screening. In addition, the physiotherapists surveyed in this study did not report confidence in identifying pathognomonic signs and symptoms of NAD IV, with a lack of clarity regarding exactly when to assess CNs. All the above may impact appropriate clinical reasoning and triage in such cases, having the potential to adversely impact on the patient and practitioner. We strongly encourage institutions and policymakers to use the findings of our study as a starting point to introduce appropriate screening for referral competencies into the Italian physiotherapy core curriculum.

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Triage of serious pathologies masquerading as neck pain before providing any evidencebased intervention is recommendation number one in clinical practice guidelines and a professional responsibility. • Cranial nerve examination may potentially impact on appropriate clinical reasoning and the screening process for referral. • It is concerning that a considerable number of Italian physical therapists who work as first line practitioners are not schooled in the fundamentals of cranial nerve examination. • Improvement of the physiotherapy core curriculum concerning screening for referral competencies and cranial nerve examination is important.

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To guide physiotherapists in their daily practice, we created an infographic for public use. Funding: This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Institutional Review Board Statement:
The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of the Universidad Rey Juan Carlos (protocol code URJC-DPTO 55-2019, approved the 10 December 2019).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: Raw data are available upon request.