Proprioceptive Cervicogenic Dizziness Care Trajectories in Patient Subpopulations: A Scoping Review

Proprioceptive cervicogenic dizziness (PCGD) is the most prevalent subcategory of cervicogenic dizziness. There is considerable confusion regarding this clinical syndrome’s differential diagnosis, evaluation, and treatment strategy. Our objectives were to conduct a systematic search to map out characteristics of the literature and of potential subpopulations of PCGD, and to classify accordingly the knowledge contained in the literature regarding interventions, outcomes and diagnosis. A Joanna Briggs Institute methodology-informed scoping review of the French, English, Spanish, Portuguese and Italian literature from January 2000 to June 2021 was undertaken on PsycInfo, Medline (Ovid), Embase (Ovid), All EBM Reviews (Ovid), CINAHL (Ebsco), Web of Science and Scopus databases. All pertinent randomized control trials, case studies, literature reviews, meta-analyses, and observational studies were retrieved. Evidence-charting methods were executed by two independent researchers at each stage of the scoping review. The search yielded 156 articles. Based on the potential etiology of the clinical syndrome, the analysis identified four main subpopulations of PCGD: chronic cervicalgia, traumatic, degenerative cervical disease, and occupational. The three most commonly occurring differential diagnosis categories are central causes, benign paroxysmal positional vertigo and otologic pathologies. The four most cited measures of change were the dizziness handicap inventory, visual analog scale for neck pain, cervical range of motion, and posturography. Across subpopulations, exercise therapy and manual therapy are the most commonly encountered interventions in the literature. PCGD patients have heterogeneous etiologies which can impact their care trajectory. Adapted care trajectories should be used for the different subpopulations by optimizing differential diagnosis, treatment, and evaluation of outcomes.


Background and Rationale
The prevalence of dizziness among people of working age (18 to 65 years old) is 20%-30% [1][2][3][4], and it is the number one reason for medical consultations for people over 75 years old [5]. Cervicogenic dizziness, cervical vertigo, and cervicogenic vertigo are interchangeable terms that refer to dizziness that is closely associated with neck pain, neck injury, or neck pathology. Many consider it to be one of the most common causes of dizziness, as it contributes to major social costs, insurance claims and handicap [3,[6][7][8]. Throughout this manuscript, dizziness is understood as a non-rotatory illusion of movement, accompanied by disequilibrium and lightheadedness.
As a consequence of the absence of a gold standard testing procedure, cervicogenic dizziness's diagnosis is based on clinical presentation and the exclusion of other possible causes of dizziness [9][10][11]. However, researchers and clinicians should not only distinguish and personalization of the final extraction tool, which allowed for all relevant results to be extracted to meet the scoping review's objective (Supplementary Appendix SB).
Data items: Due to feasibility considerations, we limited the amount of data that we reported to study designs, subpopulations, differential diagnoses, diagnostic tools, interventions and outcome measures.
Synthesis of result: A descriptive quantitative synthesis of the evidence is provided by a tabulation and census of articles that relate each aspect of the care trajectory. Review articles are treated separately in some figures, and are not considered in other figures in order to give a true representation of the literature and to avoid double counting of data. A descriptive narrative of evidence is also presented.

Extracting and Charting the Results
The aforementioned methodology yielded 1741 studies. A total of 797 articles were left after Covidence automatically removed articles recognized to be duplicates (n = 944). The selected articles were then screened by two independent reviewers based on title and abstract. Some 516 studies were excluded because they were found irrelevant based on inclusion/exclusion criteria. A total of 281 articles were assessed for eligibility in a full-text selection process by two independent reviewers. Some 125 studies were excluded following a full-text review based on the exclusion criteria (see Supplementary Appendix SC for the list and reason for exclusion). Conflicts were settled by consensus both in the title and abstract selection stage, and the full-text selection stage with the input of a third party (the last author of this paper). Finally, 156 studies were identified and selected for inclusion in the scoping review. A detailed search decision flowchart is presented in Figure 1.

Chronic cervical pain
Patients with cervical pain for more than 12 weeks with no history of trauma or presence of muscle spasm that present dizziness.

Traumatic
Patients have a history of 1 WAD or 2 PCS. Along with dizziness and cervical pain, patients may present the following symptoms: ataxia, unsteadiness of gait, postural imbalance, limited neck range of motion and potentially headache.
Pain, limitation of movement, and strains of joint capsules, paravertebral ligaments, and cervical musculature can alter cervical proprioception

Degenerative cervical disease
Mostly elderly populations presenting dizziness associated with degenerative cervical changes and cervical pain. Some patients may complain of headaches, or shoulder pain and some radicular symptoms or possible.
Histological changes and inflammatory processes can alter cervical proprioception

Subpopulations Clinical Presentation
Hypothesized Etiological Mechanism Patients with cervical pain for more than 12 weeks with no

Discussion
This article focused on the following central questions: (1) What are the main research designs used to study PCGD? (2) Which subpopulations of patients does a PCGD diagnosis represent? (3) What common differential diagnoses are associated with those subpopulations? (4) What evaluation tools are mentioned to identify the diagnosis? (5) What interventions have been considered by researchers for management? (6) Which

Discussion
This article focused on the following central questions: (1) What are the main research designs used to study PCGD? (2) Which subpopulations of patients does a PCGD diagnosis represent? (3) What common differential diagnoses are associated with those subpopulations? (4) What evaluation tools are mentioned to identify the diagnosis? (5) What interventions have been considered by researchers for management? (6) Which outcome measures have been used?
To our knowledge, this is the first scoping review undertaken on the topic of PCGD. Four subpopulations of PCGD have been identified: chronic neck pain, degenerative cervical disease, traumatic and occupational subpopulations (muscle spasm). Central causes of dizziness and BPPV are the most often-mentioned potential diagnoses that compete with PCGD. The Dix-Hallpike maneuver is the most cited tool to inform differential diagnosis. Manual therapy and exercise therapy are the most studied interventions in the field. DHI is the most often-encountered measure of change used in this literature.

Designs
Many study designs were selected for this review (see Figure 2). Randomized control trials represent only approximately 10% of the selected literature. Observational studies

Discussion
This article focused on the following central questions: (1) What are the main research designs used to study PCGD? (2) Which subpopulations of patients does a PCGD diagnosis represent? (3) What common differential diagnoses are associated with those subpopulations? (4) What evaluation tools are mentioned to identify the diagnosis? (5) What interventions have been considered by researchers for management? (6) Which outcome measures have been used?
To our knowledge, this is the first scoping review undertaken on the topic of PCGD. Four subpopulations of PCGD have been identified: chronic neck pain, degenerative cervical disease, traumatic and occupational subpopulations (muscle spasm). Central causes of dizziness and BPPV are the most often-mentioned potential diagnoses that compete with PCGD. The Dix-Hallpike maneuver is the most cited tool to inform differential diagnosis. Manual therapy and exercise therapy are the most studied interventions in the field. DHI is the most often-encountered measure of change used in this literature.

Designs
Many study designs were selected for this review (see Figure 2). Randomized control trials represent only approximately 10% of the selected literature. Observational studies are the most common designs. No qualitative protocols on the subject were found in any database; this type of research should be encouraged because evidence-informed practice, value-based healthcare approaches and patient participatory paradigms require a more qualitative knowledge of the experience of patients suffering from PCGD in order to focus on what matters to them [173].

Subpopulations
Four subpopulations of PCGD have been identified that reflect the relatively heterogeneous population of PCGD. The reasons that some people develop PCGD and others do not, even though they are part of traumatic, degenerative cervical disease, muscle spasms or chronic neck pain populations, remain unknown [158]. Maybe differences in sensorial strategies between individuals could account for that. Patients keener on using proprioceptive input will be more at risk of developing PCGD in comparison with patients who rely more heavily on vestibular or visual cues for posture and gait. As patients can be part of more than one subpopulation of PCGD, research could investigate how cumulating etiological factors could predict poor prognosis [174]. Because PCGD pertains to different subpopulations, it is a «cross-cutting complaint» that concerns different specialties. As such, our results support the Bárány Society's recommendation to form multidisciplinary research teams to study PCGD [175], and their calls for interdisciplinary efforts in the clinic.

Competing Diagnoses, Differential Diagnosis and Comorbidity
Since PCGD is an exclusion diagnosis, central causes, cardiac disease and otological pathologies are among the four most cited pathological categories to be ruled out (see Figure 4). Unfortunately, these categories lack precision because they regroup numerous pathologies and are too elusive to effectively orient the differential diagnosis process and inform clinicians. BPPV, on the other hand, is the most cited specific diagnosis in this literature. It is also cited often as an important diagnosis to rule out, no matter what the subpopulation of PCGD is (see Table 2). It is therefore no surprise that the relatively simple Dix-Hallpike maneuver is the most cited test to rule out competing pathologies with PCGD (see Figure 5). Indeed, this test associated with adequate nystagmus analysis; paroxysmal presentation of symptoms and history taking can signal a BPPV diagnosis, but only for posterior canal issues. Lateral canal issues are not objectified with this test.
Knowledge of subpopulations could orient clinicians toward the most accurate and pertinent use of resources in terms of diagnostic tools. Indeed, certain differential diagnostic processes are more often encountered in articles recognizing specific subpopulations of PCGD.
In the literature on the traumatic subpopulation of PCGD, vertebral fractures and particularly traumatic brain injury are more often mentioned than in any other subpopulation. Additionally, there are relatively fewer mentions of the necessity to exclude cardiac diseases in the literature on the traumatic subpopulation of PCGD compared with other subpopulations. Clinicians could orient their diagnostic process toward a rather orthopedic direction rather than a cardiovascular direction in this subpopulation. While MRI, neurological examination and X-ray are cited in the literature on PCGD to help with differential diagnoses (see Figure 5), there are relatively few mentions of orthopedic examination for vertebral fracture signs and ligament testing. This could indicate that clinicians rely more on imagery than clinical testing, and could use clinical testing more, especially with the traumatic population.
In the literature on the degenerative cervical disease subpopulation of PCGD, cardiac disease and drug-induced dizziness are relatively more often cited than in any other subpopulation. This might be because the degenerative cervical disease subpopulation is more likely to be elderly, have cardiac conditions and be exposed to multiple drug issues [176]. Indeed, cardiac history and testing is the 7th most cited evaluation used in differential diagnosis (see Figure 5).
Incidentally, psychogenic vertigo is cited relatively more often in both the traumatic and the degenerative cervical disease subpopulations than in the other subgroups. This could be explained by the potential psychological impacts related to trauma or ageing. Paradoxically, no mention of psychological assessment is present in the tests to inform differential diagnosis. More psychological testing should be carried out in a neurotological context, as vertigo and dizziness can also cause anxiety, panic and depression, and these could in turn also cause dizziness [177].
Other important aspects to discuss are persistent postural perceptual dizziness (PPPD) and vestibular migraine. PPPD was recognized by the International Classification of Diseases (ICD-11) only in 2017 [178], and vestibular migraine has been described by the members of the Bárány Society only since 2012 [179]. Although migraine is cited relatively often as a diagnosis of exclusion in PCGD, especially in the traumatic and chronic cervicalgia subpopulations, there is no golden standard to «rule in» migraine and diagnosis is based on clinical presentation [180]. This result supports the importance of controlling for migraine and developing subgroup analysis for migraine as a confounding factor in future interventional studies, as prompted by the Bárány Society's recent milestone article on 'Cervical Dizziness' [175]. Persistent postural perceptual dizziness is a common long-lasting cause of dizziness [178]. Paradoxically, it is not mentioned in the exclusion process of PCGD. Migraine and persistent postural perceptual dizziness are both exclusion diagnoses and can co-exist with other conditions. This situation adds to diagnosis uncertainty.
Early diagnosis and rehabilitation could optimize health outcomes for patients and add value to healthcare by reducing the social-economic burden of disease. One of the main issues with the lengthy care trajectory of PCGD is that despite being an exclusion diagnosis, it may also coexist with other disorders, and often does. Moreover, in elderly people at risk of falls, road accident victims suffering from post-concussion syndrome or whiplash, and patients suffering from neck pain or chronic headaches, 45.2% to 84% of patients have potentially one or more diagnoses in addition to PCGD [11,123,181]. In these subpopulations, dizziness is associated with higher levels of disability and more psychosocial consequences compared to patients in the same groups without dizziness [13,113,135,154,182]. This multimorbid situation makes the trajectory of care longer, and often results in therapeutic wandering for these patients, and a greater social and economic burden. There is a lack of a single gold standard test or accepted clinical prediction rule to limit diagnosis uncertainty [18]. Only one article has studied the possibility of combining different tests to shorten the exclusion process [16]. The issue of multi-morbidity calls for investigation of clinical prediction rules and the specificity of tests to «rule-in» PCGD. Indeed, while sensitive tests such as manual spinal evaluation and palpation for segmental tenderness are very often used in the literature, potentially more specific tests [10] such as cervical torsion [10,16,64,84,90,97,115], the head-neck differentiation test [10,97,123], joint position error test [10,16,50,65,87,90,98] and smooth pursuit neck torsion test [10,16,23,26,50,57,64,65,99,103,125,128] have a relatively lower rate of occurrence in the literature. Unfortunately, in comparison with the literature reporting tools to «rule out» other pathologies, the literature reporting clinical testing that is useful to «rule in» PCGD with more specific tools is scarce, and therefore should be encouraged (see Figures 5 and 6).

Measuring Change
In PCGD, many outcome measures are needed not only because of its multidimensional nature, but because self-reported outcomes and perceived level of handicap poorly correlate with the measurement of the level of sensorimotor performance [183]. This suggests they rely on other constructs [183]. The most commonly encountered outcome measures in PCGD are DHI, VAS for cervical pain, CROM and posturography (see Figure 8). Posturography and JPE are the only tests that can be found both among the tools for inclusion and for measuring change (see Figures 6 and 8), and this raises the question of their potential combined specificity and sensitivity to change. These six tools should be used to facilitate comparison between trials and meta-analysis of outcomes, and a psychological outcome such as HADS should also be included. Social engagement and personal economic impacts of disease should be reported in PCGD. As PCGD remains elusive in its exact aetiopathogenesis, primary clinical outcomes and secondary «mechanistically based» outcomes should also help to establish a basis for hypothesized pathophysiological mechanisms [175].

Interventions
Manual therapy and exercise therapy are generally the most common interventions encountered in the literature. However, surgeries were considered more often for degenerative cervical disease subpopulations suffering from PCGD than in any other subpopulation (see Table 4). The reason for this might be that surgeries are aimed at degenerative changes and herniated disc issues rather than for dizziness itself, even if they may have an indirect impact on dizziness. In the same way, injections were mostly reported in the literature for the chronic cervical pain subpopulation, as they are a common treatment for chronic neck pain. Patient education was the third most studied intervention in the muscle spasm (occupational) subpopulation. Indeed, patient education about occupational habits aims to reducing muscle spasms, and indirectly could impact dizziness.
Knowledge of subpopulations' characteristics should also be reflected in the multimorbid context of PCGD. It enables the clinician to consider not only the type of intervention but the strategy of intervention that might be considered.

Limitations
Relevant sources of information may have been omitted in the literature written in languages that were not included in the review, notably Chinese and German articles. Another limitation of this study is that the proprioceptive etiology of cervicogenic dizziness is yet to be recognized by The International Classification of Vestibular Disorders. It is a working definition and is the most plausible cause of dizziness in cervicogenic dizziness, but still requires further investigation into its pathophysiological mechanism. In this scoping review, as no quality assessment of protocols was performed, the validity of the literature has not been put to the test. Care should be taken while interpreting the results.
In the differential diagnosis process, since some authors simply excluded general cardiac, central and otologic conditions without naming any particular pathology, specific conditions pertaining to those categories might be under-represented in our results in Figure 4. Additionally, relatively recent diagnoses in otology and neurotology make some pathologies unlikely to have been put forward in the differential diagnosis of PCGD before 2010, and even today. For example, a potentially relevant competing diagnosis such as PPPD might have been reported using other terms such as phobic postural vertigo or visual vertigo, but only two articles mentioned each pathology. Some 43.9% of articles acknowledge more than one subpopulation. This introduces bias in subpopulation analysis. Particularly in the chronic cervicalgia analysis, 34 of the 53 articles also recognize at least one other subpopulation for PCGD, and in so doing, introduce bias to our data. For example, these articles could mention vertebral fractures or instability as a pathology to exclude, because the authors recognize the potential contribution of trauma or degenerative cervical disease subpopulations in PCGD.

Conclusions
This is the first scoping review of the literature on PCGD, to the authors' knowledge. Qualitative methods are inexistent in the literature on PCGD. The specific characteristics of PCGD patients differ according to their etiological categories. Subpopulation knowledge should inform subgroup analysis in PCGD trials and observational studies as well as clinical practice. Namely, there are four main subpopulations of PCGD: chronic cervical pain, traumatic, degenerative cervical disease and occupational. These subgroups have different care trajectories according to commonly encountered pathologies, probable comorbidities, usual red flags, and treatment strategies. This raised awareness will have important impact on future research in relation to subgroup analysis and in clinical practice, as it enables optimized differential diagnosis, treatment, and evaluation. Studies should also investigate the reason that some patients from a single subpopulation develop PCGD and others do not; more randomized control studies are needed. Trials should use common outcome measures encompassing all dimensions of PCGD, including the social and economic categories, to facilitate future systematic reviews and elucidate pathophysiological mechanisms. Future studies should report on clinical testing to «rule in» PCGD.