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Abstract

Study design

Systematic review.

Objective

To summarise the parameters available to measure horizontal gaze, provide their values in patients and/or asymptomatic individuals, and assess their reliability.

Methods

A literature search was conducted on 9/9/2023 using Medline and Embase, applying the following keywords: “horizontal gaze” or “gaze line”. Articles that reported on horizontal gaze were included.

Results

Twenty-six articles published between 2015 and 2023, were included, of which 15 reported on patients, 10 reported on asymptomatic individuals, and one reported on both. The three most reported horizontal gaze parameters were McGregor’s slope (n = 20 studies, asymptomatic individuals range: −8.8-10.2°), C0-C2 angle (n = 18 studies, asymptomatic individuals range: −32.0-101.5°), and chin brow vertical angle (CBVA) (n = 12 studies, asymptomatic individuals range: −5.9-12.7°). The most frequently reported correlations were between McGregor’s slope and C0-C2 angle (R,-0.390-0.676; P < 0.065; n = 4 studies), McGregor’s slope and CBVA (R, 0.679-0.862; P < 0.0001; n = 3 studies), as well as CBVA and slope of the line of sight (R, 0.592-0.996; P < 0.001; n = 3 studies).

Conclusion

The present systematic review identified 18 parameters used to measure horizontal gaze; however, there is no gold standard. Although parameters had good to excellent inter-observer reliabilities, there were large variations in measurements among asymptomatic individuals across studies, which may imply a limited clinical relevance. Therefore, there is a need for a gold standard parameter of horizontal gaze, which uses easily identifiable landmarks that are simple to measure (reliable), relates both orbital and cervical anatomical structures, and provides insight into compensatory mechanisms in deformative or degenerative conditions.

Keywords

horizontal gaze sagittal cervical alignment McGregor’s slope chin brow vertical angle systematic review

Introduction

Bipedalism and maintaining an upright posture are crucial for achieving stable horizontal gaze,¹ which enables humans to walk, interact with their surroundings, and carry out daily tasks.² Horizontal gaze is frequently assessed using the chin brow vertical angle (CBVA)³ and the McGregor’s slope.⁴ The CBVA is defined as the angle formed by a line drawn from the brow to the chin and a line drawn from the brow to the vertical.^3,5 The McGregor’s slope is defined as the angle formed by the line from the midpoint of the posterior aspect of the hard palate to the lower margin of the occipital bone and the horizontal plane.⁴

The CBVA has easy to identify landmarks and provides repeatable measurements.^2,6 However, it is often impossible to measure, as its landmarks (the chin and brow), are not always available on standard sagittal spine radiographs.^1,7,8 Additionally, it may not be a reliable measure in cases of mandible protrusion or retraction and does not accurately reflect the relationship between cranial morphology and cervical position.⁶ While, the McGregor’s slope has landmarks that are usually available on standard sagittal spine radiographs¹ and does consider head position and cervical morphology, its landmarks are difficult to locate on radiographs, especially the posterior aspect of the hard palate, the opisthion, and the most caudal point on the midline occipital curve.^2,9

There have been several attempts to introduce new parameters to measure horizontal gaze,^2,10-12 but none have been adopted on a large scale and there is no consensus regarding a gold standard parameter⁸; in contrast to pelvic incidence, pelvic tilt, and sacral slope, which are known to describe spino-pelvic sagittal balance.¹³ A recent narrative review¹⁴ has explored the parameters available to measure horizontal gaze in patients with cervical deformities, but it did not provide average physiological values for this population, nor reported their reliabilities. Furthermore, the available parameters can be grouped into two categories: “de facto” parameters that evaluate horizontal gaze vs parameters that describe the compensatory mechanisms which affect horizontal gaze. Therefore, the purpose of this systematic review is to summarise all parameters available to evaluate or describe horizontal gaze, provide their values in patients and/or asymptomatic individuals, and assess their reliability.

Methods

The search strategy and methodological protocol for this systematic review is registered with PROSPERO (CRD42023456813). This systematic review follows the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines.

Search Strategy

The authors conducted a structured electronic literature search on 9 September 2023 using the Medline and Embase databases, applying the following keywords: “horizontal gaze” or “gaze line”. Duplicate records were removed, and two reviewers (AK,TB) independently screened the title and abstracts to determine eligibility using the following inclusion and exclusion criteria.

Inclusion Criteria:

Comparative or non-comparative studies reporting:

• Normative and/or pathologic values of parameters to measure horizontal gaze.

• Reliability of parameters to measure horizontal gaze.

• Correlations between parameters to measure horizontal gaze, both among themselves and in relation to other spinal and hip parameters.

Exclusion criteria:

• Articles that report on parameters of horizontal gaze where the individual was not in the upright position (magnetic resonance imaging, computed tomography, etc).

• Articles that report on individuals who underwent measurements of their horizontal gaze following spinal surgery.

• Articles written in languages other than English or French.

• Reviews, editorial commentaries, conference proceedings, etc.

• Cadaveric, laboratory, modelling, and animal studies.

Full-texts were retrieved for all articles that were deemed relevant or if the title and abstract provided insufficient information to establish eligibility. Full text screening was performed independently by three reviewers (AK,TB,DC), with one of the reviewers screening all articles, while the other two reviewers each screened half of the records. Screening decisions were compared between reviewers and disagreements were solved through review and consensus.

Data Extraction and Quality Assessment

The following characteristics were extracted from each eligible study independently by three reviewers (AK,TB,DC), with one of the reviewers extracting data from all articles, while the other two reviewers each performed data extraction on half of the records: lead author, journal, date of publication, article type, conflicts of interest, funding, country of study, cohort type (asymptomatic individuals or patients), pathology if any, cohort size, sex, age, parameters described, definitions of parameters, normative or preoperative pathologic values, inter- and intra-observer reliability, and correlation coefficients. The data extracted was compared and disagreements were solved through review and consensus.

The same three reviewers assessed the methodological quality of eligible studies according to the methodological index for non-randomised studies (MINORS).¹⁵ The quality assessment was compared and any discrepancies in appraisal was resolved through discussion and consensus. “Question 6: Follow-up period appropriate to the aim of the study” and “Question 7: Loss to follow up less than 5%” were not completed as the present study only focused on preoperative measurements. Furthermore, questions relating to comparative studies were not completed, as there was no comparator group of interest. Therefore, the maximum score was 12 points which indicated high quality/low risk of bias, while the minimum score was 0 points which indicated low quality/high risk of bias.

Data Analysis

Parameters were grouped into two categories: “de facto” parameters that evaluate horizontal gaze vs parameters that describe the compensatory mechanisms which affect horizontal gaze. When available in the included articles, horizontal gaze parameters, their reliability, and their correlations were tabulated. Horizontal gaze parameters were reported as means and standard deviations, reliability was reported as intra- or inter-class correlation coefficients (ICC), and correlations were reported as Pearson’s’ or Kendall’s correlation coefficients. Intra- and inter-class correlation coefficients were interpreted using the thresholds defined by Cicchetti et al.¹⁶ which are as follows: <0.40 is poor, 0.40-0.59 is fair, 0.60-0.74 is good, and 0.75-1.00 is excellent. A sub-analysis was performed on the three most commonly reported parameters (McGregor’s slope, CBVA, and C0-C2) to compare differences in these values between patients with deformity pathologies vs patients with degenerative pathologies.

Results

Literature Search

The electronic literature search identified 2075 references, 780 of which were duplicates (Figure 1). The remaining 1295 articles underwent title and abstract screening, and 1261 were excluded as they did not meet the inclusion criteria. The full text of the remaining 34 articles were screened, and a further 8 articles were excluded because: three took measurements from photographs instead of radiographs,^5,17,18 two did not specify the parameters used to assess horizontal gaze,^19,20 two did not report on horizontal gaze parameters,^21,22 and one was a review.²³ This left a total of 26 articles, published between 2015 and 2023 eligible for data extraction, of which 15 reported on patients,^1,2,7,24-35 10 reported on asymptomatic individuals,^6,10,36-43 and one reported on both.⁴⁴

Figure 1.

Flowchart of the study selection procedure.

Characteristics of Included Studies and Quality Assessment

Of the 26 included articles, 18 were retrospective,^{1,2,7,24-32,34,37,39,42,44} five were prospective,^{10,33,36,38,43,44} and three did not report the type of study^6,40,41 (Table 1). Furthermore, eight studies declared conflicts of interests^{1,2,7,25,28,31,39,42,44} and three declared funding.^25,41,42 The level of evidence ranged from 3 to 4, and the majority of studies were based in the USA (n = 8)^{1,2,6,7,32,33,39,43} and Japan (n = 7).^{24,26,27,31,35,36,42}

Table 1.

Study characteristics.

Author	Date	Journal	COIs	Funding	Type of study	LOE	Country
Iplikcioglu	2023	World Neurosurgery	N	N	NR	NR	Turkey
Lamas	2023	European Spine Journal	Y	NR	Retrospective	3	France
Urata	2023	Medicina	N	N	Retrospective	NR	Japan
Charles	2022	European Spine Journal	Y	Y	Retrospective	4	France
Igawa	2022	Medicina	N	N	Retrospective	NR	Japan
Gerilmez	2021	World Neurosurgery	N	NR	Prospective	NR	Turkey
Hey	2021	Spine deformity	NR	N	Retrospective	3	Singapore
Lee	2021	J Korean Neurosurgery Society	N	NR	Retrospective	NR	South Korea
Shimizu	2021	Spine	N	N	Retrospective	NR	Japan
Abe	2020	AOTS	N	N	Retrospective	4	Japan
George	2020	Spine deformity	Y	N	Retrospective	4	USA
Lee	2019	World Neurosurgery	N	NR	Retrospective	NR	South Korea
Moses	2019	The Spine Journal	Y	N	Retrospective	NR	USA
Passias	2019	Journal of Spine Surgery	N	NR	Retrospective	NR	USA
Akbar	2018	JNS Spine	Y	NR	Retrospective	4	Germany
Hey	2018	The Spine Journal	N	N	Prospective	NR	Singapore
Iorio	2018	Global Spine Journal	Y	N	Retrospective	NR	USA
Khalil	2018	European Spine Journal	N	Y	NR	NR	Lebanon
Sabou	2018	European Spine Journal	N	N	Retrospective	NR	UK
Theologis	2018	Spine	N	NR	Prospective	3	USA
Oe	2017	European Spine Journal	Y	Y	Retrospective	NR	Japan
Ramchandran	2017	European Spine Journal	N	NR	Prospective	NR	USA
Hasegawa	2016	European Spine Journal	N	NR	Prospective	NR	Japan
Iyer	2016	Spine Deformity	N	N	NR	NR	USA
Lafage	2016	Neurosurgery	Y	NR	Retrospective	NR	USA
Matsubayashi	2015	Global Spine Journal	Y	NR	Retrospective	4	Japan

Abbreviations: COI, Conflict of interests; N, No; Y, Yes; NR, Not reported; LOE, Level of evidence

Quality assessment using the MINORS criteria indicated that four studies scored 8 out of 12 points, four scored 7 out of 12, 17 scored 6 out of 12, and one scored 5 out of 12 (Table 2).

Table 2.

Risk of bias assessment according to methodological index for non-randomised studies (MINORS)*.

Author	Date	1. A clearly stated aim	2. Inclusion of consecutive patients	3. Prospective collection of data	4. Endpoints appropriate to the aim of the study	Global score /12
Iplikcioglu	2023	2	1	2	2	7
Lamas	2023	2	2	0	2	6
Urata	2023	2	2	0	2	6
Charles	2022	2	2	1	2	7
Igawa	2022	2	2	0	2	6
Gerilmez	2021	2	2	1	2	7
Hey	2021	2	1	0	2	5
Lee	2021	2	2	0	2	6
Shimizu	2021	2	2	0	2	6
Abe	2020	2	2	0	2	6
George	2020	2	2	0	2	6
Lee	2019	2	2	0	2	6
Moses	2019	2	2	0	2	6
Passias	2019	2	2	0	2	6
Akbar	2018	2	2	0	2	6
Hey	2018	2	2	2	2	8
Iorio	2018	2	2	0	2	6
Khalil	2018	2	2	0	2	6
Sabou	2018	2	2	0	2	6
Theologis	2018	2	2	1	2	7
Oe	2017	2	2	0	2	6
Ramchandran	2017	2	2	2	2	8
Hasegawa	2016	2	2	2	2	8
Iyer	2016	2	2	2	2	8
Lafage	2016	2	2	0	2	6
Matsubayashi	2015	2	2	0	2	6

“Question 6: Follow-up period appropriate to the aim of the study” and “Question 7: Loss to follow up less than 5%” were not completed as the present study only focused on preoperative measurements.

Characteristics of Patients and Asymptomatic Individuals

Of the 15 studies that reported on patients, the most common pathologies were cervical or thoraco-lumbar deformities (n = 9), such as dropped head syndrome or scoliosis, and degenerative conditions (n = 3), such as myelopathy or arthritis (Table 3). The cohort size ranged from 13 to 2599 patients per study, with a proportion of males ranging from 0% to 100%. The mean age ranged from 15.5 to 76.7 years.

Table 3.

Patient characteristics.

Author	Date	Cohort	Pathology/symptoms (if any)	n	Sex		Age
Author	Date	Cohort	Pathology/symptoms (if any)	n	Males (%)	Females (%)	Mean ± SD	Range
Patients
Deformity pathologies
Urata	2023		Dropped head syndrome	43		100.0%	74.3 ± 6.4
Igawa	2022		Dropped head syndrome	96	11.5%	88.5%	76.7 ± 9.3
George	2020		Spine deformity w/ or w/o spinal implants	90	15.6%	84.4%	49.7	(18– 76)
Passias	2019		Cervical deformity w/ CBVA >25°	84	37%	63%	61 ± 11.0
Akbar	2018		Adolescent idiopathic scoliosis, cobb angle >40°	81	26.0%	74.0%	15.5 ± 3.5	(10– 19)
Sabou	2018		Cervico-throacic kyphotic deformity	13	100.0%		57.5 ± 11.3	(40– 74)
Ramchandran	2017		Cervical deformity w/ CBVA >25°	75	44%	56%	61.3 ± 10.4
Matsubayashi	2015		Occipitocervical deformity w/ or w/o myelopathy	27	25.9%	74.1%	56	(14– 83)
Degenerative pathologies
Charles	2022		Spondylolysis, low back or radicular pain	2599	42.7%	57.3%		(5– 93)
Shimizu	2021	Total	Rheumatoid arthritis or degenerative conditions	22	45.5%	54.5%	62.1 ± 16.8
		C0-C2 increased post-op		10	40.0%	60.0%	59.2 ± 19.3
		C0-C2 decreased post-op		12	50.0%	50.0%	64.2 ± 14.8
Abe	2020	Total	Cervical spondylotic myelopathy	110	61.8%	38.2%	72.3	(45– 88)
		CSA increased post-op	Cervical spondylotic myelopathy	63	68.3%	31.7%	72.6 ± 12.0
		CSA decreased post-op	Cervical spondylotic myelopathy	47	53.2%	46.8%	72.5 ± 9.2
Unspecified pathologies
Lee	2021		Mild neck and back pain	168	75.6%	24.4%	38.4 ± 12.6	(20– 60)
Lee	2019		Mild neck and back pain	71	33.8%	66.2%	30.8 ± 8.9
Moses	2019		Primary cervical spinal pathology	329	44.4%	55.6%	56.8 ± 14.5
Lafage	2016		Symptomatic	303	26.0%	74.0%	54.8 ± 15.1
Asymptomatic individuals
Iplikcioglu	2023	Total		78	53.8%	46.2%	30.62 ± 10.8	(16– 50)
		Cervical kyphosis		18	44.4%	55.6%
		Cervical lordosis		60	56.7%	43.3%
Gerilmez	2021			75				(18– 50)
Hey	2021			100	49.0%	51.0%	45 ± 15.9
Hey	2018			67	50.7%	49.3%	46.8 ± 17.0
Iorio	2018			118	31.4%	68.6%	50.5 ± 16.9
Khalil	2018	Total		144	50.7%	49.3%	29 ± 11.0	(18– 59)
		C2-C7 Cobb < -5° (kyphotic)		46	39.1%	60.9%	26 ± 9.0
		C2-C7 Cobb -5°– 5° (straight)		39	48.7%	51.3%	30 ± 11.0
		C2-C7 Cobb > 5° (lordotic)		59	61.0%	39.0%	30 ± 11.0
Theologis	2018	Total		87	26.4%	73.6%	49 ± 16.0	(22– 77)
		Roussouly Type I		8	50.0%	50.0%	37 ± 12.0	(23– 60)
		Roussouly Type II		47	29.8%	70.2%	47 ± 17.0	(22– 76)
		Roussouly Type III		19	15.8%	84.2%	52 ± 15.0	(28– 77)
		Roussouly Type IV		13	15.4%	84.6%	55 ± 16.0	(28– 76)
Oe	2017	W/ no mirror (2012 measurements)		354	40.1%	59.9%	72.3 ± 7.1	(52– 88)
Oe		W/ mirror (2014 measurments)		354	40.1%	59.9%	74.3 ± 7.1	(52– 88)
Hasegawa	2016			126	23.8%	76.2%	39.4 ± 11.3	(20– 70)
Iyer	2016	Total		115	31.3%	68.7%	50.1	(22– 78)
		21-30 years old		20	25.0%	80.0%
		31-40 years old		18	33.3%	72.2%
		41-50 years old		17	23.5%	88.2%
		51-60 years old		16	18.8%	81.3%
		61-70 years old		27	33.3%	51.9%
		>71 years old		17	52.9%	47.1%
Both patients (w/ deformity pathologies) and asymptomatic individuals
Lamas	2023		Adult scoliosis (symptomatic patients)	478	31.6%	68.4%		(40– 88)

Abbreviations: CSA, cervical sagittal axis; CBVA, chin-brow veritcal angle; SD, standard deviation.

Of the 10 studies that reported on asymptomatic individuals, the cohort size ranged from 67 to 354 subjects per study, with a proportion of males ranging from 23.8% to 50.7%. The mean age ranged from 29.0 to 72.3 years.

In the study that reported on both patients and asymptomatic individuals, there were 243 patients with adult scoliosis and 235 asymptomatic individuals, with an overall proportion of males of 31.6% and age ranging from 40 to 88 years.

“De facto” Parameters that Evaluate Horizontal Gaze

The two most frequently reported “de facto” horizontal gaze parameters were McGregor’s slope (n = 20 studies),^{1,2,7,10,24-32,35-37,39,40,42,44} and CBVA (n = 12 studies)^{1,2,6,7,28,33,34,37,39,41-43} (Table 4). Mean McGregor’s slope was −10.2-22.2° for patients (n = 14 studies)^{1,2,7,24-32,35,44} and −8.8-10.2° for asymptomatic individuals (n = 7 studies).^{10,36,37,39,40,42,44} Mean CBVA was −9.8-9.8° for patients (n = 6 studies)^{1,2,7,28,33,34} and −5.9-12.7° for asymptomatic individuals (n = 6 studies).^{6,37,39,41-43} Furthermore, 8 other “de facto” parameters were described to evaluate horizontal gaze, including slope of line of sight (SLS) (n = 7 studies),^{1,7,28,36,37,39,42} tangent to the hard palate (THP) (n = 3 studies),^37,38,41 orbital-internal occipital protuberance slope angle (OIOP) (n = 2 studies),^37,38 occipital incidence (n = 2 studies),^6,43 Chamberlain’s slope (n = 1 study),² cranial incidence (n = 1 study),¹⁰ midpoint of the hard palate (n = 1 study),³⁸ and base of sella turcica (n = 1 study).³⁸

Table 4.

Horizontal gaze parameters.

Author	Date	Cohort	n	“De facto” parameters that evaluate horizontal gaze											Parameters that describe compensatory mechanisms which affect horizontal gaze						Neither nor
				McGregor's slope (°)	CBVA (°)	SLS (°)	THP (°)	OIOP (°)	Occipital incidence (°)	Chamberlain's slope	Cranial incidence (°)	Midpoint of hard palate	Base of sella turcica	C0-C2 angle (°)	C0 slope (°)	C1 slope (°)	Orbital slope (°)	Orbital tilt (°)	Cranial tilt (°)	Cranial slope (°)	Mandibular slope
				Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD	Value ± SD
Patients
Deformity pathologies
Urata	2023	Pathological	43	14 ± 20.3
Igawa	2022		96	22.2 ± 24.0
George	2020		90	−1.0 ± 7.4	3.3 ± 7.5					3.5 ± 7.5											31.2 ± 10.3
Passias	2019		84	5.7
		Subaxial upper-most intrumented vertebra (UIV)		0.7 ± 11.7										33.9 ± 11.1	−3.2 ± 15.5	−2 ± 20.2
		C2 UIV		10.2 ± 15.6										35 ± 11.5	3.6 ± 15.2	6.2 ± 18.9
Akbar	2018	Total	81
		Hyperlordotic		5.4 ± 6.7	4.8 ± 3.7	8.6 ± 8.4								21.7 ± 9.6	0.32 ± 7.6	-5.8 ± 11.3
		Normolordotic		3.3 ± 6.1	9.8 ± 11.1	6.0 ± 9.0								23.1 ± 8.7	-1.5 ± 6.2	-8.4 ± 8.7
		Hypokyphotic		2.4 ± 4.2	7.3 ± 9.1	6.3 ± 7.2								25.3 ± 5.0	-2.0 ± 6.0	-7.1 ± 8.0
		Normokyphotic		5.8 ± 7.5	9.0 ± 10.6	7.7 ± 9.4								20.4 ± 10.6	0.3 ± 7.4	-7.1 ± 11.7
		Global alignment (posterior)		4.5 ± 5.1	9.1 ± 8.6	10.4 ± 6.7								23.7 ± 6.3	−0.99 ± 5.9	-8.0 ± 8.7
		Global alignment (anterior)		4.1 ± 7.9	7.1 ± 12.1	−1.6 ± 6.8								21.3 ± 11.0	-0.27 ± 7.9	-5.9 ± 11.9
Sabou	2018		13		54 ± 11.1									38.9 ± 1.9
Ramchandran	2017		75		-6.2 ± 50.3
		C2−C7 Cobb < 0° (lordotic)	29		-1.2 ± 51.1									34.5 ± 11.7
		C2−C7 Cobb 0°–10° (mildly kyphotic)	16		-3.2 ± 12.2									36.8 ± 9.3
		C2−C7 Cobb >10° (severely kyphotic)	30		-9.3 ± 53.2									43.7 ± 9.8
Matsubayashi	2015		27	−4.0 ± 6.7										4.7 ± 10.7
Degenerative pathologies
Charles	2022	Total	2599
		Female	1488	−0.5 ± 13.7										18.5 ± 10.1
		Male	1111	−0.1 ± 11.6										16.6 ± 9.7
		Low PI (<45°)	972	0.3 ± 10.7										17.0 ± 10.0
		Medium PI (45−60°)	1123	−0.7 ± 12.8										17.9 ± 9.8
		High PI (>60°)	504	−0.6 ± 16.1										18.7 ± 10.1
		5-9 years	94	−0.6 ± 10.1										13.6 ± 10.3
		10-14 years	516	2.1 ± 9.1										15.7 ± 9.4
		15-19 years	448	1.5 ± 12.0										17.1 ± 10.3
		20-34 years	224	0.7 ± 14.2										17.4 ± 8.3
		35-49 years	424	−0.4 ± 11.7										17.8 ± 9.6
		50-64 years	449	−2.7 ± 16.6										19.1 ± 9.4
		65-79 years	340	−3.5 ± 9.5										19.6 ± 10.7
		>80 years	104	−0.9 ± 20.6										22.4 ± 12.0
Shimizu	2021	Total	22
		C0-C2 increased post-op	10	−6.2 ± 7.8										7.3 ± 5.7
		C0-C2 decreased post-op	12	−2.1 ± 7.6										10.8 ± 5.5
Abe	2020	CSA increased post-op	110
		CSA decreased post-op	63	7.2 ± 5.7										16.5 ± 7.9
		47	5.5 ± 4.1											19.6 ± 11.6
Unspecified pathologies
Lee	2019	Full cohort	168	15.5 ± 8.8										26.1 ± 8.9
		Whole spine radiograph		8.4 ± 8.4										20.9 ± 9.4
		Cervical spine radiograph
		Fixed horizontal gaze group	71	11.2 ± 9.0										23.9 ± 7.1
		Whole spine radiograph		13.5 ± 7.6										25.7 ± 7.2
		Cervical spine radiograph
		Non-fixed horizontal gaze group	329	19.2 ± 6.9										28.1 ± 9.9
		Whole spine radiograph		4 ± 6.4										16.7 ± 9.1
		Cervical spine radiograph
Lee	2021		119	11.3 ± 7.3										19.2 ± 8.3		19 ± 8.0
Moses	2019		329*	5.02 ± 8.1	2.3 ± 7.6	−1.59 ± 2.0
Lafage	2016		303	−0.9 ± 8.4	0.7 ± 8.1	0.6 ± 8.5
		CBVA neutral position -4.8–17.7		1.8 ± 6.3	3.7 ± 5.3	3.7 ± 5.7								26.3 ± 13.2
		CBVA acending gaze <-4.8		−10.2 ± 6.5	−9.8 ± 4.2	-10.6 ± 4.4							32.6 ± 13.2
Asymptomatic individuals
Iplikcioglu	2023	Total	78	8.8 ± 9.6										18.6 ± 10.1		18.27 ± 9.0
		Cervical kyphosis	18	3.1 ± 6.7										21.9 ± 10.2		13 ± 9.2
		Cervical lordosis	60	10.2 ± 9.1										17.6 ± 10.2		20 ± 9.8
Gerilmez	2021	CI=CT+CS	75	3.2 ± 8.0							31.38 ± 4.6			15.9 ± 4.8					28.2 ± 8.4	3.2 ± 8.0
Hey	2021		100	−3.2 ± 5.6	1.1 ± 5.5	0.45 ± 5.3	-0.17 ± 6.3	5.0 ± 4.7
Hey	2018		67					1.5 ± 7.3	5.7 ± 6.1			-40.6 ± 4.8	−3.0 ± 5.9
Iorio	2018	Total	118
		<35	30	7.8 ± 8.1	6 ± 7.1	5.4 ± 7.8								19.1 ± 9.7
		35-44	18	0.8 ± 4.9	−1.8 ± 6.8	−2.7 ± 5.6								23.3 ± 7.9
		45−54	17	1.6 ± 7.3	0.7 ± 9.6	-1.6 ± 9.3								21.6 ± 9.3
		55-64	21	0.9 ± 9.5	1.3 ± 8.7	−1.7 ± 9.0								19.7 ± 7.7
		≥65	32	2.2 ± 7.9	1.7 ± 1.7	0.1 ± 7.7								21 ± 7.6
Khalil	2018	Total	144		4 ± 13.0
		C2-C7 Cobb < −5° (kyphotic)	46		6 ± 6		6							42 ± 8					10
		C2-C7 Cobb -5°– 5° (straight)	39		5 ± 6									36 ± 7					10
		C2-C7 Cobb > 5° (lordotic)	59		1 ± 6									30 ± 8					9
Theologis	2018	Total	87		-1 ± 9				81 ± 8					−28 ± 9	10 ± 9		19 ± 8	68 ± 9
		Roussouly Type I	8		2 ± 8				84 ± 7					−32 ± 5	12 ± 6		18 ± 6	67 ± 8
		Roussouly Type II	47		-2 ± 10				80 ± 9					−27 ± 9	8 ± 9		18 ± 9	70 ± 10
		Roussouly Type III	19		-2 ± 6				82 ± 8					−28 ± 9	11 ± 9		19 ± 7	69 ± 7
		Roussouly Type IV	13		-1 ± 8				82 ± 8					−31 ± 6	13 ± 10		21 ± 7	68 ± 8
Oe	2017	2012, without a mirror	354	2.2 ± 10.9	12.7 ± 6.9	11.5 ± 9.0
Oe		2014, with a mirror	354	−8.8 ± 7.6	2.5 ± 6.7	4.4 ± 5.1
Hasegawa	2016		126	−3.4 ± 11.1
Iyer	2016	Total	115		-1.7 ± 7.8				67.9 ± 14.5					−27.4 ± 9.4	9.4 ± 8.5		31.4 ± 13.3	68.4 ± 8.4
		21-30	20		-4.2 ± 6.0				63.9 ± 12.9					−27.3 ± 8.6	5.4 ± 7.3		31.6 ± 11.3	72.8 ± 5.9
		31-40	18		-0.1 ± 9.4				66.5 ± 13.4					−25.2 ± 11.6	8.6 ± 9.3		32.1 ± 12.8	67.6 ± 9.4
		41-50	17		-1.4 ± 6.2				68.00 ± 10.5					−29.5 ± 9.4	10.3 ± 7.3		31.8 ± 12.1	67.1 ± 7.7
		51-60	16		0.5 ± 7.0				67.00 ± 13.6					−26.3 ± 8.0	11.3 ± 8.4		34.2 ± 12.5	66.4 ± 7.6
		61-70	27		0.3 ± 8.9				70.8 ± 19.0					−25.4 ± 8.7	11.9 ± 9.7		30.7 ± 17.6	66.2 ± 10.8
		>71	17		-5.9 ± 6.8				71.4 ± 15.8					−31.1 ± 9.7	8.6 ± 7.9		27.7 ± 11.7	70.4 ± 5.7
Both patients (with deformity pathologies) and asymptomatic individuals
Lamas	2023	Total	478
		Asymptomatic (40-60y)	136	−0.33 ± 6.7										91.7 ± 15.8
		Low PI <45°(n=26)		−1.21 ± 8.1										101.5 ± 13.4
		Medium PI 45-60° (n=75)		4.3 ± 30.6										99.9 ± 10.4
		High PI >60° (n=35)
		Asymptomatic (>60y)	99	−0.38 ± 9.4										94.8 ± 20.1
		Low PI <45°(n=5)		2.6 ± 8.1										96.6 ± 11.3
		Medium PI 45-60° (n=51)		2.5 ± 8.7										97.5 ± 11.5
		High PI >60° (n=43)
		Adult scoliosis (40-60y)	72	0.78 ± 9.1										92.1 ± 12.5
		Low PI <45° (n=22)		0.72 ± 13.8										90.7 ± 12.1
		Medium PI 45-60° (n=32)		4.5 ± 12.1										95.2 ± 14.5
		High PI >60° (n=18)
		Adult scoliosis (>60y)	171	3.6 ± 6.8										91.4 ± 14
		Low PI <45° (n=35)		1.7 ± 10.2										94.8 ± 15
		Medium PI 45-60° (n=75)		3.4 ± 10.7										92.0 ± 13.4
		High PI >60° (n=61)

Abbreviations: CBVA, chin brow vertical angle; CSA, cervical sagittal axis; PI, pelvic incidence; SLS, slope line of sight; OIOP, orbital-internal occipital protuberance slope angle; THP, tangent to the Hard Palate.

Among all included patients, 171 patients (52.0%) had CBVA, 281 (85.4%) had McGregor's slope, and 259 (78.7%) had SLS visible on their full spine radiographs.

Parameters that Describe Compensatory Mechanisms which Affect Horizontal Gaze

The most frequently reported parameter that describes compensatory mechanisms which affect horizontal gaze was C0-C2 angle (n = 18 studies)^{1,6,10,25,28-35,39-41,43-45} (Table 4), with a mean value of 4.7-95.2° for patients (n = 12 studies)^{1,25,27-35,44} and −32.0-101.5° for asymptomatic individuals (n = 7 studies).^{6,10,39-41,43,44} Furthermore, 6 other parameters that describe compensatory mechanisms which affect horizontal gaze were described, including C0 slope (n = 4 studies; also known as occipital slope and McRae slope),^6,28,32,43 C1 slope (n = 4 studies),^28,29,32,40 orbital slope (n = 2 studies),^6,43 orbital tilt (n = 2 studies),^6,43 cranial tilt (n = 2 studies),^10,41 and cranial slope (n = 1 study).¹⁰

One additional parameter was identified from the literature: the mandibular slope (n = 1 study)² (Table 4), which is neither a “de facto” parameter that evaluates horizontal gaze nor a parameter that describes compensatory mechanisms, but it still provides useful information regarding horizontal gaze.

Sub-analysis to Compare Patients with Deformity Pathologies vs Degenerative Pathologies

Mean McGregor’s slope was −4.0-22.2° for patients with deformity pathologies (n = 6 studies) and −6.2-7.2° for patients with degenerative pathologies (n = 3 studies); there was a trend of lower McGregor’s slope in patients with degenerative pathologies (Table 4). Mean CBVA was −9.3-9.8° for patients with deformity pathologies (n = 4 studies), while no CBVA values were reported for patients with degenerative pathologies (n = 0 studies). Mean C0-C2 was 4.7-43.7° for patients with deformity pathologies (n = 5 studies) and 7.3-22.4° for patients with degenerative pathologies (n = 3 studies); there was a trend of lower C0-C2 in patients with degenerative pathologies.

Observer Reliability

Only two studies reported observer reliability for horizontal gaze parameters (Appendix I). George et al² reported excellent inter-observer reliabilities for McGregor’s slope (0.90, P < 0.001), Chamberlain’s slope (0.81, P < 0.001), and mandibular slope (1.0, P < 0.001). Iyer et al⁶ reported excellent inter-observer reliabilities for CBVA (0.98, p = not reported (NR)), C0-C2 angle (0.91, p = NR), orbital slope (0.80, p = NR), orbital tilt (0.97, p = NR), and C0 slope (0.95, p = NR), but good reliability for occipital incidence (0.69, p = NR).

Correlations

Many correlations have been reported between horizontal gaze parameters, both among themselves and in relation to other spinal and hip parameters (Table 5). The most frequently reported correlations were between McGregor’s slope and C0-C2 angle (R,-0.390-0.676; P < 0.065; n = 4 studies), McGregor’s slope and CBVA (R, 0.679-0.862; P < 0.0001; n = 3 studies), as well as CBVA and SLS (R, 0.592-0.996; P < 0.001; n = 3 studies).

Table 5.

Horizontal gaze parameters and their correlations with other horizontal gaze or spinal parameters.

Parameters (°)	Author	Date	McGregor’s slope (°)		CBVA (°)		C0-C2 angle (°)		C1 slope (°)		Cranial slope (°)		Occipital incidence (°)		Orbital slope (°)		Orbital tilt (°)		C0 slope (°)
Parameters (°)	Author	Date	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value	Coefficient	P-value
McGregor’s slope
CBVA	George	2020	0.810
	Moses	2019	0.830	<0.001
	Lafage	2016	0.862	<0.001
	Hey	2021	0.679	<0.001
	Iyer	2016											0.099	NS*	0.411	<0.01	−0.879	<0.01	0.727	<0.01
C1 slope	Lee	2021	0.700	<0.05
C1 slope	Iplikcioglu	2023	0.495	0.0002
Cranial slope	Gerilmez	2021					0.214	0.065
SLS	Moses	2019	0.900	<0.001	0.890	<0.001
	Lafage	2016			0.996	<0.001
	Hey	2021			0.592	<0.001
Chamberlain's slope	George	2020			0.850	<0.001
Mandibular slope	George	2020			0.800	<0.001
OIOP	Hey	2021			0.697	<0.001
THP	Hey	2021			−0.504	<0.001
Orbital slope	Iyer	2016											−0.814	<0.01
Orbital tilt	Iyer	2016											−0.156	NS*	−0.419	<0.01
C0 slope	Iyer	2016											0.436	<0.01	0.238	<0.05	−0.827	<0.01
C2 slope	Lee	2021	0.420	<0.05					0.680	<0.05
	Iplikcioglu	2023	−0.541	<0.00001			0.434	0.00024	−0.628	<0.00001
	Gerilmez	2021	−0.827	0.000							−0.827	0.000
C7 slope	Lee	2021	−0.130	NS*					−0.120	NS*
C7 slope	Gerilmez	2021	0.146	0.212			−0.136	0.246			0.146	0.212
C2−C7 SVA	Lee	2021	−0.250	<0.05					−0.370	<0.05
	Gerilmez	2021	−0.437	0.000							−0.437	0.000
	Iyer	2016			−0.552	<0.01	−0.374	<0.01					−0.052	NS*	0.162	NS*	0.407	<0.01	−0.294	<0.01
C0-C7 angle	Lee	2021	0.780	<0.05					0.570	<0.05
C0-C7 angle	Matsubayashi	2015	−0.680	<0.001			0.300	NS*
C0-C1 angle	Iplikcioglu	2023					0.638	<0.00001
C0-C2 angle	Lee	2021	0.470	<0.05					−0.040	NS*
	Matsubayashi	2015	−0.390	<0.05
	Iplikcioglu	2023	0.676	<0.00001
	Gerilmez	2021	0.214	0.065							0.214	0.065
	Iyer	2016			−0.133	NS*							−0.282	<0.01	−0.007	NS*	0.308	<0.01	−0.461	<0.01
C1-C2 angle	Iplikcioglu	2023					0.364	0.0023
C2-C7 angle	Lee	2021	0.380	<0.05			−0.440	<0.05	0.570	<0.05
	Matsubayashi	2015	−0.310	NS*			−0.500	<0.01
	Iplikcioglu	2023	0.320	0.0078			−0.281	0.0203
	Gerilmez	2021	0.583	0.000							0.583	0.000
	Hasegawa	2016	0.125	NS*
SCA	Lee	2021	0.540	<0.05			−0.050	<0.05	0.550	<0.05
SCA	Gerilmez	2021	−0.548	0.000							−0.548	0.000
SVA	Hasegawa	2016	0.318	<0.05
SVA-C7	Charles	2022	−0.053	<0.001			0.059	<0.001
SVA-sella turcica C7	Lee (St)	2021	−0.730	<0.05					−0.740	<0.05
SVA-C2	Charles	2022	0.000	<0.001			−0.149	<0.001
OHDA	Charles	2022	−0.046	<0.001			0.248	<0.001
Thoracic kyphosis	Charles	2022	−0.085	<0.001			−0.058	<0.001
Thoracic kyphosis	Hasegawa	2016	0.556	<0.05
Lumbar lordosis	Charles	2022	0.017	<0.001			0.026	<0.001
Lumbar lordosis	Hasegawa	2016	0.185	<0.05
T1 slope	Lee	2021	−0.120	NS*					−0.150	NS*
	Matsubayashi	2015	−0.160	NS*			0.080	NS*
	Iplikcioglu	2023	0.188	0.1243
	Iyer	2016			−0.256	<0.01	−0.015	NS*					0.080	NS*	−0.097	NS*	0.117	NS*	−0.068	NS*
Pelvic incidence	Charles	2022	−0.025	<0.001			−0.102	<0.001
Pelvic incidence	Hasegawa	2016	−0.093	NS*
Pelvic tilt	Charles	2022	−0.062	<0.001			−0.126	<0.001
Pelvic tilt	Hasegawa	2016	0.121	NS*
Sacral slope	Charles	2022	0.033	<0.001			−0.004	<0.001
Sacral slope	Hasegawa	2016	0.082	NS*

Abbreviations: CBVA, chin brow vertical angle; SLS, slope line of sight; OIOP, orbital-internal occipital protuberance; THP, tangent to the hard palate; SVA, sagittal vertical axis; OHDA, odontoid hip axis angle; SCA, spino-cranial angle; NS, not significant.

*Exact P-value not reported.

Discussion

The present systematic review aimed to summarise the parameters available to measure horizontal gaze, provide their values in patients and/or asymptomatic individuals, and assess their reliability. The most important findings are that, though there are 18 parameters to measure horizontal gaze, there is no gold standard. The present review found 10 “de facto” parameters that evaluate horizontal gaze, seven parameters that describe the compensatory mechanisms which affect horizontal gaze, and one parameter that does neither of the above but still provides useful information regarding horizontal gaze. Furthermore, although the parameters have good to excellent inter-observer reliabilities (0.69-1.0), there are large variations in means among asymptomatic individuals across studies, which implies they may have limited clinical relevance. The findings of this systematic review highlight the need for a gold standard parameter for horizontal gaze, which uses easily identifiable landmarks that are simple to measure (reliable), relates both orbital and cervical anatomical structures, and provides insight into compensatory mechanisms in deformative or degenerative conditions. Furthermore, future studies should investigate the pathologic values of these parameters, as well as their variability among an asymptomatic population and across different spine pathologies.

A recent narrative review¹⁴ that summarised the different measurements of horizontal gaze in patients with cervical deformities included 41 articles, of which the following parameters were described: CBVA (21 studies), McGregor’s slope (19 studies), SLS (6 studies), C0-C2 slope (3 studies), orbital-internal occipital protuberance slope angle (1 study), THP (1 study), mandibular slope (1 study), Chamberlain’s slope (1 study), and the 3-6–12 rule derived from the base of the sella turcica and OIOP (1 study). The review concluded that there is no ideal measurement of horizontal gaze and emphasised that new methods should be studied in order to improve clinical practice. This is in line with the findings of the present systematic review; however, the present review also highlights the need for a novel parameter that considers both orbital and cervical anatomical structures.

Although the literature states that a number of parameters are used to measure horizontal gaze, the present systematic review has grouped these parameters into three categories: “de facto” parameters that evaluate horizontal gaze, parameters that describe the compensatory mechanisms which affect horizontal gaze, and parameters that are neither of the two but still provide useful information regarding horizontal gaze. “De facto” parameters were taken as those that are fixed or are considered fixed, such as the CBVA. In contrast, there are other parameters, such as the C0-C2, which capture partial or complete compensatory mechanisms of the spine. In patients with spinal pathologies, compensatory mechanisms may take place in the trunk to maintain an upright position, which could produce large variations in the compensatory parameters, but not in the “de facto” parameters. There was only one parameter that did not fit either group: the mandibuar slope, which can vary with mouth opening. Interestingly, the sub-analysis to compare patients with deformity pathologies vs those with degenerative pathologies showed that the latter had lower McGregor’s slope and C0-C2. CBVA could not be compared across groups because it was not reported for patients with degenerative pathologies.

The CBVA and McGregor’s slope are the most frequently used to measure horizontal gaze, however, there is no gold standard parameter. While, the CBVA is easy to measure and highly repeatable, it does not consider the relationship between cranial morphology and cervical position and it cannot be consistently measured due to relevant landmarks (the chin and brow) often being unavailable on radiographs.^1,7,8 Furthermore, the CBVA is distorted in cases of mandible protrusion or retraction and is dependent on mouth opening.⁶ McGregor’s slope, on the other hand, accounts for cranial morphology and cervical position but relies on the correct identification of difficult-to-find landmarks (the posterior aspect of the hard palate and the opisthion) that are not always visible on radiographs.^2,9 Other parameters such as the C0-C2 angle^{1,6,10,25,28-35,39-41,43-45} and SLS^{1,7,28,36,37,39,42} have also been used to measure horizontal gaze. These parameters also exhibit high variability across studies in the asymptomatic population. The present systematic review found that asymptomatic individuals had mean CBVA that ranged from −5.9-12.7°, mean McGregor’s slope that ranged from −8.8-10.2°, mean C0-C2 that ranged from −32.0-101.5°, and mean SLS that ranged from −2.7-11.5°. Several studies have also reported high variability in SLS among a healthy population.^1,46 Nonetheless, inter-observer reliabilities were excellent for McGregor’s slope (0.90), CBVA (0.98), and C0-C2 angle (0.91),² indicating that the discrepancy across studies does not stem from difficulty in performing measurements. Furthermore, Oe et al⁴² performed imaging in asymptomatic individuals with and without the use of a mirror and found considerable differences in measurements of McGregor’s slope (−8.8 vs 2.2), CBVA (2.5 vs 12.5), and SLS (4.4 vs 11.5), which may be due to the position of the head.

Various studies have introduced alternative parameters to measure horizontal gaze. Hey et al³⁸ proposed four novel parameters: the midpoint of the hard palate, the base of the sella turcica, THP, and OIOP. The study concluded that the midpoint of the hard palate and THP were poor measures of horizontal gaze as the sloped and curved structure of the hard palate may lead to inaccurate results. Instead, they recommended the use of the base of the sella turcica and OIOP, which may more accurately measure horizontal gaze and help determine gaze direction, potentially serving as an indicator for C0 functional alignment in the measurement of cervical angles. The authors of the present study believe that it is also difficult to identify the base of the sella turcica in standard sagittal radiographs.

The same authors further investigated the use of THP and OIOP in determining gaze direction³⁷ by comparing them to existing measures of horizontal gaze. The study found that OIOP (standard deviation (SD), 4.66) exhibited lowest variability in a population of healthy subjects compared to CBVA (SD, 5.48°), McGregor’s slope (SD, 5.63°), and THP (SD, 6.27°). Among the studied parameters, the authors concluded that OIOP is the most appropriate parameter for measuring horizontal gaze as it is less prone to variations in anatomy and has easy to identify landmarks. However, the OIOP does not relate the orbit to the cervical spine.

George et al² proposed the use of the mandibular slope, defined as the angle created by the inferior edge of the mandibular body and the horizontal. Mandibular slope (1.0, P < 0.001) has a higher interobserver reliability compared to McGregor’s slope (0.90, P < 0.001) and Chamberlain’s slope (0.81, P < 0.001) and is moderately correlated with CBVA (0.80). Unlike the McGregor’s slope and Chamberlian’s slope that rely on the identifcation of the posterior aspect of the hard palate, which is difficult to locate on low-quality radiographs^2,9; the mandibuar slope uses the inferior edge of the mandibule, which is easily identifiable on most radiographs. However, it can yield inaccurate results in patients with fixed coronal plane deformities as both far and near edges of the mandible would be visible on lateral radiographs. The authors suggest using the average slope of both lines in such cases. Furthermore, variations in mandibular morphology, as well as slight mouth opening may also lead to inaccuracies.

The parameters proposed by Hey et al³⁸ and George et al² do not use any landmarks that relate the cranium to the cervical spine, and therefore cannot be used to explain compensatory mechanisms between the head and the spine in the framework of degenerative and deformative conditions. Thus, morphometric parameters that provide deeper insights into cervical spine mechanisms might be preferable to measure horizontal gaze. Gerilmez et al¹⁰ introduced the cranial slope (CS) defined as the angle between the McGregor’s line and the horizontal line; the cranial tilt (CT) defined as the angle between the line connecting the sella turcica and centre of McGregor’s line and the vertical line; and the cranial incidence (CI) defined as the angle between the line perpendicular to the centre of McGregor’s line and the line connecting the sella turcica and centre of McGregor’s line, where CI = CS + CT. Though CS had a strong correlation with McGregor’s slope (0.900, P < 0.001),⁷ it had a weak correlation with C0-C2 angle (0.214, P = 0.065).¹⁰ The study did not report correlations between CI and CT and other horizontal gaze parameters, nor did it report correlations between the three introduced parameters. The inter and intra-observer reliability of these parameters was also not reported.

Iyer et al⁶ measured the C0 slope (named occipital slope (OS) in the article); the orbital tilt (OrT), defined as an angle between the vertical and a line extending from the center of the orbit to the center of McRae’s line; and the occipital incidence (OI), which is a morphometric parameter where OI = OS + OrT. All three parameters showed good to excellent inter-observer reliabilities (OS = 0.80, OrT = 0.97, and CI = 0.69). Furthermore, only OrT had a strong correlation with CBVA (−0.879, P < 0.01), while OS and OI had a weak correlation with CBVA (0.411, P < 0.01 and 0.099, P > 0.05, respectively). Additionally, none of the three parameters had strong correlations with other sagittal spine parameters such as C0-C7 angle, C0-C2 angle and T1 slope. OS, OrT, and OI rely on the McRae line, which requires correct identification of the foramen magnum, which can be challenging to locate. Moreover, OS uses the C0 vertebra as a landmark, which is immobile and may not fully capture the relationship between the cervical spine and the cranium.

The present systematic review has several limitations. First, it was difficult to directly compare studies, as most studies stratified the cohort into different subgroups; therefore, meta-analyses could not be performed. Second, it was not possible to compare horizontal gaze values in pathologic patients due to different pathologies being reported across studies. Furthermore, two studies included patients with a CBVA >25°.^32,33

Conclusion

The present systematic review has identified 18 parameters used to measure horizontal gaze; however, there is no gold standard. Although the identified parameters have good to excellent inter-observer reliabilities, there are large variations in measurements among asymptomatic individuals across studies, which may imply a limited clinical relevance. Therefore, there is still a need for a gold standard parameter for horizontal gaze, which uses easily identifiable landmarks that are simple to measure (reliable), relates both orbital and cervical anatomical structures, and provides insight into compensatory mechanisms in deformative or degenerative conditions.

Supplemental Material

Supplemental Material - Parameters Used to Define Horizonal Gaze: A Systematic Review

Supplemental Material for Parameters Used to Define Horizonal Gaze: A Systematic Review by Féthi Laouissat, MD, Sonia Ramos-Pascual, MEng, PhD, Ankitha Kumble, BSc, Theo Broussolle, MD, Danilo Casasola, MD, Mo Saffarini, Meng, MBA, FRSM, and Alexis Nogier, MD in Global Spine Journal

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by ‘Clinque Trenel’, which provided funding for data analysis and manuscript writing.

ORCID iD

Sonia Ramos-Pascual

Data Availability Statement

Data is available upon request. *

Supplemental Material

Supplemental material for this article is available online.

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