Enthesophytes are bony projections that arise from the sites of ligament, tendon or joint capsule attachment to a bone. They are seen rarely in radiographic findings in young adults, as these bony adaptations are assumed to develop slowly over time. However, in recent years, the presence of an enlarged external occipital protuberance (EEOP) has been observed frequently in radiographs of relatively young patients at the clinic of the lead author. Accordingly, the aim of this project was to assess the prevalence of an EEOP in a young adult population. Analysis involved a retrospective analysis of 218 lateral cervical radiographic studies of 18–30‐year‐old participants. Group A ( n = 108; males = 45, females = 63) consisted of asymptomatic university students, while Group B ( n = 110; males = 50, females = 60) were an age‐matched mildly symptomatic, non‐student population. The external occipital protuberance (EOP) size was defined as the distance from the most superior point of the EOP (origin) to a point on the EOP that is most distal from the skull. To avoid ambiguity, the threshold for recording the size of an EOP was set at 5 mm, and an EOP was classified as enlarged if it exceeded 10 mm. Reliability testing was also undertaken. Results indicated that an EEOP was present in 41% of the total population, with 10% of all participants presenting with an EOP ≥ 20 mm. An EEOP was significantly more common in males (67.4%) than in females (20.3%), with the mean EEOP size for the combined male population (15 ± 7 mm) being significantly larger ( P < 0.001) than for females (10 ± 4 mm). The longest EEOP in the male population was 35.7 mm, while in the female population it was 25.5 mm. Additionally, the mean EEOP size for Group A (14 ± 7 mm) was also significantly greater ( P = 0.006) than that recorded for Group B (12 ± 6 mm). This study identified that an EEOP is a condition that is prevalent in the populations tested. The age of the populations, and the prevalence of EEOP, suggest that biomechanical drivers for this phenomenon may be the main reason for this condition in these populations.

Introduction Entheses are the sites of ligament, tendon or joint capsule attachment to a bone (Claudepierre & Voisin, 2005; D'Agostino & Olivieri, 2006; Jacques et al. 2014). A key role of the enthesis is to distribute force over a large area of the bone surface (Benjamin et al. 2000; McGonagle et al. 2001; Claudepierre & Voisin, 2005). Therefore, a substantial amount of mechanical stress can be absorbed by the interweaving fibres at the insertion (Benjamin & Ralphs, 1998). The formation of enthesophytes, bony projections that arise from the enthesis, is multifactorial, and can be attributed to biomechanical, immunological and/or genetic factors (Shaibani et al. 1993; McGonagle et al. 1998, 2001; Benjamin et al. 2000; Claudepierre & Voisin, 2005; Slobodin et al. 2007; Hardcastle et al. 2014; Jacques et al. 2014). While the hallmarks of spondyloarthritis (SpA), enthesitis and enthesophyte formation (Benjamin & McGonagle, 2001; Jacques et al. 2014) may be ascribed to functional adaptation arising from tensile or compressive mechanical stresses on the enthesis (Benjamin et al. 2000; D'Agostino & Olivieri, 2006; Jacques et al. 2014; McGonagle et al. 2014), a large proportion of research focuses on non‐mechanical aetiologies. Recently, leading researchers on the subject have acknowledged that for better understanding and treatment of SpA, it is vital that future research on the subject focuses on mechanical stress on the enthesis (Jacques et al. 2014; McGonagle et al. 2014). Enthesophytes are seen rarely in radiographic findings in young adults as they are assumed to develop slowly over time (Boden et al. 1990a; Matsumoto et al. 2010). In contrast, enthesophytes are observed commonly on radiographic studies of the aging asymptomatic population (Boden et al. 1990a,b; Shaibani et al. 1993; Malcolm, 2002; Claudepierre & Voisin, 2005; Matsumoto et al. 2010, 2013). Enthesophytes can present on both the axial and appendicular skeleton (McGonagle et al. 2001; Jacques et al. 2014). Symptoms at the entheses are more frequent at the lower extremities, and enthesitis is found most frequently at the heel (Paolaggi et al. 1984; Lehtinen et al. 1994; Olivieri et al. 1998; D'Agostino & Olivieri, 2006). This reason alone may account for the extensive research dedicated to the enthesis of the lower extremities, leaving enthesopathy in sites such as the external occipital protuberance (EOP) largely unexplored. Although not always painful, in some cases enthesitis can be both debilitating and enduring, taking several years to diminish (D'Agostino & Olivieri, 2006). While the relationship between anatomical findings and symptoms may be coincidental (Jensen, 1994), symptoms associated with the area of muscular insertion to the EOP have been documented (D'Agostino & Olivieri, 2006; Marshall et al. 2015). For example, pain at the occipital region is a common complaint by headache sufferers, and differential diagnosis to this condition may include cervicogenic headache, migraine or other primary headache disorders (Dougherty, 2014). In recent years, the presence of an enlarged external occipital protuberance (EEOP) has been observed frequently in radiographs of relatively young patients at the clinic of the lead author (Fig. 1). To the best of the authors’ knowledge, reports concerning enthesophytes projecting out of the EOP are rare in the medical literature (Singh, 2012; Marshall et al. 2015), although a few reports do exist in the anthropological and forensic science literature (Gülekon & Turgut, 2003; Marshall et al. 2015). Accordingly, the aim of this study was to: (i) quantify the prevalence of EEOP within apparently healthy, asymptomatic, young adult participants; and (ii) compare these data with a cohort of mildly symptomatic age‐matched individuals. Figure 1 Open in figure viewer PowerPoint Illustration of an enlarged enthesophyte emanating from the EOP.

Materials and methods This project was provided full ethics approval from the institutional Human Research Ethics Committee. A retrospective radiographic analysis of 218 lateral cervical radiographic studies of 18–30‐year‐old participants was carried out by an experienced observer to identify the prevalence of an EEOP in young adult participants. Group A consisted of 108 asymptomatic university students (males = 45, females = 63) who had volunteered to participate in an unrelated research project, and were radiographed by a researcher not involved with this study. The other sample of 110 lateral cervical radiographs (Group B; males = 50, females = 60) was collected over the same 18‐month period at a single chiropractic clinic by trained radiographers. The population in Group B was mildly symptomatic and reported no specific complaints concerning the EOP. The specific symptoms recorded for Group B were extracted directly from the initial‐patient‐intake‐form that was completed by each patient upon commencing care. Patients that recorded symptomatic complaints greater than mild were excluded from this analysis. The data from Group A (university students) were compared with Group B (an age‐matched non‐university student, clinical population) to determine whether findings were exclusive to this group or common across both populations tested. All radiographs, for both groups, were obtained at the same facility and by the same digital‐capturing equipment. The same capturing techniques were used to collect the radiographs for both groups, with participants instructed to stand in their normal posture looking straight ahead, with their right shoulder in contact with the wall mounted ‘Bucky’. The tube‐to‐‘Bucky’ distance was kept constant at 1.5 m. An experienced clinician conducted all radiographic analyses using standard software (Genesis OmniVue® Genesis Digital Imaging, Los Angeles, CA, USA). During analysis, the clinician was free to magnify the images to increase accuracy (Fig. 2B,D are magnified sections of Fig. 2A,C, respectively). When observed, the size of the EOP was defined and measured in this 2D analysis as the distance in millimetres from the most superior point of the EOP (origin) to a point on the EOP that is most distal from the skull (Fig. 2B,D). To avoid any ambiguity, the threshold for recording the size of an EOP in this study was set at 5 mm, and an EOP was classified as enlarged if it exceeded 10 mm. A simple size‐dependent classification system was also used to classify EOP into four categories: Class I (EOP < 10 mm); Class II (10 mm ≤ EEOP < 20 mm); Class III (20 mm ≤ EEOP < 30 mm); and Class IV (EEOP ≥ 30 mm). Comparative studies have demonstrated strong association between plain radiographic and anatomical presentations (Gore et al. 1986). Importantly, it is acknowledged that the anatomical level of degeneration is frequently worse than the level of degeneration observed in radiographs (Edeiken & Pitt, 1971; Gore et al. 1986). Accordingly, any spur identified using this method is likely to be larger than it appears on the plain radiographs. Figure 2 Open in figure viewer PowerPoint (A,B) Images of a participant from Group A; (C,D) a participant from Group B. (B,D) An enlarged representation of the area surrounding and including the EEOP in (A,C), respectively. (B,D) These images include a measurement line indicating the origin, tip and length of the EEOP. To quantify the accuracy of these measurements, a disc‐shaped metallic object (8 mm in diameter) was attached to the skin adjacent to the C7 spinous processes of all Group A participants (Fig. 2A). The diameter of this object on the radiographs was assessed in 20 participants with the same methodologies used to assess EOP size. The typical error of these measurements (TEM) was less than 1 mm (0.2 mm). Similarly, to account for any perspective‐based (projection) errors resulting from differences in the distance of each participant's EOP from the ‘Bucky’ (as a function of different torso widths), repeated measurements were taken from 11 male and nine female participants. These data differed by less than the typical error (i.e. < 1 mm). As a result, raw data were left unadjusted. Intra‐observer reliability was assessed by having the same assessor repeat the measurements of 20 participants with a minimum of 4 months between analyses. Inter‐observer reliability was assessed by comparing these data with the results recorded by a clinician external to this project who used the same methodologies. Reliability testing involved the development of TEM and intra‐class correlation coefficients (ICC). Intra‐observer reliability data showed that EOP size could be reliably recorded (TEM = 0.5 mm, ICC = 0.99). These data were similar for inter‐observer reliability, although the TEM values were slightly larger (TEM = 1.4 mm, ICC = 0.97). The differences in EEOP size between the groups and genders were determined using two‐way analysis of variance (anova). Differences between non‐parametric variables were determined using Chi‐squared analyses. Standard residual (R) testing was used to represent the magnitude by which the observed frequency of an event happening was above or below the expected value. An R‐value of ≥ 2.0 or ≤ −2.0 represented a value either substantially more or less (respectively) than the expected value (Grimm, 1993). All statistical analyses were performed using the statistics package SPSS for Windows (version 20), with an alpha level of P < 0.05. Data are presented as means [± 1 standard deviation (SD)] unless stated otherwise.

Results Results from anova testing indicated that 41% of the total population presented with EEOP equal or greater than 10 mm. The prevalence of an EEOP was significantly higher in the male (67.4%) than in the female population (20.3%), with the mean EEOP size for the combined male population (15 ± 7 mm) being significantly larger (P < 0.001) than for the combined female population (10 ± 4 mm). Although the mean EEOP size for Group A (14 ± 7 mm) was significantly greater (P = 0.006) than that recorded for Group B (12 ± 6 mm), these data differed by less than 2 mm. There was no interaction effect between gender and group (P = 0.760). The mean value for EEOP in Group A males was 16 ± 7 mm, while the mean value for EEOP size in the male population of Group B was 14 ± 6 mm. The mean value for EEOP in Group A females was 11 ± 5 mm, while the mean value for EEOP in the female population of Group B was 9 ± 3 mm. The total mean across both groups and genders was recorded as 13 ± 6 mm. The longest EEOP in the male population measured 35.7 mm, while in the female population it measured 25.5 mm. Chi‐squared analyses indicated that there were no differences in prevalence (P = 0.571) or size classification of EEOP between groups. Similarly, there were also no differences within genders between groups (females, P = 0.307; males, P = 0.409). However, females were more likely to record Class I EOP than males (P < 0.001), while males were more likely to record Class II and III EEOP than females (P < 0.001; Fig. 3). Approximately half of Group B presented with symptoms associated with the cervical (51.2%), thoracic (50.4%) and/or lumbar (57.6%) regions, with 15.2% reporting mild headaches. There were no significant relationships between the presence of an EEOP and any of the reported symptoms, and none of this group reported specific pain at the EOP. Figure 3 Open in figure viewer PowerPoint Distribution of the external occipital protuberance (EOP) within the various size classifications between genders.

Discussion This study is the first to report and quantify the prevalence of EEOP within apparently healthy, asymptomatic and mildly symptomatic young adults. Forty‐one percent of the total population in this study presented with EEOP. Furthermore, 10% of the participants in this study displayed an EEOP greater than 20 mm in length. The current data indicate that a higher percentage (67.4%) of the males presented with EEOP than the females (20.3%), with the mean size of EEOP also being larger in males than females. These gender‐based differences support those reported previously in forensic and anthropological studies (Gülekon & Turgut, 2003). In contrast to the current findings, Singh (2012) reported just one skull out of the 40 analysed displayed an enlarged spur emanating out of the EOP (8 mm long). Conversely, the conclusion from a recent report that was based on surgical intervention of painful exostosis projecting from the EOP (n = 3) suggested that this condition is a normal variant in predisposed individuals (Marshall et al. 2015). However, due to the small samples and absence of disease‐, trauma‐, postural‐, recreational‐ and occupational‐related data, conclusions cannot be drawn as to the prevalence and/or cause of EEOP. The onset of entheseal disorders may be due to abundance of pathophysiological processes as well as aging due to mechanical factors (Benjamin et al. 2000; McGonagle et al. 2001; Claudepierre & Voisin, 2005). Therefore, the current findings in the young adult population in this study raise two important considerations. Firstly, if the presence of EEOP in young adults is due to pathophysiological processes, the number of affected individuals should be considerably less than the high percentage found in the current study, particularly given that the prevalence of SpA in the young adult Caucasian‐European population is estimated at 0.5–2% (Braun et al. 1998; Sieper et al. 2006; Jacques et al. 2014). Secondly, if the presence of EEOP is due to aging and mechanical factors, the EEOP should appear at a more advanced age than that of the sample population. Accordingly, it would appear that additional factors must be considered as the predominant drivers for this phenomenon. Numerous studies associated with spur formation focus on SpA (McGonagle et al. 2014). Fewer studies implicate mechanical stress as a cause for this degenerative process (McGonagle et al. 2014). Most of the literature involving enthesopathy has been focused on spur formation at the distal joints of the lower extremities (D'Agostino & Olivieri, 2006). Occipital horn syndrome (OHS) is an X‐chromosome‐linked connective tissue disorder and is expressed mostly in male carriers (Bazzocchi et al. 2011). Patients suffering from OHS may present with a slightly subnormal intelligence and autonomic dysfunction conditions (Bazzocchi et al. 2011). In view of the high prevalence of EEOP in the test population and due to their young age, it is unlikely that members of the population involved in this study suffer from SpA or degeneration due to advanced age. Moreover, none of the symptoms associated with OHS was reported by any of the participants. The high percentage (41%) of EEOP presentation in the test population was surprising. The prevalence of an EEOP in the young age group may suggest that excessive forces are acting on the EOP at a younger age. Recent animal studies have demonstrated the significant role mechanical loads play in osteophyte formation (Jacques et al. 2014). Similarly, current magnetic resonance imaging studies have proposed that new bone deposition is more probable at sites of repetitive stress where advanced spinal degeneration and sclerosis was demonstrated unlike sites displaying acute injury that resolves completely (Maksymowych et al. 2013; Jacques & McGonagle, 2014). Although not the primary focus of this research, EEOP in the test populations may be attributed to, and explained by, the extensive use of screen‐based activities by children and adolescents (Straker et al. 2008; Torsheim et al. 2010; Gustafsson et al. 2011; Brink et al. 2015), and the associated poor posture (Brink et al. 2015). These data may also explain the significantly larger EOP size presented by Group A (university students) compared with Group B (mildly symptomatic clinical population). However, the EOP size differed by less than 2 mm between these groups, a measure close to the inter‐observer TEM, and so this difference is probably not clinically meaningful. Accordingly, in the absence of reduction in the mechanical stressors, it is likely that these enthesophytes will increase in size as part of the normal ageing processes. The original findings of this study have a number of implications for future research. The most profound value of detecting EEOP at an early age is that it may serve as an indicator, alerting clinicians and individuals to the potential risk of early development of preventable musculoskeletal disorders related to poor posture and biomechanical stress. Although the presence and size of EEOP in this young adult population appears to be asymptomatic, it is probable that increased growth of these enthesophytes may instigate or exacerbate symptoms associated with ageing. The authors acknowledge that the results may be specific to the test populations and may not be generalised to other age groups. Further research into this phenomenon across all age groups is required. Similarly, the absence of postural and ergonomic data restricts definitive conclusions on the causes of EEOP in the test population. However, the age of the population and high incidence of EEOP suggests that it is unlikely that the current observations are a result of aging‐, genetic‐ or disease‐related processes.

Conclusion This detailed analysis is the first of its kind to be used in the assessment of the prevalence of EEOP in the young adult population. The measurement techniques are shown to be both valid and reliable. The comparatively young age of the population examined and the high prevalence of EEOP recorded in this study suggest that biomechanical drivers should be considered as a primary cause of this condition in this population. The findings were more significant than anticipated with regard to the prevalence of this condition and the size of the enthesophytes with the populations tested. The current findings represent an important research advance for two reasons: (i) they identify, quantify and report the EEOP phenomenon in young adults; and (ii) the prevalence of EEOP in the young adult population serves as an early warning to the development of further preventable poor posture‐related conditions in the future. This later observation may be related to the growing concerns amongst researchers and societies pertaining to the increased use of hand‐held technologies from early childhood, and may suggest that early prevention and intervention should be considered.

Acknowledgement The authors thank Lee Daffin for his contribution during both data collection and reliability testing, and Professor Richard G. Burns for his valuable editorial advice.