Laurent Chazée

Mélanie Requier-Desjardins

Sofia Ribeiro-Lopes

Zamir Dedej

Jula Selmani

Enea Zenuni

Agim Dardha

Lorela Lazaj

Nadjiba Bendjedda

Samia Berkane

Moussouni Loutfi

Siham Bakour

Karima Rakem

Naima Ait Iftène

Sara Benkacimi

Hayat Zohra

Dekkal Rammas

Asma Ferroudja

Marijana Bechinia

Valarija Kapa

Danijel Hima

Norma Katicin

Maja Vlato Fressel

Marija Rozac

France : Veres

Ghislaine Ferrere

Serge Colombaud

Sonia Ducourtioux

Michèle Sauchis

Frédéric Lamouroux

Cécile Lamouroux

Boris Brunelin

Caroline Meffre

Marion Suc

Sophjie Disset

Alexandra Vaysse

Anaïs Cheron

Véronique Paliard

Hussam Alwayadat

Maen Smadi

Mohammed Zaarour

• Lebanon

Bassima Khatib

Jamal Hamzeh

Jano Banbokian

Ramadan Ghassan

Issam Jaradi

Montenegro : Sidawi

Aleksandra Ivanović

Marija Bajković

Aleksandar Brinić

Jelena Ducic

Nicola Stojnic

Ildiko Grnya

Novia Stankovic

Slovenia : Gordana Beltram

Iztok Stornik

Janez Kastelic

Bojana Lipej

• Tunisia

Abid Habib

Hela Guidara

Mohamed Ben Ali

Moez Hriz

Imen Rais

Iam Montpellier

Soukaina Anougmar

Christian Kull

Valérie Boisvert

Mialy Andriamahefazafy

Riccarda Wintsch

Nicolas Stenger

David Sheldon

Lucien Rüdlinger

Adrien Pernet

Christelle Pahud

Davide Guenzani

Louka Andenmatten

Celina Areski

Théo Héritier

Monitoring of recreational and educational services provided by Mediterranean wetlands -SYNTHESIS FOR DECISION-MAKERS AND MANAGERS

This synthesis targeted to decision-makers and wetlands managers is extracted from the full report of the 2017 monitoring exercise, realized by Tour du Valat and IAM Montpellier between January and August 2018. We have not analyzed the results at country level because, except Algeria, there were not enough sites to get sound results at this scale.

The 2017 monitoring results and analysis in 2017, based on 27 sites in 10 Mediterranean countries could be carried-out thanks to the participation des of Country representatives, site managers, staff including students, and visitors that were patient enough to reply to, or fill in, the questionnaires.

Synthesis for national decision-makers and wetlands managers

The Indicator

The Indicator on recreational and Educational services of Mediterranean wetlands (RES-MW) aims at measuring with a harmonized protocol among sites, the human and social impacts that wetlands provide amongst visitors of these ecosystems. This monitoring provides a contribution of cultural wetland services to the human well-being. Developed and tested between 2011 and 2016 by Tour du Valat and the Mediterranean Agronomic Institute of Montpellier (IAMM), it constitutes the first specific indicator of wetlands ecosystems for the Mediterranean Wetlands Observatory (MWO). This monitoring took place in 27 out of the 150 Mediterranean wetlands benefiting of a visitor center or permanent management team.

This indicator is a composite and non-monetary impact index, with value ranging from « 0 » to « 1 ».This index was elaborated based on the multi-capital method (Graph 1) with the following logic:

-A Natural Capital (wetlands) -When made accessible through a Constructed Capital (visitor infrastructures and services made by manager) -Generate impact on Human Capital and Social Capital among visitors.

Graph 1: Number of visitor's interviews realized by site

The indicator is then measured through a series of 12 variables (3 for each of the four capital), based on data collected from 19 questions (16 from site manager and 3 from visitors). For each site, a total of 150 visitor interviews were recommended, to take into account the diversity of recreational and educational profiles of visitors. 1 The monitoring of this indicator starts at wetland site level and aggregations of results and analysis are possible at national, ecological zones, sub-regions and Mediterranean Basin levels. This indicator is targeted to national and local decision-makers as well as to site managers, identified as key actors involved in wetlands management decision process. It informs these targeted users on social and human advantages provided by these ecosystems among general public visiting them.

For decision-makers, this new « cultural » argument, (associated to ongoing ecologic monitoring of these ecosystems), bring information that they often ignore or underestimate. The hypothesis is that the creation of "cultural" awareness could be translated in the planning process and political agenda. At local level, monitoring results should be transferred to elected people and civil servants as well as to representatives of decentralized sectors impacting wetlands (urban planning, agriculture, tourism, etc.). At national level, results should also reach sectors impacting wetlands (agriculture, fisheries, tourism, urban planning, energy, etc.). For wetland's managers, the results of this monitoring could help them in better matching their management strategies with expectations of targeted visitors, including for infrastructures and services to be developed to improve visit conditions and positive impact among visitors. Analysis may also help in timely manage visitor flows and in proposing more attractive structures and services. This may increase the efficiency of efforts, for both social and human impact. The usefulness of monitoring results for managers is considered key for the sustainability of monitoring, because managers are and will be key resource persons for this monitoring programme.

This synthesis provides the key results and analysis of 2017 monitoring exercise. The Mediterranean Wetlands Observatory (MWO), managed by Tour du Valat in the framework of the Mediterranean initiative of Ramsar (MedWet), has coordinated this work in partnership with the Mediterranean Agronomic Institute of Montpellier (IAMM). This work also aimed at establishing the first baseline reference for subsequent monitoring.

Scope, conditions and usefulness of the 2017 monitoring

In 2017, the first quantitative monitoring of this indicator covered 10 countries (37% of MedWet countries including 9 EU countries, 8 Maghreb countries, 6 Balkan countries outside EU and 4 Middle-East countries) and 27 sites validated for this exercise (about 18% of wetlands benefiting of a visitor center, Park house or relatively permanent management team) totaling 3947 visitor interviews (146 interviews per site in average) and 27 manager interviews (1 per site). (Map 1 and Graph 2)

1 See variables, questions and scoring method in annex of the main report.

Map 1: Localization of sites

Graph 2: Number of visitor's interviews realized by site

For 2017, based on the 27 sites, the mean distance of attraction to come to the site was 71 km, ranging from 40 km in Balkan sites to 94 km for Middle-East sites. At national level, it ranged from 19 km in Albania to 141 in Jordan. At site level, mean distance of visit ranged from 1 km in Karavasta (Albania) to 566 km in El Kala (Algeria). These important variations are mainly linked to the country size, site notoriety (local, national or international), distance of the site from towns, touristic zones and accommodation area and to density of protected wetlands in the territory.

If about 61% of interviewed visitors in all sites are from national origin, the ratio of foreign visitors in Balkan and Middle-East sites is important. The proportion of foreign visitors is particularly high in several internationally known Albania and Jordan sites, while the proportion is below 20% of our sample in Maghreb (Algeria and Tunisia) and in Serbia.

The 2017 monitoring exercise allows the establishment of an indicator value at the Mediterranean scale and to get a first index reference for the four sub-regions. However, for this first monitoring, except for Algeria, the desegregation of the monitoring at the national scale is not really representative due to the limited number of sites.

These monitoring scales interest mainly national decision-makers and international organizations involved in wetlands protection, as well as actors studying ecosystem services and in particular cultural services.

The detailed analysis by site is also possible for all sites in which a minimum of 80 visitor questionnaires have been validated (22 out of 27 sites) This monitoring is particularly robust for sites with at least 145 visitor interviews validated, which is the case for 12 sites : Karavasta and Narta (Albania), Reghaia, Taza, Iherir Illizi and Chréa (Algeria), Pont de Gau (France), Azrak (Jordan), Kfar Zabad (Lebanon), Pio Vlasina and Carska Bara (Serbia), Skojanski (Slovenia). This scale of monitoring interests particularly wetland's managers, local administrations, decentralized sectors and national public institutions in charge of wetlands, because they can verify the adequacy between their management strategy and visitor profiles, including their expectations and level of satisfaction.

Overall, the first 2017 monitoring exercise was implemented as planned with limited financial and human resources as well as with limited training for site managers. Results are nevertheless obtained and already ready for analysis and use. This successful outcome is due to a series of factors:

• Past and ongoing active working linkages between MWO and other stakeholders (national focal points and site managers), such as in the Projet "wetlands sentinels", MAVA and CEPF projects, national wetlands strategies, etc.). • Regular electronic guidance, support, training and communication of MWO (assisted by a M2 student of IAMM) to countries and site managers to motivate them to take part in this new monitoring, in French, English and Arab languages. Serbo-Croatian languages could have been also an advantage for Balkan countries. • The monitoring simplification that has limited the reluctance of site managers to embark in this monitoring program. • The data collection alert system and automation of the indicator that helped to keep monitoring deadlines in visitor interviews calendar and in simplifying data capture and calculation of indicator value.

For this first monitoring exercise, quality control of visitor's interviews has been kept at Tour du Valat. When visitor's questionnaires were not completed or presented some inconsistencies, Tour du Valat informed manager. If these issues could not be solved, questionnaires were not used for measuring indicator value and analyzing results.

However, some actions could have been improved along the monitoring process:

• An additional training module in each participating country before launching the monitoring exercise, including field tests, to ensure the common understanding of the questions and the social approach to visitors. This additional training could have reduced the percentage of non-validated questionnaires because of insufficient quality.

• The better control of monitoring protocol and survey sampling among visitors per site, in particular to take into account the visitors diversity (profile, recreation and education) and the repartition of interviews during the different seasons.

These two points have suffered of a lack of financial and human resources in MWO, especially during the monitoring launching period (January-March 2017).

Synthesis for decision-makers

Key results

A value of recreational and educational wetland service index above the satisfaction benchmark but presenting high site diversity

In 2017, the index value is based on a total of 3 717 validated questionnaires implemented in 27 sites of 10 countries 2 . The Mediterranean Mean index is 0.67 (Graph 3). This result is relatively similar to the qualitative one of 2015, obtained based on nine pilot sites, with a value of 0,66.

Graph 3: 2017 Index -recreational and educational Mediterranean wetlands services

This Mediterranean mean value encapsulates sites with index values ranging from 0,48 for the less performing sites to 0,80 for the ones providing larger impacts. Sites reaching and index higher than 0,61 are the ones showing a good satisfaction among the general public In 2017, 74% of the surveyed sites were within this category. To obtain this score, in about two thirds of sites, the level of protection and the status of sites are favorable and the infrastructures and services provided by managers, considered as mandatory by visitors (paths, toilets, visitor desk, access to drinking water, rest areas, information, observatories, etc.) are operational. However, for the last third of sites, the level of satisfaction is also generated by the emotional effect, landscape aesthetics, boundarybreaking and wilderness perception of the sites (for example Iherir in Algeria, Palm Island in Lebanon and Mujib in Jordan), as well as by the proximity of beach tourism center and holiday summer atmosphere conducive to satisfaction (Karavasta and Narta in Albania) Overall, wetlands from European Union countries, Middle-East and Balkans regions get indexes above the Mediterranean index. However, sites, more than countries, are the main explanatory scale of the indicator value. All sites situated in European Union are above the Mediterranean average, which is coherent with efforts and legal framework of EU for the protection of wetlands and their biodiversity since 1992. Some sites, especially in Lebanon, Algeria and Albania, suffer of a weak control de protection and/or a high level of visitor's dissatisfaction. Sites of Carska Bara in Serbia, Mujib and Azraq in Jordan and Scocjanske in Slovenia, emblematic national and well-known wetlands, get also very high indexes', higher than 0,78.

2 Albania (3 sites), Algeria (7 sites), Croatia (3 sites), France (4 sites), Jordan (2 sites), Lebanon (2 sites), Montenegro (1 site), Serbia (2 sites), Slovenia (2 sites), Tunisia (1 site). The recreational and educational impact among visitors directly linked to the manager efforts

The desegregated analysis of responses from managers and visitors show that overall, visitor's satisfaction and perception over the natural capital increase with enhanced site management and availability of diversified services. (Graph 4).

Score reached by wetlands ecosystems penalized by external pressures

Desegregated analysis of wetlands natural capital show that when site notoriety and protection status are high (maximum score for all sites), the value of the RES-MW is penalized by external pressures such as urban and public infrastructures extension and pollution around sites, generating a landscape degradation and impacting negatively on perception and satisfaction.

Key messages

• Disaggregated analysis at different scales (sites, countries, sub-regions and Mediterranean) allow targeting different decision-makers and site managers to influence their decisions.

• The level of impact and satisfaction among general public visiting wetlands is linked to the capacity and efforts of wetlands managers to ensure site accessibility and attractiveness and at the same time manage site with a cluster of services considered by general public to be mandatory for a comfortable visit.

• Landscape aesthetic and integrity as well as quietness are the values most expected by the general public visiting wetlands. These values are important to preserve in and around wetland's sites in order to maintain or improve positive impacts among visitors.

• The level of satisfaction of visitors is clearly reinforced when emotion is created during wetlands visit, or when other nearby attractions mutually reinforces this satisfaction. Sites benefiting of large space and exceptional and wild landscape and the ones receiving part of nearby mass tourists (especially beach tourism) generate this phenomena. However, especially for this last category of sites, studies about site and fauna disturbance due to people frequentation should be updated to improve the management of visitor flows.

• If the protection status and international recognition (label) of the studied sites are high, the level of pressures plays negatively on the perception of the manager and on the visitor satisfaction.

• Educational impact of wetlands among school and green club members is very high where manager develop educational service.

• Acquisition of knowledge and awareness creation are in the visit concept of about half of the recreational visitors. Its efficiency depend mainly of the level of awareness of visitors prior the visit and of the manager efforts to transfer knowledge in an innovative and attractive manner, as well as to update this knowledge in line with emerging society challenges (water management, climate change, etc.)

Recommendations to increase the impact efficiency among visitors

• Where and when possible, develop proximity accessible and managed wetlands every 35 kilometers and not beyond 70 kms distance from towns, distance considered a maximum for the general public vising wetlands.

• For sites enjoying high status of protection and with high visitor reputation, provide an additional effort to avoid or limit external pressures (urban extension, pollution, disturbance, over-exploitation of resources) that act negatively on visitor's impact and satisfaction. A high level inter-sector consultation is often necessary.

• Encourage wetlands manager's efforts, especially in terms of visitor-oriented services to ensure comfortable visit for the general public, condition considered by them as mandatory in the majority of sites to enhance their interest to positively discover nature, wetlands and their biodiversity with high level of satisfaction.

• To increase visitor's interest to better understand the functions of wetlands, motivate managers to regularly adapt information and messages for visitors, in line with emerging societal challenges and communicate them on pedagogic and attractive way, and in different languages.

• Spread monitoring results to influence development decisions and land use planning in and outside wetlands, among relevant development sectors and local administration, in order to conserve and restore landscape aesthetic and quietness in and around sites, the two key added values appreciated by recreational visitors.

Manager's efforts are key for visitor satisfaction and their acquisition of knowledge Overall, among the two capitals of condition, the manager's efforts to protect the natural capital, to adapt land use and to ensure site accessibility and attractiveness is a dominant factor of RES-MW variation including impact, compared to natural capital variables. Said differently, the natural capital impact more visitors if the manager efforts is adapted to the general public (Graph 5). By general public, we include the different visitor profiles that represent more than 85% of non-environmental specialists, including 60% adopting a social entry (the visit being a mean to share experience with friends or family) or a psychological entry (visit by individuals seeking energy, emotion, contemplation from nature). The remaining visitors (40%) adopted a "nature" key interest in visiting wetlands. (Khechimi, 2015). This result gathers also specific site situations that are important for site managers to take into account for their visit strategy. The extreme case is Mezaia site, a small artificial urban Lake of 3 ha in Algeria facing several urban pressures that succeed, thanks to the manager efforts, to impact positively visitors.

Graph 6: Efficiency level for each site between the conditions of visit and the level of impact. Level of impacts higher than conditions Level of conditions higher than impacts

Name of site

The social impact from wetlands visits is in general linked to the level of satisfaction reported by visitors, satisfaction enhanced by the manager effort to develop and manage services expected by the general public. This correlation is clearly verified in sites in EU countries, in Jordan and in some sites of Serbia, Albania and Montenegro. This is less clear for Iherir Illizi (Algeria) and Palm Island (Lebanon) proposing very few visitor services, even if visitors seems to make do with it. This is because the exceptional landscape beauty and perception of wilderness in Iherir Illizi or the scarcity of natural area and paradise Natural Island in Palm Island seems to provoke such emotion that infrastructures and services are considered much more of secondary concerns. The diversity of individual perception and social representation of wetlands by visitors is reflecting the diversity of visitor profiles, of the visit approaches (social, psychological and nature) and of their expectations (concept of visit), and also the emotional dimension of their visit.

The index helps wetland's managers to improve their impact efficiency

This visual representation of impact efficiency by site between conditions of visit and level of impact (Graph 6) is particularly useful for wetlands managers, to help them to better assess their comparative situation in the Mediterranean for recreational and educational services. The graph objective is to favor analytical understanding of each site situation, especially for the use of site manager. This graph can also be useful for managers wishing to improve their impact efficiency, by going back to the detailed results included in the general synthesis. The graph shows that Carska Bara is the only site within the category "very good conditions and satisfaction" between condition capitals and impact capitals. Sites such as Pont de Gau, Azrak and Kopacki Rit reach the highest score in terms of condition capitals, but register a less favorable impact ratio if compared with sites situated near the median line (Skojanski, Lonjsko Polje, Marais du Vigueirat, Mujib and Pio Vlasina). These last sites show a good adequacy between manager efforts and impacts on visitors.

Ideally, where emotional and external factors do not strongly influence people decisions to visit wetlands, sites should be situated near the median line, in 6-10 cells. This situation corresponds to a satisfactory or very satisfactory impact with good or very good visit conditions. Within this category, the most efficient sites are Carska Bara, Mujib, Marais du Vigueirat, Skojanske et Pio Vlasina. For some sites, such as Pont de Gau, Scamandre, Kopacki rit and Azrak, efforts should be focused on improved impact efficiency, in particular by developing innovative way of transferring knowledge, in order to better value the important efforts carried-out by managers.

For sites such as Saida, Chréa and Karavasta, efforts should focus on both conditions of visit (in particular services improving the comfort of visit, the information and the access to the natural capital) and impact capitals (especially efficiency of knowledge transfer in the human capital). Sites such as Narta, Londsko Polje and El Kala enjoy of high notoriety and impressive natural and cultural values that impact positively visitors with medium manager efforts. If effort efficiency is overall very good in this condition, condition capitals may not be appropriate for certain profiles of visitors.

Overall, at sub-region scale, better are the conditions, better are the impacts. At this scale, analysis confirms the correlation between manager efforts (constructed capital) and impact.

If sites in EU and Middle-East countries enjoy the best conditions of visit, the ripple effect of the condition capitals on impact is particularly clear in Balkan. This impact efficiency in Balkan seems to have three main reasons : 1) these countries have a small number of recently managed wetlands with visitor centers and national and sub-regional visitors are then curious to discover and learn about these ecosystems; 2) the environmental awareness is more recent compared to EU countries and wetlands have a comparative advantage to create awareness through discovery and information ; 3) an high percentage of the studied sites is situated in emblematic touristic areas and then propitious for satisfaction (external effect of holiday atmosphere on beaches and Salina with private tourist-oriented services).

Positive emotion and nearby attractions enhance satisfaction of general public visiting wetlands

The comparative analysis of results per site (Graph 7) show that if the link between the conditions of visit (condition capitals) and the impact among visitors can be verified in about two thirds of sites, this link is less clear for some sites such as Saida, Reghaia, Mezaia (Algeria), Narta (Albania), Pont de Gau, Viguerat, Scamandre (France), Lonjsko Polje (Croatia) et Krajinski (Slovenia). It is not easy to explain these results with the 12 variables included in this indicator, because they are more influenced by specific situations and external factors. Furthermore, in these conditions, detailed results show that the sum of social and human impacts can reach very different scores (Palm Island, Iherir/Illizi).

Graph 7: Contribution of condition and impact capitals on in the index per site

Key messages

• Each site displays proper context and face specific external factors that cannot be detected in the monitoring at sub-regions and country scales. These specific features represent sometimes, relatively independently tor manager efforts, important explanatory factors of monitoring results of visit conditions and social and human impacts on visitors.

• Landscape integrity and absence of pressures on site favor positive social impact among recreative visitors.

• Adequacy between offer (managers) and demand (visitors) per site is important to be considered, in order for wetland to fully play is « cultural" role among targeted public. This requires that managers better know their public and expectations, because they are not only passionate ornithologists and other naturalists that are often happy with a minimum of services.

• The appropriate management of comfort services (access, toilet, access to drinking water, security, etc…) and of nature observation services (Observatories, paths, information boards, etc.) increases the satisfaction of visitors for sites for which the reasons of visit are not influenced by strong emotional (exceptional landscape) and external factors (other nearby attractions).

• The emotional factor created by the natural capital (panorama, exceptional landscape, wilderness and also emblematic natural and cultural features) favor impact, satisfaction and souvenir.

• Some of the mass tourists coming to coastal beach areas during summer time visits nearby coastal wetlands. The visit of « natural site » during the summer holiday atmosphere is conducive to high satisfaction.

Recommendations

• Ensure the protection of natural capital by associating a landscape approach with manager, institutes and universities specialized in this approach. Altogether, panorama, water, birds and greenery constitutes the pillars of wetlands landscape identity, as expected by the large majority of visitors.

• For an efficient recreational and educational service and for the image of wetlands, favor visitor's service quality over the quantity. Indeed, without enough wetlands quality infrastructures, services and management, as perceived by the general public, the visit can become counter-productive and give a negative image of the wetlands.

• Build on the « emotion » generated by the natural capital of some sites or by the nearby mass attractions (tourist areas including beaches, monuments, culture, etc.) to develop, at wetland site, access services (road, public transport, paths and indication boards), nature observation services (observatories, binoculars) and value addition of the natural capital (value areas with best panoramic views, favorable area for aesthetic landscape discovery), while taking into account visitor flow management to avoid or limit disturbance on site, including fauna during reproduction period and the notion of discomfort of visitors, especially between profiles with diverging interests.

• For each site not influenced by the « emotional » dimension or by other nearby attractions, the increase of visitor impact efficiency is observed with the decrease or the good management of pressures on sites, the appropriate management of comfort and nature observation services as well as by the innovative way to create awareness among the general public, using attractive themes.

• Favor school contracts and projects, for which educational impact has been found very efficient with a long-term effect. The pedagogic and playful method and capacity of the staff to transfer knowledge and messages is very important.

Graph 4 :

 4 Efficiency of visitor impact as compared to manager effortsManager effort is particularly efficient in Balkans area (+ 0,14 difference between visitor index and manager index). It is less valued in Europe (+ 0,03). There are two main explanatory factors: in Balkans countries, wetlands with visitor centers, still not in big number, are often situated near coastal touristic areas and are usually well-known. In Europe, although efforts and quality services provided by managers, visitors have a large choice of wetlands to visit. They are then more demanding and often indicate that they are already aware of environmental and wetlands challenges before visiting sites. This situation decrease the impact of the visit in terms of new knowledge acquired.Landscape aesthetic and educational programs are the two main vectors of human and social impacts Landscape aesthetic and perception that include water birds, water, greenery and quietness, are the key reasons of visit as well as the main elements expected by the general recreational visitors during their visit. For educational visitors, including school children and members of green clubs, educational program with field visit are very conducive and efficient for transferring new knowledge about wetlands and challenges they face.

Synthesis for wetlands managers

Key results

Important management effort but human impact lagging behind Based on monitoring results, the natural capital of Mediterranean wetlands benefiting of visitor centers is attractive, managers are doing important efforts to value it, but human capital impact of the visits still lag behind expectation, although a relatively good satisfaction (Social capital) reported from visitors (Graph 5). Consequently, the improvement of the RES-MW index value will need to address the human capital impact issue, for which the reflexion may also be linked to the review of the constructed capital (adequacy between infrastructures and services provided by managers and visitor expectations in terms of human impact) and external effects that may influence results of the human capital.

The external factors penalizing human capital impact during the visits seems to have three main origins : 1) the general public deciding to visit wetlands expect above all the link with nature and quietness, the learning part being often a secondary reason for some groups seeking first emotion, contemplation, sport, picnic area, etc. ; 2) In Europe, a high proportion of visitors mention that they are already aware about environmental and wetlands issues and then did not acquire additional knowledge during the visits ; 3) Several sites focus information and mean of communication on biodiversity, in particular water birds, while some visitors seek other information more related with societal challenges: ecosystem modification, human-nature relationship, water management, wetlands and climate change.


Florence Nougarolis
email: florence.nougarolis@gmail.com

Fatima-Zohra Mokrane

Nicolas Sans

Hervé Rousseau

Fabrice Dedouit

Norbert Telmon

Bone age estimation based on multislice computed tomography study of the scapula

Keywords: Age assessment, Scapula, Forensic, Anthropology, Multislice computed tomography

Progress in medical imaging bas opened new areas of research in forensic anthropology, especially in the context of the study of bone age assessment. The study of bone age bas become a useful tool for age estimation at death or age of young adult migrants in an anthropological context. We retrospectively evaluated multislice computed tomography (MSCT) explorations focused on scapulae of 232 individuals (123 males; 109 females) aged between 8 and 30 years old. Computed tomography (CT) scans were viewed in axial and multiplanar reconstructed images using OsiriX 5.9 (64 bit)®. The ossification centers of the scapula studied were as follows: acromial, sub-coracoid, glenoid, coracoid, coracoid apex, and inferior angle epiphyses. Fusion status was scored based on a five--stage system (stage 1: no ossification, stage 2: vi sual ization of an ossification center, stage 3: partial ossification, stage 4: full ossification associated to an epiphyseal scar, and stage 5: fu ll

Introduction

The study of age assessment represents a significant part of forensic anthropological activity. Interest in the study of skel etal age markers is increasing due to growing requests to fo rensic practitioners to provide more accurate age estimation, one of the important factors helping in identification. Immigration is at the center of political, ethical, economic, and social debate in Europe. Forensic age estimation of living young adults bas become an important focus ofinterest during recent years; growing migration into Europe and between European countries bas led to an increased number of for eigners who cannot provide evidence for their exact date of birth. Indeed, young foreign people often have no identifica tion document proving their correct birth dates. Establishing the age of majority is therefore fundamental in orderto deter mine which system bas to be applied: the juvenile or the adult one. As well as immigration implications, forensic age esti mation is also used to determine whether a suspected offender is subject to juvenile or adult criminal law. The relevant age thresholds for judicial and administrative proceedings lie between 14 and 21 years old in most countries [START_REF] Schmeling | Statistical analysis and verification of forensic age estimation of living persons in the Institute of Legal Medicine of the Berlin University Hospital Charité[END_REF].

According to the recommendations of the Arbeitsgemeinschaft für Forensische Altersdiagnostik (AGFAD) (study group for forensic age diagnostics), age assessments in criminal proceedings should be based on general physical examination, X-ray examination of the hand, and odontological examinat i o n b y a d e n t i s t , i n c l u d i n g d e n t a l s t a t u s a n d orthopantomogram. In order to improve diagnostic reliability, these methods should always be used in combination, ensuring that each part is performed by forensically trained and experienced experts of the relevant disciplines [START_REF] Schmeling | Criteria for age estimation in living individuals[END_REF]3]. If the bony fusion of the hand and wrist is complete, an additional computed tomography (CT) examination of the clavicles is recommended, in order to demonstrate that the person has reached the age of 18 or 21 [START_REF] Schmeling | Statistical analysis and verification of forensic age estimation of living persons in the Institute of Legal Medicine of the Berlin University Hospital Charité[END_REF][START_REF] Schmeling | Criteria for age estimation in living individuals[END_REF][START_REF] Schulze | Correlation of age and ossification of the medial clavicular epiphysis using computed tomography[END_REF][START_REF] Wittschieber | Projection radiogra phy of the clavicle: still recommendable for forensic age diagnostics in living individuals?[END_REF]. Age assessment properly performed helps to enhance legal certainty by ensuring equal treatment of persons with or without valid identity documents. On one hand, they help prevent perpetrators from wrongfully benefiting from false claims to be younger than they really are. On the other hand, they supply exonerating evidence for persons who are erroneously suspected of making false statements about their age [START_REF] Schmeling | Age esti mation of living people undergoing criminal proceedings[END_REF].

Several studies demonstrated this last year's utility of staging system methods, using bone cross-sectional imaging, with CT or magnetic resonance imaging (MRI). Ekizoglu and Wittschieber demonstrated the interpretation issues related to radiographic incidence. Their studies demonstrated that the assessment of medial clavicle ossification by CT must be realized on thin-slice CT examinations, with an experienced observer [START_REF] Wittschieber | Projection radiogra phy of the clavicle: still recommendable for forensic age diagnostics in living individuals?[END_REF][START_REF] Ekizoglu | Forensic age estimation by the Schmeling method: computed tomography analysis of the medial clavicular epiphysis[END_REF][START_REF] Ekizoglu | Estimation of forensic age using substages of ossification of the medial clavicle in living individuals[END_REF][START_REF] Wittschieber | Influence of the examiner's qualification and sources of error during stage determi nation of the medial clavicular epiphysis by means of computed tomography[END_REF]. Other bone structures were also tested in age estimation, like radiographic study on cervical spine [START_REF] Cameriere | Age estimation in children and young adolescents for forensic purposes using fourth cervical vertebra (C4)[END_REF]. MR studies tend to increase in frequency, according to cross-sectional imaging increasing performances. Different bone structures were studied, like the medial clavicle, distal tibia and calcaneus [START_REF] Martin | Evaluation of an automatic method for forensic age estimation by magnetic reso nance imaging of the distal tibial epiphysis a preliminary study focusing on the 18 year threshold[END_REF][START_REF] Martin | Age estimation by magnetic resonance imaging of the distal tibial epiphysis and the calcaneum[END_REF], iliac crest [START_REF] Wittschieber | Magnetic resonance imaging of the iliac crest: age estimation in under 20 soccer players[END_REF], proximal tibial epiphysis [START_REF] Krämer | The use of mag netic resonance imaging to examine ossification of the proximal tibial epiphysis for forensic age estimation in living individuals[END_REF], hand-wrist [START_REF] Dvorak | Application of MRI of the wrist for age determination in international U 17 soccer com petitions[END_REF], and distal femur [START_REF] Krämer | Forensic age estimation in living individuals using 3.0 T MRI of the distal femur[END_REF][START_REF] Dedouit | Age assessment by magnetic resonance imaging of the knee: a preliminary study[END_REF][START_REF] Martin | Contribution of distal femur MRI to the determination of the 18 year limit in foren sic age estimation[END_REF], but also the third molar [START_REF] Guo | Dental age estimation in living individuals using 3.0 T MRI of lower third molars[END_REF].

The scapula is a flat triangular bone that lies over the posterior surface of the rib cage and forms the posterior part of the shoulder girdle. At its upper lateral corner, it exhibits a cuplike depression (glenoid fossa) that forms a socket for the head of the humerus. The posterior surface of the bone is divided by a nearly horizontal ridge (scapular spine) extending laterally to form the acromion, a projection which overhangs the glenoid fossa. The anterior surface just medial to the glenoid fossa has a beak-like projection (coracoid process) that acts as an attachment for muscles and ligaments. The scapula is a bone particularly adapted to skeletal age determination. It has several centers for ossification, uniting in various parts of the bone in a particular sequence at different ages. First, the primary center appears in the first year of life; then, seven secondary centers begin to appear at 8 years old. Fusion is generally completed at 23 years old [START_REF] Scheuer | The juvenile skeleton[END_REF]. These points give to the scapula particular importance in skeletal age estimation during growth periods [START_REF] Scheuer | The juvenile skeleton[END_REF]. Scapular development analysis appears useful for providing answers to judicial authorities.

To our knowledge, there is no three-dimensional study which has evaluated the scapula ossification centers as a method for age assessment. Obviously, the skeletal maturation of the scapula has already been studied anthropologically on dry bones [START_REF] Scheuer | The juvenile skeleton[END_REF][START_REF] Cardoso | Age estimation of adolescent and young adult male and female skeletons II, epiphyseal union at the upper limb and scapular girdle in a modern Portuguese skeletal sample[END_REF] but not radiologically on living persons. Eight scapular ossification centers were described by Scheuer and Black [START_REF] Scheuer | The juvenile skeleton[END_REF].

Study using dry bones leads to important knowledge regarding ossification centers. The primary ossification center for the coracoid usually appears within the first years of life [START_REF] Ogden | Radiology of postnatal skeletal development. VII. The scapula[END_REF], and fusion to the scapula generally occurs at around 14-15 years [23]. Among the secondary ossification centers, the sub coracoid center appears between 8 and 10 years [START_REF] Basmajian | Grant's method of anatomy: a clinical problem solving approach[END_REF]25], with complete fusion achieved by 16-17 years for both sexes [START_REF] Hodges | An epiphyseal chart[END_REF].

The glenoid center appears at around 14-15 years [START_REF] Hodges | An epiphyseal chart[END_REF][START_REF] Johnston | Sequence of epiphyseal union in a prehistoric Kentucky population from Indian Knoll[END_REF][START_REF] Birkner | Normal radiologic patterns and variances of the human skeleton: an X ray atlas of adults and children. Urban and Schwarzenberg[END_REF] and completes its fusion between 17 and 18 years [START_REF] Scheuer | The juvenile skeleton[END_REF]. The epiphysis for the apex of the coracoid process appears between 13 and 16 years and merges by the age of 20 [START_REF] Hodges | An epiphyseal chart[END_REF][START_REF] Birkner | Normal radiologic patterns and variances of the human skeleton: an X ray atlas of adults and children. Urban and Schwarzenberg[END_REF]29]. The acromial epiphysis appears between 14 and 16 years old, and fusion occurs by 18-20 years old [START_REF] Macalister | Notes on acromion[END_REF][START_REF] Stevenson | Age order of epiphyseal union in man[END_REF][START_REF] Camp | Diagrammatic chart showing time of appearance of the various centers of ossification and period of union[END_REF][START_REF] Mckern | Skeletal age changes in young American males analysed from the standpoint or age identification[END_REF][START_REF] Last | Anatomy: regional and applied[END_REF]. The inferior angle of the scapula develops from a secondary ossification center, which appears at around 15-17 years old and merges by 23 years old [START_REF] Basmajian | Grant's method of anatomy: a clinical problem solving approach[END_REF][START_REF] Hodges | An epiphyseal chart[END_REF][START_REF] Birkner | Normal radiologic patterns and variances of the human skeleton: an X ray atlas of adults and children. Urban and Schwarzenberg[END_REF]29,[START_REF] Stevenson | Age order of epiphyseal union in man[END_REF][START_REF] Camp | Diagrammatic chart showing time of appearance of the various centers of ossification and period of union[END_REF][START_REF] Mckern | Skeletal age changes in young American males analysed from the standpoint or age identification[END_REF]. It is a small epiphysis that merges directly at the angle of the scapula and then sends a small tongue along the medial border. The epiphysis of the coracoid process angle appears at around 14-15 years and merges at the age of 20 years [START_REF] Hodges | An epiphyseal chart[END_REF][START_REF] Birkner | Normal radiologic patterns and variances of the human skeleton: an X ray atlas of adults and children. Urban and Schwarzenberg[END_REF]29]. This epiphysis was not analyzed in our study because of the difficulty of identifying this structure on CT examinations. This center is angular and very difficult to identify. The vertebral border epiphysis is fragile, long, and multipartite and arises from several bone islands, which merge secondarily. These islands appear at around 15-17 years old, and fusion is completed by 23 years old [START_REF] Basmajian | Grant's method of anatomy: a clinical problem solving approach[END_REF][START_REF] Hodges | An epiphyseal chart[END_REF][START_REF] Birkner | Normal radiologic patterns and variances of the human skeleton: an X ray atlas of adults and children. Urban and Schwarzenberg[END_REF][START_REF] Stevenson | Age order of epiphyseal union in man[END_REF][START_REF] Mckern | Skeletal age changes in young American males analysed from the standpoint or age identification[END_REF][START_REF] Girdany | Centers of ossification of the skeleton[END_REF]. All ossification centers were studied, except the vertebral border because it was hardly identified on different CT examinations done on living persons.

The aim of the present study was the elaboration of a CT staging system based on the analysis of fusion of the ossification centers of the scapula of living human subjects in order to estimate bone age in a population ranging from the 8th to the 31st year of life. This permits us to assess if this age marker is a potentially useful tool for age estimation by evaluating the reliability of the staging.

Materials and methods

Sample

We carried out a retrospective study of clinical thoracic multislice computed tomography (MSCT) explorations performed between March 2013 and January 2015 in the University Hospital of Toulouse, southwest France. MSCT explorations were obtained through a local picture archiving and communication system (PACS) (McKesson Medical Imaging Group, Richmond, BC, Canada). Patients underwent MSCT examinations for various reasons, such as thoracic trauma or cardiopulmonary disease. A total of 263 MSCT examinations were included in this study (144 males, 119 females). Patients were aged from 7.4 to 30.6 years old (8th and 31st year of life, respectively). We analyzed 159 right scapulas and 104 left scapulas. Age distribution of these subjects by sex is shown in Table 1.

Thirty-one MSCT explorations with bilateral scapular study were used to evaluate statistical side differences. For these cases, left scapula CT examinations were excluded from the final analysis.

The data and images were recorded anonymously. Data were recorded for the individuals including sex, date of birth, date of the examination, and CT acquisition parameters. According to French law, the results of medical imaging examinations may be used retrospectively without the patient's consent when the examinations have been carried out for clinical purposes and when they have been recorded anonymously (Article 40-1, Law 94-548 of 1 July 1994).

The inclusion criteria consisted of the following:

-Absence of pathological modification of the shoulder: no tumor, no direct acute trauma, no infection, arthritis, nor dysplasia. -Suitable CT scan parameters: visualization of the entire shoulder, slice thickness < 2 mm, and overlapping reconstruction interval < 1 mm. -For each year of age between 8 and 30 years old, we randomly selected approximately five men and five women.

The socioeconomic level of individuals and ethnic origin was not taken into account, as it was not available.

MSCT examinations

MSCT was performed on Sensation-16 (Siemens, Erlangen, Germany) and Brilliance-16 (Philips Brilliance, Philips Medical Systems, Amsterdam, The Netherlands) systems. The image matrix was 512 × 512 pixels for the Sensation-16 and 1024 × 1024 pixels for the Brilliance-16. The following parameters were used: tube voltage, 120 kV; effective mAs, 120. Different parameters of slice thicknesses and reconstruction section thicknesses were used in our study. These elements are detailed in Table 2.

CT analysis

CT scans were saved in DICOM format (Digital Imaging and Communications in Medicine), and postprocessing was performed with OsiriX® 5.9 (64 bit). Multiplanar reconstructions (MPR) were performed along the axis of the ossification centers in the sagittal, coronal, and axial planes. This assessment was performed by a radiologist, after 6-month experience in forensic and anthropological radiology. Intra-observer variability was tested, after a lap time of 2 months between the evaluations. Also, in order to evaluate the inter-observer variability, 20 CT examinations selected randomly were also studied by an experienced radiologist. Each radiologist was totally blinded to patient identification data and the other radiologist results.

CT staging

We analyzed six ossification centers of the scapula, according to the detailed descriptions of Scheuer and Black: the acromial epiphysis, coracoid epiphysis and sub-coracoid epiphysis, glenoid epiphysis, apex of the coracoid epiphysis, and inferior angle epiphysis. They undergo fusion during adolescence and early adulthood. An illustration of these ossification centers is shown in Fig. 1. The staging system was developed based on five CT developmental stages. The six ossification centers were evaluated separately in MPR mode. The staging classification of Schmeling et al. [START_REF] Schmeling | Studies on the time frame for ossification of the medial clavicular epiphyseal car tilage in conventional radiography[END_REF] was used to evaluate the ossification status for all epiphyseal centers of the scapula except for the coracoid epiphysis. Indeed, this center usually appears within the first year of life (consequently, there was no stage 1 and only stages 2 to 5 were designated). The staging appeared as follows (Fig. 2): -

Statistical analysis

Statistical analysis was performed using R 3.1.3 software [START_REF]R: a language and environment for statistical computing[END_REF]; Cohen's kappa nonparametric test was used to evaluate intra-and inter-observer variability and side differences [START_REF] Cohen | A coefficient of agreement for normal scales[END_REF][START_REF] Ferrante | Statistical methods to assess the reliability of measurements in the procedures for forensic age esti mation[END_REF]. Descriptive statistical analysis was performed to determine the mean age, standard deviation, and age range with a 95 % confidence interval for each epiphyseal center. We then used variance analysis (ANOVA) to determine if there was a significant difference between sex groups for each epiphyseal center.

Results

Population A total of 232 patients were included, including 123 males and 109 females, with an age range of 8 to 30 years old. This large age range was chosen because it included the different threshold ages of criminal liability. The ethnic origin of the retrospectively selected patients was not taken into consideration because only the patients' names and dates of birth were available in the local PACS.

Intra-and inter-observer variability

Intra-observer variability was tested on a sample of 25 randomly selected CT examinations. A time lapse of 2 months was observed between the two reports for each case. Interobserver variability was tested on a sample of 20 CT examinations. Cohen's kappa nonparametric test revealed excellent intra-observer reproducibility and good inter-observer reproducibility (Table 3). Indeed, intra-observer variability was between 0.85 and 1 (excellent), while inter-observer variability was between 0.72 and 1 (good).

Side differences

The influence of the side differences of the scapula was also tested in our study. Among the 159 right scapulas included in our study, 31 patients had also their left scapulas included in their CT scans and were used to study side differences. For these cases, left sides were excluded from the final analysis, to avoid redundancy.

Cohen's kappa nonparametric test confirmed the absence of statistically significant differences between right and left 3).

Correlation between age and ossification stage

For both sexes and for each epiphyseal center, study of variance demonstrated that there was a good correlation between 4. This result was significant with p < 0.001. Also, there was no significant impact due to sex (p > 0.05). Illustratively, Fig. 3 shows, for each ossification center, minimum age, maximum age, age range, and mean age with their standard deviations, without sex identification.

For each epiphyseal center, some CT scans were not analyzable. These data are detailed in Table 4. However, these

✓ -

cases were not important. For example, for acromial center, only six female CT scans and three male CT scans were not analyzable (nine cases on 232 total inclusions). For inferior angle ossification center, none of the cases was excluded.

The main reason of this lack of analysis was the fact that acromion was near the limits of acquisition field and was not analyzable correctly, especially with MPR.

Acromial ossification center (Table 4, Fig. 3a)

The youngest individual in which stage 2 (beginning of ossification) was observed was 9.8 years for female group and 7.4 years for male group. The oldest individual in which stage 2 was observed was 13.6 years for female group and 14.6 years for male group. For both sexes, patients identified as stage 2 were younger than 18 years old. The oldest individual in which stage 3 was observed was 18.9 years for female group and 18 years for male group. Sub coracoid ossification center (Table 4, Fig. 3b)

The youngest individual in which stage 2 was observed was 9.2 years for female group and 8.5 years for male group. The oldest individual in which stage 3 was observed was 14.5 years for female group and 15.8 years for male group.

For both sexes, patients identified as stage 3 were younger than 18 years old. The oldest individual in which stage 4 was observed was 30.5 years for female group and 29.3 years for male group. Glenoid ossification center (Table 4, Fig. 3c)

The youngest individual in which stage 2 was observed was 9.2 years for female group and 11.5 years for male group. The oldest individual in which stage 3 was observed was 16.6 years for female group and 15.8 years for male group. For both sexes, patients identified as stage 3 were younger than 18 years old. The oldest individual in which stage 4 was observed was 19.2 years for female group and 25.2 years for male group.

Coracoid ossification center (Table 4, Fig. 3d)

The youngest individual in which stage 2 was observed was 8.5 years for female group and 7.4 years for male group. The oldest individual in which stage 4 was observed was 14.5 years for female group and 15.7 years for male group.

For both sexes, patients identified as stage 4 were younger than 18 years old. The oldest individual in which stage 5 was observed was 30.6 years for both groups.

Coracoid apex ossification center (Table 4, Fig. 3e)

The youngest individual in which stage 2 was observed was 9.2 years for female group and 9.6 years for male group. The oldest individual in which stage 3 was observed was 16.6 years for female group and 15.8 years for male group.

For the male group, patients identified as stage 3 were younger than 18 years old (the oldest individual in which stage 3 was observed was 15.8 years). However, for female group, the oldest individual in which stage 3 was observed was 16.6 years. And the oldest individual in which stage 4 was observed was 13.9 years, but this result has to be carefully considered because of the small effective in this group (n = 1).

Inferior angle ossification center (Table 4, Fig. 3f)

The youngest individual in which stage 2 was observed was 11.6 years for female group and 13.5 years for male group. The oldest individual in which stage 2 was observed was 17.6 years for female group and 16.9 years for male group.

For both sexes, patients identified as stage 2 were younger than 18 years old. The oldest individual in which stage 3 was observed was 18.8 years for female group and 20.1 years for male group.

Discussion

Determination of age in a living person is a subject of ongoing research in forensic anthropology. This problem arose with increasing migratory flow and the reception of unaccompanied young people claiming to be minors on arrival in European countries. The actual age or chronological age is the time between the birth of a person and a specific date. It is the determination of this age that is sought in medico-legal reports required by the legal authorities. Age printed on documents that could have been changed or stolen could be different from chronological age. In consequence, forensic physicians are frequently asked by the authorities to estimate the age of a living person requesting asylum and claiming to be younger than 18 years old. Indeed, above this age, they are liable to be returned to their country of origin. Forensic age estimation is also used to determine whether a suspected offender is subject to juvenile or adult criminal law. The relevant age thresholds for judicial and administrative proceedings lie between 14 and 21 years old in most countries [START_REF] Schmeling | Studies on the time frame for ossification of the medial clavicular epiphyseal car tilage in conventional radiography[END_REF]. Estimation of the correct age of the charged person is important during criminal proceedings. Verified documentation of the date of birth is the only way to determine the exact chronological age of a person. However, if the person does not possess his or her own identification documents, it is very important to verify whether this person should be accepted as juvenile or adult. Biological age is the aging of a person, taking into account all biological and physiological parameters. There is no single and objective criterion allowing an overall assessment of the degree of biological aging of an individual. Evaluation is a multifactorial process, based on the quantitative assessment of several parameters, which determine the maturity of an individual using morphological and morphometric methods. Among these methods, bone age, dental age, and puberty are subsets of biological age determination. Bone age is the stage of skeletal maturation. Its determination is based on the analysis of growth plate activity, visible on epiphyses.

Recent progress in medical imaging has opened new directions of research in forensic anthropology, especially in the context of bone age study. Several studies for estimation of bone age with CT analysis have been performed. Studies using CT staging were performed on the medial clavicle extremity [START_REF] Schulze | Correlation of age and ossification of the medial clavicular epiphysis using computed tomography[END_REF][START_REF] Ekizoglu | Forensic age estimation by the Schmeling method: computed tomography analysis of the medial clavicular epiphysis[END_REF][START_REF] Franklin | CT evaluation of timing for ossification of the medial clavicular epiphysis in a contemporary Western Australian population[END_REF][START_REF] Kellinghaus | Enhanced possibil ities to make statements on the ossification status of the medial clavicular epiphysis using an amplified staging scheme in evaluat ing thin slice CT scans[END_REF], first rib [START_REF] Moskovitch | Multislice computed tomography of the first rib: a useful technique for bone age assess ment[END_REF], pars basilaris of the occipital bone, and spheno-occipital synchondrosis [START_REF] Minier | Estimation de l'âge foetal par étude scanographique de la pars basilaris de l'os occipital[END_REF][START_REF] Bassed | Age estimation using CT imaging of the third molar tooth, the medial clavicular epiphysis, and the spheno occipital synchondrosis: a multifactorial approach[END_REF]. Use of CT examinations is more appropriate for studying bones than ultrasound (US) or MRI. Indeed, the US method is accurate and X-ray free, but it remains operator dependent. Also, it only allows a relatively superficial evaluation of bones due to limited penetration depth of ultrasonic waves [START_REF] Wittschieber | Magnetic resonance imaging of the iliac crest: age estimation in under 20 soccer players[END_REF][START_REF] Schmidt | Sonographic evaluation of apophyseal ossification of the iliac crest in forensic age diagnostics in living individuals[END_REF][START_REF] Schmidt | Sonographic exam ination of the apophysis of the iliac crest for forensic age estimation in living persons[END_REF]. MRI is a powerful tool, especially for identifying and studying growth plates. However, this technique has a lower spatial resolution than CT regarding fusion of ossification centers. Nevertheless, this limitation can be overcome by higher magnetic field strengths [START_REF] Krämer | Forensic age estimation in living individuals using 3.0 T MRI of the distal femur[END_REF]. Moreover, access to MRI is currently difficult, mainly due to limited time availability of the machines. Finally, costs of MRI studies are higher than those with other techniques (CT and US). However, the development of new methods for age assessment with crosssectional imaging increased in the last years. These methods are also useful for sporting competitions [START_REF] Wittschieber | Magnetic resonance imaging of the iliac crest: age estimation in under 20 soccer players[END_REF][START_REF] Dvorak | Application of MRI of the wrist for age determination in international U 17 soccer com petitions[END_REF][START_REF] Vieth | Age estimation in U 20 football players using 3.0 tesla MRI of the clavicle[END_REF][START_REF] Schmidt | Examination of ossifi cation of the distal radial epiphysis using magnetic resonance im aging. New insights for age estimation in young footballers in FIFA tournaments[END_REF].

Comparison of our results to literature data, like Scheuer and Black [START_REF] Scheuer | The juvenile skeleton[END_REF], demonstrated that there are noticeable differences. In fact, age ranges for the various epiphyses of the scapula show later ages, particularly with the glenoid epiphysis. This difference could be explained at least partially by the fact that material was different. Indeed, Scheuer and Black used dry bones, while actual studies use clinical situations of living subjects.

-For the acromion epiphysis, an earlier emergence and complete fusion are observed compared to Scheuer and Black and estimated respectively to 2 and 3 years. -For the coracoid apex epiphysis, we observed an earlier appearance by 3 years and an earlier fusion by 4 years. -For the coracoid epiphysis, complete fusion was observed approximately in accordance with literature data. -For the glenoid epiphysis, we observed an earlier appearance by 4 years and complete fusion was observed approximately in accordance with literature data. -For the inferior angle, emergence was identical, while fusion was earlier by 4 years. -For the sub-coracoid epiphysis, time of onset was identical and fusion was later by around 5 years.

Statistical comparison between these results could not be made. This is due mainly to the fact that the examination techniques were different. Only comparison between studies using the same imaging methods is possible [START_REF] Schulz | Radiographic staging of ossification of the medial clavicular epiphysis[END_REF]. The complete fusion of the epiphyses appears earlier in radiographic studies than in those carried out on dry bone [START_REF] Krogman | The human skeleton in forensic medicine[END_REF].

Concerning sex difference in the developmental timing of scapula, the study of Coqueugniot and Weaver [51] realized on dry bone demonstrated for the acromion epiphysis a delay of 1 or 2 years for two states of fusion: partial union and complete union. The results of Coqueugniot and Weaver for the coracoid epiphysis are not comparable because they consider sub-coracoid and coracoid secondary centers together with the coracoid epiphysis.

In our study, side differences were studied for 31 patients. In most studies in which the side difference has been evaluated, there was no significant statistical difference [START_REF] Schmeling | Studies on the time frame for ossification of the medial clavicular epiphyseal car tilage in conventional radiography[END_REF][START_REF] Schulz | Radiographic staging of ossification of the medial clavicular epiphysis[END_REF][START_REF] Schulz | Studies on the time frame for ossification of the medial epiphysis of the clavicle as revealed by CT scans[END_REF][START_REF] Cameriere | Radiographic analysis of epiphyseal fusion at knee joint to assess likelihood of having attained 18 years of age[END_REF][START_REF] Kreitner | Bone age deter mination based on the study of the medial extremity of the clavicle[END_REF][START_REF] Meijerman | Variables affecting the probability of complete fusion of the medial clavicular epiphysis[END_REF]. Our results accorded with literature data.

Meijerman and Mühler recommended a slice thickness of 1 mm, to avoid creation of incorrect images [START_REF] Meijerman | Variables affecting the probability of complete fusion of the medial clavicular epiphysis[END_REF][START_REF] Mühler | The influence of slice thickness on assessment of clavicle ossification in foren sic age diagnostics[END_REF]. In our study, 58.6 % of CT scans (136/232) were made with these criteria. The other 41.4 % CT examinations of our study were done using a slice thickness of 2 mm, which is acceptable because of the overlapping interval (1 mm). For this reason, these CT examinations were included in our study.

Besides, CT examinations in clinical practice are done using slice thicknesses of 2 mm with overlapping interval of 1 mm, which allows a good structural visualization, associated to an acceptable X-ray exposure. All CT examinations used in our study are derived from clinical CT examinations.

The observer's experiences are known to have a bias effect on data [START_REF] Wittschieber | Influence of the examiner's qualification and sources of error during stage determi nation of the medial clavicular epiphysis by means of computed tomography[END_REF]. The radiological assessment for this study was performed by a radiologist with a little experience in anthropological studies. However, intra-observer variability was excellent (0.85 to 1) and inter-observer variability was also good (0.72 to 1). This point highlights the absence of evident technical issues in scapula ossification center assessment.

Another limitation concerns the mean ages for stages 1 and 5: youngest appearance for stage 1 and oldest appearance for stage 5. These points could not be taken into account due to the fact that lower and upper limits were chosen. Indeed, we exclude individuals younger than 7.4 or older than 30.6 years old, because we estimate that they would all be classified stage 1 and stage 5, respectively. This point explains also the fact that there is no stage 1 for coracoid center, which normally appears within the first year of life.

CT scapula can probably not be considered like an option for prospective age estimation. The first reason is exposure to radiation. Nowadays, even if it seems unrealistic to practice an additional scapula CT examination to study age, new techniques such as low-dose CT scans are more and more developed and will allow, in a next future, a very low radiation exposure [START_REF] Meyer | Initial results of a new generation dual source CT system using only an in plane comb filter for ultra high resolution temporal bone imaging[END_REF][START_REF] Newell | Very low dose (0.15 mGy) chest CT protocols using the COPDGene 2 test object and a third generation dual source CT scanner with corresponding third generation iterative reconstruction software[END_REF]. The second reason is its inferiority compared to classical hand/wrist X-ray usually employed in those age segments between 10 and 18 years. Indeed, X-ray hand/ wrist region has a lower exposure to radiation and is cheaper and much easier to apply and to evaluate. Also, there is no need of posttreatment reconstructions using classical X-rays. A recent study showed that Greulich and Pyle's method was globally valid on a sample of contemporary French young people. However, up to 48 months, difference between the estimated bone age and the real age could be seen for some individuals [START_REF] Zabet | Can the Greulich and Pyle method be used on French contemporary individuals?[END_REF]. If a thoracic CT scan was performed (for a clinical reason) on this population, the use of scapula's method will allow a greater precision in age estimation. And even if CT of scapula is not an option, CT of the medial clavicle will often also include the superior part of the scapula (such as the acromion process and coracoid process). By this way, we could combine these two methods using the same CT scan acquisition.

Results of our study did not show that any ossification center appears after 18 years old. However, the use of some ossification stages allows more precise age estimation. For example, all people with a coracoid ossification center less than stage 4 were aged less than 18 years old and for acromial ossification center less than stage 2 were aged less than 18 years old.

The main limitation of our study was the lack of information about ethnic origin and socioeconomic level of the individuals. Reference methods in the field of age determination are established on samples of young healthy individuals of known age, growing up in a non-deficient environment, with a high socioeconomic level [START_REF] Schmeling | Age esti mation of living people undergoing criminal proceedings[END_REF][START_REF] Pyle | Radiographic atlas of skeletal development of the knee[END_REF]61]. Schmeling et al. [START_REF] Schmeling | Statistical analysis and verification of forensic age estimation of living persons in the Institute of Legal Medicine of the Berlin University Hospital Charité[END_REF]3] demonstrated that socioeconomic level plays a much greater role on bone maturation speed compared to ethnicity. A poor socioeconomic level slows bone maturation [START_REF] Meijerman | Variables affecting the probability of complete fusion of the medial clavicular epiphysis[END_REF]. If methods obtained from children with a good socioeconomic level are applied to individuals from disadvantaged backgrounds, there is a risk of underestimating their actual age. This underestimation, if it is a source of error in the assessment of age, is not an ethical problem itself as the error occurs for the benefit of the individual.

Conclusion

This first work carried out on CT reconstructions confirmed that the scapula presents anatomical interest in estimating bone age. The five stages defined by Schmeling et al. to describe ossification of the medial epiphysis of the clavicle on the basis of conventional radiographs can also be observed on scapula CT examinations [START_REF] Schmeling | Studies on the time frame for ossification of the medial clavicular epiphyseal car tilage in conventional radiography[END_REF]. Whatever is the epiphyseal center and whatever is the sex, all stage 2 is under the 18year-old threshold. Even if none of the ossification stages investigated in this study first appears after age of 18, study of these epiphyseal centers, particularly using a retrospective method, could be very useful. This assessment still needs to be used in complement of the preexisting age assessment methods. Obviously, further studies with larger groups are needed to support our results.

Fig. 1

 1 Fig. 1 Illustration of a scapula: anterior view (a) and sagittal view (b), showing the location of the primary and secondary ossification centers studied. 1, acromial; 2, sub coracoid; 3, glenoid; 4, coracoid apex; 5, cor acoid; 6, inferior angle

Fig. 2

 2 Fig. 2 CT reconstructions and schematic illustrations of the ossification center aspects for each stage. a CT reconstructions and schematic illustrations of the ossification aspects for acromial, sub coracoid, and

Fig. 2

 2 Fig. 2 (continued)

  [START_REF] Wittschieber | Influence of the examiner's qualification and sources of error during stage determi nation of the medial clavicular epiphysis by means of computed tomography[END_REF].9 [9.3 = 0.7] 9.2 -]0_5 [9.9 ± 0.5) 9.2 -14.5 [12 .2 = 1.7) 11.4 -30.5 [2 1.2 = 6.1) 11.6 -30.6 [21.8 = 5)

  [START_REF] Dvorak | Application of MRI of the wrist for age determination in international U 17 soccer com petitions[END_REF].2 [ o. = 1. l 9.6 -13.6 [10.9 ± 1.9] 0.4 • 15.8 [ 3. = 1. 1 16.6 -19.7 [18.2 ± 2.2] 15.1 -30.6(23.4 -18.4 [11.8 ± 2.4] 11.6 -17.6 ( 15.1 ± 1.8) 13.2 -18.8 [16.5 ± 1.6] 18.9-22.3 ( 19.9 = 1.1 ] 18.4-30.6 [25 ± 3.7] 5.4 [ 11 ± 2.2] 13.5 -16.9 (15.7 ± 1.1 ) 13.5 -20. [16.4 ± 2.3] 7 . -19.1 (18.2 ± 0.7] 18.2 -30.6 [24.6 ± 3.6)

Fig. 3

 3 Fig. 3 Box and whisker plots showing all CT stages in relation to age for the six ossification centers. Box represents inter quartile range, thick black horizontal line represents median, t bars represent extremes, and asterisks and circles represent outliers

Table 2

 2

	Multislice computed
	tomography (MSCT) reconstruc	Slice thickness/interval (mm)	1.0 0.5	1.0 1.0	2.0 1.0
	tion parameters	Number of MSCT investigations	45 (19.4 %)	91 (39.2 %)	96 (41.4 %)

Table 3

 3

	Results for intra
	observer variability, inter	Ossification	Intra observer (n = 25)	Inter observer (n = 20)	Side differences (n = 31)
	observer variability, and side's	center	Cohen's kappa	Cohen's kappa	Cohen's kappa
	differences
		Acromial	1	0.72	0.93
		Sub coracoid	0.85	0.74	0.96
		Glenoid	0.95	0.84	0.98
		Coracoid	1	1	0.94
		Apex	1	0.91	0.88
		Inferior angle	1	0.98	0.88

Table 4

 4

Age distribution for each stage

Minima maxima [mean (years) ± standard deviation]

F female, M male, NA not applicable, n number of cases for each ossification center