Oral implant placement and restoration by undergraduate students: clinical outcomes and student perceptions For figures, tables and references we refer the reader to the original paper. Introduction Oral implant therapy has become a popular, well accepted and widespread treatment modality to replace missing teeth. It is currently an established part of mainstream dentistry [1-3]. Whereas oral implant placement and restoration used to be in the hands of specialists (oral surgeon/ periodontologist/prosthodontist) at the time osseointegration was introduced, these treatments are increasingly being performed by general dentists with a special interest in oral implant dentistry. Hence, universities need to develop and implement an academic, evidence-based implant dentistry training programme at all levels in order to prepare dental professionals for the growing treatment needs [4-7]. Both the surgical and the prosthetic aspects of clinical training in oral implant dentistry are taught predominantly in postgraduate programmes. However, nowadays, basic principles in implant dentistry have become part of periodontology, oral surgery and prosthodontics courses. [2, 8-10]. It seems logical that within the duration of the undergraduate curriculum, the wide spectrum of oral implant dentistry cannot be taught in full detail. However, when graduating, a dentist should have the competence of (i) describing the risks, benefits and long- term consequences of using osseointegrated implants within an overall treatment concept, (ii) describing the principles and techniques involved in the use of osseointegrated implants for restorations, (iii) describing the indications and contraindications, principles and techniques of surgical placement of osseointegrated implants [11]. The list of required competencies was further expanded during the 1st European Consensus Workshop on Implant Dentistry University Education, 2008 [12]. A consensus was reached that students should learn basic theoretical knowledge on the biological prerequisites and clinical procedures that lead to successful implant treatment. Furthermore, they should understand the importance of including oral implants into the overall treatment concept and be able to explain the different treatment options to patients, including advantages and disadvantages. Undergraduate students should have insight into how dental implants heal into the bone and the effects on the soft tissues. They should understand the aetiology and pathogenesis of peri-implantitis and suitable therapy interventions. Finally, the consensus meeting recommended that surgical practices should be included in the dental curriculum. In 2013, the benchmarks set in 2008 were reviewed. It was concluded that the implementation of implant dentistry in the undergraduate curriculum had improved significantly, but still lagged behind the 2008 benchmarks. Moreover, there were large differences between institutions [13]. Many universities today are making efforts to include clinical experience in implant dentistry in the undergraduate curriculum, either by observing or by assisting implant surgeries and restorations. A recent systematic review [14] and survey on oral implant dentistry [4] showed that a substantial number of dental curricula are currently fulfilling the 2009 recommendation [15] to include clinical experience in implant surgery. However, this finding did not refer to the surgical act of placing oral implants. Clinical experience in oral implant prosthetics seems to increase [4]. Nevertheless, there are some barriers for implementation of oral implant dentistry into the curriculum such as (i) funding issues, (ii) lack of available time in an already overcrowded dental curriculum, (iii) insufficient number of suitably trained staff available for clinical teaching and (iv) insufficient patient flow [2, 7, 14]. When it comes to education itself, most of the centres used lectures for educational purposes. Pre-clinical laboratory hands-on courses on models were reported in high percentages [16]. These pre-clinical hands-on courses have been shown to have a positive influence on the attitude towards implant dentistry [17]. However, interestingly, graduated dentists in Hong Kong with ‘hands-on’ experience and more extensive training (50 days or more) were rather prudent and conservative in perceived benefits of oral implants [18]. Most likely this reflects different philosophies of care [15, 19]. Undergraduate students at the KU Leuven have the opportunity to treat one patient with implants, starting from the treatment planning, over the implant surgery to the prosthetic treatment and follow-up. The aim of this study was to describe how oral implant dentistry is taught at the KU Leuven and focusses on implant-related clinical outcomes. Furthermore, the perspectives of participating undergraduate students were analysed. An answer to the following research questions was provided: Q1: What is the clinical outcome of oral implants placed and restored by undergraduate students with regard to marginal bone loss in a mean follow-up period of 2 years? Q2: What is the perspective of undergraduate students on behalf of the educational strategies used in the oral implant dentistry programme? Q3: What is the perspective of students 1 year after graduation on oral implant dentistry and the influence of the oral implant dentistry programme on their clinical activities in private practice? Materials and methods Description of the educational oral implant dentistry programme Clinical oral implant dentistry training at the KU Leuven starts in the 5th semester of a 5-year dental curriculum. Theory During introductory lectures on oral implantology in the 5th, 6th and 8th semesters, undergraduate students receive basic information concerning oral implant therapy. These lectures focus on various aspects of implant dentistry from a surgical as well as a prosthetic/restorative point of view (Table 1). Additionally, radiology lectures are covered by the oral imaging department. Students thus gain insight into the different aspects of oral imaging and knowledge of 3D cross-sectional imaging as a diagnostic as well as a therapeutic (planning/drill guides) tool. Theoretical knowledge is assessed during oral/written examinations at the end of the semester. Table 1. Overview of the main aspects focused on during lectures on ‘oral implants’ at the KU Leuven at the Department of Periodontology/Restorative dentistry Seminars and hands-on training During the 5th and 6th semesters, undergraduate students come in close contact with oral implants during a series of seminars and hands-on training sessions. These focus on the partial edentulous lower jaw and the partial edentulous upper jaw (replacement of a central incisor by means of a solitary implant and fixed dental prosthesis (FDP) on two implants). Another series of seminars and hands-on training sessions focus on the treatment of the edentulous maxilla and mandible by means of an overdenture on 2 to 4 implants, respectively. Using a surgical guide and concentrating on ideal positioning (restoration-driven), students learn to make osteotomies for the partially edentulous jaws on models in phantom heads (Fig. 1). All implants placed during these hands-on sessions are used to practise the restorative/prosthetic part in the next part of the training (Fig. 2). Knowledge and surgical/restorative skills obtained during these seminars and hands-on sessions are assessed by the supervisor in various exercises. Figure 1. Practical hands-on training ‘partial edentulous lower jaw’. (A) Pre-operative view of the lower right quadrant. (B) Fit of the surgical template. (C) Crestal incision and releasing incision. (D) Reflection of a mucoperiosteal flap. (E) Further dissection and localisation of the mental foramen. (E) Verification of the correct implant positioning. (F) 2.0-mm twist drill in correct mesio-distal and vestibulo-oral inclination and final implant length. (G) Direction indicators to check correct positioning. H: Pilot drill. (I) 2.8-mm twist drill in correct inclination and final implant length. (J_ Implant placement. (K) Healing abutment placement. (L) Flap suturing and prosthetic phase. Figure 2. Practical hands-on training ‘3-unit bridge on multiunit abutments’; (A,B) Placement of multiunit abutments. (C,D) Placement of temporary cylinders on the multiunit abutments. (E) Impression is used to verify the height of the cylinders. (F) Carborandum disc on handpiece is used to shorten the cylinders. (G) Polymerisation material is used in the impression to fabricate the temporary 3-unit bridge. (H) Impression and polymerisation. (I, J, K) Access to the screw openings is created with a small round bur. (L) Removal of the 3-unit temporary bridge and further finishing of the bridge. Clinical experience Clinical exposure of undergraduate students starts in the 5th semester with a 10-h clinical internship at the departments of periodontology, prosthetic dentistry and the centre of oral imaging. Students can follow the interpretation of radiological images and treatment planning and attend postoperative consultations. From the 6th semester onwards, students need to attend (20 h) various surgical procedures at the department of periodontology. In the 6th semester, they observe and assist on the fabrication of an overdenture on 2 to 4 implants. During the 8th, 9th and 10th semesters, they need to perform small surgical interventions themselves under the supervision of a postgraduate student (e.g. small periodontal surgery, gingivectomy, crown lengthening and extractions). In the 7th semester, they are trained on how to make a removable partial prosthesis, whist in the 8th semester, they start making single restorations on teeth. In the 9th and 10th semesters, they are clinically trained how to make 3- to 4-unit FDP on teeth and how to restore multirooted teeth, single-tooth replacements on implants (up to 3) and overdentures. During the 8th, 9th and 10th semesters, patients treated by undergraduate students are screened as potential candidates for implant treatment in the undergraduate oral implant dentistry programme. Whenever the undergraduate student thinks a patient is suitable, he/she is scheduled for a cone- beam CT scan. Students interpret radiological imaging focusing on anatomical proportions, bone quality, bone quantity and any pathologies whist also focusing on the topography of the neighbouring teeth and anatomical landmarks. They then virtually plan the implants in implant planning software (Simplant®, Materialise, Leuven, Belgium). After consultation with the supervising periodontologist and prosthodontist, a patient can be included into the undergraduate implant programme. Implant indications for the undergraduate programme are as follows: (i) edentulous or partially edentulous patients with adequate bone quantity (width/height), (ii) no need for bone grafting procedures, (iii) non-aesthetic area (premolar and molar area upper jaw), (iv) positions anterior of the mental foramen and (v) no objection to being treated by an undergraduate student. In some cases, exceptions are made after approval of the tutor. Casts of upper and lower jaws are made and used for a private pre-operative hands-on session, in which the student exercises how to make the implant osteotomy, taking into consideration implant direction and depth. The preoperative preparation of the patient and the local anaesthesia is administered by the student. Students perform the surgical interventions with permanent assistance of a supervisor with vast surgical experience (MM). The latter can interfere whenever necessary. All implants (Bränemark MKIII TiUnite, Nobel Biocare AB, Gothenburg, Sweden) are placed after the reflection of a mucoperiosteal flap. Whenever a guided bone regeneration procedure is necessary, this is performed by the supervisor or by a postgraduate periodontology student. Whether the implant follows a submerged or transmucosal healing depends on the primary stability of the implant and is left to the discretion of the supervisor. Flaps are sutured to ensure a tight seal (Vycril 3/0–4/0, Silk 3/0–4/0 Ethicon/Johnson&Johnson, Hamburg, Germany). Patients are instructed on post-surgical maintenance (e.g. chlorhexidine 0.12% mouthrinse, medication, cooling). Removable prostheses are not worn until they are adjusted/relined to the new situation (approximately 7 days after implant placement). Sutures are removed 7 days after implant placement. After a 3- to 4-month osseointegration period, the implants can be restored by the same undergraduate student. After the completion of the treatment, all patients join the common implant recall programme of the departments of periodontology/prosthetic dentistry (Fig. 3). Figure 3. Case presentation of a patient in the undergraduate implant programme. (A) facial view of the patient included in the undergraduate implant programme and treated multidisciplinary by the same student. (B) panoramic slice of the CBCT indicating the direction of neighbouring teeth. (C) Crosssectional slice of the CBCT indicating adequate bone height and width. (D) Sagittal slice of the CBCT. (E) Pre-operative radiograph with direction indicator at 7 mm of depth. F: Post-operative radiograph. (G) Radiograph to check correct abutment position. H: Radiograph 6 months after loading. (I) Radiograph 1 year after loading. (J): Radiograph 2 years after loading. (K) Final frontal view. Virtual planning of the implants and surgical skills demonstrated during implant placement are considered to assess students' competences. Clinical outcome To investigate the clinical outcome of the implant therapy provided by undergraduate students, a retrospective analysis was performed. Intra-oral, long-cone radiographs were taken at implant insertion, at healing abutment connection, at restoration/prosthesis insertion and after 1 and 2 years of functional loading. The marginal bone level was measured from the implant–abutment connection to the first visible bone-to-implant contact (BIC) mesially and distally. The change in the marginal bone level was calculated by using the actual length of the inserted implant and the thread pitch distance of the implant. The marginal bone level at the time of final restoration insertion, and thus functional loading, was regarded as baseline. Marginal bone loss was defined as the difference between marginal bone levels at baseline and each follow-up appointment. The analysis of periimplant bone level alterations was performed independently by 2 calibrated periodontologists (AT & RD – calibration was performed in advance by measuring the peri-implant bone level alterations on 10 periapical radiographs and comparison/evaluation afterwards). Results were re-evaluated when there was ≥1 mm interexaminer difference. Measurements were made to the nearest 0.1 mm using the software tool (PACS Lightbox, IMPAX Pacs, Agfa). Student perceptions Every undergraduate student, who was able to find a suitable patient and had the opportunity to place an oral implant, was asked to fill in a written questionnaire after surgery. This questionnaire was distributed and collected by the supervisor and focused on various aspects that are interesting to refine the implant education programme, seminars and hands-on workshops. It contained six multiple-choice questions and 1 open question, allowing the student to give some additional advice to improve the programme. Students were asked whether they felt the need for additional information prior to surgery, and his/her feeling after surgery. Furthermore, students were asked whether they would implement implant treatment in their own practice (see Fig. 4). All questionnaires were collected immediately after the surgery and analysed. One year after graduation, the student was contacted via e-mail. They were asked whether they were working as a general dentist or had started a postgraduate programme. To gain insight into their current clinical activities with oral implants, they were asked whether they had started an extra implant dentistry course and whether they had placed implants and restored them. Figure 4. Schematic overview of the questionnaire and results. Results Clinical outcome After having ran the implant training programme for 3 years, 112 implants had been placed in 56 patients (63.5% male) with a mean age of 56.8 years (range: 30–83) by 56 undergraduate students. Three and a half percentage of these patients were smokers. Forty-nine and a half percentage of the implants were placed according to a one-stage protocol with the immediate installation of a healing abutment. Fifty and a half percentage followed submerged healing. In 4% of the implants placed, a per-operative guided bone regeneration procedure (GBR) was necessary due to a dehiscence or fenestration. The latter procedure was carried out by the supervisor or a postgraduate periodontologist. Table 2 shows an overview of the implant positions and type of restoration/prosthesis. Four patients were lost during follow-up [one died (two implants), three refused (five implants) to have a control appointment]. Two implants failed to integrate in one patient due to periapical implant lesions. These lesions could not be treated so explantation was performed [20]. Another implant was lost due to peri-implantitis after 1.5 years in function. After a follow-up time of 2 years, the cumulative implant survival rate, at implant level (105 implants), was 97.1%. Table 2. Overview of the various types of implant-supported rehabilitations and implant positions Student perceptions The total number of undergraduate students in the senior year was 91. In total, 56 students were included in the clinical programme (61.5%). Student perception of the implant dentistry training is visualised in Fig. 4. A high percentage of students were very satisfied with both theoretical and practical training, and they considered this sufficient preparation to perform implant placement under close supervision. Eighty-five percentage of them admitted to having searched for extra information before the actual surgery (such as surgical guidelines provided by the company on the website, internet movies and applications). Sixty percentage of students would prefer to attend an extra course in implant dentistry after graduation, and 26% would not place implants themselves in their own practice. Overall, the majority of undergraduate students considered the oral implant dentistry training and the opportunity to perform implant surgery and restoration as an added value to the overall dentistry curriculum. One year after graduation, students were asked to provide information about their implementation of implant dentistry in private practice. Of 56 students (response rate 100%), 15 started a postgraduate programme and 4 students were further trained as maxillo-facial surgeons. Thirty-seven students were active as general dentist, and of those, only seven started a course in oral implant dentistry to gain more insight into surgical and prosthetic procedures. All general dentists, however, restored implants themselves. Discussion The oral implant dentistry educational programme at KU Leuven, which started in 2009, was developed to give undergraduate students the opportunity to gain insight into the surgical and restorative procedures. To this end, both lectures and pre-clinical/clinical training modalities are being used. Clinical outcomes of surgical procedures performed by undergraduate students were shown to be acceptable. For all parties involved in oral implant therapy, the most important goal is to achieve a long-lasting outcome (in both supporting implants as well as in the suprastructure). An important issue in achieving this goal is maintaining osseointegration. During these 2 years of followup, 2 implants failed to integrate and 1 was lost during follow-up due to severe peri-implantitis. This resulted in a cumulative survival rate, at implant level of 97.4%. This survival rate is in line with rates achieved by undergraduate students in other implant dentistry educational programmes [10, 21, 22]. The impact of experience on achieving osseointegration of oral implants has been extensively explored. Some of these studies compared implants placed by inexperienced and experienced surgeons and concluded that the rate of osseointegration was significantly higher for experienced surgeons [23-25]. A possible explanation for the poor outcome of implants placed by inexperienced surgeons is that with less experience, the frequency of problems such as excessive heat during drilling, non-stabilisation of the implant and lack of adequate planning may increase. However, these findings could not be confirmed by others [26, 27]. In the study of Melo and co-workers [26], inexperienced surgeons were supervised by experienced surgeons, which can explain the better outcomes. In the present study, all the different steps necessary in planning and implant placement were strictly supervised by an experienced surgeon. This may account for the comparable outcomes. Peri-implant bone loss should be prevented or minimised. A degree of marginal bone loss is widely accepted as proposed in previous studies [28-30], as being 1 mm during the first year of functional loading and an annual bone loss, which does not exceed 0.2 mm after this period. The results obtained in implants placed by undergraduate students in this educational programmes match these criteria of successful implants and are comparable with findings from other studies on the Brånemark type implant [31-33]. A shortcoming of this retrospective analysis is the lack of clinical parameters that could correlate with the bone loss, such as probing pockets depth, dimensions of the gingiva. An amount of bone gain after 2 years in function has been reported recently and can probably be explained by both clinical parameters as presence of sufficiently thick keratinised gingiva (3 mm), and the axis of implant insertion perpendicular to the opposing occlusal surface [34]. As in other curricula, students only performed treatment in straightforward cases where bone quantity and quality were sufficient and in areas that were not demanding aesthetically. Indeed, the chosen areas did not involve complex hard and soft tissue augmentations and prolonged treatment time. The most common procedures were single-tooth restorations in the premolar area of the upper jaw or 2 implants in the anterior mandible to retain an overdenture. These restorations/prostheses were also the most common ones as reported by others [35]. A recent study showed that implantsupported overdentures provided by undergraduate students could achieve similar levels of improvement in patient satisfaction and quality of life as those provided by experienced dentists [36]. Concerning both theoretical and practical trainings, the results of the questionnaires showed that a high percentage of students were very satisfied with the way implant dentistry is currently taught at the KU Leuven. Furthermore, they considered this sufficient to perform implant placement and restoration under close supervision by an experienced colleague. Questionnaires were collected immediately after the implant surgery. There was no offered time for student reflection on the learning procedures on the outcomes after surgery. This can, to some degree, have influenced the students when filling out the questionnaires. Huebner [37] and Maalhagh-Fard and Nimmo [38] concluded that dentists with undergraduate implant experience are more likely to implement the restoration of implants in their private practice. Furthermore, students' perception of oral implants seems be to influenced positively after undergraduate training in this field [39]. This was confirmed in our undergraduate student population as well, where 97% of the students graduating as a general practitioner are currently restoring implants themselves. An important observation is that of the 56 undergraduate students who had had the opportunity to place and restore oral implants, 19 decided to follow postgraduate training in one of the fields in dentistry. This observation is in agreement with a current trend that more and more specialists become trained in one specific field in dentistry. One of our main concerns when starting the undergraduate implant dentistry training was the fact that this could lead to overenthusiasm, which would eventually result in dentists performing implant surgery without any additional training. In our undergraduate student population, 14% of the students considered themselves able to perform implant surgery in easy, straightforward cases. This result is not in correlation with a recently published paper by Vandeweghe et al. [22]. Perhaps this percentage of undergraduate students underestimates the influence and contributing factor of the supervisor during surgery, possible complications that may arise during surgery and the clinical environment in which they are able to perform the surgery. To compensate for this, an extra lecture on surgical complications during and after implant surgery was included in the senior year. Furthermore, it is a well-established fact that to date, the graduated dentist has a choice between a great number of postgraduate oral implant courses (on an academic and non-academic level). These courses differ largely in cost, complexity and time needed to complete the course. One year after graduation, we could conclude that 12.5% of the students started an extra course in oral implantology. Due to the fact that the questionnaires were anonymous, we cannot conclude that these are the same students that considered themselves able to perform implant surgery in easy cases. Questionnaires were mandatory to fulfil the treatment. There were no non-respondents. The most common remark made by undergraduate students was that placing or restoring implant(s) in a single patient was too little to obtain enough clinical practice for future implant-related treatments. Clinical implant training at the KU Leuven is divided over several years, but the emphasis lies on the master years. It may be interesting to move implant training to an earlier time in the dental curriculum. This can have a significant impact on the number of patients a student is able to treat and thus also on future practice in implant dentistry. The theoretical training and seminars with hands-on training sessions are obligatory parts of the dentistry curriculum resulting in an examination at the end of the year. Students need to find a suitable patient themselves. As a consequence, not every undergraduate master student will have the opportunity to treat a patient. This is definitely a weakness of the current curriculum. Whereas at the beginning of the implant dentistry programme at the KU Leuven, students were able to treat more than one patient, there currently is a restriction of one patient per student. When this patient is in need of two or more implants, these can be placed by several students accordingly. This measure was taken to make treatment with oral implants possible for more students. The widespread use of oral implants in recent years has resulted in different types of biological complications. Even with the most stringent rules for sterility, optimal surgical planning and careful patient selection/preparation, some implants fail to integrate (short-term complication) or develop peri-implantitis (medium- to long-term complication) [40]. The number of technical/mechanical complications is also increasing. Undergraduate students need to get acquainted with these different types of possible complications, and they need to be able to diagnose them. Whether the treatment of these complications should be incorporated into the dentistry curriculum can be topic of debate. The use of CBCT images plays an important role in the selection of suitable patients for the undergraduate programme. Cross-sectional imaging, considered as the ‘gold standard' in implant planning [41-46], gives the student and supervisor the chance to pre-operatively evaluate bone quality and quantity and to include only these patients that can actually be treated by undergraduate students. Furthermore, implant planning software gives the undergraduate student the opportunity to plan the implant in a restoration-driven ideal 3D position when needed, or in a bone-driven mode (overdentures). However, currently the use of a stereolithographical guide and guided surgery is not incorporated into the undergraduate oral implant dentistry programme as it is, for example, at the University of Freiburg in Germany [16]. Although our findings to implement oral implant dentistry training seem beneficial, a number of barriers have been described in literature [2, 7] and were also present during the undergraduate programme described. Such a programme is certainly time-consuming and not possible without the help of an industrial partner to give patients some kind of financial compensation (by means of implants and components) for allowing them to be treated with oral implants by undergraduate students. This will eventually facilitate a sufficient flow of patients in the undergraduate programme. Furthermore, industrials partners can provide dental schools with the necessary educational components and other support. On finishing this oral implant dentistry programme, the undergraduate student will have the ability to identify indications for implant therapy, inform patients about possible treatment options and deliver effective implant-supported restorations. Furthermore, they will have knowledge and clinical experience, although limited, in implant surgery. From a theoretical point of view, they will have the knowledge on osseointegration, the importance of follow-up, the aetiology of peri-implantitis and the biological prerequisites that lead to successful implant treatment. The following recommendations may be useful for dental schools wanting to implement implant dentistry into the curriculum: Aim for good timing to start implant dentistry education, to eventually make it possible for every undergraduate student to gain some clinical experience with oral implants (prosthetically and/or surgically). Aim for a strong theoretical basis together with good pre-clinical set-up and hands-on exercises to ensure undergraduate students become acquainted with the surgical procedure, instruments. Aim for computerised implant planning to make the correct prosthetic positioning of the implant visible and understandable for undergraduate students Aim for clinical experience by letting undergraduate students assist during surgery by postgraduates. Conclusion The results show that the clinical outcome of implant treatment performed by undergraduate students in the implant programme at the KU Leuven is similar to that reported by experienced clinicians/research teams. Clinical, surgical as well as restorative, experience in addition to theoretical and preclinical training seems beneficial when implementing implant dentistry as a part of the curriculum in the undergraduate programmes of dental schools. Therefore, further development of clinical implant education in undergraduate programmes is mandatory. After graduation, the number of students that followed an extra implant course was small, suggesting the training they had received in the undergraduate curriculum fulfilled their needs at that moment. Acknowledgements The undergraduate implant programme at the KU Leuven was supported by Nobel Biocare AB (Gothenburg, Sweden) by providing implants, abutments and restorative components free of charge, as well as, the surgical sets and phantom models used during hands-on session.