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The maxillary sinus elevation is a standard and predictable procedure allowing the realization of dental implant rehabilitation in patients with severe bone atrophy in the lateral-posterior areas of the maxilla. Despite the presence of validated surgical methods and the broad availability of biomaterials, the procedures aimed at increasing the bone volume by lateral antrostomy still entail complications with different degrees of relevance. The prosthetic and surgical outcome is based on a successful coping with these aspects. The perforation of the Schneiderian membrane is one of the most frequent events for which a variety of protocols and approaches have been suggested by different authors. In this work is presented a case study in which a technique to repair the sinus mucosa laceration occurring during a maxillary sinus elevation procedure has been successfully adopted.
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                                                                                                         Case report


    Management of the Schneiderian membrane perforation
    during the maxillary sinus elevation procedure:
    a case report




                                                                                                 li
    Deborah Meleo, DDS, PhD1                                to the development of standardized, predictable and
    Francesca Mangione, DDS1




                                                                                              na
                                                            safe regenerative techniques (1,2). The maxillary sinus
    Sergio Corbi, MD, DDS2                                  elevation is a surgical procedure that increases vertically
    Luciano Pacifici, MD, DDS1                              the available bone volume on the lateral-posterior
                                                            areas of the maxilla giving the possibility to place
                                                            osseointegrated implants (3,4). Thanks especially to the




                                                                                           io
    1
      “Sapienza” University of Rome, Italy                  ample indications from the literature (1-4), this procedure
    Department of Odontostomatological                      represents an excellent potential for the resolution of the
    and Maxillofacial Sciences                              bone atrophies associated to edentulism. Nevertheless,




                                                                      az
    2
      “San Camillo-Forlanini” Hospital, Rome, Italy         such kind of intervention is still characterized by
    Department of Odontostomatolgy                          complications, often predictable and yet unavoidable,
    and Maxillofacial Sciences                              posing limitations to its successful application (5-8).
                                                            The most common adverse events reported are: i)




                                                                    rn
                                                            haemorrhage, mainly due to lesions of the intramural
    Corresponding author:                                   artery, an anastomoses between the infraorbital artery
    Dr.ssa Deborah Meleo                                    and the posterior superior alveolar artery, frequently
    Via Guglielmina Ronconi, 55                             localized on the site in which the surgeon makes the




                                                            te
    00156 Rome - Italy                                      bone window to reach the antral cavity; ii) laceration
    Phone: + 39 3392416306                                  of the Schneiderian membrane, usually occurring with
    E-mail: deborahhh@tin.it                                a range of incidence comprised between 7% and 35%
                                                      In    of cases (9-11). The latter may occur during different
                                                            phases of the procedure: during the preparation of the
                                                            antrostomy, while removing or turning over the bone
    Summary                                                 window, during the membrane raising or upon grafting.
                                            ni
                                                            Moreover, there are some anatomical risk factors, like:
    The maxillary sinus elevation is a standard and         Underwood’s septa, which are bony walls partitioning
    predictable procedure allowing the realization of       the sinus, usually with a vertical progress; the angle
    dental implant rehabilitation in patients with severe
                                    io


                                                            between the buccal and palatal walls of the antral cavity,
    bone atrophy in the lateral-posterior areas of the      as analyzed on perpendicular tomographic sections,
    maxilla. Despite the presence of validated surgical     especially when below 30°; irregularities of the sinus
    methods and the broad availability of biomaterials,     floor due to the protrusion of the root profiles; previous
                            iz



    the procedures aimed at increasing the bone volume      sinus surgery; a decreased height of the residual
    by lateral antrostomy still entail complications        alveolar ridge. Since discontinuities in the Schneiderian
    with different degrees of relevance. The prosthetic
              Ed




                                                            mucosa impair the functional homeostasis of the antral
    and surgical outcome is based on a successful           cavity and negatively affect the surgical outcome by
    coping with these aspects. The perforation of           bacterial contamination of the graft and dispersion of the
    the Schneiderian membrane is one of the most            particulate, several authors have studied and suggested
    frequent events for which a variety of protocols        specific repair techniques for each type of perforation
    and approaches have been suggested by different         (12-16).
    authors. In this work is presented a case study
 IC




    in which a technique to repair the sinus mucosa
    laceration occurring during a maxillary sinus           Schneiderian membrane perforation: predisposing
    elevation procedure has been successfully adopted.      factors, classification and management
C




    Key words: Schneiderian membrane, maxillary sinus       The maxillary sinus elevation is a standard and
    augmentation, sinus lift complications, underwood       predictable surgical procedure to rehabilitate severe
    septa.                                                  vertical bone atrophies in the lateral-posterior areas of
©




                                                            the maxilla by placement of osseointegrated implants
                                                            (6,8,17-22). However, it is known that complications
    Introduction                                            like haemorrhage and perforation of the Schneiderian
                                                            membrane may affect negatively the outcome of such
    Nowadays, the rehabilitation by prosthetic implants,    procedure. In most reported cases, intra-operative
    even in edentulous areas of the maxillae affected by    bleeding is due to the lesion of the anastomoses
    severe bone atrophies, is an inescapable need leading   between the infraorbital artery and the posterior superior


    24                                                                            Annali di Stomatologia 2012; III (1): 24-30
    Management of the Schneiderian membrane perforation during the maxillary sinus elevation procedure: a case report



    alveolar arteries at an average distance of 19 mm from              process (46-49). In the modified method, the cover of
    the apical ridge, with a tendency to superficialize in              the sinus walls is still carried out with the support of a
    conditions of marked bone resorption. Such localization             resorbable membrane located only on the surface of the
    often coincides with the area where the antrostomy of               Schneiderian membrane, leaving the bone walls free
    access to the sinus cavity is carried out (9-11,14).                so that the blood supply from the bone can favour the
    However, the most frequent unfavourable event                       vascularization and thereby the integration of the graft




                                                                                                              li
    associated to such intervention is the laceration of the            into this virtual space. Moreover, in such technique




                                                                                                           na
    sinus mucosa. Such event is often predictable, but not              the resorbable membrane is fastened at the superior
    avoidable, since it is strictly associated to anatomo-              border of the antrostomy through titanium or surgical
    pathological predispositions (23-26). In the literature,            steel pins before being reinserted in the sinus cavity;
    the following predisposing factors have been identified:            a second membrane is positioned on the antrostomy
    previous phlogistic processes, irregularities of the                externally, to further protect the biomaterial (46). It has




                                                                                                        io
    sinus floor, e.g. due to root protrusions, thickness of             been demonstrated that the protection of the osteotomic
    the membrane below 1,5 mm, limited expansion of the                 window increases implant survival if some prerequisites
    anterior recess, angle between buccal wall and socket               are respected: membrane stability, sterility and optimal




                                                                                   az
    below 30°, former surgical treatments, reduced height of            cohesion, compactness and handiness of the graft
    the alveolar ridge (27-34). In particular, the Underwood’s          material (1,6,50-62).
    septa, present on average in 31% of the maxillary
    sinuses with a height of about 8 mm (range 3,5-2,2




                                                                                 rn
    mm), can involve all areas of the sinus. Usually they are           Case report
    partial, they run vertically in buccal-palatal direction and
    are higher at the level of the medial wall; more rarely             The reported clinical case has been managed
    they are multiple within the same antrum (8,24-26,29,35-            in collaboration with the Departmental Unit of




                                                                       te
    37).                                                                Odontostomatology and Maxillo-Facial Surgery of
    The laceration of the sinus mucosa affects negatively               the San Camillo Forlanini Hospital (Rome, Italy). The
    the surgical outcome by increasing the risk of iatrogenic           patient (female, 45 years old) asked for a functional and
    sinusitis, impairment of functional homeostasis and
                                                             In         aesthetical rehabilitation of the lateral posterior area of
    dispersion of the graft material in the antral cavity as            the right emi-maxilla. Personal anamnesis excluded the
    well its bacterial colonization (38-40). Among several              presence of pathologies contra-indicating the implant
    possibilities of repair of the perforation, as reported in          rehabilitation as well as attitudes such as smoking.
                                                  ni
    the international literature (8,19,20,41-45), we refer here         The physical exam and the radiographic evaluation
    to the study of Fugazzotto and Vlassis (2003), which                (orthopantomography) highlighted the presence of root
    classifies the lesions of the sinus mucosa in relation              residuals 1.4, 1.6 and of the element 1.8 compromised
                                           io


    to size and position and associates to each class a                 for periodontal evaluation (Fig. 1). In order to proceed in
    specific therapeutic indication (46). Class 1 identifies            the best conditions such elements have been extracted.
    the perforations below 5 mm in size that extend to the              After four weeks the mucosae upon the post-extractive
                                 iz



    upper border of the antrostomy, for which it is simply              sockets were perfectly recovered. The anatomical state,
    required a further detachment of the membrane to allow              according to Chiapasco’s classification, was attributed
    the seal of the lesioned flaps (46,47); class 2A describes          to class A in the area of element 1.5 and class C in the
                 Ed




    lacerations located at the borders of the osteotomy,                molar region (5). The individual prosthetic plan pointed
    delimited from at least 4-5 mm of intact tissue, with the           towards the choice of an implant supported cemented
    suggestion to enlarge the limits of the bone window                 fixed prosthesis, following optimization of the sites
    and to apply a resorbable membrane in case of failed                through surgical procedure of lateral maxillary right sinus
    sealing of the margins of the perforation (46-49); classes
    2B and 3 correspond respectively to lacerations that
 IC




    develop laterally from the antrostomy, delimited by less
    than 4-5 mm of intact tissue, and to central lesions, often
    preexisting and determined by former dental avulsion or
    oroantral fistulae. These latter can be managed with the
C




    same treatment, known as modified Pouch Technique
    (46-49).
    The original technique, known as “Loma Linda Pouch”,
    consists in covering the whole sinus with a collagen
©




    membrane simulating the natural membrane, and the
    graft material is completely covered in its centre by
    folding the membrane on the lateral wall. However, in
    this manner, an external barrier is created that totally
    isolates the biomaterial from the blood supply coming
    from the walls of the sinus, thus representing an
    obstacle to the maturation of the graft and the recovery            Figure 1 - Pre-operative orthopantomogram.


    Annali di Stomatologia 2012; III (1): 24-30                                                                                 25
    D. Meleo et al.



    elevation. The intervention was carried out in day hospital.    inner part of the sinus to for the graft containment (Fig.
    Four block anaesthesias were executed at the level of           3). According to the suggestions of several authors
    the superior posterior alveolar nerve, the major palatine       (11,50,51,53,54,60,62,63) we used as filler a compact
    nerve, the infraorbital nerve and the nasopalatine nerve,       and consistent material in order to avoid the dispersion
    and one anaesthesia by infiltration of the fornix and the       of particles in the sinus and thereby the possibility of
    palatine mucosa (articaine 4% and vasoconstrictor               phlogistic processes due to bacterial colonization of




                                                                                                           li
    1:100.000). Thereafter, a trapezoidal mucoperiosteal flap       the graft. The material is a human-derived bone paste




                                                                                                        na
    with linear main incision between distal margin 1.3 and         in blocks, called Bioset, available on request in Italy at
    area 1.7 has been set up, together with divergent release       Rizzoli Orthopaedic Institute (I.O.R.), that is the italian
    incisions extended 5 mm beyond the mucogingival                 national public bank of the musculoskeletal tissue; this
    line. The flap has been opportunistically detached and          product contains demineralized bone matrix (DBM)
    folded down to highlight the maxillary bone surface. The        and bone corticospongious particulate carried in a




                                                                                                     io
    antrostomy, of rectangular shape with round corners             thermoplastic gel of suine collagen (Fig. 4).
    and approximate size of 20 x 15 mm, has been carried
    out with piezoelectric devices. The detachment of the




                                                                               az
    membrane was initiated with piezoelectric devices and
    terminated with manual devices. Despite the absence
    of evident anatomical abnormalities and the accuracy of
    the surgical procedure, a perforation of the Schneiderian




                                                                             rn
    membrane of about 8 x 6 mm occurred (Fig. 2).




                                                                    te
                                                              In
                                                                    Figure 4 - A human-derived bone paste in blocks, called Bioset,
                                                                    containing demineralized bone matrix (DBM).
                                                 ni
                                       io


    Figure 2 - Maxillary sinus membrane perforation
                              iz



    Following the suggestions of Fugazzotto and Vlassis,
    we chose to continue with the procedure and decided to
                Ed




    repair the lesion through the modified Pouch Technique
    (46). A resorbable membrane of freeze-dried bovine
    pericardium (Tutopatch, Tutogen Gmbh) was modelled
    and blocked with titanium pins above the superior
    border of the antrostomy and was then folded in the
 IC




                                                                    Figure 5 - Plastic consistency and easy manipulation of Bioset.

                                                                    The particulate component acts as a natural
                                                                    osteoconductive matrix at low resorbing activity, the
C




                                                                    DBM allows the release of morphogenetic proteins,
                                                                    preserved by a peculiar sterilization process undergone
                                                                    by the material (BioCleanse®), while the carrier confers
                                                                    consistency and easy manipulation: it is preserved
©




                                                                    at –20°C for 6 months or at –80°C for 5 years and it
                                                                    becomes plastic, malleable and adhesive when warmed
                                                                    in hot water in its sterile package up to a temperature
                                                                    between 43°C and 49 °C, while becoming stable in size
                                                                    and consistency at body temperature (Fig. 5). We have
    Figure 3 - A resorbable membrane of freeze-dried bovine peri-   compacted only 2 cc of bone paste internally (Fig. 6),
    cardium positioned according to modified pouch technique.       since overfilling has been shown to be responsible of

    26                                                                                      Annali di Stomatologia 2012; III (1): 24-30
    Management of the Schneiderian membrane perforation during the maxillary sinus elevation procedure: a case report




                                                                                                               li
                                                                                                            na
                                                                                                         io
                                                                        Figure 8 - Histology of bone neoformation at six months after
                                                                        sinus lift (40x, H&E).

    Figure 6 - Maxillary sinus filled with Bioset.




                                                                                   az
                                                                                 rn
                                                                       te
                                                             In         Figure 9 - Ortopantomogram at six months after implants place-
                                                                        ment
                                                     ni

    Figure 7 - A second resorbable membrane applied above the
    antrostomy.
    the necrosis of the sinus membrane with dispersion
                                           io


    of material and chronic sinusitis; thereafter, a second
    resorbable membrane above the antrostomy has been
    applied (Fig. 7). Finally, mattress suture horizontal with
                                 iz



    non resorbable monophilament was carried out.                       Figure 10 - Paraxial views of TC dentascan at one year after
    The patient underwent antibiotic, analgesic and anti-               prosthetic rehabilitation.
    edemic therapy for seven days. After six months the
                 Ed




    case has been evaluated clinically and radiographically.
    We could ascertain complete recovery of the tissues,
    integration of the graft and absence of phlogistic
    complications. We therefore proceeded with the
    placement of three implant fixtures of conic shape,
    diameter 4,5 x 12 mm, and one of 4,5 x 10 mm sand
 IC




    blasted and acid etched (TiRADIX s.r.l.). During the
    preparation of the sites of implant a bone biopsy was
    performed with a trephine bur (internal diameter of
    2 mm). The sample was fixed by buffered formalin,
C




    stained with hematoxilin-eosin and observed at the optic
    microscope (40x). The sections showed the presence
    of lamellar bone tissue with osteocyte lacunae (Fig. 8).            Figure 11 - Panoramic views of TC dentascan at one year after
    Some lacunae appeared without cells, separated by
©




                                                                        prosthetic rehabilitation.
    fibro-vascular tissue containing amorphous material.
    We noted lamellar bone in development, deposited in                 University of Rome).
    proximity of young trabeculae. The active process of                The orthopanoramic radiography and TC exam with
    bone rearrangement was highlighted by the presence                  the specific software dentascan (Figs. 9, 10, 11),
    of osteoclasts and osteoblasts (courtesy of Prof. G.                performed one year after prosthetic rehabilitation, show
    Soda, Department of Experimental Medicine, Sapienza                 the reorganization of the hard tissues in the antrum


    Annali di Stomatologia 2012; III (1): 24-30                                                                                         27
    D. Meleo et al.



    and around the fixtures. The case was subsequently                 2. Shulman LB, Jensen OT. Sinus Graft Consensus Confer-
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                                                                                                              li
                                                                          of sinus lift procedures for dental implant rehabilitation: a
                                                                          Cochrane systematic review. Eur J Oral Implantol 2010;3




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                                                                          (1):7-26.
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                                                                       9. Elian N, Wallace S, Cho SC, Jalbout ZN, Froum S. Dis-
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                                                                  In      Floor Augmentation. Int J Oral Maxillofac Implants 2005;
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                                                    ni
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                                          io

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                                iz



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                Ed




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 IC




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