Morbidity Consequences of ILO With Implants and Bone Grafting

The resultant consequences of ILO can vary depending on the type of implant or bone grafting procedure. For implant placement with good initial fixation, primary closure is favored for one-stage surgery with placement of a permucosal abutment. For bone augmentation procedures, primary closure is of paramount importance for clinicians when performing GBR techniques and autogenous onlay grafting procedures. When incision line opening occurs during autogenous block grafting, there tends to be a greater potential for delayed healing, loss of graft particles into the oral cavity, and increased risk of infection.

Exposure of nonresorbable membranes add additional risk of infection and unsatisfactory results. If guided bone regeneration is performed in conjunction with implant placement, ILO may also lead to loss of the implant. ILO most likely will result in a bacterial smear layer on the implant body, which may inhibit bone formation. Bone resorption resulting from infection may require implant removal. The same degree of ILO, without simultaneous implant placement, could possibly be managed and compensated for by bone expansion, use of slightly narrower implants, increased number of implants, and/or additional augmentation.

Classification and Types of Wound Healing

Wound healing is an intricate process in which the body’s tissue repairs itself after injury (surgical wound). Despite having similar healing mechanisms, it is generally observed that wounds in the oral mucosa heal faster and with less scarring than extraoral wounds.⁶

Phases of Wound Healing

Surgical wound healing, whether by normal or delayed healing, will occur in three phases. Wound healing is not a linear process; rather it progresses differently depending on many patient-related factors. The three phases of wound healing are (1) inflammatory phase, (2) proliferation phase, and (3) maturation phase.

Inflammatory Phase.

The inflammatory phase is the body’s natural response to a surgical injury. It is characterized by a vascular and inflammatory response including local vasoconstriction for the first 5 to 10 minutes followed by a local vasodilatory response. This phase takes place the first few days after injury.

Within the first few minutes after injury, platelets adhere to the site, become activated, and aggregate. These events are followed by activation of the coagulation cascade, which forms a clot of aggregated platelets in a mesh of cross-linked fibrin protein. The blood vessels in the wound bed contract, forming a clot, which promotes hemostasis. The clot formed has two functions: it temporarily protects the denuded tissues and serves as a provisional matrix for cell migration.

The blood clot consists of cellular components of blood (including red and white blood cells and platelets) in a matrix of fibrin, plasma fibronectin, vitronectin, and thrombosporin.⁷ Once hemostasis is achieved, dilation of the blood vessels will result, allowing white blood cells, growth factors, antibodies, enzymes, and nutrients to invade the surgical wound. At this stage the characteristic signs of inflammation may be seen: erythema, heat, edema, pain, and functional disturbances. At the cellular level, neutrophils and macrophages will initiate a host response, which will lyse and devitalize the necrotic tissue. The strength of the wound relies mainly on the integrity of the fibrin clot. Bacteria and cell debris are phagocytized and removed from the wound by white blood cells.⁸

Proliferation Phase.

The proliferation phase is characteristic with the formation of new granulation tissue, which is mainly comprised of collagen and extracellular matrix. The proliferation phase begins within 24 hours after injury and may last 3 to 12 days. It is characterized by angiogenesis, collagen deposition, granulation tissue formation, epithelialization, and wound contraction. Epithelialization may be completed in 24 to 48 hours in primary closed wounds or delayed for 3 to 5 days in wounds healing by secondary intention. In angiogenesis, vascular endothelial cells form new blood vessels. In fibroplasia and granulation tissue formation, fibroblasts grow and form a new, provisional extracellular matrix (ECM) by excreting collagen and fibronectin. Concurrently, reepithelialization of the epidermis occurs, in which epithelial cells proliferate and migrate over the wound bed, providing cover for the new tissue.

For healthy granulation tissue to form fibroblasts, there must be adequate levels of oxygen and nutrients available, which are supplied by the blood vessels. Characteristics of healthy granulation tissue include a granular and uneven surface that is pink and does not bleed easily. Epithelial cells will begin to resurface on the surgical wound, which is termed epithelialization.

Maturation Phase.

Maturation phase is the final phase in the healing process and occurs when the wound has closed. The remodeling of collagen from type III to type I will occur. During wound contraction, myofibroblasts decrease the size of the wound by gripping the wound edges and contracting, using mechanisms that resemble smooth muscle cell contraction. The wound scar gains strength and volume, and erythema decreases. Complete scar maturation and final tensile strength generally take 12 to 18 months. When the cells’ roles are close to complete (no longer needed), they are removed by apoptosis.⁹ During maturation and remodeling, collagen is remodeled and realigned along tension lines. There will also be a reduction in the cellular activity as well as the number of blood vessels (Fig. 11.4).^10,11

Knowledge of the healing rates of the soft and hard tissues is useful to determine if a patient is healing on schedule. The time for wound repair subsequent to surgery is tissue specific:

Epithelium: heals at a rate of 0.5 to 1 mm per day (after a 12-hour lag time)

Connective tissue: heals 0.5 mm per day

Bone: heals at a rate of 50 µm per day, 1.5 mm per month

Mucoperiosteal flap: adheres to bone (or soft tissue flap) by a fibrin clot (0 to 24 hours).¹²

Types of Wound Healing

With respect to wound healing, there exist three types: (1) primary intention, (2) secondary intention, and (3) tertiary intention.

Primary Intention.

With few exceptions, surgical procedures for dental implantology involve surgical flaps, which ideally result in healing by primary intention. Healing by primary intention results when the wound edges are approximated and stabilized by sutures. Soft tissue flaps are usually maintained in positions that are “passive” and tension free. A common complication resulting in incision line opening is for the clinician to utilize sutures to actively reposition mucoperiosteal flaps. This may result in excessive tension placed on the flaps and may lead to ischemia and flap necrosis, which will usually result in incision line opening.

Achieving the goal of primary intention for closure will allow for hemostasis, less potential for infection and bone necrosis, along with improved patient comfort. When ILO occurs, the only way for the wound to heal is via secondary intention, which may lead to increased morbidity.

Wound healing is a complex and intricate process where the skin or tissues repair after injury. In the case of normal skin, the epidermis and dermis exist in a steady-state of equilibrium, forming a protective barrier against the external environment. Once the protective barrier is broken, the physiologic process of wound healing is immediately set in motion. The general principles of healing and the cellular and molecular events observed in extraoral sites also apply to healing processes that take place following oral surgical procedures.¹³

Secondary Intention.

When wounds dehisce or ILO has occurred, the wound undergoes healing by secondary intention. Secondary intention is healing by the body’s natural mechanisms, without surgical intervention. This typically occurs in large wounds with traumatic tissue loss or avulsion, so that wound edges are widely separated and cannot be apposed. Healing occurs by clot formation, granulation, deposition of collagen, and eventual epithelialization. Wound contracture brings the wound margins together (Fig. 11.5).

Tertiary Intention.

A third type of healing has been described as tertiary intention. Tertiary intention healing occurs when primary closure is delayed, allowing the wound to granulate for a short period of time. The wound is then reapproximated manually or by another technique. This method has been termed delayed primary closure and can be used to debride an infected, acute wound prior to closure.¹⁴ This type of healing is uncommon with respect to dental implants and bone grafts.

Treatment Implications

Saliva is advantageous for wound healing. Patients who exhibit xerostomia or salivary gland disorders are predisposed to wound healing complications. Salivary substitutes and more frequent recall examinations are warranted.

Bacteria

The oral cavity harbors larger numbers of bacteria, with over 500 bacterial species having been identified in the oral cavity. It is clear that bacteria affect wound healing in the oral cavity, and it is well established that wounds colonized by pathogenic bacteria have delayed healing.¹⁹ Clinicians are aware of painful complications in extraction wound repair that result from bacterial infection.

It is well recognized that small concentrations of bacteria may increase rates of wound healing. In 1921, Carrel reported that wounds of dogs treated with selected concentrations of Staphylococcus aureus healed faster than untreated wounds. Several studies have confirmed the observation using other bacterial species. Larjava found that proliferation of gingival fibroblasts in culture was increased by Prevotella intermedius but decreased with similar concentrations of Porphyromonas gingivalis.²⁰ Interestingly, there was great variation in this effect between fibroblast populations obtained from different patients. These findings imply that the potential for periodontal repair depends both on bacterial flora and the individual cell populations of periodontal wounds.

Systemic Diseases

Systemic diseases are a vital component of treatment planning and implant therapy. Specific systemic diseases and conditions affect wound healing and bone metabolism, either of which can have a direct impact on the success of implant therapy. Diabetes mellitus is a major endocrine disorder commonly reported by approximately 10% patients. With diabetes-associated insulin deficiency or metabolism defects, glucose remains in the bloodstream and increases blood glucose levels. Diabetic patients are at risk to develop infections and vascular complications. The healing process is affected by impaired vascular function, impaired cell chemotaxis, and impaired neutrophil function. Protein metabolism is decreased, and healing of soft and hard tissue is delayed. Nerve regeneration is altered, and angiogenesis is impaired.

Many non–life-threatening diseases and conditions require medications for definitive management or control of potential wound healing complications. Common examples include anticoagulants, immunosuppressants, and bisphosphonates. Bleeding problems encountered when incising and reflecting tissue for passive closure may be complicated by anticoagulants.

However, given the potential life-threatening complications of discontinuing anticoagulants such as warfarin, this is usually not recommended as long as the therapeutic drug levels are within normal limits. However, special attention must be devoted to good surgical technique and use of appropriate local hemostatic measures to control bleeding.

Two classes of immunosuppressants frequently prescribed for patients are glucocorticoids (e.g., prednisone) and cytostatics (chemotherapeutic agents). The negative impact of these medications on wound healing can be mitigated by appropriate patient selection, timing of treatment, and medical consultation.

Bisphosphonates can also lead to wound dehiscence following surgery. These drugs act by suppressing and reducing bone resorption by osteoclasts and are used to treat bone disorders including osteoporosis, metastatic bone cancer, and Paget disease (JBS figures on bone metabolism). After surgery involving the jaws, bone exposure may develop rather than the normal soft tissue closure healing mechanisms.²¹ This is common with more potent nitrogen-containing intravenous bisphosphonates, and the prevalence is lower with oral bisphosphonates.²² However, the clinician must be able to differentiate bone exposure of this bisphosphonate origin and insufficient flap closure or postextraction bony spicule formation.

In the United States, approximately 45 million adults and 21% of the population smokes cigarettes. Approximately 23% of men and 19% of women smoke cigarettes. Tobacco use has been implicated in many adverse systemic outcomes, including tooth loss and dental implant failure.²³ In fact, the entire stomatognathic system suffers from the effect of tobacco byproducts.

Tobacco smoke decreases polymorphonuclear leukocyte activity, resulting in lower motility, a lower rate of chemotactic migration, and reduced phagocytic activity. These conditions contribute to a decreased resistance to inflammation, infection, and impaired wound healing potential.²⁴

Smoking is also associated with decreased calcium absorption. Additional findings demonstrate a reduced mineral content in the bone of aging smokers and, to a greater degree, in postmenopausal female smokers. The association of tobacco with intraoral carcinoma is well recognized.

When incision line opening after surgery occurs, smoking delays secondary wound healing, may contaminate bone grafts, and contributes to early bone loss during healing. Treatment planning for any type of dental implant surgery should emphasize the need for smoking cessation protocols.

Periodontal Biotype

Although some studies report minimal long-term effects of tissue biotype on bone grafting and implant success, thicker biotypes may prevent tissue breakdown or tears during suturing. Tissue augmentation should be considered for patients with preexisting thin tissue biotypes. With thick biotype tissue, there exists more keratinized tissue, which results in better healing, easier suturing, and less likelihood of wound breakdown.

Postoperative Issues

Despite meticulous surgery, deliberate or accidental behavior patterns by patients may contribute to incision line opening. Failure to modify the diet to a soft consistency or attempted visualization of surgical sites may traumatize or place increased tension on the incision, resulting in incision line dehiscence. It is also paramount that the clinician modify any transitional prosthesis that may come in close approximation with an incision line, while also advising the patient on the proper use of these prostheses, which may include cessation early in the healing process. Poor decision making with these postoperative issues increases the risk of incision line trauma and breakdown.

Incision in Keratinized Tissue

The primary incision should ideally be located be in keratinized tissue whenever possible. This permits increased wound surface area and a resultant increase in vascularity to the incision. Not only does this reduce the initial intraoral bleeding, it also severs smaller blood vessels and reduces postoperative edema, which may add tension to the incision line. If there is 3 mm or more of attached gingiva on the crest of the edentulous ridge, the incision bisects this tissue. This places half of the attached gingiva width on each side of the incision. If there is less than 3 mm of attached keratinized tissue on the crest, the incision is made more lingually so that at least 1.5 mm of the attached tissue is placed to the facial aspect of the implant. This concept is very important in the posterior mandible because attached tissue is needed to prevent tension and pulling from the buccinator muscle (Fig. 11.6).²⁹

Broad-Based Incision Design

The apex or tip of the flap should never be wider than the base (e.g., converge from base to the apex). This will maintain adequate vasculature that will prevent ischemic necrosis to the flap, decreasing the possibility of incision line opening. The length of the flap should generally not exceed twice the width of the base. Additionally, the base of the flap should not have significant pressure or be excessively stretched or twisted, which may compromise the blood supply (Fig. 11.7).³⁰

Allow for Adequate Access

The flap should be large enough to provide adequate visualization of the surgical site and allow for the insertion of instruments to perform the surgical procedure. If the flap is too small, a retractor will not be able to maintain the flap without excessive pressure. Excessive retraction pressure will lead to increased inflammation, which may compromise the healing of the incision line (Fig. 11.8).

Vertical Release Incision to Maintain Blood Supply and Decrease Tension on Flap

The blood supply to the reflected flap should be maintained whenever possible. The primary blood supply to the facial flap, which is most often the flap reflected for an implant or bone graft, is from the unkeratinized mobile mucosa. This is especially true where muscles of facial expression or functional muscles attach to the periosteum. Therefore, vertical release incisions are made to the height of the mucogingival junction, and the facial flap is reflected only 5 mm above the height of the mucogingival junction. Both of these incision approaches maintain more blood supply to the facial flap. In addition, incisions and reflection in the mobile alveolar mucosa increase flap retraction during initial healing, which may contribute to incision line opening and may increase risk of scar formation and delayed healing of the incision line as a consequence of reduced blood supply.

Vertical release incisions should not be made over bony prominences (e.g., canine eminence) because this will increase tension on the incision line and may increase the possibility of incision line opening (Fig. 11.9).

Maintain Flap Margins Over Bone

The soft tissue flap design should also have the margins of the wound over host bone whenever possible. This is especially important when approximating tissue over bone grafts or barrier membranes. The host bone provides growth factors to the margins and allows the periosteum to regenerate faster to the site. The margins distal to the elevated flap should have minimal reflection. The palatal flap and the facial tissues distal to the reflected flap should not be elevated from the palatal bone (unless augmentation is required) because the blood supply to the incision line will be delayed. In addition, the unreflected flap does not retract during initial healing, which could place additional tension on the incision line. The soft tissue reflection distal to the graft site may be split thickness to maintain periosteum on the bone around the incision line. This improves the early vascularization to the incision line and adhesion of the margins to reduce retraction during initial healing (Fig. 11.10).

Clean, Concise Incision

A clean incision is made through the tissue in one direction with even pressure of the scalpel. A sharp blade of proper size (i.e., #15 blade) should be used to be make clean, concise incisions without traumatizing the tissue from repeated passes or strokes. Tentative strokes, especially in different planes, will increase the amount of damaged tissue and increase the amount of bleeding. Long, continuous strokes are preferable to shorter, inconsistent, and interrupted strokes.³¹

Sharp dissection will minimize trauma to the incision line, which will result in easier closure. Ideally, the incision should always be over bone. Care should be noted of vital underlying nerves, blood vessels, and associated muscles. Scalpel blades dull rather easily, especially when used on bone and tissue with greater resistance. The clinician should change blades when dulling is suspected to decrease tissue trauma.

The incision should be made with the blade held perpendicular to the epithelial surface. This will result in an angle that produces square wound margins that are easier to reorient during suturing and less likely for surgical wound necrosis to occur (Fig. 11.11).

Full Thickness Reflection and Ideal Flap Elevation

Ideally, the flap should be full thickness and include the surface mucosa, submucosa, and the periosteum. The periosteum is necessary for healing; the replacement of the periosteum in its original position will increase healing.

Tissue elevation should be completed with extreme care. To minimize trauma to the soft tissue, meticulous handling is required. Proper use of appropriate tissue forceps, avoidance of excessive suctioning by the assistant, and “tieback” sutures all contribute to improved flap management. Nonlocking tissue pick-ups, also called “thumb forceps,” are commonly held between the thumb and two or three fingers of one hand. Spring tension at one end holds the grasping ends apart until pressure is applied. These forceps are used to hold tissues in place when applying sutures and to gently retract tissues during exploratory surgery. Dressings or draping flaps may be relocated without using hands or fingers. Tissue forceps can have smooth tips, cross-hatched tips, or serrated tips (often called “mouse’s teeth”). Serrated forceps used on tissues will cause less tissue damage than smooth surface forceps because the surgeon can grasp with less overall pressure. Smooth or cross-hatched forceps are used to move dressings, remove sutures, and perform similar tasks.

During flap elevation, elevators should rest on bone and not on soft tissue. Care should be exercised to not continuously suction the tissue because this may irritate and traumatize the tissue margins. Use of variable-suction tips with fingertip control can help minimize tissue damage. After flap replacement, it is advantageous to apply pressure to the tissue for several minutes to minimize blood clot thickness and to ensure bleeding has stopped (Fig. 11.12).

Minimizing surgical operating time will directly benefit soft tissues and will reduce the risk of infection.³² The tissue retractors should be selected and placed in a position to prevent undue pressure on tissues. Maintaining the retractors on bone and not on the tissue will minimize trauma to the tissue. Excessive pressure and tension on the tissue flap will impair blood circulation alter the physiologic healing of the surgical wound and predisposes the wound to bacterial colonization.

Papilla-Saving Incisions

The interproximal soft tissue in sites next to adjacent natural teeth may be classified into three categories: (1) papillae have an acceptable height in the edentulous site, (2) papillae have less than acceptable height, or (3) one papilla is acceptable and the other papilla is depressed and requires elevation. When the interproximal papilla has an acceptable height, “papilla-saving” incisions are made adjacent to each neighboring tooth. The vertical incisions are made on the facial aspect of the edentulous site and begin 1 mm below the mucogingival junction, within the keratinized tissue. Extending the vertical incisions beyond the mucogingival junction increases the risk of scar formation at the incision site. The full-thickness incision then approaches the crest of the edentulous site, leaving 1.0 to 1.5 mm of the interproximal papilla adjacent to each tooth. The vertical incisions are not wider at the base than the crestal width of tissue. This permits the facial flap to be advanced over the implant or short and adjacent to a permucosal extension (PME) at the conclusion of the procedure, with no voids at the incision line and primary closure (Fig. 11.13).