Actinomyces species are members of normal oral flora that may give rise to a rare disease—oral actinomycosis. Presented herein is a case of early implant failure associated with actinomycosis in an otherwise healthy 43-year-old female and the treatment adopted after explantation. Clinically, 1 month after the implant placement, the peri-implant soft tissues were hyperplastic and associated with an excessive tissue reaction, bleeding, suppuration, deep probing depth, and implant mobility of #19 and #20 implants. Both implants were removed and all granulomatous tissues were thoroughly debrided. Histopathological examination revealed signs of acute ulcerative inflammatory reaction and Actinomyces colonies. The patient was prescribed short-term oral penicillins. Six months after explantation, the deficient bone was augmented using a combination of absorbable collagen membrane, autogenous block bone, and xenograft. The patient was followed for 1 year; and subsequently, 2 implants were re-inserted at the same positions. The patient was followed and no recurrences were observed. Implant failure due to actinomycosis is an extremely rare condition, and a definitive diagnosis is therefore essential for successful treatment.
Introduction
Actinomycosis is a rare bacterial infection caused by Actinomyces species that are filamentous, gram-positive, anaerobic bacteria. They are members of the resident oral, digestive, and urogenital flora in humans.1 The bacteria do not cause any disease while the integrity of the mucosal barrier is intact; however, they can become pathogenic with mucosal breakdown; and then directly invade the tissues.2 Tooth extraction, gingivitis, periodontal diseases, caries, trauma, local tissue damage by surgery, diabetes mellitus, malnutrition, and immunocompromised status are important risk factors for oral and cervicofacial actinomycosis.3 Contamination during implant placement also has been reported as a cause for oral actinomycosis.4
Primary signs and symptoms of actinomycotic lesions are nonspecific, such as swelling, erythema, ulceration, pain, bone expansion, suppuration, and sinus tracts.5 The presence of sulfur granules is suggestive, but not pathognomonic for the disease.6 Lymphadenopathy is rare, and radiographic findings are nonspecific, often indicating a chronic inflammatory condition.6 Histological examination is recommended for the definitive diagnosis of actinomycosis.7 Preferred management includes prolonged administration of antibiotics and surgical debridement.8 Penicillins are the antibiotics of choice,9 and surgical intervention is clearly indicated in patients who are nonresponsive to antibiotics or show diffuse tissue necrosis and sinus tracts.10
Dental implant failures can be categorized as early, when they occur prior to osseointegration, or late, when the achieved osseointegration is impaired.11 Early implant failure is induced by the inability to establish an intimate bone-to-implant contact.12 Biological infection, swelling, pain, bone loss, and implant mobility are clinical signs of early implant failure.13 Actinomyces species have been found on the surface of failed orthodontic mini implants14 and failed dental implants.15 Moreover, presence of actinomycosis was determined in 29.9%16 and 3.6%17 of cases in the histopathological analysis of peri-implant soft tissue biopsies of failed implants in 2 different studies. In a study by Sotorra-Figuerola et al, 4 cases with actinomycosis were reported, all in the maxilla, and three-quarters of their patients were female.17 A published case by Sun et al4 reported a failed implant associated with actinomycosis about 2 years after placement, in a medically compromised male patient. Severe bone loss was cited as the cause of explantation. The patient was followed up for 1 year and a normal healing without recurrences was reported. Information regarding the relationship between actinomycosis and implant failure is still limited. Moreover, treatment strategies for the defects caused by actinomycosis have not been reported. We present a case of early implant failure due to actinomycosis in an otherwise healthy patient. The treatment procedure adopted after explantation is also described.
Case Presentation
A 43-year-old female patient presented to Department of Periodontology for dental implant treatment in September 2017. The patient did not report any medical comorbidity, was not receiving any medication, and was a nonsmoker. History of the patient revealed that tooth #19 and #20 (universal tooth numbering system by the American Dental Association) were extracted about 25 years ago because of deep carious lesions and associated unsuccessful endodontic treatments. On clinical examination, relatively shallow vestibular sulcus, sufficient alveolar ridge width and adequate distance between tooth #18 and #21 were observed (Figure 1a and b). Then, it was decided to perform the placement of implant in tooth positions of 19, 20, and 28. Written informed consent was obtained. Prior to implant placement, the bone condition was evaluated using cone-beam computed tomography (CBCT) and no pathologic lesions were detected. In the region of tooth position #20, a radiopacity was found to be compatible with osteosclerosis due to its asymptomatic nature. At both sites, the distance between the crest of the alveolar ridge and mandibular canal was approximately 14 mm and the average width at the alveolar crest was 7 mm (Figure 1c, d and e).
Buccal (a) and occlusal (b) preoperative views of the edentulous left lower posterior region immediately after the local anesthesia. Preoperative panoramic radiography (c), and preoperative axial images of #20 (d) and #19 (e) regions.
Buccal (a) and occlusal (b) preoperative views of the edentulous left lower posterior region immediately after the local anesthesia. Preoperative panoramic radiography (c), and preoperative axial images of #20 (d) and #19 (e) regions.
In November 2017, tooth #28 was atraumatically extracted and a dental implant (Straumann Bone Level, Ø 4.1 × 12 mm) was placed into the fresh extraction socket with immediate implantation approach. Preoperatively, the patient performed an oral rinse with 0.12% chlorhexidine gluconate mouthwash for 60 seconds. Additional grafting procedure was not performed because the bone gap was smaller than 2 mm and the buccal bone plate was intact and thicker than 2 mm. The patient was prescribed 500 mg amoxicillin and ibuprofen 600 mg 3 times daily, and chlorhexidine gluconate mouthwash twice daily for 7 days, postoperatively, with standard postoperative instructions. One week later, all sutures were removed and the healing was uneventful. Two weeks after implant placement at tooth #28, implantation procedure was continued on the contralateral site. Prior to the surgery, the same preoperative protocols were followed, and 2 titanium implants (Straumann Bone Level, 4.8 × 10 mm and 4.1 × 10 mm) were placed with insertion torque 40 N/cm in the teeth regions of 19 and 20 with 1-stage approach (Figure 2). The same medical treatment and postoperative instructions as the first time were advised. All sutures were removed after 1 week and healing was uneventful. However, 1 month after implant placement, the gingival tissues around the healing caps became erythematous, soft, and hyperplastic; and an excessive tissue reaction and growth was observed in the peri-implant mucosa, especially pertaining to the implant at tooth position #19 (Figure 3a through d). Bleeding, suppuration, deep probing depth, and implant mobility were present at both implant sites. After evaluation, it was decided to remove the implants. They were easily removed with forceps (Figure 3e and f). All granulomatous tissues were thoroughly debrided, a large bony defect wider than the osteotomy site was noticed after debridement (Figure 3e and f), and a piece of sequestered bone was removed (Figure 3g). The residual healthy tissues were sutured as primarily as possible (Figure 3h). The harvested inflamed tissue samples were sent for histopathological examination that revealed an ulcerative acute inflammatory reaction with formation of granulation tissue and accompanying Actinomyces colonies (Figure 4). For treatment of the lesions, amoxicillin-clavulanic acid 1g twice a day and chlorhexidine gluconate mouthwash were prescribed for 7 days. Ten days after explantation, all sutures were removed and signs of soft tissue inflammation completely resolved in the following weeks (Figure 5).
Buccal view after implant insertion (a) and postoperative panoramic radiographic view (b).
Buccal view after implant insertion (a) and postoperative panoramic radiographic view (b).
(a, b) Erythematous, soft, and hyperplastic gingival tissues around the healing caps; (c, d) Excessive tissue reaction and growth in the mucosa immediately after explantation; (e, f) large bone defect after implant explantation, (g) granulation tissues and a piece of sequestered bone, (h) clinical view after suturation.
(a, b) Erythematous, soft, and hyperplastic gingival tissues around the healing caps; (c, d) Excessive tissue reaction and growth in the mucosa immediately after explantation; (e, f) large bone defect after implant explantation, (g) granulation tissues and a piece of sequestered bone, (h) clinical view after suturation.
Figure 4. (a) Ulcerative mucosal lesion characterized with acute inflammation and granulation tissue (H&E, x100) (b) purple colored, radial filaments of bacteria representing Actinomyces colonies with accompanying neutrophils at the base of the ulcer (H&E, ×400).
Figure 5. Buccal (a) and occlusal (b) views of early healing period after implant explantation
Figure 4. (a) Ulcerative mucosal lesion characterized with acute inflammation and granulation tissue (H&E, x100) (b) purple colored, radial filaments of bacteria representing Actinomyces colonies with accompanying neutrophils at the base of the ulcer (H&E, ×400).
Figure 5. Buccal (a) and occlusal (b) views of early healing period after implant explantation
The patient was seen at 1, 3, and 6 months after explantation. The tissue healing was unremarkable without any recurrences. Using CBCT, the left lower posterior region was evaluated and the height of residual bone was found to be insufficient for a prosthetically driven implant replacement (Figure 6). Based on the study of Plonka et al, it was decided to augment this deficiency using a mandibular corpus autogenous block graft harvested from the apical region of the relevant site.18 After standardized preparation and local anesthesia, a sulcular incision around tooth #18, #21, and #22 was made, and a crestal incision was performed on the edentulous ridge. Full-thickness mucoperiosteal flap was elevated to access the donor site with an apical split-thickness dissection to achieve a sufficient passive soft tissue closure. Decortication at the recipient site was performed with a round bur to allow for revascularization of the graft. An autogenous block graft with a width, length, and height of 7, 15, and 6 mm, respectively was harvested from the left mandibular corpus using piezoelectric equipment (NSK, Variosurg, Kanuma, Japan). The graft was adapted and fixated to the top of the ridge with 2 mini-screws (1, 2 mm × 12 mm, Trimed, Ankara, Turkey). Any residual spaces were filled with a bovine bone xenograft (Cerabone, Botiss dental GmbH, Germany), and an absorbable collagen membrane (T-barrier membrane, B&B Dental, Italy) was placed over the augmented site. The flap was primarily closed with 4-0 polypropylene (Prolene; Ethicon Inc, Somerville, NJ) sutures (Figure 7). The same pharmacologic regimen and postoperative instructions were advised for the patient as in the previous operations. Ten days postoperatively, the patient was examined and all sutures were removed. The healing was found to be satisfactory.
Six months after implant explantation (a, b) the view of gingival tissues, (c) panoramic radiography and axial images of #20 (d) and #19 (e).
Six months after implant explantation (a, b) the view of gingival tissues, (c) panoramic radiography and axial images of #20 (d) and #19 (e).
Autogenous bone augmentation procedure: (a, b) intraoperative views; (c) view of the adapted autogenous bone graft, bovine bone xenograft graft, and absorbable collagen membrane on the augmented site; (d) primary flap closure. (e, f) Clinical views of early healing after bone augmentation.
Autogenous bone augmentation procedure: (a, b) intraoperative views; (c) view of the adapted autogenous bone graft, bovine bone xenograft graft, and absorbable collagen membrane on the augmented site; (d) primary flap closure. (e, f) Clinical views of early healing after bone augmentation.
The patient was seen at 1, 3, 6, and 12 months after bone augmentation. On intraoral examination, soft tissues were healthy without any signs of inflammation. A slight increase in the keratinized tissue was achieved after bone augmentation because the flap was replaced more coronally to achieve a complete wound closure. Although, the width of the keratinized tissue decreased after implant loss and the ongoing surgical procedures, it was still adequate for achieving stable peri-implant tissues. The successful incorporation of the block graft to the host bone was confirmed and a sufficient increase in the height of the alveolar ridge (around 4 mm) was observed on radiographic examination (Figure 8).
(a) Healthy gingival tissues and no recurrence signs 1 year after augmentation. Panoramic radiograph (b), axial images of #20 (c), and #19 (d) 1 year after augmentation. The view of block graft integration (e, f), intraoperative view after re-entry for re-implant placement.
(a) Healthy gingival tissues and no recurrence signs 1 year after augmentation. Panoramic radiograph (b), axial images of #20 (c), and #19 (d) 1 year after augmentation. The view of block graft integration (e, f), intraoperative view after re-entry for re-implant placement.
One year after bone augmentation, two implants were inserted into teeth positions 19 and 20 (Straumann Tissue Level, 4.1 × 10 mm) with 1-stage approach. Before implant placement, one of the mini-screws could not be removed since its neck was fractured. As it was completely osseointegrated, noninfected, and did not violate the implant insertion procedure, it was left inside the bone. Postimplantation, healing was uneventful and a recurrence of infection was not noticed (Figure 9a and b). The prosthetic treatment was completed with screw-retained porcelain crowns (Figure 9c and d) and at this stage, successful hard tissue integration and prosthetic harmony were observed in radiographic evaluation (Figure 9e and f). In the final follow-up visit, 13 months after prosthetic loading, no recurrence was observed and the patient was satisfied with the function of the restoration (Figure 10). The complete treatment procedure has been summarized in Figure 11.
(a, b) Healthy peri-implant tissues 4 months after second implantation, (c, d) clinical view of prosthetic restoration, and peri-implant tissues 8 months after second implantation. Radiographic view around the implant 4 months (e) and 8 months (f) after second implantation.
(a, b) Healthy peri-implant tissues 4 months after second implantation, (c, d) clinical view of prosthetic restoration, and peri-implant tissues 8 months after second implantation. Radiographic view around the implant 4 months (e) and 8 months (f) after second implantation.
13-month follow-up postloading of dental implants, (a, b) clinical view of prosthetic restoration, and peri-implant tissues, (c) panoramic radiography.
13-month follow-up postloading of dental implants, (a, b) clinical view of prosthetic restoration, and peri-implant tissues, (c) panoramic radiography.
Discussion
Oral actinomycosis is a rare disease caused by Actinomyces species that are a part of the normal oral flora and may reside in calculus, periodontal pockets, caries, and oral mucosal surfaces.2 Actinomyces species also have been found around failed dental implants; however, their role in peri-implant pathology is still unclear. Inflammation of peri-implant soft tissues may lead to their invasion into the surrounding alveolar bone or may trigger chronic inflammation-related bone and implant loss.2
In the literature, tooth caries, invasive dental or maxillofacial procedures, trauma, and osteonecrosis have been identified as the most common causes for oral and cervicofacial actinomycosis.6 Racial or geographic predisposition have not been reported.19 From the information presented in this case, it is logical to discuss 3 reasons as possible cause(s) of peri-implant Actinomyces infection. First, the patient reported that teeth #19 and #20 were extracted because of deep carious lesions, and that tooth #19 underwent a root canal treatment. Thus, it may be considered that these teeth may have been infected with Actinomyces before the extraction with the possible mechanism based on the breakdown of mucosal barrier allowing the deeper bacterial colonization.2 However, in the presented patient, presence of co-infection with other bacteria might have led to such an abrupt treatment response. This first explanation seems unlikely due to years passed since the extractions and history of using antibiotic and preoperative mouthwash. Secondly, the implants may have been contaminated with the oral flora during their placement. In this scenario, the bacteria may have found a way to invade the bone from the osteotomy site and infection could have developed within a short time after the implant placement. Surgical trauma is the third possible reason. Belmont et al have reported Actinomyces infection in the cervicofacial region due to oromaxillofacial trauma.20 It has also been suggested that surgical trauma and irritation caused by dental implants may trigger actinomycosis.17 When the bone is dense, the drilling procedures and implant insertion may increase risk of surgical trauma.11 In the present case, all implants were placed with an insertion torque of 40 N/cm and since this is more likely in the lower jaw, care was taken to avoid additional stress during implant insertion. On the other hand, use of wider-diameter implants mostly surrounded with cortical bone may have increased the risk of surgical trauma.21 Therefore, a 4.8-mm diameter implant placed in contact with buccal and cortical bony walls in tooth location #19 during the first surgery might be a triggering factor inducing the risk of trauma-associated actinomycosis. In addition, the uneventful vertical bone augmentation procedure resulted in sufficient bone formation and the uneventful second implantation process used with narrower (4.1 mm) implants may also support the third explantation.
Our patient was otherwise healthy and not receiving any medications (antidepressants, proton pump inhibitors, anticoagulants, etc.), thus eliminating the possibility of an immunocompromised status. Actinomycosis developing soon after surgery in our immunocompetent patient is unusual and noteworthy.
Actinomyces spp. are sensitive to penicillins and beta-lactam antibiotics, and resistant to metronidazole, quinolones, aminoglycosides, and co-trimoxazole. Actinomyces spp. can form a biofilm that hinders effectiveness of antimicrobial treatment and necessitates debridement.3 Additionally, lack of blood supply results in poor antibiotic penetration to the infected tissues, and warrants prolonged high-dose antibiotic administration.3,8 Penicillin G is considered the gold standard treatment for actinomycosis,3 and requires hospital admission for its parenteral administration with prolonged hospital stays. Pharmacological developments have failed to meet clinical needs for new antibiotics,22 even as antibiotic resistance continues to be a major global health problem. Rational antibiotic use requires patients to receive them, appropriate to their clinical needs, in doses that meet their requirements, for an adequate period of time, and at the lowest cost.23 To decrease duration of hospital admission, switching early to oral medications has been tried and proven to be effective.10 A previous report from our center also favored oral antibiotic treatment.24 We successfully treated Actinomyces-associated gingival lesions with oral antibiotics that were discontinued at an early stage without any complications. Further, explantation and debridement, to eliminate the causative factor, were performed readily and this may have led to favorable outcomes.
Conclusion
In our patient, a definitive reason for actinomycosis could not be found; however, possible reasons were discussed. Within these limitations, the present case report shows early implant failure due to actinomycosis in an immunocompetent patient. Although this report provides limited knowledge, it may be useful to clinicians for diagnosis and treatment planning in such cases. Moreover, it may encourage clinicians to not avoid bone augmentation and implant reinsertion in such cases; however, further evidence is needed in this regard.
Notes
The authors reported no conflicts of interest related to this study.
Based on the Turkish Medicines and Medical Devices Agency, Health Ministry of Republic of Turkey and Hacettepe University Non-Interventional Clinical Research Ethics Committee, this case report did not require an ethical approval nor was there need to conduct a special ethical review. An appropriate written informed consent and permission were taken from the patient for publication of this case report, including case details and patient's images. The consent form included the permission to use the patient's personal information, details, processes, and possible complications regarding treatment options and the rights of the patient for suspending or refusing treatment.