Keywords
sequestration - osteomyelitis - maxillary - comprehensive - management - diabetes
mellitus
Introduction
Osteomyelitis comes from the ancient Greek words osteon (bone) and muelinos (marrow) and describes a bone tissue infection that includes the marrow or bone cortex
caused by polymicrobial infection.[1] Osteomyelitis also results in inflammatory conditions of the bones involving the
Haversian canals and widespread into the periosteum.[2] Most cases of osteomyelitis occur in the fifth and sixth decade of age. In general,
patients come already in an advanced stage and are accompanied by uncontrolled comorbidities,[3] like diabetes mellitus. Diabetes mellitus probably cause recurrent osteomyelitis.[4]
Clinically, the osteomyelitis resemblance to bisphosphonate-related osteonecrosis
of the jaw. But this condition, it can be distinguished from anamnesis in patients
with no history of bisphosphonate consumption and no history of radiation therapy
in the jaw area.[5]
[6]
The case of maxillary osteomyelitis was rare,[3]
[7]
[8]
[9] and some of the reports were accompanied by actinomycosis,[10]
[11]
[12] and mucormycosis,[13]
[14]
[15]
[16]
[17] but one study reported a higher prevalence than mandibular.[8] The incident rate in mandibular is around 66.7%,[18] but the maxilla is only 33.3%.[8] The maxilla is a jaw bone with good vascularity and thin cortical bones and makes
not susceptible to infection.[19]
[20] For this reason, the prevalence of maxillary osteomyelitis is low. Many cases of
osteomyelitis were obtained in the mandibles mainly due to odontogenic infections
exacerbated by immunocompromise and uncontrolled metabolic diseases such as diabetes
mellitus, acquired immunodeficiency syndrome, and malnutrition.[8]
[21] The maxillary osteomyelitis in diabetes mellitus patients also rarely reported.[4]
[22]
[23] Diabetes mellitus become a risk factor for the severity of osteomyelitis,[24] and secondary infection.[25] In India, the prevalence rate of maxillary osteomyelitis with diabetes mellitus
is 45.1%.[26] This case report aims to present maxillary osteomyelitis with diabetes mellitus
and discuss aspects of diagnosis enforcement and comprehensive management.
Case Presentation
Chief Complaint
A 58-year-old male patient came to Oral Surgery Department, at Mohammad Soewandhie
Hospital with complaints of pain in the upper left cheeks and gums after tooth extraction
of the upper jaw in January 2021. After extraction, he complained of pain and swelling
accompanied by pus discharge in the extraction area. The patient still feels pain
and pus often comes out from the exposed bone. The patient had medical history of
uncontrolled diabetes mellitus since 2010 and got treated with glimepiride, metformin,
and acarbose drugs. There was no history of chemotherapy or radiotherapy treatment
and no consumption of bisphosphonate drugs.
Extraoral and Intraoral Examination
Extraoral examination in the maxillofacial region showed facial asymmetry and the
swelling on maxillary sinistra. On palpation, there was palpable asymmetry, concavity
was felt on the left maxilla, and there was no maxillary bone and paresthesia in the
infraorbital area ([Fig. 1A]).
Fig. 1 The extraoral examination revealed an asymmetrical area of the sinistra of the maxilla
(A). The palate durum was pressed toward medial (B). The bone exposed in the buccal palate on regions 23 to 28 and 14 to 15 (C).
Intraoral examination revealed bone exposed buccal-palate region of 23 to 28 and 14
to 15. Palatum durum on the sinistra was pressed toward the medial and soft consistency.
The region of 27 was observed as gangrene radixes and hyperemic ([Fig. 1B]).
On palpation in the region 23 to 28, the area was rough and sharp surface, hard consistency,
and moveable, indicating a bone segment ([Fig. 1C]).
Radiograph Examination
The panoramic radiography and computed tomography (CT) scan were carried out. On the
panoramic radiography, there were multiple radiopaque indicated as moth-eaten appearance in the sinistra maxilla region 21 to 28 ([Fig. 2A]). The CT scan examination showed a radiopaque mass in the sinistra maxilla region
21 to 28 and extending to the dextra maxilla ([Fig. 2B]), possibly also hitting the left temporal base and the lower wall of the left maxillary
sinus ([Fig. 2C]).
Fig. 2 Panoramic radiography (A). Computed tomography (CT) scan examination (bone window) axial view (B); The three-dimensional CT scan looks frontal and axial (C). The red arrow shows a picture of bone destruction.
Complete Blood Count
A blood examination was also carried out. The value of hemoglobin A1c (HbA1c) (12.9%)
indicated uncontrolled diabetes. Other parameters, like hemoglobin (10%) and lower
mean corpuscular volume and mean corpuscular hemoglobin concentration, indicated microcytic
hypochromic anemia with suspicion of nutritional and iron deficiency. Of this finding,
the patient was also referred to internal medicine to optimize the condition.
Microbial Test
A puss was collected for the sinistra maxilla, and a microbial culture was performed.
The result showed a dominance of Klebsiella
pneumoniae and Morganella morganii.
Case Management
Chronic suppurative osteomyelitis maxilla is a preoperative diagnosis based on anamnesis,
clinical examination, and patient support examination results. The patient was previously
referred for consultation and blood glucose level regulation and given the drugs glimepiride,
metformin, acarbose, and folic acid by an internal medicine specialist to a random
blood sugar below a value of 200 mg/dL. The patient was found to have a cardiac risk
index—class I and was deemed eligible for oral surgery after being assessed by a cardiology
specialist.
The surgery was carried out; in this case, an extensive sequestrectomy was performed.
A mucoperiosteal flap incision was performed on the buccal and palatal regions 28
to 16 ([Fig. 3A] and [B]). Necrotic bone appeared in the mobile maxillary segment. The buccal section, bone
resorption, and third-degree tooth shake were obtained, and then 22 to 16 tooth extraction,
squashing, and smoothing of the bone surface were carried out ([Fig. 3D]). Postsequestrectomy defects of the nasal mucosa appeared to be still indented.
The obturator could be installed in this case because there were no bones and teeth
left, and it was adequate for retention; so suturing was carried out from the oral
mucosa to the nasal mucosa to avoid the occurrence of dead space ([Fig. 3C]).
Fig. 3 A mucoperiosteal flap of the maxillary region showed a necrotic bone (A). Postsequestrectomy defects appear that nasal mucosa is still indented (B). Postoperative intraoral mucosal suturing (C) and sequestrum specimens (D).
Bleeding during surgery was anticipated by preparing one bag of whole blood transfusion.
Before the surgery, 1.5 g cefuroxime was administered to the patient. Following the
surgery, a 1 g ceftriaxone injection was given based on the results of antibiotic
sensitivity obtained from a 5-day torture of pus culture. The patient was then instructed
to take cefixime 200 mg orally for 5 days as continued antibiotic therapy. Furthermore,
an anti-inflammatory treatment of 30 mg ketorolac injection was given.
Histopathology Diagnosis
The sequester was found to be positive for osteomyelitis based on the histopathological
examination results. The tissue is partially coated by squamous epithelium, a solid
density of inflammatory lymphocyte cells, plasma cells, neutrophils, and proliferation
([Fig. 4A]). Blood vessels appeared between the stroma (yellow arrow) of fibrous tissue and
the fat matrix, and no sign of malignancy was obtained ([Fig. 4B]).
Fig. 4 The result of surgery after a 1-month follow-up. The wound is healed and closed,
and no bone is exposed.
Postsurgery Follow-Up
Patients are instructed to a high-calorie, high-protein liquid diet for 6 days postsurgery.
The patient was instructed to follow up, 1 month after discharge from the hospital
for postoperative deflection area inspection. There was no abnormality observed both
extra and intraoral ([Fig. 5]).
Fig. 5 Microscopic picture examination of anatomical pathology (magnification 200x). The
tissue is partially coated by squamous epithelium (green arrow) and a solid density
of inflammatory cells (white arrow) (A). The necrotic part of the bone is characterized by the absence of living osteocytes
and contains mostly mononuclear lymphocyte cells. A blood vessel (yellow arrow) appeared
between the stroma and bone matrix (black arrow) (B).
Discussion
Maxillary osteomyelitis is rare due to the extensive vascular supply; so, it is not
easy to experience ischemia and necrosis in the maxillary region.[3] Typical clinical findings include pain, swelling, and odorous secretions. Microbiological
etiology is by gram-positive and gram-negative microorganisms, including Staphylococcus aureus, Staphylococcus epidermidis, Pepto streptococcus, Pneumococcus,
Hemolytic streptococci, Escherichia coli, and Bacteroides.[27] Osteomyelitis is classified into suppurative and nonsuppurative. Suppurative osteomyelitis
is primarily caused by odontogenic infections characterized by fistulas and sequestration.[28]
The case of maxillary osteomyelitis is rarely reported. The osteomyelitis is also
found with the coinfection with Mucorales and Aspergillus species.[29] The diabetes status becomes a severity factor for osteomyelitis, especially in the
maxilla.[4] Commonly seen in immunocompromised patients, diabetes mellitus is an important associated
comorbidity in the pathophysiologic development of this disease.[30] Noncognizance of diabetes mellitus can be devastating for the maxillofacial region
and may be fatal for the patient.[22] In another case, diabetes mellitus is able to trigger the exacerbation of osteomyelitis.[31]
The incidence ratio of men to women in osteomyelitis can vary up to 5.2:1. In previous
studies, the ratio of men to women was 1.1:1. The age of patients ranges from 40 to
70 years, with an average age of 51.6 years. The predilection ratio of osteomyelitis
in the mandible and maxilla is 2:1.[23]
[32] It aligns with the patients involved, a 58-year-old male. The radiographic examination
of chronic osteomyelitis is mainly in the form of a “moth-eaten appearance,” which occurs due to the expansion of the medullary space
of the canal and the dilation of the Volkmann canal caused by intramedullar inflammation
that continues into the bone ischemia of the lysis bone and granulation tissue surrounds
a necrotic bone referred to as a sequester.[3] In this case, the sequester was also observed and led to chronic conditions. Through
a CT scan, it confirmed that the sequesters extended to the maxillary region. Osteomyelitis
is characterized by necrotic bones with irregular trabeculae bone formations that
appear empty due to the absence of osteocytes, an osteoblastic layer, and inflammatory
cells such as lymphocytes. The morphological picture of chronic osteomyelitis is the
presence of a part of the bone that the absence of living osteocytes characterizes
necrosis. Most contain mononuclear lymphocyte cells, granules, and fibrous tissue
replacing bones absorbed by osteoclasts.[33]
The main predisposing factors are impaired immunity disorders such as immunodeficiency
syndrome, diabetes mellitus, autoimmune conditions, malignancies, and malnutrition.[12] According to Peravali et al, 68% of upper jaw osteomyelitis cases are associated
with diabetes mellitus because in hyperglycemic conditions, the immune system decreases
and results from impaired distribution of vascularization to the maxilla.[23] Previous study stated that the percentage of osteomyelitis in the maxilla was higher
with uncontrolled diabetes (33.3%) compared to controlled diabetes (9.5%).[8] Diabetes mellitus is known as an immune response suppressor,[27] and has a strong correlation with osteomyelitis.[32] This correlation was proven in previous studies where diabetes was found to be one
of the main factors for the occurrence of osteomyelitis (47.6%). The increased blood
glucose levels weaken and damage the walls of capillary blood vessels that supply
nerve nutrients. On the other hand, diabetic patients experience decreased chemotaxis
function in leukocytes, phagocytosis, and leukocyte life span, causing tissue inflammatory
response decreases. The reduction in the immune response is caused by impaired glucose
metabolism and causes a long-wound healing process.[26] In this case, the patient has had a history of diabetes since 2010, and the HbA1c
test indicates that the diabetes is uncontrolled. The patient also underwent an extraction
of the upper jaw teeth in January 2021 and experienced persistent pain and healing
wounds, which may have contributed to the occurrence of osteomyelitis in the patient.
Factors of trauma and odontogenic also cause osteomyelitis in the patient.
The prognosis of patients with osteomyelitis depends on several factors, including
a secondary infection. The secondary infection occurred due to the accumulation of
inflammatory exudate in the bone cavity. The patient indicated microcytic hypochromic
anemia with suspicion of nutritional and iron deficiency. Iron is essential for the
growth and proliferation of bacteria, including those that cause osteomyelitis. Therefore,
in chronic osteomyelitis cases, there is often increased demand for iron by bacteria,
leading to iron deficiency anemia, which is typically microcytic hypochromic. However,
the severity of chronic maxillary osteomyelitis cannot be solely determined by microcytic
hypochromic anemia. Other factors, such as the extent of bone involvement, duration
of the infection, and underlying medical conditions, such as diabetes, also play a
significant role in the severity of the disease.[34]
[35] Individuals with diabetes may have a compromised vascular supply, leading to tissue
ischemia, which impairs the delivery of antibiotics to the site of infection, making
it difficult to eradicate the infection. Additionally, individuals with diabetes may
have a weakened immune system, making them more susceptible to secondary infections,
especially if the initial infection is not adequately treated.[6]
[22]
[36] In this patient, the bacteria were confirmed as Morganella morganii and Klebsiella pneumoniae. These two bacteria are not commonly found in maxillary osteomyelitis. Most of the
cases reported the involvement of both bacterial and fungal infections like actinomycosis,[10]
[11]
[12] mucormycosis,[13]
[14]
[15]
[16]
[17]
Escherichia coli,[37]
Staphylococcus aureus,[38]
Veillonella species,[39]
Candida,[40] and Kocuria.[41] The identifying the bacterial and fungal involvement in osteomyelitis is needed
to provide definitive therapy on target and reduce the pathogenicity during therapy.
There are three types of osteomyelitis management: antibiotic therapy, surgical therapy,
and hyperbaric therapy. Other surgical management options include cauterization, sequestrectomy,
debridement, decortication, and jaw resection with reconstruction.[42] Chronic osteomyelitis is difficult to treat using antibiotics and hyperbaric therapy
due to the formation of pockets containing dead bone cells and organisms covered with
fibrous tissue; so, the treatment becomes ineffective. Removal of bones that have
been necrosis is the goal of chronic osteomyelitis therapy; so, invasive procedures
must be carried out.[8]
[32] In this case, extensive sequestrectomy was carried out to remove all infected tissues
and necrosis so that the opportunity for vascular reperfusion and drainage could occur
in infected areas.[29] Antibiotic therapy is given before and after surgery, which has been adjusted to
the sensitivity test of the culture test. The nasal sound that appears after surgery
appears because the missing palate bone is wide enough; so, a removable denture is
needed for subsequent rehabilitation and long-term control to monitor whether there
is a reinfection or unconscious expansion of the infection.
Conclusion
Comprehensive perioperative management in maxillary osteomyelitis in uncontrolled
diabetes mellitus includes sequestrectomy, definitive antibiotic therapy based on
culture results, and diabetes regulation to improve the successful management of this
case.
