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Temporomandibular joint involvement caused by Borrelia Burgdorferi
ARTICLE IN PRESS Journal of Cranio-Maxillofacial Surgery (2007) 35, 397–400 r 2007 European Association for Cranio-Maxillofacial Surgery doi:10.1016/j.jcms.2007.06.003, available online at http://www.sciencedirect.com
Temporomandibular joint involvement caused by Borrelia Burgdorferi Gorazd LESˇNICˇARa, Danijel ZˇERDONERb a
Department of Infectious Diseases and Febrile Conditions (Head: Prof. Gorazd Lesˇnicˇar,M.D., Ph.D.); Department of Maxillofacial and Oral Surgery (Head: Assist. Prof. Daniel Zˇerdoner, M.D., Ph.D.), Teaching Hospital Celje, Slovenia
b
Available online 17 October 2007
Background: Lyme borreliosis is an endemic disease in Slovenia with an incidence of around 150 patients per 100,000 inhabitants. Although the large joints are most typically affected in Lyme borreliosis, there are also periods of disease activity with arthritis or arthralgias involving smaller joints, including the temporomandibular joint. Patients: During the years between 2000 and 2003, two patients with Lyme borreliosis affecting the temporo-mandibular joints were treated. The patients presented with fatigue and pain in diverse muscle groups accompanied by arthralgia, which was most pronounced in the temporomandibular joint area. None of the patients were febrile or had joint effusions. Methods: Both patients were examined by means of biochemical and serological examinations for Borrelia burgdorferi using ELISA assay and Western blot test (both for IgM and IgG), plain radiographs, MR and CT scans, and scinti-scan of the temporo-mandibular joints They both had positive serum markers for an acute B. burgdorferi infection and were treated with intravenous ceftriaxone. Results: None of the patients had clinical or laboratory signs of chronic Lyme disease activity two and four years following therapy, respectively. Roentgenographic and nuclear magnetic resonance imaging of the temporo-mandibular joints had not shown any persistent sign of acute inflammation. Conclusion: There are only few reports of patients with manifest temporo-mandibular joint involvement of Lyme borreliosis in the literature. This report emphasizes the importance of differential diagnosis of acute temporo-mandibular joint arthralgia, of early diagnosis of Lyme borreliosis, and of the necessity for prompt antibiotic treatment. r 2007 European Association for Cranio-Maxillofacial Surgery SUMMARY.
Keywords: Lyme borreliosis, acute infection, temporo-mandibular joint, differential diagnosis, therapy, consequences
standardised serological methods and due to ignorance of all forms of Lyme borreliosis, probably only a small fraction of all the affected patients is duly registered. The differential diagnosis of Lyme borreliosis is wide since the varying clinical pictures resemble several other diseases. The patient may either present with a single form of the disease or the symptoms of all three stages of the disease may overlap. Sometimes the disease becomes apparent only when in its late phase (Steere, 1993; Nadelman and Wormser, 1998). Owing to the multifaceted clinical picture and varying immune response it can be very complex and demanding to make this diagnosis. Reports of Lyme borrelosis cases with involement of the temporo-mandibular joint as the main symptoms are very rare (Harris, 1988; Lader, 1989, 1990; Kelsey, 1990; Moscatello et al., 1991; Heir, 1997; Heir and Fein, 1996, 1998; Vesper et al., 2001; Rhodus and Falace, 2002). The authors point out that in the differential diagnosis of acute temporomandibular pain, infection with Borrelia burgdorferi should be considered.
INTRODUCTION Lyme borreliosis is a zoonosis primarily affecting people who have been bitten by Borrelia burgdorferi sensu lato infected insects, most frequently ticks. In Slovenia, Lyme borreliosis is endemic and affects an increasing number of patients every year. In the last decade, this disease has been diagnosed in 30,000 persons in Slovenia, the incidence being 155 per 100,000 inhabitants. Most patients were between 35 and 65 years of age. However, there were differences in morbidity between regions (Strle et al., 1995; Radsˇel-Medvesˇcˇek, 2002). Lyme borreliosis runs a diverse and variable course, and rarely are all the symptoms found in each patient . Every organ system can be affected, but the course of disease is different and versatile. The most frequent and pathognomonic clinical sign, namely erythema migrans, was first reported in Slovenia in 1981, i.e. 6 years after the discovery of Lyme disease epidemics in the Old Lyme town of the American state of Connecticut (Lesˇnicˇar, 1981). Due to incomplete reporting of erythema migrans to the epidemiological services, to the non397
ARTICLE IN PRESS 398 Journal of Cranio-Maxillofacial Surgery
CASE REPORTS Case no. 1 In January 2000, a 59-year-old patient was admitted to the Department of Infectious Diseases and Febrile Conditions with a 4-week history of typical erythema migrans extending over a 15 15 cm large area on the skin above her left knee. The skin lesions appeared 2 weeks after a tick bite. On admission, the patient also complained of fatigue and pain in her shoulder, hip and knee joints. The joints were not swollen. Serological examinations for B. burgdorferi by ELISA assay (enzyme-linked immunosorbent assay– ELISA Enzygost Borreliosis Dade Behring, Marburg, Germany) yielded positive results for IgM as well as IgG. Following 2-weeks of parenteral therapy with ceftriaxon, all complaints have disappeared. The patient was readmitted in May 2000 due to recurrent fatigue, headache and pain in her muscles and joints. The pain was most intense in her right temporomandibular joint. Both joints were not visibly altered. However, the patient had difficulty with mouth opening (max. interincisal distance 20 mm). She further complained of pain when chewing hard food; the pain radiated into her right ear. She was febrile. Serological examinations for B. burgdorferi were unchanged; the Western blot tests in IgG and IgM were still positive (Borrelia Blot IgM/IgG Mikrogen, Martinsried, Germany). The titre of antinuclear antibodies (ANA) according to the direct immunofluorescent method on Hep-2 cells (LD Diagnostika, Heiden, Germany) was borderline positive 1:40, whilst the rheumatoid factor (Mast Diagnostika, Reinfeld, Germany) was negative. A lumbar puncture yielded normal liquor and culture for the presence of B. burgdorferi was negative. Otoscopic findings were within normal limits, as were basic haematological examinations. Radiographs of the temporo-mandibular joints showed no abnormal findings, except for the uneven surface of the mandibular head. Scintigraphy with radiolabelled granulocytes and computed tomography (CT) of both temporo-mandibular joints were within normal limits. The repeated 3-week treatment with ceftriaxon was considered successful since all the symptoms had mostly regressed. The patient was followed up for several years. Joint problems have not recurred; 1 year after the disease, IgM antibodies against borreliosis were negative, whilst IgG antibodies by ELISA and Western Blot test remained positive. In 2004, a follow-up MRI for arthrosis in the temporo-mandibular joints showed evidence of initial signs of arthrosis in the right temporo-mandibular joint (Fig. 1).
Fig. 1 – 63-year-old woman, coronal MRI of the temporomandibular joints four years after Lyme borreliosis presenting only minimal arthritic alterations.
months, myalgia in the extremities as well as pain in both temporo-mandibular joints and the left arm. He had already been examined by an orthopaedic specialist. However, X-ray examination of the shoulder joints had not revealed any pathological changes. The patient was prescribed physiotherapy for limited pain and mobility of his right shoulder. At the same time, the patient was receiving amoxicillin because of a respiratory infection. There was temporary relief of joint pains. The patient was afebrile and did not complain of swollen joints. He told that he had noted a tick attached to his skin on a few occasions, however, he did not remember having had erythema migrans. Due to extreme pains in both temporo-mandibular joints, the patient was referred to a maxillofacial surgeon, who did not detect any clinical signs of inflammation, except that the temporo-mandibular joint was painful on palpation. Plain radiographs and CT scan of the temporo-mandibular joints were within normal limits. Basic haematological examinations were also with normal limits including inflammatory markers and rheumatoid factor. However, serological assays for B. burgdorferi (ELISA, Western blot) were positive for IgM and IgG. Following therapy with ceftriaxone at a daily dosage of 2 g for 3 weeks, the pain in his left shoulder and both temporo-mandibular joints gradually disappeared. Two months later the patient felt well, the clinical findings were normal and the serological assays carried out 1 year after therapy revealed only evidence of past infection, i.e. positive IgG antibodies for B. burgdorferi (ELISA, Western blot). One year after the diagnosis, a follow-up radiograph and MRI of the temporo-mandibular joints showed minimal evidence of disease, in the form of minimal arthritic changes (Fig. 2).
Case no. 2 DISCUSSION Early in 2003, a 52-year-old patient was admitted to the Department of Infectious Diseases and Febrile Conditions because of fatigue lasting for a few
B. burgdorferi-related involvement of the temporomandibular joint is rarely seen in daily clinical
ARTICLE IN PRESS Temporomandibular joint involvement caused by Borrelia Burgdorferi 399
Fig. 2 – 53-year old patient, lateral MRI of the temporo-mandibular joints at extreme mouth opening one year after Lyme borreliosis.
practice. Classically, the large joints are affected first in Lyme borreliosis, among these most frequently the knee, while smaller joints are only affected exceptionally. Generally, symptoms of arthritis interchange with periods of arthralgia. Lyme borreliosis related temporo-mandibular joint involvement as a leading clinical sign of B. burgdorferi infection has only very rarely been reported in the literature. In those cases in whom erythema migrans, the warning and pathognomonic sign for Lyme borreliosis, is either not present or remains unnoticed, the varying clinical picture and frequently weak immune response render the diagnosis very difficult. It is therefore not a coincidence that most authors reporting temporo-mandibular involvement come from the north-eastern parts of the USA, where Lyme arthritis is endemic and the most frequent sign of late and disseminated form of B. burgdorgferi infection. It occurs in as many as 70% of untreated patients with Lyme borreliosis (Steere et al., 1987; Steere, 1993). In Slovenia and other European countries, Lyme borreliosis-associated joint involvement is not such an important clinical sign of Lyme borreliosis as it is in the USA. It takes the third place only, among the clinical manifestations of the disease, being outnumbered by neurological and cutaneous forms of the disease. Joint involvement is present in approximately of cases 15%, in Slovenian which corresponds to the overall European average. Nevertheless, also in Europe there are great differences in the leading symptoms: the joint involvement is almost nonexistent in Great Britain but is among the leading forms of Lyme borreliosis in Italy where it was found in more than 50% of patients (Cimmino, 1998; LotricˇFurlan et al., 1999). This may be due to the fact that in the USA the prevailing Borrelia pathogen for man is B. burgdorferi sensu stricto, whilst in Europe these are Borrelia afzeli and Borrelia garinii. The transmitters are different as well: In the USA the prevailing species are Ixodes scapularis and Ixodes pacificus, while in Europe it is Ixodes ricinus (Strle et al., 1995; Steere, 2001).
The first description of recurrent arthropathy with symptoms in the temporo-mandibular joint in a younger patient with Lyme borreliosis was contributed by Harris (1988). Successful treatment with tetracyclines prevented further progression of the disease and made surgical intervention unnecessary. The author pointed out that this infection should be considered whenever a patient presents with ‘‘polyorganic syndrome’’ and orofacial pain failing to respond to a standard analgesic therapy. They also call attention to the possibility of negative serological assays or frequently negative tissue biopsy and synovial fluid culture in patients with active Lyme borreliosis. Heir and Fein (1998) pointed out the importance of a wide differential diagnostic list of orofacial and dental disorders; they also defined the epidemiological, clinical, diagnostic and treatment factors for Lyme borreliosis, which differentiate this from many other pathological conditions and functional disorders of the temporo-mandibular joint. These transient, cyclic or progressive functional disorders of the temporo-mandibular joint can be diagnosed using careful history and clinical examination: In Lyme borreliosis of the temporo-mandibular joint, intensive pain may be felt in the ears when chewing food or opening the mouth. However, arthritic signs present rarely and joint function is generally not affected. The pain is often cyclical and may last for two weeks with pauses with recurrences every 1 – 3 months. Vesper et al. (2001) were the first in Europe apart from Slovenia to report temporo-mandibular joint arthritis in a 49-year-old patient. The treatment with ceftriaxone proved to be successful. In Germany, where there are 40,000 – 80,000 persons diagnosed with Lyme borreliosis yearly; the joint involving form appeared in approximately 14% of patients, representing the European average (Cimmino, 1998). Although the Slovenian textbook of infectious diseases states that Lyme borreliosis may affect the TMT, relatively often many years of clinical practice as well as reports in the literature do not confirm this statement. The two cases described here represent a
ARTICLE IN PRESS 400 Journal of Cranio-Maxillofacial Surgery
rarity, but were not difficult to recognize in this endemic area. Isolation of B. burgdorferi from the synovial fluid was not performed as the procedure is rarely successful and was not feasible in these 2 patients. Early antibiotic treatment generally prevents the recurrent arthralgia. It is probably caused by persistence of borrelia in the synovia. The best outcome has been with ceftrixane-based parenteral antibiotic therapy. Treatment with highdose benzylpenicillin (20 MIU), doxicycline and amoxicilin at a dosage of 2 g/day for 2 – 4 weeks was successful as well (Lotricˇ-Furlan et al., 1999; Strle, 1999). The use of non-steroidal antirheumatic drugs seems reasonable, particularly at the outset when the pain is quite severe (Sˇibanc and Lesˇnicˇar, 2002). Chronic Lyme borreliosis is characterized by recurrences and relatively poor therapeutic response, since the causative agent is generally no longer present, while the autoimmune mechanisms, i.e. the presence of antigens stimulating the production of T-lymphocytes, are already active (Steere, 2001; Singh and Girschick, 2004). Local use of corticosteroids is not recommended, nor is arthroscopic synovectomy. No descriptions of cartilage and or bone erosion, periostitis, periarticular fibrous nodules and recurrent dislocations of the temporo-mandibular joint have been found in the literature whilst these have been described in long-lasting untreated chronic Lyme borreliosis-associated inflammations of large joints (Steere et al., 1987; Steere, 1993).
CONCLUSION Since only early treatment of Lyme borreliosis is successful, B. burgdorferi should always be taken into account in the differential diagnosis of temporomandibular joint pain.
References Cimmino MA: On behalf of the European community concerted action on risk assessment in Lyme borreliosis: relative frequency of Lyme borreliosis and of its clinical manifestations in Europea. Infection 26: 298–300, 1998 Harris RJ: Lyme disease involving the temporo-mandibular joint. J Oral Maxillofac Surg 46: 78–79, 1988 Heir GM: Differentiation of orofacial pain related to Lyme disease from other dental and facial pain disorders. Dent Clin North Am 41: 243–258, 1997
Heir GM, Fein LA: Lyme disease: considerations for dentistry. J Orofac Pain 10: 74–86, 1996 Heir GM, Fein LA: Lyme diseases awareness for the New Jersey dentist. A survey of orofacial and headache complaints associated with Lyme disease. J N J Dent Assoc 69 (19, 21): 62–63, 1998 Kelsey JH: Lyme disease: an important consideration in the differential diagnosis of TMD. J Mich Dent Assoc 72: 209–210, 1990 Lader E: Lyme disease misdiagnosed as TMJ syndrome. A case report. N Y State Dent J 55 (46, 48): 50–52, 1989 Lader E: Lyme disease misdiagnosed as a temporomandibular joint disorder. J Prosthet Dent 63: 82–85, 1990 Lesˇ nicˇar J: Erythema migrans po klopnem vbodu. Zdrav Vestn 50: 305, 1981 Lotricˇ-Furlan S, Strle F, Plesˇ ivcˇnik Novljan M: Lymski artritis— klinicˇne znacˇilnosti, diagnoza in zdravljenje. Med Razgl 38 (Suppl 1): 43–50, 1999 Moscatello AL, Worden DL, Nadelman RB, Wormser G, Lucente F: Otolaryngologic aspects of Lyme disease. Laryngoscope 101: 592–595, 1991 Nadelman RB, Wormser GP: Lyme borreliosis. Lancet 352: 557–565, 1998 Radsˇ el-Medvesˇ cˇek A: Lymska borelioza. In: Marolt-Gomisˇ cˇek M, Radsˇ el-Medvesˇ cˇek A (eds.), Infekcijske bolezni. Ljubljana: Zalozˇba Tangram, 225–234, 2002 Rhodus NL, Falace DA: Oral concerns in Lyme disease. Northwest Dent 81: 17–18, 2002 Singh SK, Girschick HJ: Lyme borreliosis: from infection to autoimmunity. Clin Microbiol Infect 10: 598–614, 2004 Steere AC: Pathogenesis, diagnosis and treatment of Lyme arthritis. Ann Rheum Dis 52: 391–393, 1993 Steere AC: Lyme diseases. N Engl J Med 345: 115–125, 2001 Steere AC, Schoen R, Taylor E: The clinical evaluation of Lyme arthritis. Ann Intern Med 107: 725–731, 1987 Strle F: Principles of the diagnosis and antibiotic treatment of Lyme borreliosis. Wien Klin Wochenschr 22–23: 911–915, 1999 Strle F, Cheng Y, Nelson JA, Picken MM, Bouseman JK, Picken RN: Infection rate of Ixodes ricinus ticks with Borrelia afzelii, Borrelia garinii, and Borrelia burgdorferi sensu stricto in Slovenia. Eur J Clin Microbiol Infect Dis 14: 994–1001, 1995 Sˇibanc B, Lesˇ nicˇar G: Complex regional pain syndrome and Lyme borreliosis: two different diseases?. Infection 6: 93–96, 2002 Vesper M, Ro¨der K, Siegert J, Friedrich RE, Schmelzle R: Inflammation of the left temporomandibular joint after Lyme disease. Mund Kiefer Gesichts Chir 5: 258–260, 2001
Danijel Zˇerdoner, M.D. Ph.D., Assist. Prof. Department of Maxillofacial and Oral Surgery Celje Teaching Hospital Oblakova 5, SI-3000 Celje Slovenia Tel.: +386 3 4233150 Fax: +386 3 4233754 E-mail: [email protected] Paper received 17 January 2006 Accepted 8 June 2007
Temporomandibular joint involvement caused by Borrelia Burgdorferi Gorazd LESˇNICˇARa, Danijel ZˇERDONERb a
Department of Infectious Diseases and Febrile Conditions (Head: Prof. Gorazd Lesˇnicˇar,M.D., Ph.D.); Department of Maxillofacial and Oral Surgery (Head: Assist. Prof. Daniel Zˇerdoner, M.D., Ph.D.), Teaching Hospital Celje, Slovenia
b
Available online 17 October 2007
Background: Lyme borreliosis is an endemic disease in Slovenia with an incidence of around 150 patients per 100,000 inhabitants. Although the large joints are most typically affected in Lyme borreliosis, there are also periods of disease activity with arthritis or arthralgias involving smaller joints, including the temporomandibular joint. Patients: During the years between 2000 and 2003, two patients with Lyme borreliosis affecting the temporo-mandibular joints were treated. The patients presented with fatigue and pain in diverse muscle groups accompanied by arthralgia, which was most pronounced in the temporomandibular joint area. None of the patients were febrile or had joint effusions. Methods: Both patients were examined by means of biochemical and serological examinations for Borrelia burgdorferi using ELISA assay and Western blot test (both for IgM and IgG), plain radiographs, MR and CT scans, and scinti-scan of the temporo-mandibular joints They both had positive serum markers for an acute B. burgdorferi infection and were treated with intravenous ceftriaxone. Results: None of the patients had clinical or laboratory signs of chronic Lyme disease activity two and four years following therapy, respectively. Roentgenographic and nuclear magnetic resonance imaging of the temporo-mandibular joints had not shown any persistent sign of acute inflammation. Conclusion: There are only few reports of patients with manifest temporo-mandibular joint involvement of Lyme borreliosis in the literature. This report emphasizes the importance of differential diagnosis of acute temporo-mandibular joint arthralgia, of early diagnosis of Lyme borreliosis, and of the necessity for prompt antibiotic treatment. r 2007 European Association for Cranio-Maxillofacial Surgery SUMMARY.
Keywords: Lyme borreliosis, acute infection, temporo-mandibular joint, differential diagnosis, therapy, consequences
standardised serological methods and due to ignorance of all forms of Lyme borreliosis, probably only a small fraction of all the affected patients is duly registered. The differential diagnosis of Lyme borreliosis is wide since the varying clinical pictures resemble several other diseases. The patient may either present with a single form of the disease or the symptoms of all three stages of the disease may overlap. Sometimes the disease becomes apparent only when in its late phase (Steere, 1993; Nadelman and Wormser, 1998). Owing to the multifaceted clinical picture and varying immune response it can be very complex and demanding to make this diagnosis. Reports of Lyme borrelosis cases with involement of the temporo-mandibular joint as the main symptoms are very rare (Harris, 1988; Lader, 1989, 1990; Kelsey, 1990; Moscatello et al., 1991; Heir, 1997; Heir and Fein, 1996, 1998; Vesper et al., 2001; Rhodus and Falace, 2002). The authors point out that in the differential diagnosis of acute temporomandibular pain, infection with Borrelia burgdorferi should be considered.
INTRODUCTION Lyme borreliosis is a zoonosis primarily affecting people who have been bitten by Borrelia burgdorferi sensu lato infected insects, most frequently ticks. In Slovenia, Lyme borreliosis is endemic and affects an increasing number of patients every year. In the last decade, this disease has been diagnosed in 30,000 persons in Slovenia, the incidence being 155 per 100,000 inhabitants. Most patients were between 35 and 65 years of age. However, there were differences in morbidity between regions (Strle et al., 1995; Radsˇel-Medvesˇcˇek, 2002). Lyme borreliosis runs a diverse and variable course, and rarely are all the symptoms found in each patient . Every organ system can be affected, but the course of disease is different and versatile. The most frequent and pathognomonic clinical sign, namely erythema migrans, was first reported in Slovenia in 1981, i.e. 6 years after the discovery of Lyme disease epidemics in the Old Lyme town of the American state of Connecticut (Lesˇnicˇar, 1981). Due to incomplete reporting of erythema migrans to the epidemiological services, to the non397
ARTICLE IN PRESS 398 Journal of Cranio-Maxillofacial Surgery
CASE REPORTS Case no. 1 In January 2000, a 59-year-old patient was admitted to the Department of Infectious Diseases and Febrile Conditions with a 4-week history of typical erythema migrans extending over a 15 15 cm large area on the skin above her left knee. The skin lesions appeared 2 weeks after a tick bite. On admission, the patient also complained of fatigue and pain in her shoulder, hip and knee joints. The joints were not swollen. Serological examinations for B. burgdorferi by ELISA assay (enzyme-linked immunosorbent assay– ELISA Enzygost Borreliosis Dade Behring, Marburg, Germany) yielded positive results for IgM as well as IgG. Following 2-weeks of parenteral therapy with ceftriaxon, all complaints have disappeared. The patient was readmitted in May 2000 due to recurrent fatigue, headache and pain in her muscles and joints. The pain was most intense in her right temporomandibular joint. Both joints were not visibly altered. However, the patient had difficulty with mouth opening (max. interincisal distance 20 mm). She further complained of pain when chewing hard food; the pain radiated into her right ear. She was febrile. Serological examinations for B. burgdorferi were unchanged; the Western blot tests in IgG and IgM were still positive (Borrelia Blot IgM/IgG Mikrogen, Martinsried, Germany). The titre of antinuclear antibodies (ANA) according to the direct immunofluorescent method on Hep-2 cells (LD Diagnostika, Heiden, Germany) was borderline positive 1:40, whilst the rheumatoid factor (Mast Diagnostika, Reinfeld, Germany) was negative. A lumbar puncture yielded normal liquor and culture for the presence of B. burgdorferi was negative. Otoscopic findings were within normal limits, as were basic haematological examinations. Radiographs of the temporo-mandibular joints showed no abnormal findings, except for the uneven surface of the mandibular head. Scintigraphy with radiolabelled granulocytes and computed tomography (CT) of both temporo-mandibular joints were within normal limits. The repeated 3-week treatment with ceftriaxon was considered successful since all the symptoms had mostly regressed. The patient was followed up for several years. Joint problems have not recurred; 1 year after the disease, IgM antibodies against borreliosis were negative, whilst IgG antibodies by ELISA and Western Blot test remained positive. In 2004, a follow-up MRI for arthrosis in the temporo-mandibular joints showed evidence of initial signs of arthrosis in the right temporo-mandibular joint (Fig. 1).
Fig. 1 – 63-year-old woman, coronal MRI of the temporomandibular joints four years after Lyme borreliosis presenting only minimal arthritic alterations.
months, myalgia in the extremities as well as pain in both temporo-mandibular joints and the left arm. He had already been examined by an orthopaedic specialist. However, X-ray examination of the shoulder joints had not revealed any pathological changes. The patient was prescribed physiotherapy for limited pain and mobility of his right shoulder. At the same time, the patient was receiving amoxicillin because of a respiratory infection. There was temporary relief of joint pains. The patient was afebrile and did not complain of swollen joints. He told that he had noted a tick attached to his skin on a few occasions, however, he did not remember having had erythema migrans. Due to extreme pains in both temporo-mandibular joints, the patient was referred to a maxillofacial surgeon, who did not detect any clinical signs of inflammation, except that the temporo-mandibular joint was painful on palpation. Plain radiographs and CT scan of the temporo-mandibular joints were within normal limits. Basic haematological examinations were also with normal limits including inflammatory markers and rheumatoid factor. However, serological assays for B. burgdorferi (ELISA, Western blot) were positive for IgM and IgG. Following therapy with ceftriaxone at a daily dosage of 2 g for 3 weeks, the pain in his left shoulder and both temporo-mandibular joints gradually disappeared. Two months later the patient felt well, the clinical findings were normal and the serological assays carried out 1 year after therapy revealed only evidence of past infection, i.e. positive IgG antibodies for B. burgdorferi (ELISA, Western blot). One year after the diagnosis, a follow-up radiograph and MRI of the temporo-mandibular joints showed minimal evidence of disease, in the form of minimal arthritic changes (Fig. 2).
Case no. 2 DISCUSSION Early in 2003, a 52-year-old patient was admitted to the Department of Infectious Diseases and Febrile Conditions because of fatigue lasting for a few
B. burgdorferi-related involvement of the temporomandibular joint is rarely seen in daily clinical
ARTICLE IN PRESS Temporomandibular joint involvement caused by Borrelia Burgdorferi 399
Fig. 2 – 53-year old patient, lateral MRI of the temporo-mandibular joints at extreme mouth opening one year after Lyme borreliosis.
practice. Classically, the large joints are affected first in Lyme borreliosis, among these most frequently the knee, while smaller joints are only affected exceptionally. Generally, symptoms of arthritis interchange with periods of arthralgia. Lyme borreliosis related temporo-mandibular joint involvement as a leading clinical sign of B. burgdorferi infection has only very rarely been reported in the literature. In those cases in whom erythema migrans, the warning and pathognomonic sign for Lyme borreliosis, is either not present or remains unnoticed, the varying clinical picture and frequently weak immune response render the diagnosis very difficult. It is therefore not a coincidence that most authors reporting temporo-mandibular involvement come from the north-eastern parts of the USA, where Lyme arthritis is endemic and the most frequent sign of late and disseminated form of B. burgdorgferi infection. It occurs in as many as 70% of untreated patients with Lyme borreliosis (Steere et al., 1987; Steere, 1993). In Slovenia and other European countries, Lyme borreliosis-associated joint involvement is not such an important clinical sign of Lyme borreliosis as it is in the USA. It takes the third place only, among the clinical manifestations of the disease, being outnumbered by neurological and cutaneous forms of the disease. Joint involvement is present in approximately of cases 15%, in Slovenian which corresponds to the overall European average. Nevertheless, also in Europe there are great differences in the leading symptoms: the joint involvement is almost nonexistent in Great Britain but is among the leading forms of Lyme borreliosis in Italy where it was found in more than 50% of patients (Cimmino, 1998; LotricˇFurlan et al., 1999). This may be due to the fact that in the USA the prevailing Borrelia pathogen for man is B. burgdorferi sensu stricto, whilst in Europe these are Borrelia afzeli and Borrelia garinii. The transmitters are different as well: In the USA the prevailing species are Ixodes scapularis and Ixodes pacificus, while in Europe it is Ixodes ricinus (Strle et al., 1995; Steere, 2001).
The first description of recurrent arthropathy with symptoms in the temporo-mandibular joint in a younger patient with Lyme borreliosis was contributed by Harris (1988). Successful treatment with tetracyclines prevented further progression of the disease and made surgical intervention unnecessary. The author pointed out that this infection should be considered whenever a patient presents with ‘‘polyorganic syndrome’’ and orofacial pain failing to respond to a standard analgesic therapy. They also call attention to the possibility of negative serological assays or frequently negative tissue biopsy and synovial fluid culture in patients with active Lyme borreliosis. Heir and Fein (1998) pointed out the importance of a wide differential diagnostic list of orofacial and dental disorders; they also defined the epidemiological, clinical, diagnostic and treatment factors for Lyme borreliosis, which differentiate this from many other pathological conditions and functional disorders of the temporo-mandibular joint. These transient, cyclic or progressive functional disorders of the temporo-mandibular joint can be diagnosed using careful history and clinical examination: In Lyme borreliosis of the temporo-mandibular joint, intensive pain may be felt in the ears when chewing food or opening the mouth. However, arthritic signs present rarely and joint function is generally not affected. The pain is often cyclical and may last for two weeks with pauses with recurrences every 1 – 3 months. Vesper et al. (2001) were the first in Europe apart from Slovenia to report temporo-mandibular joint arthritis in a 49-year-old patient. The treatment with ceftriaxone proved to be successful. In Germany, where there are 40,000 – 80,000 persons diagnosed with Lyme borreliosis yearly; the joint involving form appeared in approximately 14% of patients, representing the European average (Cimmino, 1998). Although the Slovenian textbook of infectious diseases states that Lyme borreliosis may affect the TMT, relatively often many years of clinical practice as well as reports in the literature do not confirm this statement. The two cases described here represent a
ARTICLE IN PRESS 400 Journal of Cranio-Maxillofacial Surgery
rarity, but were not difficult to recognize in this endemic area. Isolation of B. burgdorferi from the synovial fluid was not performed as the procedure is rarely successful and was not feasible in these 2 patients. Early antibiotic treatment generally prevents the recurrent arthralgia. It is probably caused by persistence of borrelia in the synovia. The best outcome has been with ceftrixane-based parenteral antibiotic therapy. Treatment with highdose benzylpenicillin (20 MIU), doxicycline and amoxicilin at a dosage of 2 g/day for 2 – 4 weeks was successful as well (Lotricˇ-Furlan et al., 1999; Strle, 1999). The use of non-steroidal antirheumatic drugs seems reasonable, particularly at the outset when the pain is quite severe (Sˇibanc and Lesˇnicˇar, 2002). Chronic Lyme borreliosis is characterized by recurrences and relatively poor therapeutic response, since the causative agent is generally no longer present, while the autoimmune mechanisms, i.e. the presence of antigens stimulating the production of T-lymphocytes, are already active (Steere, 2001; Singh and Girschick, 2004). Local use of corticosteroids is not recommended, nor is arthroscopic synovectomy. No descriptions of cartilage and or bone erosion, periostitis, periarticular fibrous nodules and recurrent dislocations of the temporo-mandibular joint have been found in the literature whilst these have been described in long-lasting untreated chronic Lyme borreliosis-associated inflammations of large joints (Steere et al., 1987; Steere, 1993).
CONCLUSION Since only early treatment of Lyme borreliosis is successful, B. burgdorferi should always be taken into account in the differential diagnosis of temporomandibular joint pain.
References Cimmino MA: On behalf of the European community concerted action on risk assessment in Lyme borreliosis: relative frequency of Lyme borreliosis and of its clinical manifestations in Europea. Infection 26: 298–300, 1998 Harris RJ: Lyme disease involving the temporo-mandibular joint. J Oral Maxillofac Surg 46: 78–79, 1988 Heir GM: Differentiation of orofacial pain related to Lyme disease from other dental and facial pain disorders. Dent Clin North Am 41: 243–258, 1997
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Danijel Zˇerdoner, M.D. Ph.D., Assist. Prof. Department of Maxillofacial and Oral Surgery Celje Teaching Hospital Oblakova 5, SI-3000 Celje Slovenia Tel.: +386 3 4233150 Fax: +386 3 4233754 E-mail: [email protected] Paper received 17 January 2006 Accepted 8 June 2007