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A mycobacterium malmoense infection of the hand presenting as carpal tunnel syndrome
A MYCOBACTERIUM HAND PRESENTING
MALMOENSE AS CARPAL
INFECTION OF THE TUNNEL SYNDROME
HEATHER PRINCE, PURVIN ISPAHANI and M. BAKER From the University Hospital, Nottingham We report an atypical tuberculous infection by Mycobacterium Malmoense of the synovium of the flexor tendons at the wrist presenting as carpal tunnel syndrome. This is the first time this organism has been described in a site other than the lungs or the cervical lymph nodes. Skeletal and articular tuberculosis usually result from reactivation of the original haematogenous seeding. Tuberculous tenosynovitis, although rare, presumably arises in a similar manner. The wrist and hand tendons are the commonest sites involved, and account for between 0.7% and 5% of all diagnosed synovial lesions (Feldman et al., 1971; Hodgson and Smith, 1972). The infection often presents in this region as a compound palmar ganglion with an associated carpal tunnel syndrome (Pimm and Waugh, 1957). In developed countries the incidence of infection caused by Mycobacterium tuberculosis has decreased, while that caused by opportunistic mycobacteria has become more common (Lancet, 1981; Grange and Yates, 1986). However, infections of the hand caused by these atypical mycobacteria are uncommon. Of those reported, M. marinum has been the most frequent agent (Cortez and Pankey, 1973; Williams and Riordan, 1973; Chow et al., 1983; Hurst et al., 1987). Other less frequent organisms reported have been M. kansasii (Kelly et al., 1979), A4. avium-intracellulare (Gunther et al., 1977), A4. terrae (Love and Melchior, 1985), M. fortuitum (Crick and Vandevelde, 1986) and M. chelonei (Stern and Gula, 1986). In 1977, Schroder and Juhlin described a new pathogenic species of mycobacterium which was isolated from four patients with pulmonary disease from the town of Malmo in Sweden; they called this organism M. Malmoense. Since then there have been other reports, mainly from the United Kingdom, of pulmonary infections in adults and cervical lymphadenitis in children (Jenkins, 1985; Banks et al., 1985); Connolly et al., 1985; France et al., 1987; Alberts et al., 1987). We report what we believe is the first case of M. Malmoense infection of the locomotor system. The patient presented with a severe carpal tunnel syndrome. This case illustrates the difficulty in diagnosis, resulting in delay in treatment. Case Report A 61-year-old widow presented to her General Practitioner in September 1985 with a two-month history of numbness and tingling in the right thumb, Received: 19 January 1988 Miss Heather Prince, F.R.C.S., Senior Lecturer in Orthopaedic Wood Orthopaedic Hospital, near Mansfield, Notts.
328
and Accident
Surgery,
Harlow
index and middle fingers. She was a known asthmatic and suffered from hypertension. For the former, she had been on prednisolone 5 mg daily for the last ten years and was using a ventolin inhaler. In March 1986 she was referred to the rheumatologists and a diagnosis of right carpal tunnel syndrome was made. A Futuro w&t splipt was prescribed and local corticosteroid was injected once into the right carpal tunnel, but her symptoms failed to improve and she was referred to the Hand Clinic where she was seen in February 1987. At that time she had loss of sensation in the median nerve distribution and wasting of the thenar muscles. In addition, there was an obvious fluctuant swelling on the volar aspect of the forearm, just proximal to the wrist, which was regarded as a compound ganglion. She was apyrexial, there was no lymphadenopathy and X-ray films of the wrist and hand were normal, except for soft tissue swelling. The white blood cell count was normal and the E.S.R. was 30 mm in the first hour. There was no past history of rheumatoid disease or tuberculosis. On 6 February 1987, under general anaesthesia, an extended decompression of the right carpal tunnel was performed. Gross cystic tenosynovitis was found, with numerous “rice bodies” and fraying of several of the flexor tendons to the wrist and fingers. To the naked eye, the appearance was that seen in rheumatoid disease, but tuberculosis was also considered as a possibility: therefore after synovectomy of the flexor tendons, specimens were sent for microbiology and histology. Clinically, at this stage, it was felt that the lesion was compatible with rheumatoid disease, but that tuberculosis was also a possibility. The histological appearances were those of a non-specific, severe, active, chronic synovitis, compatible with rheumatoid arthritis. All routine aerobic and anaerobic cultures as well as the initial smear for acid-fast bacilli were negative. The patient’s symptoms improved after the operation, but over the following two months the swelling recurred and the signs of median nerve compression recurred. Nine and a half weeks after surgery, a slow-growing mycobacterium was isolated from the original culture. The organism was sent to the Public Health Laboratory Service Mycobacterium Reference Unit in Cardiff for identification and sensitivity tests. THE JOURNAL OF HAND SURGERY
MYCOBACTERIUM
MALMOENSE
By June 1987, the patient had developed a large mass on the volar aspect of the right forearm and in the palm of the hand. A chest X-ray taken at this time was normal. On close questioning, it transpired that she was a keen gardener and there was a possible history of injury to the right thumb with a rose thorn in 1984. By July 1987, the Mycobacterium Reference Unit in Cardiff had identified the organism as M. Malmoense, resistant to isoniazid and pyrazinamide and partially resistant to streptomycin, but sensitive to rifampicin, ethambutol, ethionamide, capreomycin and cycloserine. A needle aspiration of the swelling was carried out on 23 July 1987. This yielded about 3 ml of turbid fluid which was sent for culture and microscopy. Despite a prolonged search acid-fast bacilli were not seen. Gramstains showed no bacteria and routine cultures remained negative. In view of the pronounced swelling of her wrist and the deterioration in median nerve function, on 17 August 1987 the wrist was re-explored: again gross tenosynovitis was found, with marked involvement and partial rupture of the flexor digitorum sublimis tendons to the index and ring fingers. An extensive tenosynovectomy was performed and the synovial tissue obtained was sent for further histological and microbiological studies. On this occasion, however, after an intensive search, acid-fast bacilli were seen on the initial smear, so on the following day, treatment with isoniazid, rifampicin, ethambutol and pyrazinamide was started. The clinical picture has steadily improved; when last seen in January 1988,20 weeks after surgery, the wound had healed, the swelling resolved and the median nerve sensation had recovered, although wasting of the thenar muscles was still evident. Almost 13 weeks after aspiration of the synovial fluid and nine weeks after the second surgical exploration, all specimens cultured for mycobacterium became positive. These isolates were once again identified as M. Malmoense by the Mycobacterium Reference Unit in Cardiff. Tissue sections from the first and second surgical explorations were reviewed, and the appearances, though not classical, were thought to be compatible with tuberculosis. Discussion It is important
to consider atypical mycobacterial infection in patients presenting with this combination of history and clinical picture, especially in patients who are immune-compromised or, as in this case, on steroid therapy. Unlike M. tuberculosis, which is an obligate pathogen, opportunistic mycobacteria are environmental saprophytes which are widely distributed in nature, and can be isolated from soil, water, vegetation and faeces . VOL. 13-B No. 3 AUGUST
1988
INFECTION
OF THE HAND
Infections of the hand caused by opportunistic mycobacteria usually follow the innoculation of the organisms into superficial abrasions, puncture wounds or cuts. So far, the natural reservoir of M. Mahoense remains unknown (Jenkins, 1985). However, it is possible that the organisms might have gained access into the hand of this patient following an injury with a rose thorn while gardening, as was the case in some other reports of infections by atypical mycobacteria (Love and Melchiar, 1985; Stern and Gula, 1986). The local injection of steroid into the carpal tunnel in this patient may have reactivated an already present organism introduced by the rose thorn. Clinically, mycobacterial tenosynovitis may closely mimic rheumatoid tenosynovitis. The correct diagnosis in this patient was delayed until some time afer the first surgical debridement, even though the tissues obtained were submitted for both culture and histopathological examination. The finding of acid-fast bacilli in stained smears is often the first bacteriological evidence of the presence of disease, but the success rate is dependent upon the number of organisms present per gram of tissue. In a recent report of extra pulmonary tuberculosis, direct smears for acid-fast bacilli were negative in all I9 patients with bone and joint tuberculosis, and culture was positive in only 12 (Alvarez and McCabe, 1984). M. Malmoense grows very slowly on primary culture, and it may take eight to ten weeks before the colonies are clearly visible (Jenkins, 1985). In 1979, we decided to incubate cultures for mycobacteria from all suspected specimens for twelve weeks, instead of six weeks, before discarding them as negative. The value of this change in policy is evident, in that not only would we have failed to isolate M. Malmoense from this patient but we would have missed the diagnosis in another three adults with pulmonary disease and three children with cervical lymphadenitis. Furthermore, the significance of the mycobacterium isolated from the tissues obtained at the time of the first debridement was in some doubt. The histological findings were not of the caseating granulomas typical of tuberculosis, but consisted of a mixture of acute and chronic inflammation, not unlike the findings in some other reports of infection with an atypical mycobacterium (Stern and Gula, 1986; Wood and Washington, 1987) Antimicrobial therapy for infections due to opportunistic mycobacteria depends upon the organism isolated and the disease process. Lymphadenitis in children and localised post-injection abscesses generally respond to surgery alone (Grange and Yates, 1986; Woods and Washington, 1987). In general, drug sensitivity tests have not proved helpful: combinations of drugs to which the bacilli are resistant in vitro may prove effective in vivo (Grange and Yates, 1986). The best 329
HEATHER PRINCE, PURVIN ISPAHANI AND M. BAKER
therapy for M. Malmoense is not known, but the most favourable response has been noted in those patients who received prolonged courses of ethambutol combined with other first line drugs (Banks et al., 1985; France et al., 1987). Some opportunistic mycobacteria are fastidious, and for their isolation may require a prolonged incubation (M. Malrnoense), incubation at a lower temperature (M. marinum), or addition of haemin to the medium (M. haemophilum). Therefore, specimens which may contain these organisms are unlikely to be isolated if the request card simply states ‘for TB cultures please’. The key to success is good communication between the surgeon and the microbiologist. References ALBERTS W. M., CHANDLER K. W., SOLOMON D. A., and GOLDMAN A.L. (1987). Pulmonary disease caused by Mycobacterium malmoense. American Review of Respiratory Diseases 135: 13751378. ALVAREZ S. and MCCABE W. R. (1984). Extrapulmonary Tuberculosis Revisited: A review of experience at Boston City and other hospitals. Medicine, 63: 25-55. BANKS J., JENKINS P. A. and SMITH A. P. (1985). Pulmonary infection with Mycobacterium malmoense - a review of treatment and response. Tubercle 66: 197203. CHOW S. P., STROEBEL A. B., LAU J. H. K. and COLLINS R. J. (1983). Mycobacterium marinum infections of the hand involving deep structures. Journal of Hand Surgery 8A: 5: (1); 568-573. CONNOLLY M. J., MAGEE J. G., HENDRICK D. J. and JENKINS P. A. (1985). Mycobacterium malmoense in the north-east of England. Tubercle, 66: 211-217. CORTEZ L. M. and PANKEY G. A. (1973). Mycobacterium ma&urn infections of the hand. Journal of Bone and Joint Surgery, 55A: 363-370.
330
CRICK J. C. and VANDEVELDE A. G. (1986). Mycobacterium fortuitum midpalmar space abscess: a case report. Journal of Hand Surgery 11A: 3: 438-440. FELDMAN F., AUERBACK R. and JOHNSTON A. (1971). Tuberculous dactylitis in the adult. American Journal of Rheumatology, 112: 460. FRANCE A. J., McLEOD D. T., CALDER M. A. and SEATON, A. (1987). Mycobacterium malmoense infections in Scotland: an increasing problem. Thorax, 42: 8: 593-595. GRANGE J. M. and YATES M. D. (1986). Infections caused by opportunist mycobacteria: a review. Journal of Royal Society of Medicine, 79: 4: 226-229. GUNTHER S. F., ELLIOT R. C., BRAND R. L. and ADAMS J. P. (1977). Experience with atypical mycobacterial infection in the deep structures of the hand. Journal of Hand Surgery, 2A: 2: 90-96. HODGSON A. P. and SMITH T. K. (1972). Tuberculosis of the wrist with a note on chemotherapy. Clinical Orthopaedics, 83: 73-83. HURST L. C., AMADIO P. C., BADALAMENTE M. A., ELLSTEIN J. L. and DATTWYLER R. J. (1987). Mycobacterium marinum infections of the hand. Journal of Hand Surgery, 12A: 3: 428-435. JENKINS P. A. (1985). Mycobacterium malmoense. Tubercle, 66: 193-195. KELLY P. J., KARLSON A. G., WEED L. A. and LIPSCOMB P. R. (1967). Infection of the synovial tissues by micobacteria other than Mycobacterium tuberculosis. Journal of Bone and Joint Surgery, 49A: 1521-1530. LANCET: EDITORIAL (1981). Opportunistic mycobacterium. Lancet 1: 424-425. LOVE G. L. and MELCHIOR E. (1985). Mycobacterium terrae tenosynovitis. Journal of Hand Surgery, 1OA: 730-732. MALES B. M., WEST T. E. and BARTHOLOMEW W. R. (1987). Mycobacterium haemophilum infection in a patient with acquired immune deficiency syndrome. Journal of Clinical Microbiology, 25: 186-190. PIMM L. H. and WAUGH W. A. (1957). Tuberculous tenosynovitis. Journal of Bone and Joint Surgery, 39B: 91-101. SCHRODER K. H. and JUHLIN I. (1977). Mycobacterium malmoense sp. nov.International Journal of Systematic Bacteriology, 27: 241-246. STERN P. J. and GULA D. C. (1986). Mycobacterium chelonei tenosynovitis of the hand: A case report. Journal of Hand Surgery, 11A: 4: 596-599. WILLIAMS C. S. and -RIORDAN D. C. (1973). Mycobacterium marinum (atypical acid fast bacillus) infections of the hand: a report of six cases. Journal of Bone and Joint Surgery, 55A: 1042-1050. WOODS G. L. and WASHINGTON J. A. (1987). Mycobacteria other than mycobacterium tuberculosis: review of microbiological and clinical aspects. Reviews of Infectious Diseases, 9: 2: 275-294.
THE JOURNAL OF HAND SURGERY
MALMOENSE AS CARPAL
INFECTION OF THE TUNNEL SYNDROME
HEATHER PRINCE, PURVIN ISPAHANI and M. BAKER From the University Hospital, Nottingham We report an atypical tuberculous infection by Mycobacterium Malmoense of the synovium of the flexor tendons at the wrist presenting as carpal tunnel syndrome. This is the first time this organism has been described in a site other than the lungs or the cervical lymph nodes. Skeletal and articular tuberculosis usually result from reactivation of the original haematogenous seeding. Tuberculous tenosynovitis, although rare, presumably arises in a similar manner. The wrist and hand tendons are the commonest sites involved, and account for between 0.7% and 5% of all diagnosed synovial lesions (Feldman et al., 1971; Hodgson and Smith, 1972). The infection often presents in this region as a compound palmar ganglion with an associated carpal tunnel syndrome (Pimm and Waugh, 1957). In developed countries the incidence of infection caused by Mycobacterium tuberculosis has decreased, while that caused by opportunistic mycobacteria has become more common (Lancet, 1981; Grange and Yates, 1986). However, infections of the hand caused by these atypical mycobacteria are uncommon. Of those reported, M. marinum has been the most frequent agent (Cortez and Pankey, 1973; Williams and Riordan, 1973; Chow et al., 1983; Hurst et al., 1987). Other less frequent organisms reported have been M. kansasii (Kelly et al., 1979), A4. avium-intracellulare (Gunther et al., 1977), A4. terrae (Love and Melchior, 1985), M. fortuitum (Crick and Vandevelde, 1986) and M. chelonei (Stern and Gula, 1986). In 1977, Schroder and Juhlin described a new pathogenic species of mycobacterium which was isolated from four patients with pulmonary disease from the town of Malmo in Sweden; they called this organism M. Malmoense. Since then there have been other reports, mainly from the United Kingdom, of pulmonary infections in adults and cervical lymphadenitis in children (Jenkins, 1985; Banks et al., 1985); Connolly et al., 1985; France et al., 1987; Alberts et al., 1987). We report what we believe is the first case of M. Malmoense infection of the locomotor system. The patient presented with a severe carpal tunnel syndrome. This case illustrates the difficulty in diagnosis, resulting in delay in treatment. Case Report A 61-year-old widow presented to her General Practitioner in September 1985 with a two-month history of numbness and tingling in the right thumb, Received: 19 January 1988 Miss Heather Prince, F.R.C.S., Senior Lecturer in Orthopaedic Wood Orthopaedic Hospital, near Mansfield, Notts.
328
and Accident
Surgery,
Harlow
index and middle fingers. She was a known asthmatic and suffered from hypertension. For the former, she had been on prednisolone 5 mg daily for the last ten years and was using a ventolin inhaler. In March 1986 she was referred to the rheumatologists and a diagnosis of right carpal tunnel syndrome was made. A Futuro w&t splipt was prescribed and local corticosteroid was injected once into the right carpal tunnel, but her symptoms failed to improve and she was referred to the Hand Clinic where she was seen in February 1987. At that time she had loss of sensation in the median nerve distribution and wasting of the thenar muscles. In addition, there was an obvious fluctuant swelling on the volar aspect of the forearm, just proximal to the wrist, which was regarded as a compound ganglion. She was apyrexial, there was no lymphadenopathy and X-ray films of the wrist and hand were normal, except for soft tissue swelling. The white blood cell count was normal and the E.S.R. was 30 mm in the first hour. There was no past history of rheumatoid disease or tuberculosis. On 6 February 1987, under general anaesthesia, an extended decompression of the right carpal tunnel was performed. Gross cystic tenosynovitis was found, with numerous “rice bodies” and fraying of several of the flexor tendons to the wrist and fingers. To the naked eye, the appearance was that seen in rheumatoid disease, but tuberculosis was also considered as a possibility: therefore after synovectomy of the flexor tendons, specimens were sent for microbiology and histology. Clinically, at this stage, it was felt that the lesion was compatible with rheumatoid disease, but that tuberculosis was also a possibility. The histological appearances were those of a non-specific, severe, active, chronic synovitis, compatible with rheumatoid arthritis. All routine aerobic and anaerobic cultures as well as the initial smear for acid-fast bacilli were negative. The patient’s symptoms improved after the operation, but over the following two months the swelling recurred and the signs of median nerve compression recurred. Nine and a half weeks after surgery, a slow-growing mycobacterium was isolated from the original culture. The organism was sent to the Public Health Laboratory Service Mycobacterium Reference Unit in Cardiff for identification and sensitivity tests. THE JOURNAL OF HAND SURGERY
MYCOBACTERIUM
MALMOENSE
By June 1987, the patient had developed a large mass on the volar aspect of the right forearm and in the palm of the hand. A chest X-ray taken at this time was normal. On close questioning, it transpired that she was a keen gardener and there was a possible history of injury to the right thumb with a rose thorn in 1984. By July 1987, the Mycobacterium Reference Unit in Cardiff had identified the organism as M. Malmoense, resistant to isoniazid and pyrazinamide and partially resistant to streptomycin, but sensitive to rifampicin, ethambutol, ethionamide, capreomycin and cycloserine. A needle aspiration of the swelling was carried out on 23 July 1987. This yielded about 3 ml of turbid fluid which was sent for culture and microscopy. Despite a prolonged search acid-fast bacilli were not seen. Gramstains showed no bacteria and routine cultures remained negative. In view of the pronounced swelling of her wrist and the deterioration in median nerve function, on 17 August 1987 the wrist was re-explored: again gross tenosynovitis was found, with marked involvement and partial rupture of the flexor digitorum sublimis tendons to the index and ring fingers. An extensive tenosynovectomy was performed and the synovial tissue obtained was sent for further histological and microbiological studies. On this occasion, however, after an intensive search, acid-fast bacilli were seen on the initial smear, so on the following day, treatment with isoniazid, rifampicin, ethambutol and pyrazinamide was started. The clinical picture has steadily improved; when last seen in January 1988,20 weeks after surgery, the wound had healed, the swelling resolved and the median nerve sensation had recovered, although wasting of the thenar muscles was still evident. Almost 13 weeks after aspiration of the synovial fluid and nine weeks after the second surgical exploration, all specimens cultured for mycobacterium became positive. These isolates were once again identified as M. Malmoense by the Mycobacterium Reference Unit in Cardiff. Tissue sections from the first and second surgical explorations were reviewed, and the appearances, though not classical, were thought to be compatible with tuberculosis. Discussion It is important
to consider atypical mycobacterial infection in patients presenting with this combination of history and clinical picture, especially in patients who are immune-compromised or, as in this case, on steroid therapy. Unlike M. tuberculosis, which is an obligate pathogen, opportunistic mycobacteria are environmental saprophytes which are widely distributed in nature, and can be isolated from soil, water, vegetation and faeces . VOL. 13-B No. 3 AUGUST
1988
INFECTION
OF THE HAND
Infections of the hand caused by opportunistic mycobacteria usually follow the innoculation of the organisms into superficial abrasions, puncture wounds or cuts. So far, the natural reservoir of M. Mahoense remains unknown (Jenkins, 1985). However, it is possible that the organisms might have gained access into the hand of this patient following an injury with a rose thorn while gardening, as was the case in some other reports of infections by atypical mycobacteria (Love and Melchiar, 1985; Stern and Gula, 1986). The local injection of steroid into the carpal tunnel in this patient may have reactivated an already present organism introduced by the rose thorn. Clinically, mycobacterial tenosynovitis may closely mimic rheumatoid tenosynovitis. The correct diagnosis in this patient was delayed until some time afer the first surgical debridement, even though the tissues obtained were submitted for both culture and histopathological examination. The finding of acid-fast bacilli in stained smears is often the first bacteriological evidence of the presence of disease, but the success rate is dependent upon the number of organisms present per gram of tissue. In a recent report of extra pulmonary tuberculosis, direct smears for acid-fast bacilli were negative in all I9 patients with bone and joint tuberculosis, and culture was positive in only 12 (Alvarez and McCabe, 1984). M. Malmoense grows very slowly on primary culture, and it may take eight to ten weeks before the colonies are clearly visible (Jenkins, 1985). In 1979, we decided to incubate cultures for mycobacteria from all suspected specimens for twelve weeks, instead of six weeks, before discarding them as negative. The value of this change in policy is evident, in that not only would we have failed to isolate M. Malmoense from this patient but we would have missed the diagnosis in another three adults with pulmonary disease and three children with cervical lymphadenitis. Furthermore, the significance of the mycobacterium isolated from the tissues obtained at the time of the first debridement was in some doubt. The histological findings were not of the caseating granulomas typical of tuberculosis, but consisted of a mixture of acute and chronic inflammation, not unlike the findings in some other reports of infection with an atypical mycobacterium (Stern and Gula, 1986; Wood and Washington, 1987) Antimicrobial therapy for infections due to opportunistic mycobacteria depends upon the organism isolated and the disease process. Lymphadenitis in children and localised post-injection abscesses generally respond to surgery alone (Grange and Yates, 1986; Woods and Washington, 1987). In general, drug sensitivity tests have not proved helpful: combinations of drugs to which the bacilli are resistant in vitro may prove effective in vivo (Grange and Yates, 1986). The best 329
HEATHER PRINCE, PURVIN ISPAHANI AND M. BAKER
therapy for M. Malmoense is not known, but the most favourable response has been noted in those patients who received prolonged courses of ethambutol combined with other first line drugs (Banks et al., 1985; France et al., 1987). Some opportunistic mycobacteria are fastidious, and for their isolation may require a prolonged incubation (M. Malrnoense), incubation at a lower temperature (M. marinum), or addition of haemin to the medium (M. haemophilum). Therefore, specimens which may contain these organisms are unlikely to be isolated if the request card simply states ‘for TB cultures please’. The key to success is good communication between the surgeon and the microbiologist. References ALBERTS W. M., CHANDLER K. W., SOLOMON D. A., and GOLDMAN A.L. (1987). Pulmonary disease caused by Mycobacterium malmoense. American Review of Respiratory Diseases 135: 13751378. ALVAREZ S. and MCCABE W. R. (1984). Extrapulmonary Tuberculosis Revisited: A review of experience at Boston City and other hospitals. Medicine, 63: 25-55. BANKS J., JENKINS P. A. and SMITH A. P. (1985). Pulmonary infection with Mycobacterium malmoense - a review of treatment and response. Tubercle 66: 197203. CHOW S. P., STROEBEL A. B., LAU J. H. K. and COLLINS R. J. (1983). Mycobacterium marinum infections of the hand involving deep structures. Journal of Hand Surgery 8A: 5: (1); 568-573. CONNOLLY M. J., MAGEE J. G., HENDRICK D. J. and JENKINS P. A. (1985). Mycobacterium malmoense in the north-east of England. Tubercle, 66: 211-217. CORTEZ L. M. and PANKEY G. A. (1973). Mycobacterium ma&urn infections of the hand. Journal of Bone and Joint Surgery, 55A: 363-370.
330
CRICK J. C. and VANDEVELDE A. G. (1986). Mycobacterium fortuitum midpalmar space abscess: a case report. Journal of Hand Surgery 11A: 3: 438-440. FELDMAN F., AUERBACK R. and JOHNSTON A. (1971). Tuberculous dactylitis in the adult. American Journal of Rheumatology, 112: 460. FRANCE A. J., McLEOD D. T., CALDER M. A. and SEATON, A. (1987). Mycobacterium malmoense infections in Scotland: an increasing problem. Thorax, 42: 8: 593-595. GRANGE J. M. and YATES M. D. (1986). Infections caused by opportunist mycobacteria: a review. Journal of Royal Society of Medicine, 79: 4: 226-229. GUNTHER S. F., ELLIOT R. C., BRAND R. L. and ADAMS J. P. (1977). Experience with atypical mycobacterial infection in the deep structures of the hand. Journal of Hand Surgery, 2A: 2: 90-96. HODGSON A. P. and SMITH T. K. (1972). Tuberculosis of the wrist with a note on chemotherapy. Clinical Orthopaedics, 83: 73-83. HURST L. C., AMADIO P. C., BADALAMENTE M. A., ELLSTEIN J. L. and DATTWYLER R. J. (1987). Mycobacterium marinum infections of the hand. Journal of Hand Surgery, 12A: 3: 428-435. JENKINS P. A. (1985). Mycobacterium malmoense. Tubercle, 66: 193-195. KELLY P. J., KARLSON A. G., WEED L. A. and LIPSCOMB P. R. (1967). Infection of the synovial tissues by micobacteria other than Mycobacterium tuberculosis. Journal of Bone and Joint Surgery, 49A: 1521-1530. LANCET: EDITORIAL (1981). Opportunistic mycobacterium. Lancet 1: 424-425. LOVE G. L. and MELCHIOR E. (1985). Mycobacterium terrae tenosynovitis. Journal of Hand Surgery, 1OA: 730-732. MALES B. M., WEST T. E. and BARTHOLOMEW W. R. (1987). Mycobacterium haemophilum infection in a patient with acquired immune deficiency syndrome. Journal of Clinical Microbiology, 25: 186-190. PIMM L. H. and WAUGH W. A. (1957). Tuberculous tenosynovitis. Journal of Bone and Joint Surgery, 39B: 91-101. SCHRODER K. H. and JUHLIN I. (1977). Mycobacterium malmoense sp. nov.International Journal of Systematic Bacteriology, 27: 241-246. STERN P. J. and GULA D. C. (1986). Mycobacterium chelonei tenosynovitis of the hand: A case report. Journal of Hand Surgery, 11A: 4: 596-599. WILLIAMS C. S. and -RIORDAN D. C. (1973). Mycobacterium marinum (atypical acid fast bacillus) infections of the hand: a report of six cases. Journal of Bone and Joint Surgery, 55A: 1042-1050. WOODS G. L. and WASHINGTON J. A. (1987). Mycobacteria other than mycobacterium tuberculosis: review of microbiological and clinical aspects. Reviews of Infectious Diseases, 9: 2: 275-294.
THE JOURNAL OF HAND SURGERY