Acupuncture -

BASIC/CLINICAL SCIENCE Outbreak of Acupuncture-Associated Cutaneous Mycobacterium abscessus Infections Patrick Tang, Scott Walsh, Christian Murray, Cecilia Alterman, Monali Varia, George Broukhanski, Pamela Chedore, Joel DeKoven, Dalal Assaad, Wayne L. Gold, Danny Ghazarian, Michael Finkelstein, Marjolyn Pritchard, Barbara Yaffe, Frances Jamieson, Bonnie Henry, and Elizabeth Phillips Background: Cutaneous atypical mycobacterial infections have been increasingly described in association with cosmetic and alternative procedures. Objective: We report an outbreak of acupuncture-associated mycobacteriosis. Between April and December 2002, 32 patients developed cutaneous mycobacteriosis after visiting an acupuncture practice in Toronto, Canada. Results: Of 23 patients whose lesions were biopsied, 6 (26.1%) had culture-confirmed infection with Mycobacterium abscessus. These isolates were genetically indistinguishable by amplified fragment length polymorphism. The median incubation period was 1 month. Of 24 patients for whom clinical information was available, 23 (95.8%) had resolution of their infection. All patients developed residual scarring or hyperpigmentation. Conclusion: Nontuberculous Mycobacteria should be recognized as an emerging, but preventable, cause of acupuncture- associated infections. Antecedents: Les infections cutanees a mycobacteries atypiques sont de plus en plus decrites en lien avec des procedures ´ ´ ´ ` ´ ´ ´ cosmetiques et alternatives. ´ Objectif: Nous rapportons le cas d’une mycobacteriose causee par des traitements d’acuponcture. Entre avril et decembre 2002, ´ ´ ´ 32 patients ont contracte une mycobacteriose cutanee a la suite d’une visite a une clinique d’acuponcture a Toronto (Canada). ´ ´ ´ ` ` ` Resultats: Une biopsie a ete effectuee sur les lesions de 23 de ces patients. Parmi ce groupe, six (soit 26.1%) ont montre une ´ ´ ´ ´ ´ ´ infection a Mycobacterium abscessus. Il etait impossible de distinguer genetiquement ces isolats au moyen du polymorphisme de ` ´ ´ ´ longueur de fragments amplifies. La periode mediane d’incubation etait de 1 mois. Une resolution de l’infection a ete signalee chez 23 ´ ´ ´ ´ ´ ´ ´ ´ des 24 patients dont les renseignements cliniques etaient disponibles (soit 95.8%). Tous les patients ont developpe des cicatrices ´ ´ ´ residuelles ou de l’hyperpigmentation. ´ Conclusion: Les mycobacteries non tuberculeuses doivent etre reconnues comme cause emergente d’infections dues au ´ ˆ ´ traitement d’acuponcture. Toutefois, ces infections peuvent etre evitees. ˆ ´ ´ CUPUNCTURE has been an integral part of Chinese ; From the University of Toronto, Toronto, ON; Sunnybrook and Women’s College Health Sciences Centre, Toronto, ON; Toronto Public Health, Amedicine for over 4,000 years. Although considered a relatively safe procedure, acupuncture can be associated Toronto, ON; Canadian Field Epidemiology Program, Health Canada, Ottawa, ON; Central Public Health Laboratory, Toronto, ON; University with severe adverse events, ranging from pneumothorax Health Network, Toronto, ON; and BC Centre for Excellence in HIV/ and cardiac tamponade from improper needle placement AIDS, University of British Columbia, Vancouver, BC. ;to septicemia, endocarditis, or hepatitis from improperly sterilized needles.1–4 Recently, sporadic cases of infection with nontuberculous Mycobacteria (NTM) have also been reported.5,6 NTM infections have been associated with the use of < < contaminated products or inadequate infection control Address reprint requests to: Elizabeth Phillips, British Columbia Centre techniques during various cosmetic procedures. There = for Excellence in HIV/AIDS, St. Paul’s Hospital, 1081 Burrard Street, have been outbreaks of Mycobacterium fortuitum asso- > Vancouver, BC V6T 1B9; E-mail: ephillips@cfenet.ubc.ca. =ciated with8 footbaths,7 Mycobacterium chelonae from > DOI 10.2310/7750.2006.00041 liposuction, and Mycobacterium abscessus from augmen- Journal of Cutaneous Medicine and Surgery, Vol 10, No 4 (July/August), 2006: pp 000–000 1 Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:32 The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

2 Tang et al tation mammoplasty and injections of an unapproved attack rate of 19.0%. As one clinic was associated with alternative medication.9,10 We report herein an outbreak of a women’s health center, most of the patients were cutaneous M. abscessus in patients exposed to a single female (30 of 32; 93.8%). The median age was 49 years acupuncture practice in Toronto, Canada. (range 22–81 years). None of the patients were immuno- compromised. As many of the patients did not associate their skin Methods infections with the acupuncture, some continued to receive We conducted a retrospective case study of an outbreak of acupuncture treatments while they had lesions on their cutaneous M. abscessus infections at an acupuncture practice body. Of 22 patients for whom there were defined dates for in Toronto. All patients who attended either of two clinics termination of therapy and development of the skin lesions, attended by a single acupuncturist were contacted by the median incubation time was 1 month (range 0.5–5 Toronto Public Health. Clinical and demographic data were months). The median time to a correct diagnosis by a collected through patient interviews, clinical examination, physician was 3 months (range 0–6 months), as measured and retrospective chart reviews. Data were abstracted using a from the appearance of the first lesion to either skin biopsy standardized questionnaire. Suspect cases were defined as results verifying granulomatous inflammation or initiation patients who self-reported a skin infection (subcutaneous of appropriate antibiotic treatment. nodules, skin abscesses, cellulitis, or ulcers) located at the Skin biopsies were performed on 23 patients. insertion site of an acupuncture needle and lasting more Hematoxylin-eosin staining showed granulomatous than 2 weeks. Probable cases were those meeting the suspect inflammation in 21 patients (91.3%) and nonspecific case definition and diagnosed by a physician to have lesions chronic inflammation in 2 (8.7%). All of the biopsies compatible with M. abscessus infection. Confirmed cases showing granulomatous inflammation were suppurative in were those meeting the probable case definition and having nature, and none had evidence of caseation (Figure 1). In laboratory isolation of M. abscessus from a clinical specimen. one of the two patients with nonspecific inflammatory Skin punch biopsy specimens were sent to the Central lesions, therapy was initiated prior to biopsy. No speci- Public Health Laboratory (Ministry of Health and Long- mens submitted for culture were positive for acid-fast Term Care) for mycobacterial testing. Tissue specimens bacilli (AFB) by smear microscopy, but AFB were observed were homogenized and treated with N-acetyl-L-cysteine in one formalin-fixed specimen (4.3%). M. abscessus was NaOH. Smears were made from the treated homogenate isolated from the specimens of six patients (26.1%), but and stained with auramine-rhodamine. Samples were Mycobacteria could not be cultured from the one patient ¨ cultured for Mycobacteria on Lowenstein-Jensen media who was AFB positive by histology only. The mean growth and in Mycobacteria Growth Indicator Tubes (Becton time for the six isolates was 17.5 days (range 10–24 days). Dickinson, Sparks, MD). Mycolic acid analysis by high- performance liquid chromatography was used to speciate Mycobacteria isolates. Molecular typing of M. abscessus isolates was done by amplified fragment length polymorphism (AFLP).11 Antibiotic susceptibility was deter- mined by E-test.12 Routine bacterial and fungal cultures and pathology (hematoxylin-eosin and Ziehl-Neelsen stains) were performed at local hospital laboratories. The research ethics boards of the Sunnybrook and Women’s College Health Sciences Centre and Toronto Public Health approved this study. Results Between April 1 and December 16, 2002, 168 patients visited the two clinics. Of 32 patients (19.0%) meeting the case definition for acupuncture-associated M. abscessus Figure 1. Micrograph of a Mycobacterium abscessus lesion. Suppurative granulomatous inflammation with neutrophilic infiltrate. infection, 5 were suspect (15.6%), 21 were probable A giant cell is present in the lower right corner. Skin punch biopsy was (65.6%), and 6 were confirmed (18.8%) for an overall stained with hematoxylin and eosin (3200 original magnification). Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:33 The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

Outbreak of Acupuncture-Associated Cutaneous Mycobacterium abscessus Infections 3 All six isolates were clarithromycin susceptible but Sixteen patients (66.7%) received appropriate therapy; resistant to other antibiotics, including cefoxitin, cipro- 15 patients completed at least 6 months of oral floxacin, doxycycline, imipenem, and sulfamethoxazole clarithromycin (500 mg twice daily), and 1 patient and intermediate or resistant to amikacin. All six isolates completed 3 months of oral azithromycin (600 mg once were genetically indistinguishable by AFLP; clinical isolates daily). Two patients (8.3%) began taking clarithromycin of M. abscessus unrelated to this outbreak were distinct but discontinued after 10 and 30 days. One patient (4.2%) from one another and from the outbreak strain according chose naturopathic topical therapy, whereas five patients to AFLP. No other pathogenic bacteria or fungi were (20.8%) declined medical treatment. Overall, 23 patients isolated from the specimens. (95.8%) had clinical resolution. One patient continued to Of 24 patients for whom clinical information was have 12 active lesions distributed over the abdomen and available, 9 patients (37.5%) had 10 or more lesions. All extremities after 12 months of therapy with clarithromy- lesions developed over previous acupuncture sites (Figure cin. The patient’s age (47 years) was not significantly 2). These lesions began as erythematous papules that later different from the median age of 49 years. In this case, developed into large tender pustules over a period of there were no comorbidities or immunocompromising several weeks to months. Some of these pustules later factors, but tolerance and compliance with the antibiotic progressed into painful, ulceronodular lesions. Lesions therapy may have been an issue. Of the 16 patients who appeared mostly on the lower extremities (95.8% of completed antibiotic therapy, 15 (93.8%) had clinical patients), followed by the upper extremities (70.8% of resolution within 12 months. All of the eight patients who patients) and the trunk (50.0% of patients). None of the did not choose to receive or complete antibiotic therapy patients had systemic symptoms such as fever or malaise. had resolution of their infections within 12 months. One There were no cases of lymphangitic spread or dissemi- patient who did not receive antibiotic therapy required nated disease, and no patients required hospitalization. ´ surgical debridement of a single lesion. Residual scarring and/or hyperpigmentation was found in all 24 patients regardless of antibiotic therapy. After a minimum of 9 months of follow-up after the last acupuncture therapy, none of the 32 patients with cutaneous lesions had seroconversion to hepatitis B, hepatitis C, or human immunodeficiency virus (HIV). Discussion We describe an acupuncture-associated outbreak of M. abscessus cutaneous disease linked to the practice of a single acupuncturist. At the time a formal public health investigation of the acupuncturist’s clinics was carried out, the practice had already changed back to an acceptable standard (single-use needles); hence, much of the information implicating a breach in infection control was obtained historically. Interviews with the patients and acupuncturist revealed that there was reuse of needles and that needles were kept in a container of glutaraldehyde disinfectant prior to insertion. The glutaraldehyde solution was no longer available at the time of the investigation but was likely improperly diluted with tap water. Previously published reports of sporadic acupuncture-associated mycobacterial disease and contamination of medical supplies and instru- ments with Mycobacteria suggest that even transient breaches Figure 2. Cutaneous Mycobacterium abscessus lesions. A, Adjacent lesions at previous acupuncture sites on the leg. B, Symmetric lesions in infection control techniques can be significant owing to on both legs. the ubiquitous nature of NTM and their relative resistance to Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:40 The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

4 Tang et al alcohol, glutaraldehyde, and other common antiseptic 2. Leavy BR. Apparent adverse outcome of acupuncture. J Am Board solutions used in outpatient and hospital settings.5,13 Fam Pract 2002;15:246–8. 3. Shin HR, Kim JY, Kim JI, et al. Hepatitis B and C virus prevalence Our cluster of cases and other previously described in a rural area of South Korea: the role of acupuncture. Br J Cancer sporadic cases in the literature illustrate that NTM, such as 2002;87:314–8. M. abscessus, are an emerging, but preventable, cause of 4. Chung AB. Adverse effects of acupuncture. Which are clinically acupuncture-associated infections.5 Such infections may be significant? Can Fam Physician 2003;49:985–9. initially unrecognized by primary care physicians if exposure 5. Woo PC, Leung KW, Wong SS, et al. Relatively alcohol-resistant mycobacteria are emerging pathogens in patients receiving to acupuncture is not elicited as part of the medical history. acupuncture treatment. J Clin Microbiol 2002;40:1219–24. This could lead to unnecessary treatment with antibiotics 6. Ara M, de Santamaria CS, Zaballos P, et al. Mycobacterium known to be ineffective against NTM. However, the role of chelonae infection with multiple cutaneous lesions after treatment antibiotics against NTM in patients with localized cutaneous with acupuncture. Int J Dermatol 2003;42:642–4. lesions requires further study. In this outbreak, the rate of 7. Winthrop KL, Abrams M, Yakrus M, et al. An outbreak of mycobacterial furunculosis associated with footbaths at a nail clinical resolution after appropriate antibiotic therapy was salon. N Engl J Med 2002;346:1366–71. 93.8% (15 of 16 patients) at 12 months, whereas all of 8 8. Meyers H, Brown-Elliott BA, Moore D, et al. An outbreak of patients who did not receive or complete antibiotic therapy Mycobacterium chelonae infection following liposuction. Clin Infect also resolved their lesions at 12 months. Our study was Dis 2002;34:1500–7. inadequate for addressing the degree of the postinflamma- 9. Clegg HW, Foster MT, Sanders WE Jr, Baine WB. Infection due to tory hyperpigmentation and scarring with and without organisms of the Mycobacterium fortuitum complex after augmen- tation mammaplasty: clinical and epidemiologic features. J Infect antibiotic treatment. Finally, this outbreak also highlights the Dis 1983;147:427–33. importance of appropriate infection control practices and 10. Galil K, Miller LA, Yakrus MA, et al. Abscesses due to instrument sterilization in health care settings, including Mycobacterium abscessus linked to injection of unapproved those of alternative medical practitioners. alternative medication. Emerg Infect Dis 1999;5:681–7. 11. Valsangiacomo C, Baggi F, Gaia V, et al. Use of amplified fragment length polymorphism in molecular typing of Legionella pneumo- Acknowledgments phila and application to epidemiological studies. J Clin Microbiol 1995;33:1716–9. We thank Heather Rowe and Rebecca Stuart from Toronto 12. Woods GL, Bergmann JS, Witebsky FG, et al. Multisite Public Health for their assistance in database management. reproducibility of Etest for susceptibility testing of Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium fortuitum. J Clin Microbiol 2000;38:656–61. References 13. Manzoor SE, Lambert PA, Griffiths PA, et al. Reduced glutaraldehyde susceptibility in Mycobacterium chelonae associated with 1. Kao CL, Chang JP. Bilateral pneumothorax after acupuncture. J altered cell wall polysaccharides. J Antimicrob Chemother 1999;43: Emerg Med 2002;22:101–2. 759–65. Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:50 The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

Acupuncture -

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