1. 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
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cosmetiques et alternatives.
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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).
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Resultats: Une biopsie a ete effectuee sur les lesions de 23 de ces patients. Parmi ce groupe, six (soit 26.1%) ont montre une
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infection a Mycobacterium abscessus. Il etait impossible de distinguer genetiquement ces isolats au moyen du polymorphisme de
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longueur de fragments amplifies. La periode mediane d’incubation etait de 1 mois. Une resolution de l’infection a ete signalee chez 23
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des 24 patients dont les renseignements cliniques etaient disponibles (soit 95.8%). Tous les patients ont developpe des cicatrices
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residuelles ou de l’hyperpigmentation.
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Conclusion: Les mycobacteries non tuberculeuses doivent etre reconnues comme cause emergente d’infections dues au
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traitement d’acuponcture. Toutefois, ces infections peuvent etre evitees.
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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
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2. 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 poly-
morphism (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).
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3. 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 investiga-
tion 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
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4. 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.
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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.
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