4
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. Ante ´ ce ´ dents: Les infections cutane ´es a ` mycobacte ´ ries atypiques sont de plus en plus de ´ crites en lien avec des proce ´ dures cosme ´ tiques et alternatives. Objectif: Nous rapportons le cas d’une mycobacte ´ riose cause ´ e par des traitements d’acuponcture. Entre avril et de ´ cembre 2002, 32 patients ont contracte ´ une mycobacte ´ riose cutane ´e a ` la suite d’une visite a ` une clinique d’acuponcture a ` Toronto (Canada). Re ´ sultats: Une biopsie a e ´ te ´ effectue ´e sur les le ´ sions de 23 de ces patients. Parmi ce groupe, six (soit 26.1%) ont montre ´ une infection a ` Mycobacterium abscessus. Il e ´ tait impossible de distinguer ge ´ ne ´ tiquement ces isolats au moyen du polymorphisme de longueur de fragments amplifie ´ s. La pe ´ riode me ´ diane d’incubation e ´ tait de 1 mois. Une re ´ solution de l’infection a e ´ te ´ signale ´ e chez 23 des 24 patients dont les renseignements cliniques e ´ taient disponibles (soit 95.8%). Tous les patients ont de ´ veloppe ´ des cicatrices re ´ siduelles ou de l’hyperpigmentation. Conclusion: Les mycobacte ´ ries non tuberculeuses doivent e ˆ tre reconnues comme cause e ´ mergente d’infections dues au traitement d’acuponcture. Toutefois, ces infections peuvent e ˆtre e ´ vite ´ es. A CUPUNCTURE has been an integral part of Chinese medicine for over 4,000 years. Although considered a relatively safe procedure, acupuncture can be associated with severe adverse events, ranging from pneumothorax and cardiac tamponade from improper needle placement 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 techniques during various cosmetic procedures. There have been outbreaks of Mycobacterium fortuitum asso- ciated with footbaths, 7 Mycobacterium chelonae from liposuction, 8 and Mycobacterium abscessus from augmen- 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) ; < = > From the University of Toronto, Toronto, ON; Sunnybrook and Women’s College Health Sciences Centre, Toronto, ON; Toronto Public Health, Toronto, ON; Canadian Field Epidemiology Program, Health Canada, Ottawa, ON; Central Public Health Laboratory, Toronto, ON; University Health Network, Toronto, ON; and BC Centre for Excellence in HIV/ AIDS, University of British Columbia, Vancouver, BC. Address reprint requests to: Elizabeth Phillips, British Columbia Centre for Excellence in HIV/AIDS, St. Paul’s Hospital, 1081 Burrard Street, Vancouver, BC V6T 1B9; E-mail: [email protected]. DOI 10.2310/7750.2006.00041 Journal of Cutaneous Medicine and Surgery, Vol 10, No 4 (July/August), 2006: pp 000–000 1

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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

traitement d’acuponcture. Toutefois, ces infections peuvent etre evitees.

A CUPUNCTURE has been an integral part of Chinese

medicine for over 4,000 years. Although considered a

relatively safe procedure, acupuncture can be associated

with severe adverse events, ranging from pneumothorax

and cardiac tamponade from improper needle placement

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

techniques during various cosmetic procedures. There

have been outbreaks of Mycobacterium fortuitum asso-

ciated with footbaths,7 Mycobacterium chelonae from

liposuction,8 and Mycobacterium abscessus from augmen-

Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:32The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;;

<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<<

==========================================================

>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>>

From the University of Toronto, Toronto, ON; Sunnybrook and Women’s

College Health Sciences Centre, Toronto, ON; Toronto Public Health,

Toronto, ON; Canadian Field Epidemiology Program, Health Canada,

Ottawa, ON; Central Public Health Laboratory, Toronto, ON; University

Health Network, Toronto, ON; and BC Centre for Excellence in HIV/

AIDS, University of British Columbia, Vancouver, BC. ;

<Address reprint requests to: Elizabeth Phillips, British Columbia Centre

for Excellence in HIV/AIDS, St. Paul’s Hospital, 1081 Burrard Street,

Vancouver, BC V6T 1B9; E-mail: [email protected]. =>DOI 10.2310/7750.2006.00041

Journal of Cutaneous Medicine and Surgery, Vol 10, No 4 (July/August), 2006: pp 000–000 1

Patrick Tang
Patrick Tang
Patrick Tang
Patrick Tang
Page 2: Acupuncture -

tation mammoplasty and injections of an unapproved

alternative medication.9,10 We report herein an outbreak of

cutaneous M. abscessus in patients exposed to a single

acupuncture practice in Toronto, Canada.

Methods

We conducted a retrospective case study of an outbreak of

cutaneous M. abscessus infections at an acupuncture practice

in Toronto. All patients who attended either of two clinics

attended by a single acupuncturist were contacted by

Toronto Public Health. Clinical and demographic data were

collected through patient interviews, clinical examination,

and retrospective chart reviews. Data were abstracted using a

standardized questionnaire. Suspect cases were defined as

patients who self-reported a skin infection (subcutaneous

nodules, skin abscesses, cellulitis, or ulcers) located at the

insertion site of an acupuncture needle and lasting more

than 2 weeks. Probable cases were those meeting the suspect

case definition and diagnosed by a physician to have lesions

compatible with M. abscessus infection. Confirmed cases

were those meeting the probable case definition and having

laboratory isolation of M. abscessus from a clinical specimen.

Skin punch biopsy specimens were sent to the Central

Public Health Laboratory (Ministry of Health and Long-

Term Care) for mycobacterial testing. Tissue specimens

were homogenized and treated with N-acetyl-L-cysteine

NaOH. Smears were made from the treated homogenate

and stained with auramine-rhodamine. Samples were

cultured for Mycobacteria on Lowenstein-Jensen media

and in Mycobacteria Growth Indicator Tubes (Becton

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

infection, 5 were suspect (15.6%), 21 were probable

(65.6%), and 6 were confirmed (18.8%) for an overall

attack rate of 19.0%. As one clinic was associated with

a women’s health center, most of the patients were

female (30 of 32; 93.8%). The median age was 49 years

(range 22–81 years). None of the patients were immuno-

compromised.

As many of the patients did not associate their skin

infections with the acupuncture, some continued to receive

acupuncture treatments while they had lesions on their

body. Of 22 patients for whom there were defined dates for

termination of therapy and development of the skin lesions,

the median incubation time was 1 month (range 0.5–5

months). The median time to a correct diagnosis by a

physician was 3 months (range 0–6 months), as measured

from the appearance of the first lesion to either skin biopsy

results verifying granulomatous inflammation or initiation

of appropriate antibiotic treatment.

Skin biopsies were performed on 23 patients.

Hematoxylin-eosin staining showed granulomatous

inflammation in 21 patients (91.3%) and nonspecific

chronic inflammation in 2 (8.7%). All of the biopsies

showing granulomatous inflammation were suppurative in

nature, and none had evidence of caseation (Figure 1). In

one of the two patients with nonspecific inflammatory

lesions, therapy was initiated prior to biopsy. No speci-

mens submitted for culture were positive for acid-fast

bacilli (AFB) by smear microscopy, but AFB were observed

in one formalin-fixed specimen (4.3%). M. abscessus was

isolated from the specimens of six patients (26.1%), but

Mycobacteria could not be cultured from the one patient

who was AFB positive by histology only. The mean growth

time for the six isolates was 17.5 days (range 10–24 days).

Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:33The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

Figure 1. Micrograph of a Mycobacterium abscessus lesion.Suppurative granulomatous inflammation with neutrophilic infiltrate.A giant cell is present in the lower right corner. Skin punch biopsy wasstained with hematoxylin and eosin (3200 original magnification).

2 Tang et al

Page 3: Acupuncture -

All six isolates were clarithromycin susceptible but

resistant to other antibiotics, including cefoxitin, cipro-

floxacin, doxycycline, imipenem, and sulfamethoxazole

and intermediate or resistant to amikacin. All six isolates

were genetically indistinguishable by AFLP; clinical isolates

of M. abscessus unrelated to this outbreak were distinct

from one another and from the outbreak strain according

to AFLP. No other pathogenic bacteria or fungi were

isolated from the specimens.

Of 24 patients for whom clinical information was

available, 9 patients (37.5%) had 10 or more lesions. All

lesions developed over previous acupuncture sites (Figure

2). These lesions began as erythematous papules that later

developed into large tender pustules over a period of

several weeks to months. Some of these pustules later

progressed into painful, ulceronodular lesions. Lesions

appeared mostly on the lower extremities (95.8% of

patients), followed by the upper extremities (70.8% of

patients) and the trunk (50.0% of patients). None of the

patients had systemic symptoms such as fever or malaise.

There were no cases of lymphangitic spread or dissemi-

nated disease, and no patients required hospitalization.

Sixteen patients (66.7%) received appropriate therapy;

15 patients completed at least 6 months of oral

clarithromycin (500 mg twice daily), and 1 patient

completed 3 months of oral azithromycin (600 mg once

daily). Two patients (8.3%) began taking clarithromycin

but discontinued after 10 and 30 days. One patient (4.2%)

chose naturopathic topical therapy, whereas five patients

(20.8%) declined medical treatment. Overall, 23 patients

(95.8%) had clinical resolution. One patient continued to

have 12 active lesions distributed over the abdomen and

extremities after 12 months of therapy with clarithromy-

cin. The patient’s age (47 years) was not significantly

different from the median age of 49 years. In this case,

there were no comorbidities or immunocompromising

factors, but tolerance and compliance with the antibiotic

therapy may have been an issue. Of the 16 patients who

completed antibiotic therapy, 15 (93.8%) had clinical

resolution within 12 months. All of the eight patients who

did not choose to receive or complete antibiotic therapy

had resolution of their infections within 12 months. One

patient who did not receive antibiotic therapy required

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

in infection control techniques can be significant owing to

the ubiquitous nature of NTM and their relative resistance to

Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:40The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

Figure 2. Cutaneous Mycobacterium abscessus lesions. A, Adjacentlesions at previous acupuncture sites on the leg. B, Symmetric lesionson both legs.

Outbreak of Acupuncture-Associated Cutaneous Mycobacterium abscessus Infections 3

Page 4: Acupuncture -

alcohol, glutaraldehyde, and other common antiseptic

solutions used in outpatient and hospital settings.5,13

Our cluster of cases and other previously described

sporadic cases in the literature illustrate that NTM, such as

M. abscessus, are an emerging, but preventable, cause of

acupuncture-associated infections.5 Such infections may be

initially unrecognized by primary care physicians if exposure

to acupuncture is not elicited as part of the medical history.

This could lead to unnecessary treatment with antibiotics

known to be ineffective against NTM. However, the role of

antibiotics against NTM in patients with localized cutaneous

lesions requires further study. In this outbreak, the rate of

clinical resolution after appropriate antibiotic therapy was

93.8% (15 of 16 patients) at 12 months, whereas all of 8

patients who did not receive or complete antibiotic therapy

also resolved their lesions at 12 months. Our study was

inadequate for addressing the degree of the postinflamma-

tory hyperpigmentation and scarring with and without

antibiotic treatment. Finally, this outbreak also highlights the

importance of appropriate infection control practices and

instrument sterilization in health care settings, including

those of alternative medical practitioners.

Acknowledgments

We thank Heather Rowe and Rebecca Stuart from Toronto

Public Health for their assistance in database management.

References

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Journal of Cutaneous Medicine and Surgery JCM_2006_00041.3d 31/7/06 12:57:50The Charlesworth Group, Wakefield +44(0)1924 369598 - Rev 7.51n/W (Jan 20 2003)

4 Tang et al