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J Clin Microbiol. Apr 2002; 40(4): 1219–1224.
PMCID: PMC140401

Relatively Alcohol-Resistant Mycobacteria Are Emerging Pathogens in Patients Receiving Acupuncture Treatment

Abstract

Acupuncture has been gaining popularity as a form of alternative medicine. In the past, only blood-borne viruses and anecdotal reports of bacterial infections have been associated with acupuncture. We report on four patients with mycobacterial infections complicating acupuncture who were encountered in a 2-year period. All had clinical and/or radiological lesions at acupuncture point- and meridian-specific locations. There was no other history of trauma or other clinical foci of infections, and the chest radiographs were normal. Histological studies of biopsy specimens of all four patients showed changes compatible with chronic inflammation, with granulomatous inflammation present in three patients and acid-fast bacilli present in two. Conventional biochemical tests and whole-cell fatty acid analysis for identification were inconclusive for all four nonpigmented mycobacteria recovered from tissue biopsies. 16S rRNA gene sequencing showed that the strains from two patients were Mycobacterium chelonae and that those from the other two were Mycobacterium nonchromogenicum. Alcohol resistance assay using the quantitative suspension test revealed that all four strains showed prolonged survival in 75% alcohol compared to other skin flora. Mycobacterial infections transmitted by acupuncture are an emerging problem. A high index of suspicion is essential to recognize this clinical syndrome, and strict implementation of proper infection control guidelines for acupuncture is mandatory.

Acupuncture has been gaining popularity as a form of alternative medicine in both Asian and Western countries for chronic pain problems, digestive disorders, allergic disorders, psychosomatic problems, menstrual disorders, and drug and alcohol rehabilitation. However, in most countries, monitoring and control over the practice and its associated complications are far from adequate. Although infection control guidelines for acupuncture are available (1), the implementation, especially in developing countries where acupuncture is very popular, is far from ideal. In the past, needles used for acupuncture were usually reused and often inadequately sterilized. Such inadequate disinfection has led to the transmission of infectious diseases from patient to patient. The best-documented acupuncture-transmitted microorganisms are the blood-borne viruses, including human immunodeficiency virus, hepatitis B virus, and hepatitis C virus (13, 32, 44). Apart from blood-borne infections due to patient-to-patient transmission, acupuncture can also be complicated by infections caused by environmental microorganisms or the patient's own skin flora, as the most commonly used skin disinfectant in acupuncture clinics is alcohol. There have been case reports of such bacterial infections as well as abscess formation without proven microbiological causes complicating acupuncture (4, 10, 11, 12, 14, 16, 19, 24, 26, 45).

Mycobacteria are well known to be relatively resistant to disinfectants, and the mechanism of disinfectant resistance has been described for some mycobacteria (18). Outbreaks of infections caused by mycobacteria resistant to disinfectants are of great concern (9). In the past, there has been no report on mycobacterial infections complicating acupuncture in the English literature (based on a MEDLINE search covering 1966 to 2000). Recently, we reported the first case of Mycobacterium chelonae skin and soft tissue infection transmitted by acupuncture (41). In the present study, we report the clinical and microbiological characteristics of three additional cases of mycobacterial infections complicating acupuncture. The characteristic sites of infection in relation to acupuncture points are discussed, and the degree of resistance of the corresponding isolates to alcohol was ascertained.

MATERIALS AND METHODS

Patients and microbiological methods.

The four patients described in this report were hospitalized at the Queen Mary Hospital in Hong Kong during a 2-year period (1999 to 2000). All clinical data were collected prospectively as described previously (17). Clinical specimens were collected and handled according to standard protocols for culture of aerobic and anaerobic bacteria, fungi, and mycobacteria, and all suspect colonies were identified by standard conventional biochemical methods (21).

Whole-cell fatty acid analysis by gas chromatography.

A 5890A gas chromatograph (Hewlett-Packard, Avondale, Pa.) equipped with the Microbial Identification System (MIDI Inc.) was used for matching the test organism with the built-in standard Microbial Identification System library. A similarity index, which expresses how close the fatty acid composition of the test isolate is to that of the standard library, was calculated. A similarity index of 0.6 to 1.0 is an excellent match, that of 0.3 to less than 0.6 is a fairly good match, and that of less than 0.3 indicates that the organism does not match well with any of the organisms in the standard library.

PCR, gel electrophoresis, and 16S rRNA gene sequencing.

Bacterial DNA extraction, PCR amplification, and DNA sequencing of the 16S rRNA gene were performed as described previously (6, 34, 35, 36, 38, 39, 40, 42, 43). Briefly, 1 U of DNase I (Pharmacia, Uppsala, Sweden) was added to 40 μl of distilled water or PCR master mix (which contains deoxynucleoside triphosphates, PCR buffer, and Taq polymerase). The mixture was incubated at 25°C for 15 min and subsequently at 95°C for 10 min to inactivate the DNase I. The bacterial DNA extract and control were amplified with 0.5 μM primers (LPW81, 5′-TGGCGAACGGGTGAGTAA-3′; LPW58, 5′-AGGCCCGGGAACGTATTCAC-3′) (Gibco BRL, Rockville, Md.) as described previously (43). The PCR mixture (50 μl) contained bacterial DNA, PCR buffer (10 mM Tris-HCl [pH 8.3], 50 mM KCl, 2 mM MgCl2, and 0.01% gelatin), a 200 μM concentration of each deoxynucleoside triphosphate, and 1.0 U of Taq polymerase (Boehringer, Mannheim, Germany). The mixtures were amplified with 40 cycles of 94°C for 1 min, 55°C for 1 min, and 72°C for 2 min, with a final extension at 72°C for 10 min, in an automated thermal cycler (Perkin-Elmer Cetus, Gouda, The Netherlands). DNase I-treated distilled water was used as the negative control. Ten microliters of each amplified product was electrophoresed in a 1.5% (wt/vol) agarose gel with a molecular size marker ([var phi]X174 HaeIII digest; Boehringer) in Tris-borate-EDTA buffer at 100 V for 1.5 h.

Both strands of the PCR product were sequenced twice with an ABI 377 automated sequencer according to the instructions of the manufacturer (Perkin-Elmer, Foster City, Calif.), using the PCR primers LPW81 and LPW58 and additional primers designed from the sequencing data from the first and second rounds of the sequencing reaction (LPW99, 5′-TTACTGGGCGTAAAGAGC-3′; LPW100, 5′-TAATCCACATGCTCCGCC-3′; LPW102, 5′-GCTCTTTACGCCCAGTAA-3′; and LPW103, 5′-GGCGGAGCATGTGGATTA-3′). The sequences of the PCR products were compared with known 16S rRNA gene sequences in GenBank by multiple-sequence alignment using the CLUSTAL W program (31), and phylogenetic tree construction was performed using the PileUp method with GrowTree (Genetics Computer Group, Inc.).

Alcohol resistance assay.

The resistances of the four strains of mycobacteria to killing by 75% alcohol were compared to those of Mycobacterium smegmatis (ATCC 14469), Staphylococcus epidermidis (ATCC 14990), and Corynebacterium jeikeium (ATCC 43216) by using the quantitative suspension test (2). For each sample, 1 ml of bacteria at McFarland standard 4 was added to 9 ml of 83% (vol/vol) alcohol or sterile water (control). After thorough mixing, the mixture was incubated at room temperature. At 5-s intervals for 60 s, 1 ml of the mixture was transferred to 9 ml of brain heart infusion broth. The resultant mixture was serially diluted and plated out in duplicate. For each strain, the test was performed five times, and the times taken for the strains to achieve a 5-log10-unit reduction in bacterial counts were compared using one-way analysis of variance.

RESULTS

Patient characteristics.

During the 2-year period, a total of four patients with mycobacterial infections complicating acupuncture were encountered. The clinical details for patient 1 have been reported previously (41). The characteristics of the four patients are summarized in Table Table1.1. The interval between the first session of acupuncture and the development of symptoms ranged from 1 month to 1 year. Patient 2 developed an erythematous induration over the left ankle after acupuncture at the BL 60 (Kunlun) acupuncture point along the bladder meridian. Patients 3 and 4 developed right and left wrist tenosynovitis, respectively, after acupunture at the HT 7 (Shenmen) and PC 7 (Daling) acupuncture points along the heart and pericardium meridians, respectively. Magnetic resonance imaging (MRI) of the left wrist of patient 4 showed fluid-distended sheaths that invested the long flexor tendons, i.e., flexor digitorum superficialis and profundus and flexor pollicis longus. After intravenous gadolinium injection, strong enhancement of the thickened synovial lining of the synovial sheaths and the surface of the flexor tendons was noted, which is typical of tenosynovitis. There was no other trauma or other clinical foci of infections, and the chest radiographs of all four patients were normal. Histological studies of the biopsy specimens of all four patients showed changes compatible with chronic inflammation, with granulomatous inflammation present in three patients (patients 1, 3, and 4) and tests for acid-fast bacilli positive in two patients (patients 1 and 2). All four patients responded to 3 to 6 months of antimycobacterial therapy.

TABLE 1.
Characteristics of patients with mycobacterial infections complicating acupuncture

Conventional phenotypic characteristics.

Cultures of the tissue biopsies for aerobic and anaerobic pyogenic bacteria and fungi were negative. Nonpigmented colonies of acid-fast bacilli were observed on Lowenstein-Jensen medium after 7 to 28 days of incubation at 37°C. Conventional phenotypic tests failed to reveal a pattern identical to that of any known Mycobacterium species.

Whole-cell fatty acid analysis by gas chromatography.

Whole-cell fatty acid analysis of the nonpigmented Mycobacterium isolates from patients 1, 2, 3, and 4 was equivocal. The best matches for the four isolates were M. chelonae (similarity index, 0.500), M. chelonae (similarity index, 0.528), M. nonchromogenicum (similarity index, 0.506), and M. nonchromogenicum (similarity index, 0.475), respectively.

16S rRNA gene sequencing.

PCR of the 16S rRNA genes of the four isolates showed bands of about 1,280 bp. There was one base difference between the 16S rRNA gene sequences of isolates 1 and 2 and that of M. chelonae (GenBank accession number M29559), indicating that isolates 1 and 2 were M. chelonae by this “gold standard” (Fig. (Fig.1).1). There were 6 and 10 base differences between the 16S rRNA gene sequences of isolates 3 and 4, respectively, and that of M. nonchromogenicum (GenBank accession number X52928), indicating that isolates 3 and 4 were M. nonchromogenicum by this gold standard (Fig. (Fig.11).

FIG. 1.
Phylogenetic tree showing the relationship of the four isolates to related species. The tree was inferred from 16S rRNA sequence data by the neighbor-joining method. The scale bar indicates the estimated number of substitutions per 100 bases, using the ...

Alcohol resistance assay.

The survival of the four strains of mycobacteria, M. smegmatis, S. epidermidis, and C. jeikeium after incubation with 75% alcohol is shown in Fig. Fig.2.2. The times (mean ± standard error of the mean) for a 5-log10-unit reduction in bacterial counts for isolate 1 (29.0 ± 0.05 s), isolate 2 (17.5 ± 0.16 s), isolate 3 (27.5 ± 0.16 s), and isolate 4 (28.9 ± 0.10 s) were significantly longer than those for M. smegmatis, S. epidermidis, and C. jeikeium (<5 s) (P < 0.0001 for all four isolates).

FIG. 2.
Survival curves of the four clinical strains of Mycobacterium species, M. smegmatis, S. epidermidis, and C. jeikeium after incubation with 75% alcohol. Error bars indicate standard errors of the means.

DISCUSSION

We report a series of four patients with acupuncture mycobacteriosis with clinical and/or radiological lesions at acupuncture point- and meridian-specific locations. For patient 4, acupuncture at the HT 7 acupuncture point required insertion of the acupuncture needle at the skin crease in the fossa on the lateral side of the tendon of the flexor carpi ulnaris muscle, through the skin and subcutaneous tissue, to a depth of 0.3 to 0.5 in., whereas acupuncture at the PC 7 acupuncture point required insertion of the acupuncture needle at the transverse crease of the wrist, between the tendons of the flexor carpi radialis and the palmaris longus muscles, through the skin and subcutaneous tissue, passing through the tendons of the flexor pollicis longus, flexor digitorum superficialis, and flexor digitorum profundus muscles, to a depth of 0.3 to 0.5 in. (5). This is in line with the tenosynovitis observed by MRI. All four cases were associated with clinical diagnostic problems, requiring tissue biopsy for histology and mycobacterial culture. For all four mycobacterial isolates, conventional microbiological tests failed to identify them to the species level, and 16S rRNA gene sequencing was performed for complete species determination. All patients had serious morbidity, requiring hospitalization and prolonged courses of antimycobacterial therapy with multiple antibiotics.

In our experience, acupuncture mycobacteriosis is associated with delay in clinical diagnosis. First, patients delayed seeking medical advice because the symptoms were relatively mild and indolent; therefore the patients tended to observe. Furthermore, patients failed to associate the acupuncture with the clinical illness due to a relatively long incubation period. In contrast to other pyogenic bacterial infections with shorter incubation periods, i.e., in terms of days, infections due to rapidly growing mycobacteria had incubation periods of 1 to 3 months (3, 7, 8, 22, 30). This is in line with the long interval between acupuncture and medical consultation in our cases. Second, the diagnostic delay is also related to failure of the attending clinicians to recognize acupuncture-induced mycobacteriosis due to the lack of clinical awareness of such a disease entity. Most clinicians are aware of acupuncture-related human immunodeficiency virus, hepatitis B virus, and hepatitis C virus infections. On the other hand, the lack of awareness of acupuncture mycobacteriosis is related to the apparently rare occurrence of this indolent skin and soft tissue infection, as well as the facts that apparently adequate skin disinfection with alcohol is generally practiced in most acupuncture clinics and that disposable acupuncture needles are used. In all four cases, the diagnosis was made during subsequent infectious disease consultations, when the patients recalled the history of acupuncture only on direct questioning of whether the involved site has been penetrated by sharp objects months ago.

16S rRNA gene sequencing was useful for identifying all four strains of mycobacteria, which had ambiguous biochemical profiles. Identification of mycobacteria traditionally relies on isolation of the mycobacteria and subsequent phenotypic characterization by conventional biochemical tests or whole-cell fatty acid analysis. However, these two systems are associated with many drawbacks. The turn-around time for identification is long when conventional tests are used, as some biochemical reactions may take up to 28 days to complete. Furthermore, some isolates exhibit ambiguous biochemical profiles and hence are termed unidentifiable. For whole-cell fatty acid analysis using gas chromatography, the special equipment and expertise required are generally not available in routine clinical microbiology laboratories. Although commercially available molecular-based methods have revolutionized the rapid identification of some mycobacteria, such as M. tuberculosis and M. avium (20, 25, 47), no commercially available molecular-based methods are available for the identification of most other mycobacteria, as they are not as commonly encountered in clinical specimens. 16S rRNA gene sequencing has been shown to be useful for identification of noncultivable organisms and organisms with ambiguous biochemical profiles (6, 15, 23, 27, 28, 34, 35, 36, 37, 39, 40, 43, 46). In the present study, all four strains of mycobacteria were not identified to the species level with conventional biochemical tests, although the best match provided by fatty acid analysis was the same as the identification by 16S rRNA gene sequencing. The final identification of two strains as M. nonchromogenicum is in line with previous reports that this species is especially associated with tenosynovitis (29).

Acupuncture mycobacteriosis is probably related to infection of immunocompromised patients and/or inoculation into deep tissue spaces with relatively alcohol-resistant Mycobacterium species. We showed that both M. chelonae and M. nonchromogenicum, compared to other skin flora or M. smegmatis, need relatively longer times to achieve a 5-log10-unit decrease in bacterial counts when treated with 75% alcohol. When mycobacteria are introduced into an immunocompromised patient (e.g., patient 2) or into a deep tissue plane such as tendon sheath or intermuscular fascia with concomitant introduction of foreign bodies or any particulate matter (such as soil particles or dust) which facilitates bacterial biofilm formation, acupuncture mycobacteriosis may occur. The association of mycobacterial infections with acupuncture is in line with the occurrence of a relatively high incidence of trauma-related cutaneous infections caused by rapid growers. In one large study, 74 of 125 cases (59%) of disease due to rapidly growing mycobacteria were cutaneous infections, where all were due to either a surgical procedure (40 cases) or accidental penetrating trauma (34 cases) (33).

The existing infection control guidelines for acupuncture may need revision. Since mycobacteria are resistant to chlorhexidine, we recommend that the acupuncturist wash his or her hands properly with alcoholic chlorhexidine or povidone iodine. A bath with soap and water may be necessary if the patient's hygiene is poor. The patient's skin should be disinfected by concentric swabbing with 75% alcohol that is properly reconstituted without top up. Since there was no evidence to support a minimum waiting time, the Australian Acupuncture Association Infection Control Guidelines for Acupuncture recommended that the site of insertion should be “just dry” before the patient's skin is pierced (1). However, from our results, we recommend a skin disinfection time of at least 60 s.

Acknowledgments

This work is partly supported by the University Development Fund, University Research Grant Council, and the Committee for Research and Conference Grant, The University of Hong Kong.

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