Outbreak of Mycobacterium chelonae Infection Associated with Tattoo Ink

On January 4, 2012, we and colleagues at the Monroe County Department of Public Health began investigating an outbreak on the basis of a report from a dermatologist of the development of a persistent granulomatous rash on the arm of a person who had received a tattoo on that area in October 2011. This index patient was a previously healthy 20-year-old man who had a history of multiple tattoos without any health problems. He was treated unsuccessfully with glucocorticoids by his primary care provider before being referred to a dermatologist. Histopathological examination and culture of a biopsy specimen confirmed the presence of M. chelonae.

After the interview with the index patient, investigators at the Monroe County Department of Public Health learned that similar reactions had developed in other persons who had obtained tattoos from the same artist at the same tattoo parlor. During a site visit, investigators interviewed the tattoo artist and learned that since May 2011, he had been using a new, hand-blended, diluted black ink (gray wash) that contained pigment, distilled water, witch hazel, and glycerin. Gray wash is used to achieve shading and a three-dimensional quality in tattoos; it is a prominent component of portrait and photography tattoos, which are currently popular.

According to the artist, the manufacturer diluted the black ink with distilled water before packaging and shipping the ink. This premixed ink was prepackaged in three dilution strengths per set: a 30%, or light, wash (i.e., greatest dilution); a 60%, or medium, wash (i.e., intermediate dilution); and a 90%, or dark, wash (i.e., least dilution). The tattoo artist originally purchased the ink in April 2011 at a tattoo trade show in Arizona, and he later ordered an additional supply. The product labeling contained no lot number or other unique manufacturing identification. He stopped using the premixed ink in December 2011.

To identify cases of infection, a number of steps were taken. First, a regional pathology laboratory used by many dermatologists was alerted to report any cases of ink-associated granulomatous reactions. Second, a list of patrons who were tattooed between May and December 2011 was obtained from the tattoo artist. The artist did not maintain detailed records that included the type of ink that was used with each patron. Third, all local tattoo parlors within Monroe County were identified, contacted by telephone, and queried about ink products used in their establishments as well as any reports of rashlike illnesses. No other parlor used this premixed ink, and no rashlike illnesses were reported. Finally, exposed patrons were contacted by telephone and interviewed, with the use of a standard questionnaire, about receiving a tattoo and any subsequent rashlike illness.

An environmental health assessment suggested that best practices were generally observed at the parlor where the index patient received his tattoo, and no concerns about hygiene were noted. In particular, the artists used sterile instruments, wore clean disposable gloves, poured ink into single-use containers, and provided appropriate aftercare to the tattooed site. Importantly, no dilution or mixing of inks at the parlor occurred, and the artist avoided contamination of ink from tap water at the facility. These practices were confirmed by all interviewed patrons.

The Food and Drug Administration (FDA) inspected the Arizona-based manufacturer and distributor of the ink. The FDA collected samples of ink and of the ingredients used in its preparation and packaging, and the Centers for Disease Control and Prevention (CDC) cultured them.

The clinical findings in all but two patients were evaluated at the University of Rochester Medical Center; of the two patients with findings that were not evaluated, one had follow-up in another state and another declined evaluation and treatment. Patients were evaluated by dermatologists, who performed skin biopsies of the tattooed lesions; tissue specimens were then sent for histologic and microbiologic analysis. Patients were referred to an infectious-disease expert for follow-up care and offered empirical treatment with appropriate antimicrobial agents.

Laboratory investigations were conducted at the University of Rochester Medical Center, the Wadsworth Center of the New York State Department of Health, and the CDC. Samples from clinical isolates, one opened bottle of 60% premixed gray ink wash and three unopened bottles (one containing 30% wash, one containing 60% wash, and one containing 90% wash), and water and swabs from faucets (biofilm) were submitted for various microbiologic tests, including acid-fast bacilli smears, cultures and antimicrobial sensitivity profiles, DNA sequencing, and pulsed-field gel electrophoresis (PFGE), according to standard protocols.^15–20

In this outbreak of M. chelonae infections associated with tattoos, 19 cases were identified: 14 confirmed cases, 4 probable cases, and 1 suspected case (see Table S1 in the Supplementary Appendix, available with the full text of this article at NEJM.org). On the basis of a list of 167 patrons provided by the tattoo artist, the attack rate increased from zero during the period from May through August to a peak of 65% in November (Figure 1). Rashes were confined to areas of the skin tattooed with the premixed gray ink (Figure 2). The average age of the 13 men and 6 women with M. chelonae infection was 35 years (range, 18 to 48).

Biopsy specimens were obtained from 17 of the 19 patients: sparse lymphohistiocytic infiltrates in the upper dermis were observed in 12 specimens, granulomas in 5, and acid-fast organisms in 2 (Figure S1 in the Supplementary Appendix). M. chelonae was isolated in 14 of the 17 tissue specimens and confirmed by DNA sequencing.

Antimicrobial susceptibility studies for atypical mycobacteria are not routinely performed in the United States; however, these studies were performed in two patients. In the first patient, M. chelonae was sensitive to clarithromycin, doxycycline, and linezolid; had intermediate sensitivity to ciprofloxacin; and was resistant to cefoxitin. In the second patient, M. chelonae was sensitive to clarithromycin and doxycycline, had intermediate sensitivity to linezolid, and was resistant to ciprofloxacin and cefoxitin.

The CDC results confirmed the isolation of M. chelonae and showed an indistinguishable PFGE pattern in 11 clinical isolates and one of three unopened bottles of ink (i.e., the 30% gray wash) (Figure S2 in the Supplementary Appendix). M. chelonae was not isolated from the water or faucet in the tattoo parlor.

We collected the remaining bottles of premixed ink from the tattoo parlor. We also provided information and education to both tattoo artists and patrons at a large tattoo trade show hosted in Rochester, New York. The materials provided included information on New York State law, which bans tattooing of persons younger than 18 years of age, regardless of whether parental consent is given; tattooing best practices, including the use of sterile products and aseptic techniques as well as appropriate aftercare; risks associated with tattooing; signs of a reaction from a tattoo; and steps to be taken if a reaction to a tattoo occurs.

The CDC issued a nationwide alert about the outbreak. The manufacturer voluntarily recalled the ink. Appropriate antimicrobial therapy (macrolides at first, based on the recommendations from relevant prior case reports, and then macrolides, doxycycline, or both, once sensitivities were available) was initiated in 18 of the 19 patients, and their condition improved, although the speed of recovery in each patient varied.