Abstract
Aims:
Tattooing and use of permanent makeup (PMU) has dramatically increased over the last decade, with a concomitant increase in ink-related infections. The aim of this study was to determine whether micro-organisms are present, and if so, the number and their identification in the commercial tattoo and PMU inks available in the United States.
Methods and Results:
We surveyed 85 unopened tattoo and PMU inks, purchased from 13 companies. We incubated 100 μl of ink samples on trypticase soy agar plates for bacterial growth, 7H10 Middlebrook medium for mycobacterial growth, and Sabouraud dextrose medium for fungal growth. In total, 42 inks were contaminated with micro-organisms (49%). Thirty-three inks were contaminated with bacteria, 2 inks with fungi, and 7 inks had both bacterial and fungal growth. Mycobacteria were not detected in any of the examined tattoo and PMU inks. In 26 inks, microbial concentrations ranged between 101 and 103 CFU per ml, but higher counts (>103 CFU per ml) were recorded in 16 inks. We identified 83 bacteria by their 16S rDNA sequences, including 20 genera and 49 species. Strains of Bacillus spp. (53%) were dominant, followed by Lysinibacillus fusiformis (7%) and Pseudomonas aeruginosa (5%). Thirty-four (41%) possibly clinically relevant strains were identified, including P. aeruginosa, Dermacoccus barathri and Roseomonas mucosa, some of which have been previously reported to be associated with human skin infections.
Conclusions:
The results indicate that commercial tattoo and PMU inks on the US market surveyed in this study contain a wide range of micro-organisms, including pathogenic bacteria.
Significance and Impact of the Study:
Microbial contaminants in tattoo and PMU inks are an emerging safety concern for public health. This study provides evidence that microbial contamination of tattoo and PMU inks available in the United States is more common than previously thought and highlights the importance of monitoring these products for potentially pathogenic micro-organisms.
Keywords: identification of bacteria, microbial contamination, microbiological survey, pathogenic bacteria, permanent makeup ink, tattoo ink, US market
Introduction
Tattooing is the introduction of exogenous pigments and dyes into the skin to obtain a permanent design (Goldstein 2007). It has, along with permanent makeup (PMU), became increasingly common globally for the past two decades, particularly among young people (Kluger 2016). It is roughly estimated that 29% of US adults (over the age of 18 years) have at least one tattoo, according to the 2015 Harris poll. This is up from the 21, 16 and 14%, when the poll was done in 2012, 2008 and 2003, respectively (The Harris Poll 2015). There have been reports published in the literature, indicating an increase in ink-related adverse effects that include dermatological disorders and complications, such as infections, immunological responses, such as inflammatory and allergic hypersensitivity reactions, and skin tumours (Wenzel et al. 2013; Serup et al. 2015; Kluger 2016).
Infectious complications associated with tattooing are caused by transdermal transmission of pathogenic micro-organisms. Hepatitis B and C, human papillomavirus and Staphylococcus, Streptococcus, Pseudomonas, Clostridium species and nontuberculous mycobacteria (NTM) are commonly reported (Wenzel et al. 2013; Bonadonna 2015; Serup et al. 2015). Infections may result from insufficient hygienic practices, nonsterile tattooing instruments, sharing contaminated needles and use of nonsterile diluents, including water, in the tattoo inks (LeBlanc et al. 2012; Bonadonna 2015; Serup et al. 2015). Secondary infection of the tattooed skin area may result from a lack of appropriate aftercare during healing (Bonadonna 2015). In addition, the inks themselves may be microbially contaminated with pathogenic micro-organisms. During 2011–2012, several outbreaks of tattoo-associated skin infections with NTM were reported (Centers for Disease Control 2012). Mycobacterium chelonae was found in sealed bottles of grey tattoo ink from one company, suggesting contamination before distribution (Centers for Disease Control 2012; Kennedy et al. 2012; Conaglen et al. 2013).
In the current manufacturing processes, inks could be microbially compromised by contaminated ingredients or at other points along the production chain (Centers for Disease Control 2012; LeBlanc et al. 2012; Conaglen et al. 2013). However, little is known about the occurrence of microbial contamination in unopened tattoo and PMU inks. In 2004, tattoo inks from one company were withdrawn from market because the unopened inks were contaminated with Pseudomonas aeruginosa and a fungus, Acremonium sp. (Harp 2011). In Europe, microbial growth has been observed in 10–86% of unopened tattoo inks surveyed (Charnock 2004; Baumgartner and Gautsch 2011; Hogsberg et al. 2013; Bonadonna 2015). Bacterial strains belonging to the genera, Bacillus, Staphylococcus, Pseudomonas, Streptococcus, Sphingomonas, Cronobacter, Enterococcus and Acinetobacter, were identified.
The aim of this study was to determine whether micro-organisms are present in the commercial tattoo and PMU closed inks available on the US market. In addition, this study will assess the level of microbiological contamination, with particular interest in pathogenic bacterial species.
Materials and methods
Tattoo and PMU inks
We purchased commercial tattoo and PMU inks from 13 different companies in the United States during November 2015 and April 2016. Inks were purchased either as individual bottles or as sets of multiple bottles of different colours, including black or grey. Upon receipt and before microbiological tests, we examined the bottles for intact packaging and sealing. Ingredients, sterility claims, lot numbers and manufacturing locations were recorded, if available, from product labels or material safety data sheets. In addition, expiration dates were recorded when provided although they are not required by law for cosmetics.
Microbiological analysis
Tattoo and PMU inks were surveyed for contamination by bacteria, mycobacteria and fungi using trypticase soy agar, 7H10 Middlebrook agar containing the PANTA antibiotic mixture (Donaghy et al. 2003) and Sabouraud dextrose agar, respectively. We spread approximately 100 μl of each ink solution onto triplicate agar plates of each type and incubated them at 30°C for 5–7 days, 34°C for 2 weeks and 28°C for 2 months, respectively. Agar plates with no spread-plating were also incubated to exclude the possibility of false negatives. We recorded total count of microbial colonies on the surface of the agar. The ink sample was considered contaminated when growth of micro-organisms was consistently found on all triplicate agar plates. When the number of colonies was less than 3 per 0·1 ml of ink sample and/or only one or two agar plates produced microbial growth, we repeated the incubation to confirm the microbial contamination. For identification of bacteria, colonies were initially isolated based on features of the colony, such as size, morphology, and colour, by streaking onto the same type of agar plates, and then 16S rRNA gene sequence of each isolates was determined. Colonies were individually preserved in glycerol and stored at −70°C.
Identification of bacterial isolates
We used a colony PCR amplification method for identification of bacterial isolates. Briefly, colonies on the surfaces of agar plates were suspended in a 1·5 ml microtube containing 200 μl of lysis buffer (1% Triton X-100, 20 mmol l−1 Tris-HCl, pH 8·0, 2 mmol l−1 EDTA) and boiled for 10 min. After cell debris was pelleted, 2 μl of the supernatant was directly used for PCR. The reaction mixture (25 μl) contained 1·25 units of Takara Ex Taq DNA polymerase (Clontech, Mountain View, CA), 1× Ex Taq reaction buffer, 200 μmol l−1 of each dNTP and 0·2 μmol l−1 of each of the 16S rRNA gene primers 27f and 1492r. The cycling conditions were 95°C for 5 min, followed by 30 cycles of 94°C for 1 min, 55°C for 1 min and 72°C for 1 min, with a final extension at 72°C for 10 min. The amplified DNA fragments were cloned into pGEM-T Easy TA cloning vector (Promega, Madison, WI), and the nucleotide sequences were determined at the University of Arkansas for Medical Sciences (http://mbim.uams.edu/research-cores/dna-sequencing-core-facility) using a 3130XL Genetic Analyzer (Applied Biosystems, Foster City, CA). We analysed each DNA sequence via BlastN searches at the NCBI website and determined isolates’ affiliation to known genera and species by their sequence similarity.
Results
Microbial contamination of tattoo and PMU inks
We surveyed 85 inks in total, including 62 tattoo inks and 23 PMU inks, from 13 different companies available in the United States (Table 1). The results of the microbiological analysis showed the following percentages of contamination in these previously unopened, sealed tattoo and PMU inks. As a whole, 42 of 85 inks (49%) from 12 of 13 companies (92%) were contaminated with micro-organisms, which included 31 of 62 tattoo inks (50%) and 11 of 23 PMU inks (48%) (Table 1 and Fig. 1).
Table 1.
Cultural detection of micro-organisms in tattoo and PMU inks.
Company* | Colour† | Ink type | Bacterial | Fungal | CFU per ml‡ | Identified bacterial isolates§ |
---|---|---|---|---|---|---|
1 | Black A | Tattoo | + | − | 1.17 × 103 |
Lysinibacillus fusiformis
Bacillus acidiceler Alcaligenes faecalis |
Black B | Tattoo | + | − | >2 × 103 | Bacillus pumilus | |
Black C | Tattoo | + | − | 3·0 × 102 |
Bacillus pumilus
Bacillus horneckiae |
|
Purple | Tattoo | − | − | − | ||
Green | Tattoo | − | − | − | ||
Red | Tattoo | − | − | − | ||
White | Tattoo | + | − | >2 × 103 | Pseudomonas aeruginosa | |
Grey | Tattoo | + | − | 3·1 × 102 | Pseudomonas aeruginosa | |
Yellow A | Tattoo | + | − | >2 × 103 |
Brachybacterium faecium
Brachybacterium paraconglomeratum |
|
Yellow B | Tattoo | + | + | >2 × 103 |
Desemzia incerta
Brachybacterium paraconglomeratum |
|
Brown | Tattoo | − | − | − | ||
Dark Brown | Tattoo | + | + | >2 × 103 |
Sporosarcina luteola
Roseomonas mucosa |
|
Blue | Tattoo | − | − | − | ||
2 | Brown | Tattoo | − | − | − | |
Black A | Tattoo | − | − | − | ||
Black B | Tattoo | − | − | − | ||
White | Tattoo | + | − | 7·7 × 102 | Pseudomonas aeruginosa | |
3 | White | Tattoo | − | − | − | |
Black | Tattoo | − | − | − | ||
Red | Tattoo | − | − | − | ||
Orange | Tattoo | − | − | − | ||
Blue A | Tattoo | + | − | >2 × 103 | Lysinibacillus fusiformis | |
Blue B | Tattoo | + | − | 30 | Bacillus licheniformis | |
Purple | Tattoo | − | − | − | ||
Yellow | Tattoo | − | − | − | ||
4 | Black A | PMU | − | − | − | |
Black B | PMU | + | 50 |
Brevibacillus parabrevis
Psychrobacillus psychrodurans Lysinibacillus fusiformis Paenibacillus glucanolyticus Staphylococcus hominis |
||
Black C | PMU | − | − | − | ||
Pink | PMU | + | − | 50 |
Bacillus thermoamylovorans
Paenibacillus amylolyticus |
|
Brown A | PMU | + | − | 1·8 × 102 | Paenibacillus amylolyticus | |
Brown B | PMU | + | − | 2·5 × 102 |
Paenibacillus amylolyticus
Bacillus licheniformis |
|
Brown C | PMU | + | − | 20 | Micrococcus luteus | |
5 | Black | Tattoo | + | − | >2 × 103 | Paenibacillus lautus |
Red A | Tattoo | − | − | − | ||
Red B | Tattoo | − | − | − | ||
Yellow A | Tattoo | − | − | − | ||
Yellow B | Tattoo | − | − | − | ||
Orange | Tattoo | + | − | >2 × 103 | Bacillus aquimaris | |
Light purple | Tattoo | − | − | − | ||
White | Tattoo | + | + | 30 |
Lysinibacillus fusiformis
Bacillus subtilis |
|
Green A | Tattoo | − | − | − | ||
Green B | Tattoo | − | − | − | ||
Pink | Tattoo | + | − | 30 | Lysinibacillus fusiformis | |
6 | Brown A | Tattoo | − | − | − | |
Brown B | Tattoo | + | − | >2 × 103 | Oceanobacillus chironomi | |
Black | Tattoo | + | 1·1 × 102 |
Bacillus cohnii
Kocuria marina Dermacoccus barathri Paenibacillus lautus Barrientosiimonas humi Bacillus amyloliquefaciens |
||
Grey | Tattoo | + | − | 50 | Bacillus gottheilii | |
Green | Tattoo | + | − | >2 × 103 | Pseudomonas aeruginosa | |
Red | Tattoo | − | + | 6·9 × 102 | ||
Blue A | Tattoo | − | − | − | ||
Blue B | Tattoo | + | − | 1 × 102 | Bacillus subtilis | |
Blue C | Tattoo | + | − | >2 × 103 | Bacillus licheniformis | |
7 | Black | PMU | − | − | − | |
Yellow | PMU | − | − | − | ||
Red | PMU | − | − | − | ||
8 | Black A | Tattoo | + | − | >2 × 103 | Bacillus horneckiae |
Black B | Tattoo | + | + | 10 | Bacillus cohnii | |
Red | Tattoo | − | − | − | ||
Grey | Tattoo | + | − | >2 × 103 | Atopostipes suicloacalis | |
9 | Black | PMU | + | 1 × 102 |
Fictibacillus phosphorivorans
Bacillus chungangensis Bacillus aquimaris Bacillus horikoshii Fictibacillus arsenicus Bacillus aryabhattai |
|
Brown A | PMU | − | − | − | ||
Brown B | PMU | − | − | − | ||
Brown C | PMU | − | − | − | ||
Red A | PMU | − | − | − | ||
Red B | PMU | + | − | 60 | Bacillus pumilus | |
10 | Red A | Tattoo | + | − | >2 × 103 | Oceanobacillus chironomi |
Red B | Tattoo | − | − | − | ||
Red C | Tattoo | − | − | − | ||
Yellow | Tattoo | + | − | 1·4 × 102 | Atopostipes suicloacalis | |
Pink | Tattoo | + | − | 20 | Bacillus gottheilii | |
White | Tattoo | + | + | 20 | Lysinibacillus fusiformis | |
Orange | Tattoo | + | − | >2 × 103 | Providencia rettgeri | |
Blue | Tattoo | − | − | − | ||
11 | Black | PMU | + | 40 |
Bacillus simplex
Bacillus subtilis Bacillus niacini |
|
Brown | PMU | − | − | − | ||
12 | Black A | PMU | + | + | 1·5 × 102 |
Bacillus amyloliquefaciens
Bacillus cereus acillus thuringiensis Bacillus firmus Bacillus arbutinivorans Bacillus pumilus Brevibacillus laterosporus Brevibacillus brevis |
Black B | PMU | + | + | 5 × 102 |
Bacillus cohnii
Bacillus halodurans Bacillus mannanilyticus Bacillus aryabhattai Bacillus pumilus Bacillus thuringiensis Bacillus acidiceler |
|
Red A | PMU | − | − | − | ||
Red B | PMU | − | − | − | ||
Brown | PMU | + | 2·2 × 102 |
Bacillus megaterium
Bacillus cereus Bacillus cohnii Bacillus litoralis Bacillus benzoevorans Bacillus niacini |
||
13 | White | Tattoo | − | − | − | |
Green | Tattoo | − | − | − | ||
Blue | Tattoo | − | − | − | ||
Yellow | Tattoo | − | + | 70 | ||
Purple | Tattoo | − | − | − |
Companies, 1, 7, 11 and 13 claim their products to be sterile.
The closest colour to the ink was used. For example, dark brown was called brown.
CFU number is the mean of triplicate plate counts per ml of ink solution. Number of fungal contaminants was counted only when they could be individually counted. Fungi were not identified in this study.
Nearest phylogenetic neighbour identified following BLAST analysis of the 16S rRNA gene sequence.
Figure 1.
A schematic representation of microbiological survey results of commercial tattoo and PMU inks. Forty-two of 85 inks were contaminated with micro-organisms. Bar graphs show number of inks contaminated based on type of micro-organisms (a) and CFU per ml (b), respectively. () fungal only; (
) bacterial only; (
) both fungal and bacterial; (
) <100 CFU per ml; (
) 100 <1000 CFU per ml; (
) >1000 CFU per ml.
Microbial contamination across companies and colours
Among the tested 13 companies, only one company (Company 7) showed no microbial contamination (Table 1 and Table S1), whereas 12 companies had products with some contamination. For three products (ink companies 1, 6 and 8, respectively), microbial growth was observed in 8 of 13 (62%), 7 of 9 (78%), and 3 of 4 (75%) of the examined inks. There were four companies (ink companies 1, 7, 11 and 13), claim on the package label that their products were sterile, but only products from company 7 were found to not have any microbial growth. All 11 coloured inks with the exception of purple inks showed microbial contamination (Table S2).
Bioburden level of microbial contamination
Microbial contamination was mostly bacterial (40 inks), but fungal growth (9 inks) was also detected. Thirty-three inks had bacterial contamination only, while seven inks had both bacterial and fungal contamination (Fig. 1). We observed fungi only in two inks from companies 6 and 13 (Table 1). Some of the contaminated tattoo and PMU inks showed multiple bacteria that were morphologically different. More than two morphologically different colonies in 15 inks were observed (Table 1). In particular, black A and B PMU inks from company 12 were contaminated with 8 and 7 different strains of bacteria, respectively. The contamination level was lower than 102 CFU per ml in 13 inks (31%), 102–103 CFU per ml in another 13 inks (31%) and higher than 103 CFU per ml in 16 inks (38%; Fig. 1). We observed relatively higher numbers of colonies from tattoo inks compared with PMU inks. The 16 samples with higher than 103 CFU per ml of contamination were all from tattoo inks (Table 1).
Identification of bacterial strains isolated from tattoo and PMU inks
From 42 tattoo and PMU inks, we identified 83 bacterial isolates based on their 16S rDNA sequences. The isolates included 20 genera and 49 species (Table 1). In terms of number of genera, more diverse bacteria were identified from tattoo inks than from PMU inks; 15 genera and 24 species from tattoo inks and 8 genera and 33 species from PMU inks, respectively. The most frequently identified bacteria were Bacillus spp. (53%), followed by Lysinibacillus fusiformis (7%), Paenibacillus spp. (7%) and P. aeruginosa (5%). We identified other spore-forming bacteria, such as species of Sporosarcina, Brevibacillus, Psychrobacillus, Fictibacillus and Oceanobacillus (Table 1).
We identified 34 possibly clinically relevant strains (41%; Fig. 2). They included strains of Bacillus and P. aeruginosa. Many other probable pathogens, not previously associated with tattooing, were also identified. These included species of Dermacoccus, Kocuria, Providencia, Alcaligenes and Roseomonas. No isolates were identified as mycobacteria, using 7H10 Middlebrook with PANTA, which is generally used to grow mycobacteria.
Figure 2.
Proportion (41%) and the list of 34 of 83 possibly clinically relevant bacteria identified in this study. Number of isolates is shown in parentheses.
Discussion
The results of this investigation showed that microbial contamination in unopened, sealed bottles of tattoo and PMU inks is common. The inks from only one company out of 13 showed no microbial contamination. The range of bacterial contamination was wide, ranging from lower than 10 CFU per ml to higher than 103 CFU per ml. These results were consistent with previous surveys of unopened inks sold in Europe, which revealed contamination in 5–86% of inks surveyed (Charnock 2004; Baumgartner and Gautsch 2011; Hogsberg et al. 2013; Bonadonna 2015; Dieckmann et al. 2016). The 86% result came from an examination of seven unopened inks (Bonadonna 2015).
Previously, black and grey pigments have been reported to be contaminated with M. chelonae, which have been implicated in tattoo ink-related infections (Drage et al. 2010; Kappel and Cotliar 2011; Centers for Disease Control 2012; Kennedy et al. 2012; Conaglen et al. 2013; Falsey et al. 2013). We screened for nontuberculosis mycobacteria, especially M. chelonae, using 7H10 Middlebrook agar media containing the PANTA antibiotic mixture. However, no mycobacteria were detected from the direct plating analysis of 85 inks that included black and grey pigments. Contamination with micro-organisms, including probable pathogens, was indiscriminately distributed among all colours, although 15 of 21 black and grey ink samples were contaminated, which was higher (71%) than the contamination of inks in chromatic colours (33%) (Table S2).
In this study, inks from only four companies were labelled as sterilized, but only one did not have any microbial growth. It showed that the sterilization claims on the product label were not often reliable. These results suggest that either mislabelling of the tattoo and PMU ink bottles occurred, whether intentionally or unintentionally, or because the sterilization process was incomplete. Recently, a study reported microbial contamination of as many as 10% of new inks claiming sterility (Hogsberg et al. 2013). In relation to sterility of pigments, we were interested in whether companies use preservatives or not, and if there was an association of preservation and microbial contamination. According to product labels or MSDS (Material Safety Data Sheet) attached to the product, it appears that none of the companies mentioned the use of preservatives.
The direct plating of tattoo and PMU inks identified a wide variety of bacterial species, which have not been previously been identified from tattoo inks (Table S3). We found many species from spore-forming genera, along with the genera Kocuria and Dermacoccus. The presence of Bacillus and Micrococcus-related species, which are often known as extreme environment survivors (Greenblatt et al. 2004), in tattoo ink products has previously been reported (Baumgartner and Gautsch 2011; Bonadonna 2015) and was assumed to be due to extraordinary resistance to harsh environmental conditions.
Among pathogenic bacteria, P. aeruginosa is the most common bacterium involved in tattoo-associated infections (Mathur and Sahoo 1984; Korman et al. 1997; Porter et al. 2005; Maloberti et al. 2015). Pathogenic strains of Bacillus were also identified. However, other bacterial species, such as Streptococcus, Enterococcus and mycobacteria, which were often related to infections after tattooing (Wenzel et al. 2013; Bonadonna 2015; Serup et al. 2015), were not found. We instead identified probable pathogens, Alcaligenes faecalis, Bacillus pumilus, Bacillus megaterium, and strains belonging to Dermacoccus, Kocuria, Providencia and Roseomonas. These have been involved in skin and soft-tissue infection, cutaneous skin infection, severe sepsis, catheter-related blood stream infection, ulcer formation and wound infections, but were previously never reported as associated with tattoos (Tena et al. 2007, 2015; Lee et al. 2009; Bard et al. 2010; Duncan and Smith 2011; Kahveci et al. 2011; Takahashi et al. 2015; Washington et al. 2015).
We did not detect NTM in the test samples. This finding may reflect that the tattoo and PMU inks surveyed in this study were not contaminated with those rapidly growing mycobacteria or it could be the result of limit of detection used in the experiment. Technically, the method used in this investigation would detect mycobacterial contamination over 10 CFU per ml. However, if below this level, then it would be problematic to observe the presence of NTM in the tattoo and PMU inks.
Although the present study initially aimed to profile microbial contamination in tattoo and PMU inks with an emphasis on bacteria, examination of nine ink samples (16%) revealed fungi (Tables 1 and 2). Pigments contaminated with fungi, including Cephalosporium spp., Acremonium spp., Penicillium spp., Cryptococcus albidus and Neosartorya hiratsukae, have been previously reported (Bonadonna 2015; US Food and Drug Administration 2015). The identification of the fungi observed in this study will be the subject of a separate investigation.
Table 2.
Number of tattoo and PMU inks contaminated with micro-organisms.
No. of inks surveyed | No. of inks with bacterial contamination | No. of inks with fungal contamination | No. of inks contaminated in total (%) | |
---|---|---|---|---|
Tattoo inks | 62 | 29 | 7 | 31 (50) |
PMU inks | 23 | 11 | 2 | 11 (48) |
The results presented here clearly demonstrate that commercial tattoo and PMU inks sold in the United States surveyed in this study contain a wide range of micro-organisms including pathogenic bacteria and fungi. The skin is an efficient barrier against bacterial, fungal and viral infections; however, when that barrier is breached, as in wounding or tattooing, an important defence against infection has been compromised. Compromise of the skin barrier by tattooing, and subsequent exposure to ocean water, recently led to sepsis and death emphasizing the risk of skin compromise under certain conditions (Hendren et al. 2017). Prevention of growth of bacteria, fungi or viruses that have been introduced into the skin is determined by (i) the pathogenic nature of the organism (e.g. genus species and ability to sustain growth in human tissues), (ii) the number of introduced organisms (e.g. dose) and (iii) the immunological status of the individual. Since infections following tattooing and PMU application are common (Wenzel et al. 2013; Serup et al. 2015; Kluger 2016), controlling the sterility of the injected material would be a key step in preventing infections.
Supplementary Material
Table S1 Detection of micro-organisms in tattoo and PMU inks according to companies.
Table S2 Microbial contamination in tattoo or permanent makeup inks associated with colours.
Table S3 A list of bacterial organisms identified in previous and current tattoo and PMU ink survey.
Acknowledgements
We thank John Sutherland, Huizhong Chen and Linda Katz for critical review of the manuscript. This work was supported, in part, by an appointment to the Postgraduate Research Fellowship Program at the National Center for Toxicological Research, administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the U. S. Department of Energy and the U. S. Food and Drug Administration. The opinions and views presented in this article do not necessarily reflect current or future opinions or policies of the US FDA. The mention of companies or trade names should not be considered an endorsement. This work was funded by U.S. FDA (E0759301).
Footnotes
Conflict of Interest
No conflict of interest declared.
Supporting Information
Additional Supporting Information may be found in the online version of this article:
References
- Bard JD, Deville JG, Summanen PH and Lewinski MA (2010) Roseomonas mucosa isolated from bloodstream of pediatric patient. J Clin Microbiol 48, 3027–3029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumgartner A and Gautsch S (2011) Hygienic-microbiological quality of tattoo- and permanent make-up colours. J Verbrauch Lebensm 6, 319–325. [Google Scholar]
- Bonadonna L (2015) Survey of studies on microbial contamination of marketed tattoo inks. Curr Probl Dermatol 48, 190–195. [DOI] [PubMed] [Google Scholar]
- Centers for Disease Control (2012) Tattoo-associated nontuberculous mycobacterial skin infections-multiple states, 2011–2012. Morb Mortal Wkly Rep 61, 653–656. [PubMed] [Google Scholar]
- Charnock C (2004) Colourants used for tattooing contaminated with bacteria. Tidsskr Nor Laegeforen [Article in Norwegian] 124, 933–935. [PubMed] [Google Scholar]
- Conaglen PD, Laurenson IF, Sergeant A, Thorn SN, Rayner A and Stevenson J (2013) Systematic review of tattoo-associated skin infection with rapidly growing mycobacteria and public health investigation of a cluster in Scotland, 2010. Euro Surveill 18, 20553. [DOI] [PubMed] [Google Scholar]
- Dieckmann R, Boone I, Brockmann SO, Hammerl JA, Kolb-Maurer A, Goebeler M, Luch A and Al Dahouk S (2016) The risk of bacterial infection after tattooing. Dtsch Arztebl Int 113, 665–671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donaghy JA, Totton NL and Rowe MT (2003) Evaluation of culture media for the recovery of Mycobacterium avium subsp. paratuberculosis from Cheddar cheese. Lett Appl Microbiol 37, 285–291. [DOI] [PubMed] [Google Scholar]
- Drage LA, Ecker PM, Orenstein R, Phillips PK and Edson RS (2010) An outbreak of Mycobacterium chelonae infections in tattoos. J Am Acad Dermatol 62, 501–506. [DOI] [PubMed] [Google Scholar]
- Duncan KO and Smith TL (2011) Primary cutaneous infection with Bacillus megaterium mimicking cutaneous anthrax. J Am Acad Dermatol 65, e60–61. [DOI] [PubMed] [Google Scholar]
- Falsey RR, Kinzer MH, Hurst S, Kalus A, Pottinger PS, Duchin JS, Zhang J, Noble-Wang J et al. (2013) Cutaneous inoculation of nontuberculous mycobacteria during professional tattooing: a case series and epidemiologic study. Clin Infect Dis 57, e143–147. [DOI] [PubMed] [Google Scholar]
- Goldstein N (2007) Tattoos defined. Clin Dermatol 25, 417–420. [DOI] [PubMed] [Google Scholar]
- Greenblatt CL, Baum J, Klein BY, Nachshon S, Koltunov V and Cano RJ (2004) Micrococcus luteus – survival in amber. Microb Ecol 48, 120–127. [DOI] [PubMed] [Google Scholar]
- Harp B (2011) FDA Webinar on Tattoos and permanent makeup. Retrieved from https://www.fda.gov/Cosmetics/ProductsIngredients/Products/ssLINK/UCM246155.
- Hendren N, Sukumar S and Glazer CS (2017) Vibrio vulnificus septic shock due to a contaminated tattoo. BMJ Case Reports. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hogsberg T, Saunte DM, Frimodt-Moller N and Serup J (2013) Microbial status and product labelling of 58 original tattoo inks. J Eur Acad Dermatol Venereol 27, 73–80. [DOI] [PubMed] [Google Scholar]
- Kahveci A, Asicioglu E, Tigen E, Ari E, Arikan H, Odabasi Z and Ozener C (2011) Unusual causes of peritonitis in a peritoneal dialysis patient: Alcaligenes faecalis and Pantoea agglomerans. Ann Clin Microbiol Antimicrob 10, 12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kappel S and Cotliar J (2011) Inoculation of Mycobacteria chelonae from a tattoo. J Am Acad Dermatol 64, 998–999. [DOI] [PubMed] [Google Scholar]
- Kennedy BS, Bedard B, Younge M, Tuttle D, Ammerman E, Ricci J, Doniger AS, Escuyer VE et al. (2012) Outbreak of Mycobacterium chelonae infection associated with tattoo ink. N Engl J Med 367, 1020–1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kluger N (2016) Cutaneous and systemic complications associated with tattooing. Presse Med 45, 567–576. [DOI] [PubMed] [Google Scholar]
- Korman TM, Grayson ML and Turnidge JD (1997) Polymicrobial septicaemia with Pseudomonas aeruginosa and Streptococcus pyogenes following traditional tattooing. J Infect 35, 203. [DOI] [PubMed] [Google Scholar]
- LeBlanc PM, Hollinger KA and Klontz KC (2012) Tattoo ink-related infections–awareness, diagnosis, reporting, and prevention. N Engl J Med 367, 985–987. [DOI] [PubMed] [Google Scholar]
- Lee JY, Kim SH, Jeong HS, Oh SH, Kim HR, Kim YH, Lee JN, Kook JK et al. (2009) Two cases of peritonitis caused by Kocuria marina in patients undergoing continuous ambulatory peritoneal dialysis. J Clin Microbiol 47, 3376–3378. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maloberti A, Betelli M, Perego MR, Foresti S, Scarabelli G and Grassi G (2015) A case of Pseudomonas aeruginosa commercial tattoo infection. G Ital Dermatol Venereol, Epub ahead of print. [DOI] [PubMed] [Google Scholar]
- Mathur DR and Sahoo A (1984) Pseudomonas septicaemia following tribal tatoo marks. Trop Geogr Med 36, 301–302. [PubMed] [Google Scholar]
- Porter CJ, Simcock JW and MacKinnon CA (2005) Necrotising fasciitis and cellulitis after traditional Samoan tattooing: case reports. J Infect 50, 149–152. [DOI] [PubMed] [Google Scholar]
- Serup J, Carlsen KH and Sepehri M (2015) Tattoo complaints and complications: diagnosis and clinical spectrum. Curr Probl Dermatol 48, 48–60. [DOI] [PubMed] [Google Scholar]
- Takahashi N, Shinjoh M, Tomita H, Fujino A, Sugita K, Katohno Y, Kuroda T and Kikuchi K (2015) Catheter-related blood stream infection caused by Dermacoccus barathri, representing the first case of Dermacoccus infection in humans. J Infect Chemother 21, 613–616. [DOI] [PubMed] [Google Scholar]
- Tena D, Martinez-Torres JA, Perez-Pomata MT, Saez-Nieto JA, Rubio V and Bisquert J (2007) Cutaneous infection due to Bacillus pumilus: report of 3 cases. Clin Infect Dis 44, e40–42. [DOI] [PubMed] [Google Scholar]
- Tena D, Fernandez C and Lago MR (2015) Alcaligenes faecalis: an unusual cause of skin and soft tissue infection. Jpn J Infect Dis 68, 128–130. [DOI] [PubMed] [Google Scholar]
- The Harris Poll (2015) Tattoo takeover: three in ten Americans have tattoos, and most don’t stop at just one. [Google Scholar]
- US Food and Drug Administration (2015). FDA warns tattoo artists and consumers not to use certain tattoo inks. A constituent Update retrieved from https://wayback.archive-it.org/7993/20170404185355/https://www.fda.gov/Food/NewsEvents/ConstituentUpdates/ucm457439.htm.
- Washington MA, Barnhill J and Griffin JM (2015) A case of wound infection with Providencia rettgeri and coincident gout in a patient from Guam. Hawaii J Med Public Health 74, 375–377. [PMC free article] [PubMed] [Google Scholar]
- Wenzel SM, Rittmann I, Landthaler M and Baumler W (2013) Adverse reactions after tattooing: review of the literature and comparison to results of a survey. Dermatology 226, 138–147. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Table S1 Detection of micro-organisms in tattoo and PMU inks according to companies.
Table S2 Microbial contamination in tattoo or permanent makeup inks associated with colours.
Table S3 A list of bacterial organisms identified in previous and current tattoo and PMU ink survey.