Volume 79, Issue 10 , Pages 587-593, October 2008
Microbial contamination associated with mascara use
Article Outline
Abstract
Background
Microbial organisms are normally present on human eyelashes. Application of mascara to lashes has the potential to inoculate the mascara tube with microbes. This pilot study of a real-world situation investigated the microbial contamination of 2 brands of mascara used daily for 3 months.
Methods
Forty women between the ages of 18 and 39 were randomly assigned to use 1 of 2 brands of nonwaterproof mascara. All mascara tubes were unexpired and purchased on the same day. Subjects were instructed to use the mascara on both the upper and lower lids every day for 3 months. After 3 months, the mascara tubes were collected, cultured, and examined for microbial growth.
Results
Mascara tubes were collected from 33 of 40 (82.5%) subjects who began the study. Microbial growth was found in 36.4% of the subject tubes. Based on growth on selective media, most of the organisms were determined to be Staphylococcus epidermidis, Streptococcus species, or fungi. We did not attempt to quantify the numbers of bacteria or fungi present within the tubes.
Conclusions
Because microbial presence was found in 36.4% of the mascara tubes cultured after 3 months of use, we recommend a maximum 3-month use of a mascara tube used on a daily basis. More frequent replacement may be warranted with further study.
Keywords: Bacteria, Cosmetics, Mascara, Microbial growth
Bacteria that cause serious infections often are organisms native to the human body.1, 2 Facial skin is covered with bacteria that are part of the normal ocular flora. Most require oxygen to survive.3 Haemophilus species (sp.), Staphylococcus sp., Pneumococcus sp., Corynebacterium sp., and Streptococcus sp. bacteria are commonly found on, or near, the eye. Although usually not harmful, under the right circumstances these bacteria frequently cause dangerous ocular infections.1, 2 A scratch or an abrasion in the corneal epithelium can allow these microorganisms to gain entry to the cornea and cause infection. Some pathogenic species can penetrate an intact corneal epithelium. Neisseria gonorrhoeae, Haemophilus aegyptius, Corynebacterium diptheroides, and Listeria sp. each are capable of penetrating an intact epithelium.4
In the United States, the majority of bacterial corneal infections in non-contact lens wearers are caused by Staphylococcus sp.5 Infections found in contact lens wearers are mostly from Pseudomonas aeruginosa, a pathogenic organism.6 Fungal species can be found on the normal ocular surface; however, they are not always considered to be a part of the normal ocular flora.3
The most common factor associated with bacterial infections of the ocular surface is the wearing of soft contact lenses.5, 7, 8 Soft contact lenses are implicated in half of all bacterial corneal infections.8 Contact lens wear, cosmetic use, and bacterial infection often occur together.
Corneal epithelial damage resulting from an improperly fitted soft contact lens or lens overwear creates a prime opportunity for the bacteria to invade the cornea.9 When mascara is used at the same time contact lenses are worn, the bacterial flora around the ocular surface may be increased. Therefore, the control of bacterial growth in the mascara tube is important to minimize the risk of infection.
Manufacturers use preservatives to keep cosmetics free of microbial contaminants. Wilson and Ahearn10 tested some of these preservative systems. Tubes of mascara were inoculated with strains of Staphylococcus epidermidis and P aeruginosa, organisms often implicated in corneal infections. A heavy growth of bacteria was seen in 2 of the mascara brands investigated (brand B and brand D), which used imidazolidinyl urea or p-hydroxybenzoate in their preservative formulation. A third brand of mascara (brand C) did not allow for additional microbial growth and had moderate bactericidal activity after 2 inoculations with microbes. However, this third brand of mascara contained approximately twice the concentration of p-hydroxybenzoate found in brand D. Wilson and Ahearn10 concluded that inadequate preservatives were the major factor in bacterial contamination of mascara samples. They also found that personal hygiene and product usage (i.e., addition of water to mascara) were factors as well. Interestingly, 6 of the 7 cases reported in the Wilson and Ahearn study involved patients scratching their cornea with a mascara applicator brush just before developing a Pseudomonas corneal infection.
The repeated use of mascara by multiple users at cosmetic counters creates greater exposure to contaminants. Repeated use of a mascara tube by a single user does the same thing, but at a slower rate. In a study by Wilson et al.11 preservatives in cosmetics were tested by inoculating new tubes of liquid eyeliner with bacteria. They concluded that to incapacitate the function of preservatives in the cosmetic, contaminants had to exceed 5,000 organisms per milliliter. They also found that P aeruginosa was only seen in eyeliners diluted with tap water.
Increased microbial content with increased usage was seen in a study by Wilson et al.12 as well. Their study determined the microbial content of numerous mascaras by culturing them before and after use. Several types were tested, including oil-based and water soluble–based brands. Cosmetics, as well as the skin and fingers of users, were cultured. Microbes isolated included Klebsiella pneumonia, Staphylococcus epidermidis, Bacillus sp., Corynebacterium sp., and the fungus Candida. Both the eyelids and the cosmetics of 22 patients with chronic eyelid inflammation yielded S epidermidis, a species linked to blepharoconjunctivitis.
Fungal contaminants have also been observed in mascara.10, 12, 13 The Penicillium sp. is the most common fungi observed in mascara, but Fusarium sp. is seen as well.10 Fusarium corneal infections are rare, but they have a great potential to cause permanent vision loss caused by corneal scarring.14
Cosmetics are defined by the U.S. Food and Drug Administration (FDA) as “articles intended for cleansing, beautifying, promoting attractiveness, or altering appearance.”15 The FDA established the Cosmetic Ingredient Review Program in 1976 to monitor the ingredients used in cosmetics. This program tests thousands of ingredients. Before a new product can be put on the market for consumer use, an expert panel must evaluate the item so that ingredients are ensured to be safe and efficacious. Ingredients are categorized as either “safe as used, safe with qualifications, unsafe, or insufficient evidence.”15 The panel then puts a label on each product with the appropriate indications, warnings, and active ingredients.16
The FDA does not require cosmetics to be sterile but does require that microorganisms that cause infection not be present.17 If the cosmetic contains microorganisms that do not cause infection, their density must be low. Manufacturers of cosmetics look for ways to keep their products free from contamination in the production stages.18, 19, 20 Most companies have difficulty with microorganism contamination because microbes can adapt to and survive in many environments. Therefore, product contamination is monitored continuously during manufacturing.
Once a product is manufactured, contamination must still be monitored. Contamination may be easy to determine, especially if a product has changed in color, odor, clarity, or thickness.20, 21 The United States Pharmacopeia “Total Aerobic Microbial Count (FN1)” is the standard test used in the cosmetic industry to determine the density of microorganisms.20 Organisms should be isolated and identified to evaluate their pathogenic potentials. The presence of gram-negative bacteria is unacceptable because of their high potential for pathogenicity. Gram-positive bacteria are less likely to become pathogenic and are accepted at low numbers of organisms.
Self-preserved cosmetics typically contain ethanol, propylene glycol, or glycerol.17 However, many manufacturers use ingredients such as tetrasodium edetate and trisodium as preservatives. Antimicrobials such as parabens and phenoxyethanol may also be used as part of the formulation in cosmetic products.22
When attempting to determine microbial content, researchers must use culturing techniques to isolate individual microbial types. Culturing can yield undesirable results unless steps are taken to maximize recovery.23 One technique to improve recovery of bacteria is to provide an adequate temperature of the agar plate. Because removing plates from the refrigerator can prolong time to desired temperature, plates often are warmed in an incubator. This is the technique used in most microbiology laboratories; however, in a clinical setting, warming rarely is done because clinicians often find themselves pressed for time.
Rudometkin et al.23 suggested that pathogens associated with corneal infection do not survive on a cold plate. Their research showed an increase in recovery by allowing the plate to warm to room temperature, and, in only one of their cases, recovery increased further when warmed by an incubator to 37°C. In the past, researchers thought that cold conditions only slowed the metabolism of organisms. In light of this study, cold conditions appear to be much more devastating than previously thought. The study also indicated that plates immediately incubated after culturing compared with plates with delayed incubation had similar recoveries, except in the case of S pneumoniae. S pneumoniae had decreased bacterial recovery when there was a delay in returning plates to the incubator.
To avoid infection associated with contamination, many doctors recommend that cosmetics be replaced every 6 months for non–contact lens wearers and every 3 to 4 months for those who wear contact lenses.24, 25, 26, 27 Appropriate use of mascara is recommended as well. Recommendations include: (1) do not share cosmetics, (2) replace cosmetics after bacterial infections, (3) do not use old applicators in new containers of cosmetics, and (4) insert contact lenses before applying mascara.24, 27
The Avon company, a top-10 cosmetic company, recommends that mascara be discarded after 3 months.28, 29 Most people, however, will not throw their makeup away until the makeup is gone. Some will add water, and even saliva, to make their makeup last longer.25 A survey done at the University of Alabama showed the reported range of cosmetic age was anywhere from 6 months to 5 years.30 This same study reported that 25% of the eye makeup cultured contained viable microbes. When limited to only mascara, the percentage increased to 37%.
Even though infection attributable to mascara contamination is rarely documented, it likely occurs. Often, in a busy clinical environment, treating the infection is of greater concern for doctors than determining the source of the infection. Because ocular surface infections have the potential to cause devastating effects on vision, there is a need for further study of preservative efficacy in cosmetics being used today.
Our study looked at microbial contamination of 2 brands of nonwaterproof mascara after 3 months of daily use. The 2 mascara brands investigated were made by 2 of the top 10 cosmetics companies ranked by Global Cosmetics Industries.29
Methods
The approval of the use of human subjects was obtained from the Northeastern State University Human Experimentation Advisory Committee before beginning the study. Potential subjects completed a prestudy questionnaire. If a current eyelid disease, an eyelid disease within the last 6 months, or oral or topical antibiotic use was noted on the prestudy questionnaire, the potential subject was excluded from participation. Reports of itching or burning eyes, a mucous or watery discharge from the ocular surface, eyelid pain or irritation, or trauma of the eyelid or eye also resulted in exclusion. Because dry eye problems are more prevalent in women as they age, anyone older than 40 years of age was excluded because of increased risk of ocular infection. Contact lens wearers were not excluded; however, contact lens type (gas-permeable or soft lenses) was noted.
Once they were offered the opportunity to participate and they accepted, subjects agreed to continue their normal daily hygiene routine for 3 months. No specific hygiene regimen was given. Brief ocular examinations were performed at the beginning of the study to rule out any pre-existing pathology of the ocular surface or eyelids. We documented the presence or absence of lid debris, conjunctival injection, eyelid redness, mucous or watery discharge, loss of lashes, collarettes, and mattering. Potential subjects were excluded if any ocular surface or eyelid pathology was present.
Informed consent was obtained from 40 women between the ages of 18 and 39 who agreed to complete the study. The women were randomly assigned to use 1 of 2 brands of nonwaterproof mascara purchased on the same day by the investigators. An unused, unexpired tube of either Beyond Color Mascara by Avon (New York, New York) or Great Lash® Mascara by Maybelline® (New York, New York) was distributed to each subject at the beginning of the study (see Figure 1, Figure 2). The distributed mascara samples were labeled A1 through A20 for Avon and B1 through B20 for Maybelline for tracking purposes. Subjects were asked to use the mascara daily, on the upper and lower lashes of both eyes, for 3 months. To track compliance with mascara usage, subjects were given a log sheet to record the days the mascara was worn. Subjects were allowed to wear other cosmetics but were asked not to wear anything on the eyelashes besides the assigned mascara.
Figure 1.
Sample of the Beyond Color Mascara by Avon used in this study.
Figure 2.
Sample of the Great Lash® Mascara by Maybelline® used in this study.
At the end of the 3-month period, 33 of the 40 subjects were available for an objective examination and sample collection. The remaining 7 subjects could not be reached for collection of the samples. Each available subject was given a brief ocular examination and asked to complete a poststudy questionnaire. Again, examinations documented the presence or absence of lid debris, conjunctival injection, eyelid redness, mucous or watery discharge, loss of lashes, collarettes, and mattering. Poststudy questionnaires were evaluated to determine if subjects reported any treatment for eyelid disease and if any ocular medications or oral antibiotics were used by the subject. Questionnaires were also evaluated for reports of itching or burning eyes, a mucous or watery discharge from the ocular surface, eyelid pain or irritation, or trauma of the eyelid or eye.
Immediately upon collecting a used tube of mascara, an investigator took a sample and stored it using BBL Culture Swab Plus transport medium (Becton Dickinson and Company, Sparks, Maryland; see Figure 3). The BBL Culture Swab Plus was brushed against a mascara applicator wand, capped, and stored at room temperature. Because all tubes could not be collected at the same time, storage time varied from 17 to 69 hours. Once all samples were collected, the culture swabs from each sample were plated on mannitol salt, blood, and chocolate agar media plates. The plates were equilibrated to room temperature at the time of culturing. All plates were inoculated using the Streak Method illustrated in Figure 4.
Figure 3.
Disassembled BBL Culture Swab Plus transport device used to transfer samples.
Figure 4.
The Streak Method used to plate mascara samples.
Samples from 39 tubes of mascara were plated. This included 33 subject tubes (16 Avon and 17 Maybelline) and 6 unused environmental control tubes (3 each of both companies). Control tubes were cultured at the same time as subject tubes. The Avon control tubes were labeled A21 through A23; the Maybelline control tubes were labeled B21 through B23 for tracking purposes.
Immediately after culturing, all plates were placed in an incubator. The plates were incubated at 37°C for 32 hours and then evaluated. Each plate was examined for microbial growth characteristics and number of colonies. The percentage of each brand of mascara that showed microbial growth was calculated. Microbes were identified using the Gram staining method.
Staphylococcus sp. were identified by the appearance of clusters of cocci upon microscopic observation.31 The species was further differentiated into Staphylococcus aureus and Staphylococcus epidermidis because S aureus ferments mannitol salt and gives a yellow halo, whereas S epidermidis does not.
Streptococcus sp. were determined by growth on blood agar and a chain appearance under the microscope.31 Alpha hemolytic Streptococcus shows a green zone around the colony. Beta hemolytic Streptococcus has a clear zone around the colony, whereas gamma hemolytic Streptococcus shows no zone around the colony.
Gram-positive rods could be identified by their appearance.31 Propionibacterium acnes forms small white-to-pink colonies and are rod shaped under the microscope. Corynebacterium presents as opaque white to gray colonies that are rod-shaped.
If present, Haemophilus and Neisseria gram-negative rods have growth on chocolate, but not blood agar.31 Another gram-negative rod, P aeruginosa, produces pyocyanin. Isolates on blood agar that appear green, have a fruity odor, and are beta hemolytic can be presumed to be Pseudomonas.
Because fungal infections are rare, specific species of fungi were not differentiated for this study.31 However, the presence of fungus was noted and determined by feathery borders on culture plates and a tubulelike appearance upon microscopic examination.
If a particular agar plate showed multiple colonies of the same appearance, 3 of each of the similar colonies were stained to determine the microbe. When all 3 colonies stained were found to be the same microbe, all of the remaining colonies of similar appearance on the media plate were assumed to be the same bacteria or fungus.
Results
None of the subjects indicated any symptoms of itching, burning, or irritation on the prestudy questionnaire, yet several were on medications that are often prescribed for ocular irritation. Four subjects were using combination antihistamine/anti-inflammatory drops. Three were using Patanol® (Alcon, Fort Worth, Texas), and one was using Elestat® (Allergan, Inc., Irvine, California, and Inspire Pharmaceuticals, Inc., Durham, North Carolina). Four other subjects were using artificial tears at the beginning of the study or had used artificial tears within the 6 months preceding the study.
Four subjects reported eyelid irritation during the study. Each of these subjects was advised to discontinue mascara wear and was offered a free ocular health examination. Three subjects declined; the 1 subject who sought treatment independently was treated with fluoroquinolone drops (Vigamox®; Alcon).
Eight other subjects failed to report ocular irritation to researchers until after the study was completed, but each independently sought treatment for their symptoms. Only the medication used to treat their symptoms was reported to us. We did not know the condition for which they were treated. One was treated with steroid (Lotemax®; Bausch & Lomb Inc., Tampa, Florida) and 2 different antihistamine/anti-inflammatory drops, Patanol® and Optivar® (MedPointe Pharmaceuticals®, Somerset, New Jersey), 2 were treated with Vigamox ophthalmic drops alone, 2 were treated with Patanol drops alone, 1 was treated with an antibiotic/steroid (Tobradex®; Alcon) and artificial tears, 1 was treated with Tobradex drops alone, and 1 was treated with artificial tears alone. All 8 of these subjects completed the study and showed no signs of infection when examined at the end of the 3-month period.
Other relevant data collected from the poststudy questionnaire were that 1 subject reported the presence of styes but was not treated. Two subjects were treated with systemic antibiotics for other infections during the study. Ocular trauma from mascara application was not reported by any of the subjects.
Contact lens wear was also noted in this study. Thirteen of the 33 subjects returning tubes of mascara were contact lens wearers. Only 1 wore gas-permeable lenses. Of the 13 contact lens wearers, the mascara tubes from 2 of soft lens wearers showed evidence of growth on culture plates.
Twelve of the 39 cultured mascara samples showed microbial growth, with 2 of those being environmental control tubes for the Avon brand mascara (see Table 1). None of the Maybelline control tubes were positive for microbial growth. For each brand, 5 tubes of mascara used by subjects showed microbial growth. Avon brand mascara had growth in 5 (31.3%) of the 16 tubes, and Maybelline brand mascara showed presence of bacteria or fungi in 5 (29.4%) of 17 tubes.
Table 1. An overview of growth from mascara swabs on plated media
| Mascara | Number of tubes tested | Growth on blood agar | Growth on chocolate agar | Growth on Mannitol salt agar | Total number of tubes with microbial growth |
|---|---|---|---|---|---|
| Avon | 16 | 4 | 1 | 0 | 5 (31.3%) |
| Maybelline | 17 | 5 | 3 | 0 | 5 (29.4%) |
| Avon control | 3 | 1 | 1 | 0 | 2 (66.7%) |
| Maybelline control | 3 | 0 | 0 | 0 | 0% |
| Total | 39 | 10 | 5 | 0 | 12 (36.4%) |
Using the previously described method of determining bacterial type, 2 tubes showed S epidermidis growth, 8 showed Streptococcus growth, and 4 showed fungal growth. Bacteria or fungi were present in 30.3% of the 33 tubes collected from subjects at the end of 3 months.
Discussion
During the 3-month course of our study, 8 subjects were known to be treated for ocular surface symptoms. Although there was treatment for eye disease, the disease itself was neither reported nor identified to us. However, reported incidents of symptoms and treatments led the investigators to believe that other subjects may also have experienced unreported symptoms. Because subjects admitted to symptoms suggestive of ocular surface infections yet continued to wear the mascara, the argument could be made that they strongly influenced our results. However, we were studying daily, real world mascara use in which mascara preservatives must be effective.
Previous studies found that bacterial content increased with increased use of an ocular cosmetic.10, 12 Because our study only determined microbial presence and not microbial quantity, we can only determine if bacterial presence was a greater likelihood in mascara tubes used for longer periods. In our study, an average of 79.7 days of mascara use was seen in tubes that had microbial growth, and an average of 80.8 days of mascara use was seen in tubes that had no microbial growth. These results appear to infer no relationship between increased use of mascara wear and the presence of microbial contamination. Mascara tube contamination often appeared to be a characteristic of individual subjects. Given that it is impossible for a mascara user to periodically culture her mascara tube, common sense indicates that shorter use is better than longer use. We feel that a 3-month use of a single tube of mascara should be a maximum safe time.
Another interesting aspect of this study is that in the Avon brand mascara, 2 of the 3 control tubes of mascara showed evidence of bacterial growth. Each grew one small colony of hemolytic Streptococcus. This could be caused by factory contamination of the tubes or by the conditions under which the plating and culturing were performed. In our study, 2 lots from each brand were used, but in the Avon control mascara tubes, growth was seen in tubes from both lots. We are uncertain whether factory contamination or contamination caused by our clean, but not sterile, working conditions was responsible for microbial growth in the 2 Avon controls. If our working conditions led to contamination, then, logically, all plates should have been affected. In a future study, we plan to use 1 control tube for every participant tube and to sample the control tube and participant tube at the same time.
Because past studies suggested that pathogens are not likely to survive if plated onto cold media plates,23, 32 the media used in this study were stored at room temperature 24 hours before plating to ensure the plates warmed to room temperature. The plates were not opened until inoculation occurred. In addition, the plates were not further warmed to incubator temperature of 37°C because Rudometkin et al.23 suggested that further warming of the media plates to 37°C did not increase the recovery of microbes.
The bacteria isolated in this study were limited to S epidermidis and gamma hemolytic Streptococcus. These results are similar to those of Wilson et al.12 who found that several subjects with infections yielded S epidermidis.
Only 3 of the 12 subject tubes that produced growth showed multiple colonies. The remainder of the 12 tubes grew single colonies, which may or may not be significant. Although keeping mascara free from all microbial growth is the goal of a preservative, keeping quantities low is also noteworthy. As mentioned previously, Wilson et al.11 found that for the preservative function to be inefficient in protecting wearers from infection, the contaminants had to exceed 5,000 cells per milliliter. Our study had no regard for exact cell quantity; rather, the existence versus absence of microbial growth was the measure.
Because the Staphylococcus species are a part of the normal ocular flora and S aureus is the most likely culprit of infection in non–contact lens wearers,5 the fact that the mannitol salt agar showed no evidence of growth was surprising because growth of the S aureus species is seen on this media.31 S epidermidis, however, was found in 2 of the tubes of mascara collected from subjects. Preservatives in mascara are likely designed to be most effective at killing the most likely causes of microbial infection. This may also be the reason that no gram-negative bacteria, such as P aeruginosa, were found because this species is the likely offender of infection in contact lens wearers.6
Conclusion
Some clinicians recommend different replacement times of cosmetics for contact lens wearers than for non–contact lens wearers.26, 28, 29, 30 Because we saw growth in both contact lens wearers and non–contact lens wearers, we suggest that a mascara tube be discarded after a maximum of 3 months' use, providing the mascara has been used daily. (Microbial growth of mascara used on an infrequent basis was not addressed in this study.) Further study is needed to determine if a more frequent replacement of mascara is indicated. In addition, we suggest that mascara tubes be discarded when patients show signs of ocular surface disease that may or may not warrant an antibiotic.
Disclaimer
The authors have no affiliation with any of the companies whose products were used or mentioned in this article.
Acknowledgments
The authors thank Dr. Jeff Miller, Sandra Martin, and David Hayes for their assistance during the study. The authors also thank St. Edwards Mercy Medical Hospital of Fort Smith, Arkansas, for its donation of culturing supplies.
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PII: S1529-1839(08)00379-5
doi:10.1016/j.optm.2008.02.011
© 2008 American Optometric Association. Published by Elsevier Inc. All rights reserved.
Volume 79, Issue 10 , Pages 587-593, October 2008
