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Acknowledgement to Reviewers of Cosmetics in 2015
Open AccessArticle

Microbiologically Contaminated and Over-Preserved Cosmetic Products According Rapex 2008–2014

Department of Biotechnologies, Chemistry and Pharmacy, University of Siena, Via Aldo Moro 2, Siena 53100, Italy
*
Author to whom correspondence should be addressed.
Academic Editors: Lidia Sautebin and Immacolata Caputo
Cosmetics 2016, 3(1), 3; https://doi.org/10.3390/cosmetics3010003
Received: 25 December 2015 / Revised: 21 January 2016 / Accepted: 25 January 2016 / Published: 30 January 2016

Abstract

We investigated the Rapid Alert System (RAPEX) database from January 2008 until week 26 of 2014 to give information to consumers about microbiologically contaminated cosmetics and over-preserved cosmetic products. Chemical risk was the leading cause of the recalls (87.47%). Sixty-two cosmetic products (11.76%) were recalled because they were contaminated with pathogenic or potentially pathogenic microorganisms. Pseudomonas aeruginosa was the most frequently found microorganism. Other microorganisms found were: Mesophilic aerobic microorganisms, Staphylococcus aureus, Candida albicans, Enterococcus spp., Enterobacter cloacae, Enterococcus faecium, Enterobacter gergoviae, Rhizobium radiobacter, Burkholderia cepacia, Serratia marcescens, Achromabacter xylosoxidans, Klebsiella oxytoca, Bacillus firmus, Pantoea agglomerans, Pseudomonas putida, Klebsiella pneumoniae and Citrobacter freundii. Nine cosmetic products were recalled because they contained methylisothiazolinone (0.025%–0.36%), benzalkonium chloride (1%), triclosan (0.4%) in concentrations higher than the limits allowed by European Regulation 1223/2009. Fifteen products were recalled for the presence of methyldibromo glutaronitrile, a preservative banned for use in cosmetics. Thirty-two hair treatment products were recalled because they contained high concentrations of formaldehyde (0.3%–25%).
Keywords: microbiologically contaminated; over-preserved cosmetics; formaldehyde; RAPEX microbiologically contaminated; over-preserved cosmetics; formaldehyde; RAPEX

1. Introduction

The European Commission (EC) has an early warning system for safety management called the Rapid Alert System (RAPEX). In the database of this system we can find information about dangerous cosmetic products sold in EU markets. Dangerous cosmetic products pose a risk to the consumers due to the presence of certain substances which are banned or the use of which is restricted in these products under cosmetic legislation [1].
Cosmetic products are recognized to be substrates for the survival and development of a large variety of microorganisms, since they posses some of the nutrients that facilitate growth such as water, lipids, polysaccharides, alcohol, proteins, amino acids, glycosides, peptides and vitamins [2]. The presence of pathogenic microorganisms in cosmetic products can pose a health risk for consumers. The use of preservatives, Good Manufacturing Practices (GMP) and quality control programs has improved the quality, but several studies have reported cases of contaminated cosmetic products [3,4,5,6,7,8]. Studies have shown that the most frequently found microorganisms in cosmetics are P. aeruginosa, K. oxytoca, B. cepacia, S. aureus, E. coli, C. albicans, E. gergoviae, and S. marcescens, but also other bacteria, fungi, and yeasts. Skin and mucous membranes are protected from microorganisms; however, these may be damaged and slight trauma may be caused by the action of some cosmetics that may enhance microbial infection [9]. Research studies have shown cases of infections caused by contaminated cosmetics [10,11,12]. According to SCCP’s (Scientific Committee on Consumer Products) “Notes of Guidance”, cosmetic products are divided into two different categories: (1) Products specifically intended for children under three years or to be used in the eye area and on mucous membranes and (2) other products. Products intended for use on babies and the eye area (category 1) should have not more than 102 Cfu/g or mL of aerobic mesophilic microorganism (other products not more than 103 Cfu/g or mL). Staphylococcus aureus, Pseudomonas aeruginosa, Candida albicans or Escherichia coli must not be detectable in 0.5 g or 0.1 mL of product category 1 and in 0.1 g or 0.1 mL of product category 2 [13]. To prevent the microbial contamination of cosmetic products, chemical substances with known antimicrobial properties are used. The EU regulation 1223/2009 provides a list of allowed preservatives in cosmetic products with maximum concentrations in ready-for-use preparation. Preservatives are known as one of the most relevant allergens found in cosmetic products [14,15]. Studies suggest that the problem is much bigger because contact dermatitis prevalence appears to be underestimated [16]. In recent years a significant increase in cases of methylisothiazolinone contact allergy (MI) has been reported [17,18,19,20,21].

2. Experimental Section

We used the RAPEX database to find microbiologically contaminated cosmetic products from January 2008 until week 26 of 2014. We also selected recalled cosmetic products with high concentrations of preservatives.

3. Results and Discussion

3.1. Microbiologically Contaminated Cosmetics

The risks of recalled cosmetic products were divided in two categories: chemical and microbiological. Chemical risks were the leading cause of the recalls (87.47%). Sixty-two cosmetic products contaminated with microorganisms were recalled during this period. The most frequently found microorganism was the pathogenic Pseudomonas aeruginosa (35.48%). Other microorganisms found were: mesophilic aerobic microorganisms (bacteria, yeast and molds), Burkholderia cepacia, Klebsiella oxytoca, Serratia marcescens, Enterobacter gergoviae, Enterobacter cloacae, Staphylococcus aureus, Achromabacter xylosoxidans, Rhizobium radiobacter, Candida albicans, Pantoea agglomerans, Citrobacter freundii, Pseudomonas putida, Enterococcus faecium and Klebsiella pneumoniae. The types of cosmetic products contaminated were different: skin lightening products, eye creams, eye make-up products, children’s shampoos, skin care products, baby creams, baby balms, toothpastes (Table 1). The recalled products were notified by 14 different countries and 41.67% of them were notified by Germany. The number of recalled contaminated cosmetic products was higher in the last two years (2013, 2014).
In 21 cosmetic products (33.87%), Pseudomonas were present, especially Pseudomonas aeruginosa. P. aeruginosa is a pathogenic Gram-negative bacteria frequently found in cosmetics but also in ophthalmic preparations and, as such, is responsible for a variety of infectious diseases affecting the eye and surrounding tissues (corneal ulcer, bacterial keratitis) [22,23,24,25,26]. Six hair shampoo products were contaminated with P. aeruginosa or P. putida and these products can come in contact with eyes. These bacteria are widely recognized as nosocomial infection–causing pathogens [27,28]. P. aeruginosa in some cases had showed resistance to preservatives in cosmetic products.
Burkholderia cepacia, an opportunistic pathogen, was found in five products: make-up remover, bath gel, mouth spray and mouth wash, body scrub products (4.1 × 105–100 × 105 Cfu/g). Other studies have showed that the presence of B. cepacia in products used for mouth hygiene has frequently been implicated in B. cepacia infection [29,30,31]. Contamination of cosmetics and pharmaceuticals with B. cepacia is also a frequent problem in the United States and it is a cause of major product recalls [32,33,34]. B. cepacia can cause diseases primarily among immuno-compromised populations [35].
Table 1. Microbiologically contaminated products.
Table 1. Microbiologically contaminated products.
Contaminated ProductMicroorganismsCfu/gCountry of Origin
Shea butterP. aeruginosa, S. aureus, C. albicans1000Germany
Children’s make-up setMesophilic aerobic microorganism1300Hong Kong
Skin lightening productAerobic mesophilic flora1083Spain
Make-up removerBurkholderia cepaciaNot specifiedAustria
Massage creamS. aureusNot specifiedAustria
Cleasing milkTotal aerobic mesophile (yeast and mold)430,000/820,000/6,000,000/7,500,000Italy
Cotton budsP. aeruginosaNot specifiedTurkey
Natural hair dyeMesophilic aerobic microorganism140,000/19,000/26,000Czech Republic
Skin lotionP. aeruginosa19,000,000Hungary
Massage gelEnterobacteriaceae5,100,000Thailand
Eye creamE. gergoviae290,000Israel
Herbal tooth powderP. aeruginosa, K. pneumonie, E. faecium540,000India
MouthwashAerobic mesophileNot specifiedUnited Kingdom
ToothpasteMesophilic aerobic microorganisms1,100,000Not specified
Shampoo/shower gelE. cloaceae-C. freundii, P. putida, K. pneumoniae1,100,000/19,000,000Germany
Body paint powderP. aeruginosa3000/15,000United Kingdom
Henna Hand paintP. agglomerans, B. firmus2,600,000India
Hand soapK. oxytocaHighUnknown
ToothpasteEnterobacteriaceae10,000/1600Ireland
Bath gelB. cepacia10,000,000China
Mouth spray and mouth washB. cepaciaNot specifiedGermany
Hand creamP. aeruginosaNot specifiedSwitzerland
Eye make-upAerobic mesophilic flora5000Pakistan
Skin care productAerobic mesophilic flora, A. xylosoxidans3,000,000Poland
Body scrubMesophilic bacteria, B. cepacia480,000China
Hand washing pasteP. aeruginosa8,200,000Germany
Make-up setMouldNot specifiedChina
Rose facial milkP. aeruginosa600Germany
Shampoo-HairP. aeruginosa570,000Philippines
Sun creamP. aeruginosaNot specifiedCzech Republic
Bath milk for babiesS. marcescensNot specifiedGermany
Tattoo inkAerobic mesophiles, P. aeruginosa, yeasts3,600,000/1,100,000/900,000United States
Anti-wrinkle serumPseudomonas.spp15,000United States
Natural hair dyeNot specified300,000Russian Federation
Fitness gelB. cepacia410,000–520,000Turkey
Eye contour creamR. radiobacterNot specifiedFrance
LubrificantMesophilic microorganisms (yeast)Not specifiedFrance
Herbal shampooP. aeruginosaNot specifiedIndia
Hair dyeMesophilic aerobic microorganismNot specifiedCzech Republic
Skin creamP. aeruginosa, mesophilic bacteria13,000Germany
Hair dyeMesophilic aerobic microorganismNot specifiedCzech Republic
Hair dyeMesophilic aerobic microorganismNot specifiedCzech Republic
Baby creamNot specified3168Germany
Hair dyeMesophilic aerobic microorganismNot specifiedIndia
Hair dyeMesophilic aerobic microorganismsNot specifiedIndia
Shower gelAerobic mesophilic bacteria50,000United Kingdom
Hair dyeMesophilic aerobic microorganisms370,000Germany
Marmot fatAerobic mesophilic bacteria, P. aeruginosa760,000/610,000Denmark
Children‘s shampooE. gergoviaeNot specifiedUnknown
Shampoo and bath gelMesophilic aerobic microorganismsNot specifiedUnknown
Skin creamAerobic mesophilic bacteria, E. gergoviae120,000Germany
Liquid hand soapMesophilic aerobic microorganismsNot specifiedUnknown
Hair dyeMesophilic aerobic microorganisms90,000Germany
Hand cleaning pasteAerobic mesophlic bacteria , E. gergoviae19,000,000Unknown
Baby balmP. aeruginosaNot specifiedBelgium
Tinted day creamP. aeruginosa3,000,000Italy
Skin creamP. aeruginosa, aerobic mesophilic bacteria60,000/2,600,000Germany
ShampooP. aeruginosa, aerobic mesophilic bacteria27,000Germany
Hair shampooP. putida, P. aeruginosa24,000/8700Austria
CreamE. gergoviae4,400,000/160,000Germany
Sun lotionE. cloacae, E. faecium, E. spp.8,000,000Austria
Hair shampooP. aeruginosa10,000Germany
Staphylococcus aureus was found in two products: shea butter and massage cream. S. aureus is also one of the most frequently found contaminants in cosmetic products [36]. S. aureus is a Gram-positive microorganism and a potential human pathogen which can cause impetigo and conjunctivitis [37]. Enterobacter gergoviae was present in eye creams and children’s cosmetic products (shampoo, foam soap, gel, creams and lotions, skin cream, etc.) at concentrations of 1.6 × 105–44 × 105 Cfu/g. E. gergoviae is naturally resistant to parabens at the concentrations used in cosmetics [38,39]. The germs are often resistant to antibiotics and this makes treatment more difficult. Serratia marcescens is a Gram-negative bacillus (Enterobacteriaceae). S. marcescens was generally considered non-pathogenic for humans [40], but since the 1950s has become an important cause of nosocomial infection [41]. Infants are at the greatest risk of S. marcescens infection (severe septicemia) or colonization [42,43,44,45]. Baby death has been reported from S. marcescens meningitis and septicemia after use of contaminated baby shampoo [46]. One recalled product was bath milk for babies and it was contaminated with S. marcescens. Two recalled products were contaminated with Klebsiella pneumoniae, a shampoo/shower gel and an herbal tooth powder. Klebsiella pneumonia, a Gram-negative bacterium in the Enterobacteriaceae family, is a human pathogen and can cause severe fulminating pneumonia [47]. Klebsiella present in hand creams and liquid soaps in the past has caused epidemic septicemia in patients with intravenous catheters [48]. Molds and yeasts were also present in two products. A make-up set was contaminated with mold which, according to RAPEX, may cause irritation, inflammation to skin around the eye, respiratory infection if inhaled or loss of eye sight. Candida albicans was isolated in one product (shea butter, Germany).
Rhizobium radiobacter (known as Agrobacterium radiobacter) was present in an eye contour cream product. It is usually of low virulence in humans and rarely acts as an opportunistic human pathogen [49].

3.2. Over-Preserved Cosmetic Products

Twenty-four cosmetic products were recalled because they contained methylisothiazolinone (0.025%–0.36%), methyldibromo glutaronitrile, triclosan (0.4%) and benzalkonium chloride (1%) in concentrations higher than the limits allowed by European Regulation 1223/2009 (Table 2).
Table 2. Over-preserved cosmetics.
Table 2. Over-preserved cosmetics.
ProductPreservativeCountry of OriginConcentration
Shower GelMethyldibromo glutaronitrileRussiaNot specified
Skin creamMethyldibromo glutaronitrileSpainNot specified
ShampooMethyldibromo glutaronitrileItalyNot specified
Shampoo “Tea tree oil”Methyldibromo glutaronitrileRussiaNot specified
Shower gelMethyldibromo glutaronitrileRussiaNot specified
Hair straightening treatmentMethyldibromo glutaronitrileUnited StatesNot specified
Skin lightening creamMethyldibromo glutaronitrileSouth AfricaNot specified
Shampoos and haircare productsMethyldibromo glutaronitrileItalyNot specified
Shower gelMethyldibromo glutaronitrileTurkeyNot specified
WetwipesMethyldibromo glutaronitrileTurkeyNot specified
Children’s shampooMethyldibromo glutaronitrileUkraineNot specified
Children’s shampooMethyldibromo glutaronitrileUkraineNot specified
Liquid cleanserMethyldibromo glutaronitrileItalyNot specified
CreamsMethyldibromo glutaronitrileGermanyNot specified
Hair straightening treatmentMethyldibromo glutaronitrileUnited StatesNot specified
Facial maskMethylisothiazolinoneRussian Federation0.03%
Baby care creamMethylisothiazolinoneRussian Federation0.027%
Body mousseMethylisothiazolinoneRussian Federation0.028%
Body butterMethylisothiazolinoneRussian Federation0.026%
Foot creamMethylisothiazolinoneRussia0.03%–0.08%
Foot creamMethylisothiazolinoneRussian Federation0.36%
Facial maskMethylisothiazolinoneRussian Federation0.025%
Eyelash enhanserBenzalkonium chlorideChina1%
Children creamTriclosanSpain0.4%
Fifteen cosmetic products recalled (shower gels, skin creams, shampoo and children’s shampoo, wet wipes) contained methyldibromo glutaronitrile. This preservative has been banned in EU countries because of increasing rates of contact allergy [50,51,52,53].
Seven cosmetic products recalled contained the preservative methylisothiazolinone (0.01% or 0.0015% of a mixture in the ratio 3:1 of methylchloroisothiazolinone and methylisothiazolinone) in excess (0.025%–0.36%) of the approved concentration limit. The country of origin of the products was the Russian Federation. MI is a sensitizing agent and may cause skin sensitization and allergic skin reactions when it exceeds the approved maximum concentration [54,55]. MI is also is an emerging allergen in the pediatric population. Wet wipes with MI were frequently the cause of allergy contact dermatitis [56,57,58,59,60].
One product contained benzalkonium chloride in a concentration 10 times higher than the maximum allowed (eyelash enhancer, 1%). Benzalkonium chloride is a well-recognized irritant for skin and eyes at concentrations greater than 0.1%. According to EU regulation 1223/2009, contact of benzalkonium chloride with eyes should be avoided.
Thirty-two cosmetic products contained formaldehyde (0.3%–25%) in concentrations higher than the limits allow (Table 3). All products recalled were hair treatment products. In the European Union, formaldehyde is not authorized as an active ingredient in hair straightening products. Formaldehyde is a chemical substance used in cosmetics as a preservative for its antimicrobial properties. According to Cosmetics Regulation 1223–2009 Annex V, formaldehyde can be used in oral products in concentrations of not more than 0.1% (free formaldehyde) and 0.2% in other products. Formaldehyde can also be used in nail-hardening products at concentrations of up to 5% (Annex III).
Table 3. Cosmetic products with high concentration of formaldehyde.
Table 3. Cosmetic products with high concentration of formaldehyde.
ProductConcentrationCountry of Origin
Stabilizer for cosmetics25%Spain
Hair straightening treatment1.6%Italy
Hair treatment product3.5%United States
Hair treatment product0.3%United States
Hair treatment product2.89%Brazil
Hair straightening6.7%Brazil
Hair treatment product7.0%Brazil
Hair treatment1.6%United States
Hair treatment1.7%United States
Hair straightening product2.15%China
Hair treatment1.7%Brazil
Hair treatment1.8%, 1.9%United States
Hair treatment product1.77%Italy
Hair treatment1.7%, 2%United States
Hair treatment product0.5%, 0.8%Brazil
Hair treatment product0.9%, 1.5%, 1.6%, 1.7%Brazil
Hair straightening treatmentFree formaldehyde 8.85% and 9.5%United States
Hair treatment product2.64%Brazil
Hair treatment product0.61%Brazil
Hair treatmentFree formaldehyde 1.9% and 1.7%United States
Hair treatment2.0%United Kingdom
Hair treatment product7.7% free and liberated formaldehyde and 7.4% free formaldehydeBrazil
Hair treatment product2.3%Unknown
Hair treatment products1.0%, 1.3%, 1.7%, 10.8%Mexico
Hair treatment product0.95%, 0.7%, 2.3%, 2.4%, 2.5%, 2.6%Brazil
Hair straightening product0.98%Brazil
Cosmetics pack0.7%Brazil
Hair straightener2.6%United States
Hair straightening treatment0.49%United States
Hair lotion2%Italy
Hair treatment products>1.2%United States
Hair treatment product1.4%Brazil
Formaldehyde is classified as a carcinogen [61,62]. Some epidemiologic studies have also found increased numbers of nasopharyngeal carcinoma and leukemia in humans exposed to formaldehyde [63].

4. Conclusions

European consumers are exposed to microbiologically contaminated and over-preserved cosmetic products. Hair treatment products with high concentrations of formaldehyde were also found. These products may pose a health risk to consumers. Measures must be taken to guarantee the safety of cosmetic products.

Author Contributions

The authors have equally contributed in data analyzing and paper writing.

Conflicts of Interest

The authors declare no conflict of interest.

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