1. Introduction
Currently, most cosmetics are based on artificial chemicals, although there is increasing interest in products formulated on natural compounds to reduce exposure to endocrine disruptors present in many artificial goods [
1]. Civilizations throughout human history have used different natural compounds to decorate their bodies [
2] as part of their daily rituals [
3]. Analyses of the chemical composition of these cosmetic products, as well as the consequences of their use, had not been thoroughly addressed until the mid-20th century. Some substances can enter the body through the skin, usually at lower rates than through oral ingestion or inhalation [
4]. As is the case for any chemical compound introduced into the human body, some of these cosmetics show clear benefits, while others are harmful to human health [
5] depending on the exposure mode, dose, and frequency of application.
Kohl (also known as surma) is a traditional cosmetic based on antimony (stibnite, Sb2S3) and used as a (medicinal) eye drop in ancient Egypt [
2,
6]. Over the past decades, the most common composition of kohl has been changed to galena stone, based on lead (Pb2SO4), and has become very popular in the Middle East, North and East Africa, and Asia (particularly Pakistan, Bangladesh, Nepal, India, and Iran). The popularity of kohl among these populations is not only cosmetic or cultural, but also by the believe it has therapeutic effects on eyes and as coagulant, especially in newborns and infants [
7,
8,
9]. Antimony (Sb) is more expensive and scarcer than lead (Pb), which explains the increase in the use of the latter. In addition, Pb has been widely used by ancient physicians in the treatment of their patients, including children, and maintained over time [
10]. Other components, such as carbon, titanium, or iron (gives kohl its characteristic red sheen) are also found in kohl specimens [
11]. The amount and nature of the materials employed in kohl vary widely depending on where it is produced and the desired final color.
Some studies highlight the ophthalmic benefits of kohl as antimicrobial and stimulator of non-specific immunological defenses due to its ability to induce the production of nitric oxide [
12]. On the other hand, there is evidence of the potential health risk of these cosmetic products due to their high content of heavy metals [
13]. The human body needs certain heavy metals at specific amounts for different processes, while some elements, such as Pb or mercury, show no benefits and result in toxicity. Moreover, metals considered essential for the general homeostasis can generate toxic effects in human tissues and organs when are in excess.
Pb is mainly responsible of kohl’s toxic effects, being associated with high concentrations of this element in blood samples from regular users of this cosmetic [
14,
15,
16]. Several studies have demonstrated that Pb levels are extremely high in this product and its use has been associated with the development of plumbism [
17]. Pb is particularly harmful to the developing brain [
18,
19,
20,
21]; thus, pregnant women and children are particularly vulnerable to kohl exposure. Developmental anomalies due to prenatal and postnatal Pb exposure is correlated to reduced intellectual and learning capacities [
22], as well as behavioral problems [
4]. Different exposure patterns may generate distinct diseases or health problems.
The composition and the way kohl-based products are applied are factors associated to their harmful effects. These cosmetics are mixed with saliva before being applied on women’s eyebrows or the skin of children. Kohl enters the organism orally or through skin. Some authors report that <1% of Pb absorption occurs through skin, while the absorption rate of inhaled or orally ingested Pb rises to 11% in adults and 30–75% in children [
23,
24,
25]. It is worth noting that although the rate of dermal absorption is lower, numerous pathologies have been associated to the contact with kohl. Severe corneal edema, abnormal pigmentation of the conjunctiva, and lacrimal sac and canalicular obstruction have been described [
26,
27].
Although Pb is the main component of kohl, other elements such as aluminum (Al) or Sb may also promote pathological dysfunctions. Exposure to Al alters neurotransmitter levels and induces choline toxicity [
28,
29]. Sb produces dermal and DNA strand lesions [
30,
31].
Immigration from regions where kohl is part of everyday life has been the route of entrance into western countries of cosmetics such as the kohl-based eyeliner. Although kohl has been banned in several countries, it can still illegally be found in some local shops worldwide [
32]. The first European study evaluating the effects of kohl (1968) reported Pb-related encephalopathy in an Asian child, diagnosed in London [
33]. Between 1970 and 2000, a few other studies focusing on the toxic effect of kohl were carried out in the USA and UK [
34,
35]. Studies analyzing the presence and effects of kohl in other European countries are scarce [
36,
37,
38].
Although the use of certain heavy metals is prohibited in most countries, they can be present as impurities in cosmetics. There is no international agreement regarding the minimum levels of heavy metals allowed in cosmetics, and every country has its own regulations. Each country defines the legal limits and concentrations using different techniques. European Union (EU) legislation establishes its recommendations according to a risk-based approach (Pb but not kohl was banned since 1976 [
39,
40]), regulating that cosmetic products placed on the market in the EU cannot contain Pb, Sb, Se, or Cd, and only controlled levels of Zn. However, Germany uses technical limitations established from the element concentration in the 90th percentile after analyzing different products [
4]. In the USA, kohl is not permitted in cosmetics or in any other FDA-regulated products [
41].
The aim of this study was to determine the content of heavy metals in kohl products that can be purchased in Spanish and German local shops and websites to establish whether European consumers are exposed to Pb or other hazardous substances when using this type of cosmetics.
4. Discussion
Over the last decades, many countries have developed laws to regulate the composition of cosmetic products, with special attention to the content of heavy metals and other toxic elements. European Parliament Regulation no. 1223/2009; the Federal Food, Drug, and Cosmetic Act Chapter VI; the German
BVL; and the Canadian Cosmetic Regulations (C.R.C., c. 869) indicate different thresholds for the amount of toxic elements and heavy metals allowed in cosmetics [
40,
41,
46,
72]. Presence in cosmetics of elements such as Pb, As, Cd, Sb, and Ni is unauthorized in all of them, only allowing their presence as trace elements derived from manufacturing processes. The primary source of metal impurities in cosmetics is the use of natural ingredients during their production. However, in some cosmetics such as kohl, the addition of mineral pigments may result in product contamination with Pb, Cd, Cr, Co, Cu, Ni, and other elements [
73]. Trace amounts have to be small enough to be technically unavoidable in good manufacturing practice and safe for human health. However, differences among legislations in the limits allowed for these elements and lack of specific limits for traces that a cosmetic can contain, allowing the commercialization of traditional products manufactured with a high content of toxic elements for human health.
Kohl is one of the most used traditional cosmetics in different countries of Africa and Asia, especially by women and children. In fact, use of kohl has been detected in children under five years of age, following the advice of the family or for cosmetic reasons [
74]. In some regions, it is applied to the umbilical stump of newborn babies [
75]. Because of the migratory phenomena of populations from these continents to Europe over the last decades, kohl arrives through post offices, travels, or commercialization from migration origin countries to the European markets [
35]. Furthermore, most exposures to this product are not detected or its risks are not considered a public health problem.
Kohl can enter the body through eyes, skin, or mouth. The toxic elements and heavy metals contained in kohl-based eye cosmetics have different absorption rates. Moreover, all heavy metals are susceptible to bioaccumulation, generating harmful effects in women and children, especially during pregnancy [
76,
77,
78,
79,
80]. Studies on the effects of cosmetic and dermal Pb exposure in pregnant women are scarce. A study carried out in the Aseer (Saudi Arabia) with 176 pregnant women showed no statistically significant effects of dermal Pb exposure on pregnancy outcomes such as preterm delivery, premature rupture of the membrane, or birth weight [
81]. In other studies with pregnant kohl users, Pb concentrations in blood were higher than normal levels, but lower than sub-toxic concentrations [
19,
82]. However, it has been emphasized that cosmetic use is a risk factor for low Pb exposure in pregnant women.
In recent years, many authors have concluded that exposure to environmental contaminants during the prenatal and perinatal periods may promote neurological and developmental impairments [
83]. Pb exposure during pregnancy and childhood has been largely analyzed due to its harmful effects on development. Blood Pb levels are similar in the soon-to-be mother and the fetus because Pb can readily cross the placental barrier by simple diffusion [
83]. Thus, prolonged fetal exposure to Pb due to maternal use of kohl during pregnancy may lead to adverse outcomes, including spontaneous abortion [
83], low birth weight, gestational hypertension [
84], and neurodevelopmental impairments [
85,
86]. Kohl is also commonly used as a cosmetic in children among these populations, producing mental and physical disabilities, including slowed growth, brain damage, and behavioral and learning problems [
87]. The ICP-OES analysis of kohl products purchased in Spain and Germany show that half of the samples largely exceed the allowed values, with very worrying levels for human health in three of the samples (#2, #6, and #12). Our study found Pb values several orders of magnitude above the EU permitted limits (20 ppm), confirming the results of the few previous studies performed in Europe [
16,
43,
63,
88,
89,
90]. Our results are also in line with previous studies reporting high amounts of Pb in kohl products commercialized in America [
89], Africa [
17,
20,
32,
62], and Asia [
5,
24,
71,
79,
80,
91,
92]. Moreover, Gouitaa et al. [
15] pointed out that Pb concentration of kohl products varies depending on the texture and cosmetic presentation, being higher in powder than in paste, and higher in the latter than in pencils. Our analyses confirm these differences in Pb concentrations; samples with the highest Pb concentration corresponded to kohl powders (#1, #2, #6, #7, #12), followed by kohl pastes (#3, #8), and kohl pencils (#4, #5, #9, #10), with the exception of sample #11, which is probably not based on galena.
Toxic concentrations found in our study are similar to those reported in other European studies with kohl. The range of toxic Pb concentrations in kohl described in European studies vary from 8 to 460,000 ppm [
90]. Conversely, our study shows higher Pb concentrations in kohl if compared to other countries. Pb concentration in kohl found in Tunisian traditional cosmetics varies between 51.1 ppm and 4839.5 ppm [
91], demonstrating lower maximum levels if compared to our results. Similarly, the content of Pb in most frequently used brands of cosmetic products in Morocco showed that Pb concentrations in kohl samples were between 0.01 and 973.8 mg/g [
15]. In a study conducted in Afghanistan, 70% of the surma-based samples contained high levels of Pb (range 35–83%) [
93].
With regard to other different cosmetic products used in Nigeria, Pb levels ranged from 12 to 240 ppm [
62], in Pakistan 141.6 ± 0.016 ppm [
5], and in Poland between 17 and 35 ppm [
63]. In eye shadow samples manufactured in different countries (China, Italy, and the USA), Pb levels varied from 0.25 to 81.50 ppm [
89]. These studies report low Pb levels in different cosmetics when compared to Pb levels found in kohl-based products in our study.
The above-mentioned findings show there are several kohl products available in the European markets (retail shops or internet) without accurate information on their chemical composition or the information in the packaging is missing or confusing and contain prohibited concentrations of Pb and other toxic elements.
The analysis carried out in this study shows unauthorized As levels (from 5.6 to 12.6 ppm; the limit established by the EU is 5 ppm) in samples #3, #5, #6, #11, and #12. This toxic semimetal has high affinity for skin, nails, and hair and causes adverse effects such as skin eruptions, alopecia, keratosis, and striation of the nails, and has also been associated with skin cancer and heart disease [
93,
94]. According to the FDA, dermal absorption of As from soil is 3%, representing dermal absorption 1% compared to ingestion [
95]. According to our results, previous studies found As concentrations from 0 to 12 ppm in kohl cosmetic products [
96,
97,
98,
99,
100,
101,
102,
103,
104,
105,
106], considered as impurities despite exceeding the established EU limits [
67,
89,
107].
Cd toxicity after chronic exposure can cause anemia, weight loss, liver damage, and cancer. Moreover, harmful effects on steroidogenesis during pregnancy may also occur, leading to developmental impairments, suboptimal fetal growth, and spontaneous abortion [
44,
67,
77,
78,
80,
108]. The main route of Cd entry is by inhalation, but it can also be absorbed by ingestion and to a lesser extend through the skin [
88,
89]. Our ICP-OES results indicate amounts of this metal over the required limit (the EU establishes a limit of 5 ppm) in samples #2, #6, and #12 (range between 10 and 20 ppm). Cd is widely used as a color pigment in the cosmetic industry and is considered a trace element. However, several studies found prohibited amounts ranging between 0.5 and 200 ppm in different kohl-based cosmetic products in Europe [
89,
90] and other continents [
67,
79,
88,
89,
102,
103,
109], in line with the results obtained for the products evaluated in this study purchased in European markets.
Sb and Ni levels are within the allowed European legislation range (100 ppm for Sb and 200 ppm for Ni), but not for the limits allowed in German regulations (0.5 and 10 ppm, respectively) where products #2, #3, #6, and #12 for Sb and #3 for Ni exceeded the allowed levels. As previously mentioned, traditional cosmetics were initially based on Sb (stibnite, Sb2S3) [
6]. However, in recent years it has been replaced by galena stone (Pb
2SO
4), which may explain the moderate levels of Sb found in the studied products. Sb is absorbed mainly by inhalation or ingestion, but also through skin. Chronic exposure to this element produces dermatitis, Sb spots on the skin, irritation of the eyes, and gastrointestinal problems such as stomach pain and diarrhea [
30,
57,
78,
88]. Concentrations obtained in the samples of this study range between 0 and 75 ppm, in line with previous studies with kohl-based samples [
56,
57,
79,
88]. Although dermal absorption rate is 0.25% [
110,
111], Sb values above 5 ppm, according to German and Canadian laws, should be considered inadequate for cosmetics products. Dermal Ni absorption due to the use of kohl cosmetics produce dermatological and gastrointestinal problems [
60,
62,
65,
66,
67,
88]. Our results do not show high levels of this metal in our kohl-based samples, with concentrations withing the range of previous studies and far from the high values (above 100 ppm) found in some of them [
14,
20,
62,
63,
67,
88,
89,
102].
It is also important to highlight the presence of other metals and elements that may be toxic for human health, especially pregnant women and children. Co (0–8 ppm), Cr (0–20 ppm), Mn, Se, Al, and Fe levels determined in this study are in the lower limits of previous studies and are not considered dangerous for human health at low levels [
14,
64,
65,
67,
88,
89,
90,
98,
112]. Surprisingly, only sample #3 shows very high levels of Co, Cr, and especially Al (12,263 ppm). Chronic exposure to Co, Cr, Cu, and Mn can cause skin problems [
65,
66,
67,
79,
88,
89]; some studies associate high Al exposure to neurological diseases as Alzheimer’s disease [
113,
114]. Moreover, the amount of Zn was elevated in 8 of the 12 cosmetics analyzed, showing higher concentrations than previous studies in Europe, Africa, and America [
61,
63,
115]. However, Zn is considered a non-toxic compound in cosmetics [
5,
59].
Overall, ICP-OES analyses demonstrated that kohl-based cosmetics #2, #3, #6, and #12, purchased in Europe and representing 33% of the products evaluated in this study, contain amounts above the required levels according to EU legislation of at least two heavy metals or elements. The results of this study show that it is necessary to reinforce supervision and control measures of traditional products exported to Europe due to the high demand by African and Asian populations living in European countries. Alarmingly high levels of some highly toxic compounds, used regularly by these populations, may lead to the development of various diseases. A continuous risk communication forum might be an interesting way to bring together all aspects regarding current legislations, labeling, and toxicology. This would help industry professionals and consumers understand and communicate the risks of using this type of products. Finally, it is necessary to unify the criteria and threshold values to improve the control of heavy metal content during the manufacturing process of these cosmetic products.