Body Malodours and Their Topical Treatment Agents

International Journal of Cosmetic Science, 2011, 33, 298–311

doi: 10.1111/j.1468-2494.2011.00649.x

Review Article

Body malodours and their topical treatment agents M. Kanlayavattanakul and N. Lourith School of Cosmetic Science, Mae Fah Luang University, Chiang Rai, Thailand

Received 4 October 2010, Accepted 3 February 2011

Keywords: anti-perspirant, body odour, deodourant, foot odour, treatment

Synopsis Body malodour, including foot odour, suppresses social interaction by diminishing self-confidence and accelerating damage to the wearer’s clothes and shoes. Most treatment agents, including aluminium anti-perspirant salts, inhibit the growth of malodourous bacteria. These metallic salts also reduce sweat by blocking the excretory ducts of sweat glands, minimizing the water source that supports bacterial growth. However, there are some drawback effects that limit the use of aluminium anti-perspirant salts. In addition, over-the-counter anti-perspirant and deodourant products may not be sufficiently effective for heavy sweaters, and strong malodour producers. Body odour treatment agents are rarely mentioned in the literature compared with other cosmetic ingredients. This review briefly summarizes the relationship among sweat, skin bacteria, and body odour; describes how odourous acids, thiols, and steroids are formed; and discusses the active ingredients, including metallic salts and herbs, that are used to treat body odour. A new class of ingredients that function by regulating the release of malodourants will also be described. These ingredients do not alter the balance of the skin flora. ´ sume ´ Re Les mauvaises odeurs corporelles, y compris celles des pieds, atte´nue l’interaction sociale en diminuant la confiance en soi et favorisant des dommages aux veˆtements et aux chaussures porte´s. La plupart des agents inclus dans les traitements, y compris les sels d’aluminium antiperspirants, inhibent la croissance de bacte´ries malodorantes. Ces sels me´talliques re´duisent aussi la sueur en bloquant les canaux excre´teurs des glandes sudoripares, re´duisant ainsi au minimum l’eau, source de la croissance bacte´rienne. Cependant, il y a quelques inconve´nients qui limitent l’utilisation de sels d’aluminium anti-transpirants. De plus, les produits antiperspirants et de´odorants OTC peuvent ne pas eˆtre suffisamment efficaces pour des personnes produisant une grande quantite´ de sueur et producteurs de fortes odeurs. Les agents actifs sur les Odeurs corporelles sont rarement mentionne´s dans la litte´rature comparativement a` d’autres Ingre´dients cosme´tiques. Cette revue re´capitule brie`vement la relation entre la Sueur, les bacte´ries cutane´es et l’odeur corporelle; elle de´crit comment des acides odorants, des thiols, et des ste´roı¨des sont forme´s; et examine les principes actifs, y compris les sels me´talliques Correspondence: Nattaya Lourith, School of Cosmetic Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand. Tel.: +66 53 916834; fax: +66 53 916831; e-mail: [email protected]

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et les ve´ge´taux utilise´s pour traiter l’odeur corporelle. Une nouvelle classe d’ingre´dients dont la fonction est de re´guler la libe´ration de mauvaises odeurs est e´galement de´crite. Ces ingre´dients ne modifient pas l’e´quilibre de la flore cutane´e. Introduction Body odour, which encompasses axillary and foot odour, can communicate a strong non-verbal signal [1, 2]. These odours are often unnoticed by the offender because that person has specific anosmia [3]. As a result, the individual is embarrassed when alerted, and his or her self-confidence is compromised. The offensive body odour also has economical consequences stemming from the need to replace damaged/stained clothes and shoes [4, 5]. In contrast to clear findings in animals, the presence of human vomeronasal organs is still being debated. Clearly, the ability to appreciate underarm and foot odours depends solely on an individual’s evolutionary culture and perceptual development. However, the emission of odourless human pheromones has been reviewed and is becoming a popular discussion topic [6]. The human scent is genetically controlled and systemically influenced by dietary and medicinal intake, as well as the application of fragrance products [6–8]. Heavy sweating or hyperhidrosis, particularly at axillary sites, leads to unpleasant odours that cause social embarrassment and reduce self-confidence, especially among women. Hyperhidrosis results from the oversecretion of sweat. Because there is an excessive amount of water in which bacteria can grow, hyperhidrosis is often accompanied by bromhidrosis or osmidrosis or offensive body odour. Both conditions can be treated by topically applying anti-perspirant and deodourant products. Body odour treatment products are part of a multibillion dollar industry [9]. High levels of fragrance are often used in these products to mask malodour [10]. Surprisingly, there is little discussion of odour treatment products in the literature [6], in contrast to other personal care products [11, 12]. This review will summarize the chemical composition and formation of body odour, the use of anti-perspirant, deodourant and herbal products to treat body odour, and a new class of treatment agents that do not change the balance of the skin’s bacterial population. Sweat glands and body odour Sweat is necessary for thermoregulation control, enabling humans to live in different climate zones. There are three types of sweat glands: eccrine, apocrine and apoeccrine. The eccrine glands are

ª 2011 The Authors ICS ª 2011 Society of Cosmetic Scientists and the Socie´te´ Franc¸aise de Cosme´tologie

M. Kanlayavattanakul and N. Lourith

Body malodours and treatment agents

distributed throughout the human body, particularly in the palms, soles and armpits. Sweat glands vary in density and size depending on race, sex, body site and determination techniques [13–15]. Apocrine gland secretions, which are initially odourless, are metabolized by normal skin flora, producing malodour. Eccrine glands exist and function at birth. Apocrine glands exist at birth, but they do not begin to function until the onset of puberty. Within the axilla, apocrine glands outnumber eccrine glands by 10–1 [16]. Apoeccrine glands develop from the eccrine gland during adolescence, as the number of eccrine glands is observed to decrease with age. Although the eccrine glands are mainly responsible for thermoregulation, emotional stimuli also initiate a response, particularly from those glands found in the palms, soles and forehead. Emotional stimuli also initiate responses from the apoeccrine and apocrine glands within the axilla [17]. Apocrine glands open into hair follicles and secrete malodour precursors and microbial nutrients that provide an excellent environment for the growth of cutaneous microorganisms [18]. Some examples of apocrine gland secretions include: proteins, lipids, sulphur-containing amino acids, volatile short-chain fatty acids and steroids such as dehydroepiandrosterone (DHEA), DHEA sulphates (DHEAS), androsterone and testosterone [19–21]. In adolescents, a high amount of 5a-reductase type I has been identified that converts testosterone to dihydrotestosterone (DHT), another androgen that contributes to malodour [22]. Such cutaneous microorganisms include aerobic cocci of the Micrococcaceae family, aerobic diphtheroids (mainly Corynebacterium), anaerobic diphtheroids (Propionibacterium) and yeast (Pityrosporum) [23]. Some of the resulting malodourous species include: (E)-3-methyl-2-hexenoic acid or 3M2H and 3-hydroxy-3-methyl hexanoic acid (HMHA) [24], 3-sulphanylalkanol (particularly 3-methyl-3-sulphanyl hexanol; 3M3SH) [25–27], androstenone (5a-androst-16-en-3-one) and androstenol (5a-androst-16-en-3a-ol). Trans-3M2H is detected more frequently than its cis-isomer. The E/Z ratio is 10 : 1 in men and 16 : 1 in women [18, 28, 29], of which detection thresholds of these characteristic malodourants were shown in Table I. It is the presence of those bacteria population that metabolizes apocrine gland secretions producing axillary odour. Hypersweating by eccrine glands, commonly known as hyperhidrosis, produces a water-rich environment that supports the bacteria population (i.e. Corynebacteria, Stapphylococci and Propionibacteria) that causes extreme body malodour known as osmidrosis or bromhidrosis. Hypersweating does not occur before the onset of puberty, similar to emotional sweating in the axillary region. Axillary hyperhidrosis is defined as a sweat rate >20 in men and 10 mg min)1 in women. However, palmar hyperhidrosis in both sexes is defined as a rate of sweat secretion >30–40 mg min)1 [30]. The axillary odour is stronger given differences in the bacterial populations at the different sites. Young females are often hypersensitive to the resulting axillary malodour, perhaps because male body odour from this site acts as a human pheromone [6]. Sweat from the eccrine gland mainly consists of water (99%) and amino acids, ions, lactic acid, glycerol, urea, peptides and proteins (particularly cysteine containing) [31, 32]. Propionibacteria, Staphylococcus and Corynebacteria that are apart of the normal skin flora catabolize glycerol, and lactic acid to short-chain (C2–C3) volatile fatty acids (VFAs) such as acetic, and propionic acids. These bacteria also degrade amino acids into C4–C5 methylbranched VFAs such as isovaleric acid, a common foot odourant [25, 33, 34]. Valine is transformed into isobutyric acid, leucine is converted to isovaleric acid, and isoleucine is degraded to 2-methyl butyric acid through aerobic metabolism [35]. The apoeccrine

glands secrete some of the same compounds that are found in eccrine sweat [36] because these glands are believed to develop from eccrine glands. Sweat collected from the skin surface contains a diverse range of metabolites, depending on the physiology status of the donor as well as the functional, and developmental states of the sweat glands. Sebaceous glands also secrete odourless compounds that include wax esters, cholesteryl esters, cholesterol and other sterols, squalenes, hydrocarbons and triglycerides. These compounds are further metabolized into malodourants by means of cutaneous bacteria lipase. Triglycerides are hydrolysed yielding glycerol and subsequently VFAs. Odourous acids Staphylococci metabolize amino acids to generate short-chain methyl-branched VFAs that contribute to malodour. Corynebacteria metabolize skin lipids to generate medium-chain VFA (C6–C11). These bacteria transform, for example isopalmitic acid to isobutyric acid [35]. Corynebacteria, previously called lipophilic diphtheroids, populate the axillary region and are believed to be the main bacterial contributor to axillary odour [37, 38]. The metabolic efficiency of odourant generation by means of Coryneform lipase activity was found to be superior to that mediated by Staphylococci and Propionibacterium. Propionibacterium was found to be the least efficient bacteria with regard to the generation of malodourants [37]. 3-Hydroxy-3-methyl hexanoic acid, a very pungent axillary odour, was the most abundant odourant identified in axillary secretions [39] quantified by means of LC-MS/MS [12] and confirmed by GC-MS [24] and GC techniques [25]. This odourant acid was detected in a larger amount than its dehydroxylated analogue (3M2H) [12]. HMHA might be a precursor of 3M2H, resulting from an acid-catalysed dehydrolysis reaction [40]. HMHA, 3M2H and 28 other acids were determined to be degradation products of leucine, isoleucine and tyrosine [39]. The bacterial exoenzyme, aminoacylase, was shown to cleave these odourants from water-soluble proteins, namely apocrine secretion odour-binding proteins 1 and 2 (ASOB1 and ASOB2). ASOB2, a stable protein [41], was identified as apolipoprotein D (apoD), which is an a2l-microglobulin in the lipocalins family [42]. The mechanism of VFA transportation to the skin involves the covalent binding of 3M2H (3M2H : apoD = 2 : 1) and its hydroxylated derivative, HMHA, a spicy note characteristic of axillary odour to a glutamine (Gln) residue of the ASOB proteins, Na-3-methyl-2-hexenoyl-l-glutamine and Na-3-hydroxy-3-methylhexanoyl-l-glutamine [30]. These odourants are released by a Zn2+-containing Na-acyl-Gln-aminoacylase specifically from Corynebacterium striatum strain Ax20, as shown in Fig. 1. This dipeptidase has a certain affinity towards Na-acyl-Gln conjugates [12] and Na-acyl-Gln-aminoacylase. This affinity is specific to cleaving at the Gln residue and low for cleaving the Na-acyl bond [12, 24, 25]. Subsequently, the odourant acids cleaved from Na-acyl-Gln conjugates [43] are volatilized off of the skin surface [12]. Odourant acids are covalently bound to apoD at their carbonyl terminal ends. The ASOB2 concentration was found to vary with race [20], confirming the race-related differential intensity of body odour [13, 15]. Nonetheless, the concentration of axillary bacteria did not vary [20]. Therefore, an understanding of the molecular mechanism underlying metallopeptidase enzyme activity will facilitate the design of inhibitors to terminate the release of malodourous compounds [12]. In addition to ASOB2, the ABCC11 gene, whose protein is expressed and localized in apocrine glands, has recently been found

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OH O

O

OH H N

O

O NH2

HO O

H N O NH2

Corynebacterium aminoacylase

HO

HO O

HO

O

to be associated with the presence of axillary malodour. This protein is essential for Na-acyl-Gln conjugates in odourous acids [44]. The enzymatic release of these conjugates results in long-lasting malodour. Using HMHA with a detection threshold of 4 ppt, the enantiomeric excess (ee) of the (+)-(S)-isomer (>97%) was observed at a S : R ratio of 72 : 28. The S-isomer exhibited a strong spicy odour, whereas its optical isomer exhibited a weak animal-like odour [25]. However, the ABCC11 protein was less associated with the production of straight-chain acids. The straight-chain acids might derive from b-oxidation or bacterial degradation of skin or sebum lipids [44]. Transportation and formation of odourous acids are prospectively illustrated, as shown in Fig. 2. The above learning suggests that controlling ABCC11 will control the secretion and formation of amino acid precursors and axillary odourants. ABCC11 protein was also associated with a dry white earwax phenotype among Asian individuals. Asians having this particular

HMHA-Gln-ABCC11

Figure 1 Corynebacterium sp. function in 3-hydroxy-3methyl hexanoic acid and 3-methyl-2-hexenoic acid formations.

phenotype had less body odour and lower levels of apoD than Caucasians [20, 45]. Therefore, determination of whether the ABCC11 gene is present, and whether this gene expresses a dry vs. wet earwax phenotype, represents a good way to screen for osmidrosis. In contrast to body odour, foot odour is mostly due to short-chain fatty acids catabolized from components found in eccrine sweat. Acetic, butyric and isobutyric acids, and particularly isovaleric acid, are the main components in eccrine sweat, with traces of propionic, valeric and isocaproic acids [34]. Isovaleric acid is an odourant derived from leucine; acetic and propionic acids are produced via the fermentation of glycerol and lactic acid; isobutyric acid is derived from valine, 2-methyl butyric acid from isoleucine and short-chain, branched fatty acids are formed by incomplete degradation of skin lipids. ABCC11 not only contributes to axillary odour but also is associated with foot odour and strongly involved in isovaleric acid formation and leucine/isoleucine degradation [44]. Odourous thiols

HMHA-Gln

HMHA-apoD-HMHA

HMHA Figure 2 Odourous 3-hydroxy-3-methyl hexanoic acid transportation and cleavage.

Odouriferous sulphanylalkanols include 3-sulphanylhexanol (3SH), 2-methyl-3-sulphanylbutanol (2M3SB), 3-sulphanylpentanol (3SP) and 3M3SH. These compounds were found in low amounts in human axillary sweat (1–10 ppt) [26], but human sensitivity to them is high. Cystathione-b-lyase is the enzyme involved in catalysing the release of sulphur-containing malodourous compounds. The strong meaty, fruity odour of 3M3SH is contributed by the 97% stereometric excess of ())-(S)-isomer, which possesses a characteristic sulphuric odour, whereas its (+)-(R)-isomer (>97% enantiomeric excess) has a fruity odour. The odour of 3SP is described as onion-like, sulphuric and weakly reminiscent of grapefruit. The threshold for this compound is 2 ppt, whereas 3M3SH, the major odourous sulphanylalkanol, has a lower threshold of 1 ppt. An isomeric mixture of 2M3SB has a threshold of 8 ppt (Table I). Such a mixture has an onion- and sweat-like odour. Although these compounds are found at very low concentrations, they strongly contribute to body odour [25]. These compounds are secreted from apocrine glands [26] as Cys-(S) or Cys-Gly-(S) conjugates [43, 46, 47]. A metal-dependent dipeptidase hydrolyses the Cys-Gly bond. Corynebacterium C-S lyase then releases the powerful odourant thiol (Fig. 3). Na-acyl-Gln-aminoacylase was also found to cleave Cys-Gly-(S) conjugates [43]. Corynebacterium b-lyase doses release the sulphuric notes from fresh sweat. Similar to HMHA formation,

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M. Kanlayavattanakul and N. Lourith

Body malodours and treatment agents

O HO

NH2

NH2 H N

S

OH

Corynebacterium

O

Dipeptidase

HO

S

OH

O

Corynebacterium cystathioninebeta-lysase HS

OH

Figure 3 Corynebacterium sp. function in 3-sulphanyl-3-methylhexanol formation.

odourous acids and thiol formations are linked. Furthermore, the 1,4-addition of Cys to the a,b-unsaturated acids including an ester, and aldehyde appears necessary for biosynthesis of the 3M3SH precursor [26]. Therefore, the cross-specificity of these two metallopeptidases plays an important role in axillary odour formation. Thus, dual metallopeptidase inhibitors blocking Na-acyl-Gln conjugates associated with odourant acids and thiols should be designed as treatment for body odour [43]. ABCC11 regulates the Cys-Gly-(S) conjugate of 3M3SH, which is further catabolized into 3M3SH by b-lyase [44]. Direct hydrolysis of 3-sulphanyl-3-methylhexanol (3M3SH), which was isolated from human sweat, was proposed as the mechanism. The (S)-isomer of this precursor was 75–78% more prevalent than the (R)-isomer in sweat and had an onion-like odour. In contrast, the (R)-enantiomer exhibited a fruity, grapefruit-like odour [25, 27]. The transportation and cleavage of odourous thiols are graphically summarized in Fig. 4.

ABCC11-Cys-Gly-3M3SH

Cys-Gly-3M3SH

Gly-3M3SH

3M3SH Figure 4 Odourous 3-sulphanyl-3-methylhexanol transportation and cleavage.

Odourous steroids Axillary sweat and hair contain androsterone (5a-androst-16en-3a-ol), 17-oxo-5a-androstan-3a-yl sulphate (androsterone sulphate; AS), 17-oxo-5a-androsten-3b-yl sulphate (DHEAS), DHEA, 3b-androstadienol and androstadienone (androst-4, 16-dien-3-one), which are secreted by apocrine glands [19]. These precursors are converted to 4,16-dienone, and 5a-androstenone by Corynebacteria producing a characteristic urine-like odour. 5aAndrostenone is catabolized to 3a- and 3b-androstenols, which have musk, and urine scents, particularly the a-isomer. Coryneform and Staphylococcus epidermidis cleave DHEAS, which is transported by the ABCC11 protein [48], and androsterone sulphate by means of sulphatases delivering their unconjugated corresponding steroids (e.g. 5a-androst-2-en-17-one). In addition, 3b-androstenyl sulphate is converted to 3b-androstenol. Corynebacteria is the most efficient in transforming 5a-androst-5,16diene-3a-ol to androst-4,16-diene-3-one, the malodourous steroid [49, 50]. The transformation is significantly associated with the presence of oxygen, confirming the aerobic nature of Coryneform. Thus, 5,6-dehydrostenols created by Coryneform 5a-reductase play an important role in malodour steroid production. 4,5-Isomerase is associated with odourous steroid formation through isomerization of androst-5,16-dien-3-one into androst-4,16-diene-3-one following the oxidation of androst-5,16-diene-3a-ol [49]. The configuration of 3-hydroxy contributes to the odour of the steroids produced. An equatorial arrangement of hydroxyl (3b-ol) showed less odour, whereas axial configurations (3a-ol) increased the malodour. Notably, androst-16-en-3a-ol creates the characteristic male body odour. The enzymatic activity was stereospecific towards b-isomer, as 3b-sterol dehydrogenase activity was much greater than 3a-sterol dehydrogenase activity [48]. Thus, transformation of androst-5,16-diene-3-ol, androst-16-en-3-ol and androst-4,16-diene-3-ol are key components in the biosynthesis of malodourous androst-16-en-3a-ol (in male body odour), androst4,16-dien-3-one and 5a- androst-16-en-3-one, which contribute to the characteristic underarmpit odour, as proposed in Fig. 5. These 3-oxo-steroids have very low thresholds (Table I), particularly 5a-androst-16-en-3-one (0.2 ppb), which is a powerful urinous odour. However, androstenone is perceived by only 50% of the human population. Furthermore, testosterone is not a precursor of 3-oxo-steroid (androst-4,16-dien-3-one) [50]. Therefore, the action of axillary odour treatment agents should be reviewed to

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O

O

H

H

H

H

H

H

HO

HO

HO4SO

H

H

H

H

H

Androsterone sulfate

Androsterone

Androstadienol

OH

H

H

H H

H

H

H

HO

HO

H

H

H

O

H

3,17-androstadiol

Androst-16-ene-3-ol

H

Androst-16-ene-3-one

H H

H

H H

HO

H

H

HO

Androst-4,16-ene-3-ol

Androst-5,16-ene-3-ol

H

H H

O

H

H

O

Androst-4,16-ene-3-one

Androst-5,16-ene-3-one

Figure 5 Odourous steroids formation.

effectively combat body malodour which do not affect skin homeostatis by novel ways of action [24]. Thus, the remaining sections of this review article aim to describe the topical treatment agents that are currently used, as well as the newest generation of active ingredients in body odour treatments. In addition, laundry products with active agents preventing malodour are included, as typical axillary odour appears on the cloth within approximately 2 h of wearing and stays until washing. Indeed, skin microorganisms, particularly S. epidermidis and other malodour-producing bacteria, were found to survive, low temperature washing and slow drying conditions [51].

Table I Characteristic body odours and their detection thresholds [23, 25]

Odourant

Organoleptic property

Detection threshold

HMHA 3M2H Isovaleric acid 3M3SH 2M3SB 3SP Androstenone Androstenol

Spicy Sweaty Sweaty Sweaty Sweaty Sulfuric Urinous Musky

4 ppt 14 ppb 1 ppm 1 ppt 8 ppt 2 ppt 0.2 ppb 6.2 ppb

HMHA, 3-hydroxy-3-methyl hexanoic acid; 3M2H, 3-methyl-2-hexenoic acid; 3M3SH, 3-methyl-3-sulphanyl hexanol; 2M3SB, 2-methyl-3-sulphanyl butanol; 3SP, 3-sulphanyl pentanol.

Active ingredients for body odour treatment Topical anti-perspirants are the first line of body odour improvement because they are inexpensive, with minimal side effects [52]. Anti-perspirants are used to diminish sweat secretion by blocking the excretory ducts of sweat glands. Most types of antiperspirants contain metallic salts, particularly aluminium. The types of aluminium salts include: aluminium chlorohydrate (ACH), aluminium bromohydrate, aluminium chloride, aluminium sulphate, potassium alum and sodium aluminium chlorohydroxy lactate. Aluminium salts are anti-bacterial. Aluminium antiperspirant salts (most notably ACH, aluminium sulphate, ACH lactate and aluminium chloride) polymerize with increasing pH, forming aluminium hydroxide gel plugs in the sweat tubule [23]. These plugs prevent new sweat movement towards the skin surface. However, they are not permanent, and the acidic nature of these salts can be irritating to the skin which limits their use. In an attempt to reduce skin irritation, salicylic acid was used in combination with ACH [5]. The formulation, consisting of aluminium salts and salicylic acid, had a reduced incidence of skin irritation and had good anti-bacterial and anti-fungal properties [53]. Zinc salts The anti-DHT activity of zinc gluconate, zinc glycerinate, zinc acetate, zinc sulphate, zinc oxide, zinc citrate and zinc chloride was used in combination with other anti-perspirants, natural androgen receptor expression inhibitors and malodour carrier proteins inhibitors in the formulations for body odour control [54]. Water-soluble zinc salts (zinc pidolate or zinc pyrrolidonecarboxylate, zinc chloride, zinc gluconate, zinc lactate, zinc phenolsulphate and zinc sulphate) were used to absorb human axillary smells [55]. This function is an additional benefit of Zn salts, highlighting their

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efficacy in malodour treatment. Furthermore, zinc pyrithione and zinc phenolsulphonate were formulated with a 1,3-diketone in a laundry product [56] designed to suppress undesirable odour. Similar to the case with micronized ACH, zinc oxide powder with a particle size of 0.02–200 lm was compounded with sesquiterpene alcohols and volatile silicone, producing a dry-texture deodourant [56] characterized by control-release enhancement and moisture absorption, which eliminated microbial growth. Mn salts In addition to zinc and aluminium, porous manganese was used as a deodourant carrier that exerted anti-bacterial activity [57]. Furthermore, divalent manganese salts (manganese chloride, manganese acetate and manganese sulphate) were found to reduce axillary, foot and scalp odours in aerosol, spray, roll-on, cream, stick and laundry detergents suitable for woven or non-woven fibres [58]. Anti-microbial agent A good anti-bacterial deodourant should work specifically against axillary bacteria within an effective time period as well as exhibit good stability and compatibility with other ingredients in the formulation. Furthermore, such formulations should be non-toxic and non-irritating and safe. Thus, anti-microbial metal ions known as anti-microbial ceramics (ACs) have become increasingly important in people’s day-to-day lives because of their wide range of applications in personal and home care products (i.e. fabrics and cosmetics). Formulations of ACs, for instance, zeolite AC, calcium phosphate AC and amorphous silica AC, are used as anti-microbial agents in household and personal care products because of their good biocompatibility. ACs based on hydroxyapatile and nitrateapatile complexed to Ag+ demonstrated an obvious anti-microbial effect [59] that allowed for controlled release, which was superior in terms of safety and durability to the casual anti-bacterial vehicles [60]. The bactericidal action of silver zeolite ACs resulted from the transfer of silver ion to the bactericidal cell and the formation reactive oxygen species. This action mode was proved in the bacteria treated, and untreated with Ag-zeolite, and in anaerobiosis condition as well [61]. Furthermore, Ag-zeolite concentrated to 5–40% ww)1 was found to act as an anti-microbial against skinresident bacteria. Its activity was superior to that of triclosan. It was long-lasting and had no adverse effects. It was promoted as an excellent agent for anti-axillary odour preparations [62]. Ag salts of fusidic acid were also found to be effective against S. epidermidis growth, particularly silver fusidate (minimum inhibitory concentration; MIC = 60–8000 ppm), which was more effective than silver sulphadiazine (MIC = 8000–16 000 ppm). These Ag salts were additional candidate topical agents for use as body odour treatment products [63]. Triclosan was used as a broad-spectrum anti-microbial agent for more than 40 years. Body odour control preparations were first launched in 1967, because of the compound’s efficacy and stability, as well as the lack of resistance among malodour-forming bacteria [64]. Corynebacterium sp. inhibition was found to be effective at an MIC of 3 ppm; activity against Staphylococcus sp., and Propionibacterium acnes was also observed [65]. Triclosan and triclocarban were included as anti-microbial agents in combination with sodium hydroxymethyl glycinate (used as a preservative) and aromatic compounds such as eucalyptol, menthol, methylsalicylate and thymol [66].

Anti-microbial agents that could be used in deodourants include cetyl trimethyl ammonium bromide; cetyl pyridinium chloride; benzethonium chloride; diisobutyl phenoxy ethoxy ethyl dimethyl benzyl ammonium chloride; sodium N-lauryl sarcosine, sodium N-polymethyl sarcosine; N-myristoyl glycine, potassium N-lauroyl sarcosine; stearyl trimethyl ammonium chloride; 2,4,4¢-trichloro2¢-hydroxydiphenyl ether; zinc pyrithione; sodium bicarbonate; 2,2¢-methylene-bis-(3,4,6-trichlorophenol); zinc phenolsulphonate; 2,2¢-thio-bis-(4,6-dichorphenol); p-chloro-m-xylenol; dichloro-m-xylenol; and diaminoalkyl amide. These agents were formulated with a 1,3-diketone to obtain deodourant effects. Notably, 5-chloro-2(2,4-dichlorophenoxy)-phenol and 2,2-dimethyl-1,3-dioxane,4,6-dione were deodourant agents that were suitable at concentrations of 0.01–20% for topical application and in cloth worn in contact with skin. In addition, these diketones were found to be compatible with anti-microbial agents that were used in the conventional formulations such as sticks, roll-on, cleansing and laundry products [67]. The diketones were entrapped in cyclodextrin for controlled release of active components, and for the absorption of malodourous perspiration, with no associated irritation [68]. In addition, benzalkonium chloride was used as an anti-microbial agent in a deodourizing emulsion containing isopropyl myristate or isopropyl sterate [69]. In addition to the use of the above agents, stick, spray and lotion anti-microbial piroctone [70] (0.1–1.0%, w w)1), formulations were used to control body odour [71]. Coryneform growth inhibition was also exerted by b-chloro-d-alanine, and d-cycloserine at an MIC of 0.001 and 0.005% wv)1, respectively, similar to that of triclosan which was 0.001% wv)1 [72]. Propylene glycol can also function in deodourant formulations as a bacteria growth inhibition agent. Aryl 2-acetoxyethanoic acids (phenyl 2-acetoxyethanoic acid, diphenyl 2-acetoxyethanoic acid (4-chlorophenyl) 2-acetoxyethanoic acid, (2-chlorophenyl) 2-acetoxyethanoic acid, (4-chlorophenyl)-(2-chlorophenyl) 2-acetoxyethanoic acid) were also applicable to the development of deodourant products as they inhibited the bacterial growth [73]. A formulation consisting of hexamethylene biguanide hydrochloride inhibited body odour more effectively than triclosan and was used in the production of solutions, lotions, creams, ointments, powders, suspensions, soaps, gel sticks and aerosols [74]. Azole anti-fungal agents include clotrimazole, miconazole, tioconazole, butoconazole, econazole, terconazole, ketoconazole and fenticonazole, as well as terbinafine and tolnaftate. These compounds were used in creams for axillary odour treatment, in combination with undecylenic and salicylic acids, and benzoyl and hydrogen peroxides [75]. x-Cyclohexylalkan-1-oles with anti-microbial activity were formulated into body odour treatment products [76]. Androstenone odour was found to decrease following application of povidone, which is an anti-bacterial agent [77]. Odour-neutralizing agent Axillary malodour neutralizing agents can act via a sulphydryl reactant, yielding N-ethylmaleimide and N-coumarylmaleimide. This technology was patented [78] in addition to the neutralization effect of NaHCO3 towards odourous acids for instance 3M2H [23]. Metal oxide silicates in particular calcium silicate act as odour absorbents and neutralizers to absorb and neutralize body malodours accordingly. The silicate particles allow for the volatilized malodourants, and fatty acids to be easily adsorbed onto the surfaces. Therefore, less fatty acids evaporate, and less odour is perceived [79, 80].

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Odour absorbers

deodourant activity because of synergistic effects. The axillary malodour could be controlled by sequestering iron depriving the bacteria of a needed food source [88]. The use of DTPA and BHT were found to significantly reduce body odour [89].

Cyclodextrins are used to entrap active ingredients and thereby control the release of polyols, anti-microbials, zinc salts, polymers, bicarbonate salts, chelating agents, zeolites and activated carbon. Cyclodextrin formulations can be sprayed or wiped onto the skin [66]. Cyclodextrins absorb moisture and odour-causing molecules. In addition, silicates, silicas and carbonates absorb moisture [79– 81] which indirectly reduces malodour formation by eliminating cutaneous flora that cause the odour. Bacteria prefer cool and dry to hot and humid environments. Polyamines hybridized with inorganic oxide materials [e.g. SiO2, TiO2, ZnO, Al2O3 or Mg(OH)2] have also been shown to absorb odour [82].

Steroidal axillary malodour production was inhibited by exoenzyme inhibition. The exoenzymes involved were arylsulphatase and b-glucuronidase. The inhibitors with deodourant effects were Cu2+, hexametaphosphate, d-glucaro-D-lactone, ethylenediaminetetraacetic acid (EDTA), nitrilotriacetic acid, O-phenanthroline and sodium sulphate or other phosphates [90].

Novel ingredients for the treatment of body malodour

Control of malodour with fabrics

Inhibition of androgen receptor expression Resveratrol, epigallocatechin-3-gallate and flufenamic acids were used to prevent body odour by inhibiting the expression of androgen receptors [68]. Androgen receptor blocking of DHT binding was employed by a C-19 steroid with an androsten-17(OR)-3-one structure, with R representing a hydrogen, or an alkyl, aryl or acyl group [83]. Competitive inhibition of the malodour-producing enzymes, aminoacylase and cystathionine b-lyase [12, 24, 26] resulted in a neutral or pleasant odour. This result was achieved through the use of O-acyl serine and threonine compounds at a concentration of 0.01–10% ww)1, in both stick and roll-on formulations [84, 85]. ASOB2 inhibitor Monesin, tunicamycin, amphomycin, diumycin, showdomycin, tsushimycin, amphortericine, mycospocidin, streptovirudin and d-glucosamine [86] are thought to be involved in apoD suppression through the inhibition of N-linked oligosaccharide-processing glycoprotein synthesis. Therefore, terminal glycosylation was prevented, and body malodour was limited. Accordingly, a screening method for enzymes mediating malodour involving incubation of Na-acylGln-aminoacylase with precursors, and measurement of the release of HMHA or MHA and free l-Gln [87] was shown to be effective in identifying agents that inhibited the aminoacylase-catalysed malodour-generating reaction. Ethylendiaminedisuccinic acid (EDDS) and pentetic acid, for example, significantly reduced the enzyme activity, and subsequent malodour production by chelating Zn2+ [25] rather than by acting as bacteriostatic agents. Indeed, there could be other chelating agents that could provide sequestration of the active-Zn2+-site in a similar way. Alternatively, deodourants have been designed using fragrance precursors that bind with Gln residues. Corynebacteria enzymes use these residues as substrates, providing a way to engineer enzyme specificity towards Gln but not acyl groups [24]. Thus, cutaneous bacterial degradation of amino acid conjugates could one day provide pleasant odourant precursors. Homeostasis of the skin would be retained, as none of the skin’s normal flora would be eliminated through the use of this novel deodourant system. Nutrient deprivation A combination system consisting of diethylenetriamine pentaacetic acid (DTPA), and butylated hydroxytoluene (BHT) might exert

Exoenzyme inhibition

Fe(III)-4,4¢,4¢¢,4¢¢¢-tetracarboxylic acid phthalocyanine, a deodourizing complex, was grafted onto the surface of polypropylene nonwoven fabric. This fabricated fabric showed high deodourizing performance for 2-mecaptoethanol [91]. The production of odour-controlling textiles also incorporated the use of a polymeric amine coating [92] of hydroxyl-containing amines, particularly trialkanol amines on cellulose fibres. The use of trialkanol amines conferred anti-microbial properties to the fabric. The soft resinous coating was durable to cleaning procedures. The anti-microbial activity was regenerated at pH 10 or above. This process controlled certain odours and diminished the offensive body odour [93]. A laundry cleansing product containing lysostaphin (Gly-Gly endopeptidase), which hydrolyses the Gly-Gly bond in the polyglycine interpeptide link joining staphylococcal cell wall peptidoglycans, was also patented as a component of a detergent composition, suitable for all types of textiles, and fabrics. The detergent system consisted of amylase, arabinase, galactanase, lipase, mannanase, pectinase, protease and xylanase [94]. Herbs to treat body odour Herbs and naturally derived compounds are alternatively available for applications in body odour treatment. Natural flavonoids exert deodourizing effects [95] because of 3¢,4¢-hydroxyl units. The additional 5,7-dihydroxyl groups enhance anti-microbial activity [96, 97] in addition to their efficiency in androgen receptor inhibition [64]. The toxicity of flavonoids is minimal [98]. Traditional remedies can also be used to control body odour; i.e. the Kampo formulation. This traditional medicine contains Rehmanniae radix, Cnidii rhizoma, Angelicae radix, Scutellariae radix (17%, each) and Phellodendri cortex, Coptidis rhizoma and Gardenae fructus (8%, each). The mixture was found to suppress lipase activity of P. avidum, which significantly reduced the production of butyric acid (P = 0.047) [59]. Therefore, herbal extracts with high amounts of these natural compounds and bactericidal activity towards malodour-generating microorganisms are applicable in herbal deodourant product development and the development of bactericidal essential oils. Herbal extracts Anti-microbial activity towards nine pathogenic Arctopus species has been studied in A. dregei, A. echinatus and A. monacanthus. The root of each plant was extracted using 20% aqueous methanol. Arctopus spp. showed the strongest activity against S. epidermidis; A. monacanthus was found to be the most potent (MIC = 20–50 ppm), followed

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by A. echinatus (MIC = 50–200 ppm) and A. dregei, respectively (MIC = 100–900 ppm), whereas the MIC of ciprofloxacin was 600 ppm [99]. Caesalpinia minosoides, which is freshly consumed as a vegetable in Thailand, is a calming agent with carminative effects that reduce dizziness. The anti-microbial activity of this compound was investigated. To do so, the plant was macerated with several solvents at different polarities to yield crude acetone, aqueous, chloroform and ethanolic extracts. All parts of the extract were able to inhibit S. epidermidis, particularly the aqueous extract, which potently inhibited S. epidermidis at an MIC of 3130 ppm; streptomycin (MIC = 63 ppm) was used as a positive control [100]. Tea or Camellia sinensis has remarkable biological activity with respect to catechins and is widely used for its health benefits. Tea components, mainly catechins, and other polyphenolic compounds are used in pharmaceutical and cosmetic applications. Certain components of tea are anti-oxidants as well as bacterial growth inhibitors. Susceptibility of tea towards S. epidermidis was evaluated. Tea showed bactericidal and inhibitory effects at an minimum bactericidal concentration (MBC) and MIC of 550 and 410 ppm, respectively. Gallocatechins and their gallates were claimed as the main constituents responsible for anti-bacterial activity [101], with an additional effect on androgen receptors [64] that synergistically prevented and reduced body malodour. Furthermore, tea anti-bacterial activity was enhanced (11–17%) by irradiation at 40 kGy that resulted in the reduction in tea dark colour, enabling more applications in cosmetics [102]. Furthermore, a mixture of C. sinensis, Hibicus sabdariffa, Malva sylvestris, Vitis viticola, Daucus carota, Commiphora myrrh, Simmondsia chinensis and Calendula officinalis was used to examine probiotic effects that inhibited the growth of odour-producing microbes. Mixtures of these herbs were then incorporated into deodourant aerosols, gels, emulsions, sticks, creams, powders, soaps and lotions [103]. Cassia alata (Senna alata) is also used as a traditional medicine to treat body odour [104, 105]. Its S. epidermidis inhibitory effect was compared with that of other medicinal plants used in Thailand. Cassia alata showed a moderate MIC and MBC (2500 and >5000 ppm), similar to Barleria lupulina, Lawsonia inermis and Psidium guajava. In the same study, Garcinia mangostana was found to be the most potent S. epidermidis inhibitor (MIC = 39 ppm), followed by H. sabdariffa and Eupatorium odoratum (MIC = 625 ppm, each) [106]. Hibicus sabdariffa was formulated into deodourant products [103]. Chaenomeles speciosa is used in China because of its hepatoprotective effect, anti-microbial, anti-inflammatory and anti-tumour activities. The essential oil of this species contains b-caryophyllene as a major constituent (12.52%) and a moderate amount of linalool (1.33%). The compound was effective against several microorganisms including S. epidermidis (MIC and MBC of 1570 and 3130 ppm) when compared with standard treatments (e.g. levofloxacin; MIC = 610, MBC = 1220 ppm) [107]. Garlic is used for a number of infectious diseases and for its antibacterial activity, including inhibition of S. epidermidis. It was found that S. epidermidis was sensitive to garlic extract, particularly crude aqueous. The majority of S. epidermidis was killed by garlic (90– 93%) in 1 h, although resistance was found following 3–4 h of incubation [108]. Furthermore, the MIC and MBC of garlic juice were evaluated: the concentration was low, and the active compound was found to be equally active at a dilution factor of 128. In addition to garlic, some vegetables and fruits play a role in S. epidermidis inhibition. For example, the MIC of pomegranate was found to be effective at a dilution factor of 16, whereas that of

rhubarb was effective at a dilution factor of 4. In addition, beet, cherry, cranberry, red onion, red cabbage, raspberry and strawberry inhibited S. epidermidis with a dilution factor of 2 [109]. Ginkgo biloba leaf and Phellodendron amurens bark extracts were used as deodourants because of their inhibition of the degradation of the apoD-chelating odourant. The extracts could be effectively used at 0.1–20% ww)1, although the most commonly used amount was 0.5–10% ww)1 [95]. Gunnera perpensa, an herb traditionally used for psoriasis treatment, was purified, and benzoquinone, benzopyran (2-methyl6-(3-methyl-2-butenyl)benzo-1,4-quinone and 6-hydroxy-8-methyl2,2-dimethyl-2H-benzopyran) were isolated from leaves and stems. The isolated benzoquinone significantly inhibited the growth of microorganisms, particularly S. epidermidis, at an MIC of 9.8 ppm. Additionally, benzopyran showed moderate activity towards this microbe with an MIC of 187 ppm, whereas that of ciproflaxin was 1.25 ppm [110]. Resinous exudates from twigs and leaves of Haplopappus spp. were shown to inhibit S. epidermidis, with an inhibition zone of 9–10 mm. Terpenoids in H. diplopappus, H. anthylloides, H. schumannii, H. cuneifolius, H. velutinus, H. uncinatus and H. foliosus were found to be effective, in combination with flavonoids in H. velutinus and H. foliosus [111]. Harungana madagascariensis is well known for its topical anti-bacterial properties and has been used to treat cutaneous mycoses because of its high levels of biologically active flavonoids, alkaloids, saponins, glycosides and tannins [112, 113]. Its in vitro inhibition of skin microflora was evaluated. Crude leaf extract, particularly the ethyl acetate fraction, was found to inhibit armpit- and foot odour-producing bacteria with MIC and MBC ranges of 25–250 and 100–750 ppm, respectively. Furthermore, Corynebacterium xerosis was killed at 200 ppm, whereas the growth of S. epidermidis was inhibited at 250 ppm. This effect was mediated by flavanones (i.e. astilbin or 3-O-a-l-rhamnoside-5,7,3¢,4¢-tetrahydroxydihydroflavonol) [114]. Furthermore, hop (Humulus lupulus L.) supercritical fluid extraction was used to test related anti-microbial activity against odourant-producing bacteria. MIC and MBC of hop extract were found to be 6.25 and 25 ppm, respectively, against C. xerosis and 25 and >25 ppm, respectively, towards S. epidermidis. Deodourant-containing hop extract (0.2%) was formulated and compared with the deodourant base. It was found that 0.2% hop deodourant inhibited C. xerosis four times more stronger than S. epidermidis (inhibition zone of 8, and 2 mm, respectively). In addition, axillary malodour decreased from 6.28 ± 0.70 to 1.80 ± 0.71, 1.82 ± 0.74 and 2.24 ± 0.77 following 8, 12 and 24 h of application, respectively [115]. Anti-bacterial activity of methanolic extract of Hypercicum perforatum or St. John’s Wort against S. epidermidis had been reported at 1000 ppm. Isolated hyperforin inhibited Corynebacterium diptheriae at 100 ppm [116]. Anti-bacterial activity of lichen ethanol extract was evaluated. It was found that Cetrelia olivetorum (10 ppm), Lecanora muralis (10 ppm), Ramalina farinacea (10 ppm) and Rhizoplaca melanophthalma (50 ppm) inhibited S. epidermidis with inhibition zones of 11, 13, 10 and 16 mm, respectively, whereas those of tobramycin and cephalothin, standard antibiotics, were 18, and 20 mm, respectively [117]. In addition, lichen extract-containing usnic acid was found to inhibit body malodour microorganisms at an MIC of 0.002% [118]. Licorice root extract was used to formulate aerosol, roll-on, powder, cream, lotion, stick and detergent deodourants to control

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axillary odour. The active ingredient, glycyrrhetic acid, was effective at a concentration of 0.01–5% ww)1. The preparation comprised tannic acid, resorcin, phenol, sorbic acid and salicylic acid with odour-masking agents: musk, skatole, lemon oil, lavender oil, absolute jasmine, vanillin, benzoin, benzyl acetate and menthol [119]. Androstenone generation was inhibited >95% by incubation of androsterone sulphate with C. xerosis in the presence of 500 ppm of plant extracts. The suppressive effect of androstenone was further evaluated with lower concentrations of plant extracts (125 and 62.5 ppm). Apricot (Prunus armeniaca) kernel extract was more effective than gentian, prune and triclosan, which was used as a positive control [120]. Inhibition of isovaleric acid generation was screened by means of anti-microbial activity. Sophora flavescens significantly inhibited the growth of C. xerosis, eliminating malodour. Furthermore, S. flavescens showed broad-spectrum inhibition of resident skin microbes, mediated by flavonoids [121]. Madder, or Rubia tinctorium, which is widely used as a natural dye and folkloric anti-bacterial in Turkey, was Soxhlet-extracted by ethanol and water, individually. The crude extracts (483 lg disc)1) were susceptibility tested against several bacteria including C. xerosis. The aqueous extract exerted stronger activity against C. xerosis than the ethanolic fraction (inhibition zones were 12 and 7 mm, respectively), whereas the inhibition zone of ampicillin (10 mg), a standard, was 15 mm [122]. Traditional astringent, and tonic Tamarix ramosissima or salt cedar rich in tannins, and phenolics potently inhibited C. diphtheriae. The ethyl acetate extract in particular displayed an MIC of 25 ppm, whereas the butanoic extract isolated from tamarixetin showed lower activity at an MIC of 1000 ppm [123]. Usnea barbata, Salvia officinalis, Rosmarinus officinalis, Boswellia serrata, Harpagophytum procumbens and Menyanthes trifoliata were screened against S. epidermidis and Corynebacterium spp. for antimicrobial activity. Usnea barbata was the strongest inhibitor with an MIC of 1 ppm, followed by R. officinalis with an MIC of 10 and 2 ppm, respectively. Although B. serrata showed stronger activity against Corynebacterium spp. (MIC = 1–10 ppm), its effect on S. epidermidis was reduced (MIC = 100 ppm). Harpagophytum procumbens had similar activity on the test microorganisms (MIC = 10 ppm; S. epidermidis, and 10–20 ppm; Corynebacterium spp.). However, S. officinalis was the least effective anti-bacterial agent (MIC = 20 ppm; S. epidermidis, and 10–20 ppm; Corynebacterium spp.). Isolated (+)-usnic and carnosic acid exhibited stronger activity than the crude extract. (+)-Usnic acid inhibited S. epidermidis at an MIC of 4 ppm, and Corynebacterium spp. at 4–8 ppm, whereas values for carnosic acid were 64 and 32–64 ppm, respectively [124]. Essential oils Abies cilicica, Cilician fir, is native to the Mediterranean region, and affords resin traditionally used for antiseptic, anti-inflammatory, anti-pyretic and anti-bacterial applications in Turkey. Essential oil extracted from the cones was investigated on Gram-positive bacteria including C. xerosis; the oil showed a potent inhibitory effect with an MIC of 1.5 ppm. Aroma compounds in the oil were extracted; limonene was the most potent inhibitor of C. xerosis with an MIC of 3 ppm. a-, and b-pinene as well as myrcene had an MIC of >8 ppm [125]. Anethum graveolens oil inhibited Corynebacterium growth at 4.5, 0.09, 0.04 and 0.02 lg filter paper disc)1 [126]. Staphylococcus

epidermidis was inhibited by essential oil extracted from Anthemis aciphylla [127, 128]. Grammosciadium platycarpum oil was found to inhibit malodour-producing microorganisms: limonene inhibited S. epidermidis at an MIC of 600–5000 ppm [129]. In addition, essential oils that inhibit Gram-positive bacteria may be applicable to control malodour [130]. Hydrodistillation of essential oil from Inula helenium was conducted. S. epidermidis was found to be inhibited by the oil (MIC = 3700 ppm, MIC of streptomycin = 60 ppm); alantolactone and isoalantolactone were reported as the main constituents [131]. Melaleuca alternifolia or tea tree oil was also applicable in deodourants because it contains terpinen-4-ol, the active antimicrobial agent. The MIC and MBC against Corynebacterium spp. were found to be 0.5% and 2% (vv)1), respectively. In addition, it inhibited Staphylococcus spp. at an MIC and MBC of 0.5% and 1–2% (vv)1), respectively, in particular S. epidermidis (MIC = 0.5% and MBC = 2% vv)1) [132]. Coriander (Corriandrum sativum) oil inhibited micrococci and diphtheroids at an MIC of 0.1% because of its oxygenated terpenoids. The lichen extracts and coriander oil could be incorporated into a stick deodourant at 0.1–3% and 1.0–6.0% ww)1, respectively, although the preferred amounts were 0.038–0.42% and 1.8–2.2% ww)1, respectively. In the same deodourant formulation, witch hazel, Aloe vera and chamomile extracts were additionally incorporated. This formulation absorbed moisture [118] and thereby inhibited microbial metabolism. Essential oils from commercialized spices such as oregano (Origanum minutiflorum and O. onites), black thyme (Thymbra spicata) and savoury (Satureja cuneifolia), which contains cavracrol, were tested against C. xerosis. Inhibition was observed at the dilution range of 1 : 50–1 : 200 [133]. Furthermore, Satureja species were distilled to obtain essential oils and evaluated with regard to their antimicrobial activities and chemical composition. Staphylococcus masukensis potently inhibited S. epidermidis, followed by Staphylococcus pseudosimensis and Staphylococcus biflora (MIC = 370, 750 and 980 ppm, respectively). Linalool levels were highest in S. masukensis oil (4.44%); this compound was found to be the strongest inhibitor against S. epidermidis (MIC = 250 ppm), compared to caryophyllene oxide and pulegone (MIC = 900 and 950 ppm, respectively). The antibiotics amoxicillin with clavulanic acid and netilmicin had an MIC of 3 and 4 ppm, respectively [134]. Therefore, it could be concluded from this study that essential oils containing linalool, caryophyllene oxide and/or pulegone should be considered S. epidermidis growth inhibitors. In addition, essential oils from cumin (Cuminum cyminum), sweet fennel (Foeniculum vulgare), laurel (Laurus nobilis), mint (Mentha spicata), marjoram (O. majorana), pickling herb (Echinophoria tenuifoli), sage (Salvia aucheri) and thyme (T. sintenesi) were found to inhibit C. xerosis at the oil concentration of 0.2–2% [135]. Anti-oxidant and anti-bacterial activities of Salvia eremophila extracts were analysed by means of hydrodistillation and Soxhlet extraction in methanol to obtain essential oil and crude methanol extract, respectively. Free radical scavenging and lipid peroxidation inhibitory activities of crude methanol were more potent than those of the essential oil. However, the inhibitory effect of essential oil that contained linalool was greater than methanol extract against S. epidermidis (MIC = 125, and 250 ppm, respectively); activity towards P. vulgaris was relatively low (MIC = 500, and 125 ppm, respectively) [136]. The anti-bacterial activity of thyme oil prepared at different developmental stages was compared. Essential oil prepared from thyme (Thymus caramanicus) at floral budding, and flowering states showed two-fold greater S. epidermidis inhibition (MIC = 900 ppm) than essential oil from seed

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and vegetative stages (MIC = 1800 ppm). Cavacrol inhibited S. epidermidis at an MIC of 0.22 lL (of 70% carvacrol solution in methanol). The flowering stage of T. caramanicus development yielded compounds that were the most potent (68.9%), followed by floral budding (66.9%), seed (60.2%) and vegetative (58.9%) stages [137]. The essential oil of Semenovia tragioides, which is an endemic plant with highly flavoured leaves that are frequently used in jam, and pickles in Iran, was prepared and tested against S. epidermis. Its MIC was found to be 2000 ppm compared with an MIC of 500 ppm for rifampin and gentamicin, which were used as positive controls. A lipid peroxidation inhibitory effect was also observed (% inhibition = 9.1 ± 0.3; 0.7 mg of test sample), although it was less potent than that of the positive control (BHT = 95.6 ± 1.3%). Chemical composition analysis revealed anti-bacterial effects of linalool 5.7 ± 1% together with lavandulyl acetate and geranyl acetate [138]. In addition to S. tragioides oil, essential oils from two cultivars of Sideritis erythrantha (erythrantha, and cedretorum cultivars) were evaluated on S. epidermidis. The cedretorum cultivar, which elicited greater anti-oxidant effects by means of 1,1-diphenyl-2-picrylhydrazyl radicals (DPPH), b-carotene bleaching and reducing power assays, showed stronger S. epidermidis inhibition than the other cultivar. However, the cedretorum cultivar showed good anti-bacterial activity (10.00 ± 0.24 mm at 10 lL) compared to vancomycin (10.00 ± 0.24 mm at 30 lg). In addition, the more potent cultivar contained higher amounts of pulegone. However, linalool content was similar [139]. Therefore, anti-bacterial activity was consistent with the description of linalool and pulegone reported previously [140]. Smyrniopsis aucheri oil containing a-bisabolol (19.91%), widely used in cosmetics including underarm deodourants, as well as a- and b-pinene (15.10% and 6.58%), was found to potently inhibit S. epidermidis [141]. Staphylococcus epidermidis was inhibited by essential oil extracted from Ziziphora clinopodioides at 10-lL filter paper disc)1 [127] with an MIC of 60–1000 ppm [128]. Ziziphora clinopodioides oil (10 lg) contained (+)-pulegone (31.86%) 1,8-cineole (12.21%) and limonene (10.48%) as the major aroma compounds and inhibited Corynebacterium spp. at an MIC of 15.60–31.25 ppm, whereas its methanolic extract showed less activity (MIC = 250 ppm) [142]. In addition, Ziziphora persica oil containing high levels of (+)-pulegone (79.33%) but low levels of limonene (6.78%), and no 1,8-cineole exhibited a wide range of Corynebacterium spp. inhibition (MIC = 250– 7.81 ppm); its methanolic extract showed the same activity [143]. Essential oils and the aromatic compounds contained therein should be incorporated into anti-perspirant and deodourant products. Linalool and dihydromyrcenol were combined at a ratio of 4 : 1–1 : 4 in body odour-controlling products. The concentration of aroma compounds ranged from 0.2% to 1% (ww)1). Furthermore, avocado and vegetable oils as well as lichen extract were added, for their soothing effects [144]. Essential oils also mask unexpected odours and exert bactericidal effects. Vegetable and animal oils incorporated in a deodourizing emulsion were as follows: sweet almond, groundnut, wheatgerm,

References 1. Ackerl, K., Atzmueller, M. and Grammer, K. The scent of fear. Neuro Endocrinol. Lett. 23, 79–84 (2002). 2. Prehn, A., Ohrt, A., Sojka, B. et al. Chemosensory anxiety signals augment the startle

linseed, jojoba, apricot stone, walnut, palm, pistachio, sesame, rapeseed, cade, maize germ, peach stone, poppy seed, pine, castor, soya, avocado, safflower seed, coconut, hazelnut, olive, grapeseed, sunflower, whale lard, horsehoof, tuna, caballine, otter, egg, sheep, seal, turtle, halibut liver, marmot, cod liver, neat-foot and carbon oils. The combination of these oils in the emulsion was stable and washable with conventional detergents [145]. In addition to the above herbs, those with astringency, and folkloric use as tonics should be applicable for body odour control. Adiantum capillus, Bergenia ciliate, Bombax ceiba, Cannabis sativa, Cynodon dactylon, Cyperus rotundus, Dalbergia sissoo, Dodonaea viscose, Fumaria indica, Juglans regia, Olea ferruginea, Phyla nodiflora, Punica granatum, Pyrus pashia, Rumex chalepensis, Sapindus mukorossi, Solanum miniatum and Woodfordia fruticosa were recently investigated because of their ethnopharmacological uses in folk cosmetics in Pakistan [146]. In particular, Pinus roxburghii was used as a traditional deodourant [147]. Furthermore, Cassia occidentalis, an Ayurvedic plant, contains flavonoids (particularly apigenin, flavones, alkaloids, tannins and saponins) with biological activity including C. diphtheriae inhibition that is applicable to deodourant development [106]. In addition, some of the traditionally used herbs might be applicable for body malodour treatment product development because of their S. epidermidis inhibitory effect. For instance, Bersama abyssinica, Erlangea cordifolia, Hoslundia opposite, Lantana trifolia, Phyllanthus guineense, Physalis peruviana, Podocarpus milanjianus, Rubus apetalus, Steganotaenia araliacea and Vernonia auriculifera that are traditionally used for their anti-microbial activity in Africa [147]. Conclusions Body or axillary odour is offensive chemical communication that strongly adheres to clothes and shoe fibres (remaining even after laundering), negatively impacting one’s self-confidence. Topical compounds that inhibit microorganisms growth or bacteria enzyme reactions, absorb sweat and malodour, neutralize odours, and/or limit sweat secretion have been discussed in this review in terms of their ability to reduce malodour. These ingredients are natural, naturally derived and synthetic in nature. Research involving the use of fragrance precursors as alternative substrates to bacteria enzymes has also been discussed. Using this approach, bacteria enzymes catalyse the release of pleasant, aromatic scents vs. unpleasant malodourleaving the natural skin flora unaltered. Although some deodourant products can irritate the skin with long-term use, the many options described in this review present a plethora of choices that have minimal safety or skin irritation concerns. Acknowledgements The authors acknowledge Mae Fah Luang University on facility support for this manuscript preparation and the reviewers on their valuable suggestions that make the article more comprehensive.

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