Introduction
Genital hair is one of the secondary sexual traits that alongside with thelarche marks the beginning of puberty 1. From a social and sexual perspective, it is believed that pheromonal signaling, through dense apocrine sweat glands in the pubic area, serves as a communication method to improve attractiveness 2. Its biological functions include: pheromone dissemination through apocrine glands, protection of genitalia against cloth friction, and the control of genital moisture 2), (3. Recent studies have associated the presence of pubic hair with greater capacity to trap and stop microorganisms, as well as the production of bacteriostatic peptides from sebum produced by hair follicles 4.
On the other hand, body hair removal has been a practice inherent to the human since the beginning of time 1, overstepping many cultures and periods of human history 5, being evidenced in ancient Egypt and Greek engravings 6. It has been a notably increasing practice in western countries for diverse reasons: hygienic, aesthetic, and/or erotic 7. The most common methods of genital hair removal are shaving and waxing 8. In Colombia, a recent study reported a prevalence of genital hair removal in women of 57,9% (IC 43,7%-70,8%; P<0,001) 7.
In the case of Colombia, a recent study which intended to establish the prevalence of genital hair removal in 1964 necropsies, registered a prevalence of genital hair removal between men of 31,1% and women of 57,9% 7. Although it has become a relatively mundane, normalized, unquestioned part of many men and women’s lives 5, as with any practice it is subject to adverse health consequences; ranging from less serious complications such as mechanic or infectious folliculitis and contact dermatitis6 all the way to genital burns from waxing, skin irritation, vulvar and vaginal irritation and infection, and spread of sexual transmitted infections 9. Another study in Colombia during 2015 reported a prevalence of clinical problems of 10,4% (IC95% 8,3 - 13%) related to genital hair removal which were also seen in association with one out of ten individuals over fourteen-years-old who sought medical attention by conditions not related with genital skin disorders. Out of ten individuals, six went through infectious processes, three attributed to trauma and one by alterations that underwent cutaneous symptoms 6. One plausible and modifiable factor that may change the vaginal microbiome is the presence of pubic hair.
For the above, we propose to conduct a narrative review regarding the normal skin microbiota and its impact under genital hair removal and microenvironment changes, accessing its possible risk of disbalance and disease.
Method
A specialized literature search was carried out, during the period from March to May of 2018 in PubMed, ScienceDirect and Scielo databases, using the following search words: female genitalia, microbiota, hair removal as MESH terms and genitales femeninos, microbiota, remoción del cabello as DECS terms. Inclusion criteria included articles that discussed the relationship between the removal of genital hair and the impact on the female genital microbiota, as well as the normal and abnormal bacterial flora in the female genitalia. Articles that did not have women as a population study were excluded. A total of 69 articles were initially obtained, of which 39 were finally included for the elaboration of the article, articles that discussed changes in physiological properties (transepidermal water loss, changes in pH, among others) in relation to microbiota were not included because it did not correspond to our proposed objective.
The normal female genitalia and normal skin microenviroment
As with any portion of this large organ of the integumentary system 10, vulvar skin undergoes a series of physiological changes over time which altogether have an impact on its mechanical properties 11. Morphology and physiology of the vulva and vagina change over a lifetime. Newborns exhibit the effects of residual maternal estrogens; labia majora appear thick and labia minora seem well developed. As the estrogen levels dissipate, the vaginal epithelium becomes thinner. Pubertal changes are induced by adrenal and gonadal maturation. Pubic hair growth proceeds in five stages and as estrogen production rises, vaginal epithelium thickens, cervix and vagina increase in size and fat begins to establish alongside the mons pubis and labia majora. During reproductive years, the menstrual cycle is already established and plays a key role in vulvar and vaginal changes. During mid-cycle, estrogen keeps leading the vulvar epithelial rise, glycogen content and parakeratosis of the vaginal epithelium. Pregnancy also becomes a significant variable, as an increase in total blood volume heightens the coloration of the vulva and vagina. Venous distensibility rises in association with progesterone levels. Delivery represents a change in morphology and dimensions of the vaginal tract, which are generally reversed over the next six weeks. Following menopause, pubic hair becomes scarce, the labia majora loses subcutaneous fat, labia minora, vestibule and vaginal mucosa undergo atrophy, vaginal secretions decrease, tissue loses its thickness and becomes predisposed to irritation and susceptible to infection 10.
Normal genital microbiome
An abundant and diverse community of microorganisms including bacteria, fungi and virus inhabit the human skin 12. The human microbiome is almost as unique as a person’s own genome 13. An estimated of over 100 distinct species, making up a total of 1 million microorganisms, colonize each square centimeter of human skin 14. The terms normal skin flora and commensal skin flora are used to describe those microorganisms that are usually found in the skin of healthy individuals 15. Bacterial composition is dependent on the physiology of the skin site, with specific bacteria being associated with moist, dry, and sebaceous microenvironments. Different body habitats have different microbiome compositions 13), (16. These precise environment characteristics allow bacteria to produce extracellular substances that result in networks (or biofilms), which enable multicellular functions, differentiation and community-like living 17. Anatomical sites with partial occlusion (such as axilla and perineum) yield a greater density of microorganisms than less occluded areas (legs, arms and trunk) 18.
The vulvar structure, acidic vaginal pH (3.8-4.4 in reproductive age), vulvar pH (3,7- 4,7) and vaginal discharge altogether protect the genital tract from infection 19. The tract has a variety of habitats that are determined by differences in epithelium, moisture content, density of glands, degree of occlusion, proximity to other densely populated sites, among others. Vulvar folds are sites of microbial collections; balance among microbial species are usually determined by changes in moisture, sweat, menses and hormonal fluctuations19. Contaminant products such as panty liners may also have influence on vulvar environment characteristics. Runeman et al observed a mean skin temperature increase of 1.1°C as well as pH values significantly higher at labia majora and perineum in the presence of non-breathable panty liners when compared with the absence of panty liners 20.
Resident vulvar microbiota consists of organisms which are characteristic to both cutaneous and vaginal environments 21. Several studies have intended to determine and quantify the microbiology of human vulva, these studies have been summarized in table 1 (See table 1).
Aly et al reported relative proportions of bacteria at various sites on 18 individuals in the United States; vulvar microorganisms included coagulase-negative staphylococci (100%), lipophilic diphtheroids (100%) non-lipophilic diphtheroids (67%), Lactobacilli (40%), S. aureus (67%) and Micrococci (56%). Vulvar bacteria are noted in greater density and higher incidence when compared to other sites of the human body (such as forearm) 18. Runeman et al examined the differences in microenvironment and biota between standard and string panty liners. Coagulase-negative staphylococci and Corynebacterium were the most prevalent microorganisms found in locations such as perineum, labia majora and panty liner (both regular and string) 22.
Vulvar samples taken from four healthy women recovered Lactobacillus crispatus and Lactobacillus iners as the most frequent bacterial organisms; 70.5 - 97% and 28.3-96.2% of these clones respectively, reported the same phylotype found in labia minora 23. Moreover, yeast species were not frequently isolated from genital areas 23) ; Bentubo (2015), in a sample taken in Brazil, examined the presence of this organisms in genital regions, reportedly finding non-C. albicans candida yeasts and Candida parapsilosis as the most prevalent species 24. Labia and groin tend to have more bacteria than other genital skin sites 25. Lactobacillus spp was also reported as the predominant species by Miyamoto et al among healthy Japanese women, with Staphylococcus epidermidis likewise observed with a corresponding 98%, 100% and 95% of detection on labia and groin, mons pubis, and inner thigh, respectively 25.
The microbial organisms of the labia majora are significantly different from those found inside the vagina 26. The normal microbiota of the vagina mainly consists of Lactobacillus crispatus, Lactobacillus gasseri, Lactobacillus jensenii and Lactobacillus iners27. The importance of Lactobacillus spp. relies on its ability to produce lactic acid (by glycogen conversion) contributing to its enhanced acidic pH, thus protecting the growth of potential pathogens. Yeast cells (Mycoplasma and Ureaplasma species) may also colonized up to 20% 27.
Changes of female genital skin microenviroment: menses and experience with Herpes virus type 2 seropositive patients
The microbiota of the human vulva is complex and unique 23, constant influences, both internal (vaginal fluid and menstruation) and external (urine and fecal material) may affect its microbial type-diversity 26. Molecular methods have been developed to identify the microbial community of the genital region. Reports from healthy Japanese women showed that the most abundant phylotypes in the labia minora were most similar to either Lactobacillus crispatus or L. iners. In addition L. crispatus or L. iners were also the predominant bacteria on the labia minora at premenstruation period and clones similar to L. crispatus were predominant at both premenstruation and during menstruation 26. A previous study by Lansdell et al., intended to recover S. aureus from the external labia and tampons at the time of menstruation; a total of 7.2% of S. aureus were recovered on labia 28.
Löwhagen et al assessed microbiota in the vulvar skin between Herpes virus type 2 seropositive patients with and without clinical recurrences which showed a tendency towards more lactobacilli and E. coli on the labia majora in the asymptomatic group 29; moreover, coagulase-negative Staphylococci appeared to be the most frequent sampled microorganism (See table 2).
Genital hair removal: side effects and health concerns
Pubic hair is anatomically structured by cortex and cuticle cells, hair follicle and sebaceous glands. It is the heavier, longer hair that develops during puberty 30. These structures form a microenvironment of their own, which supports the establishment of an unique and characteristic microbiota in the pubic hair. Among the most distinctive taxa found are Corynebacterium, Staphylococcus, Finegoldia, and Micrococcus. Other studies have found abundance of Lactobacillus31. Evidence has suggested that there are differences in the bacterial composition between individuals. Tridico et al., found clear distinctions between male and female pubic hairs, which is mainly explained by the prevalence of Lactobacillus spp in women’s pubic hair in contrast with, a taxa that wasn’t found in men’s samples. However, they also observed that cross-transference of microbial pubic taxa could occur as a result of intercourse, affecting the variation in microbiota and similarities between partners 32.
Extensive hair removal leads a risk of hair microtrauma, vulvovaginal irritation (especially due to shaving) and potential spread of infectious agents throughout the pubic área 19.
Infections associated to barrier impairments in activities such as sexual intercourse were reported in a study including 61 patients, Molluscum contagiosum was found in 71% and Human Papilloma virus in 11% 33), (34. Herpes virus has been found in 2-4% of patients with grooming practices. This is commonly explained by an epidermis impairment, that facilitates the penetration and dissemination of these entities 35), (36.
Some authors have suggested the introduction of pubic hair removal and the positive rate of Phthirus pubis infestation 34; by contrast, recent observations have also suggested pubic hair as a preventive procedure against P. pubis, arguing that eradication of pubic lice (by pubic hair removal) may destroy the parasite habitat.
In addition, women who are admitted to a hospital to give childbirth may receive perineal shaving. It is believed that this measure reduces the risk of infection caused by spontaneous perineum tear or if an episiotomy is performed, consequently making episiorrhaphy easier as well as aiding with instrumental deliveries 37. However, when viewed over overall anatomical wounds (not only genital or perineal) previous studies have also appointed this measure as potentially deleterious. A 10-year prospective study of 62,939 wounds appointed perineal shaving as methods that increased the infection rate of clean wounds 38. In a more specific view of perineal shaving versus no perineal shaving, Johnson and Sidall, in 1922, compared skin preparation and perineal shaving as the control variable, and clipping of vulvar hair only as the experimental variable, with the primary outcome being febrile puerperium (if an elevation of 100.4” or above occurred on two successive days, excluding the day of delivery); no significant differences were found between both preparations 39. There is little evidence to suggest that perineal shaving benefits women entering child labor and clinical significance of the difference in women having Gram-negative bacteria is sparse 37. Although more investigations are needed to stablish links between genital hair removal and de novo infections or recurrences, it is possible that complete removal of pubic hair, being the physical barrier for the vulvovaginal area, could lead to increase susceptibility to infections 34.
Conclusions
Genital hair removal has a noteworthy effect on genital skin microenvironment; skin lesions and microbiota disturbances are prone to short- and long-term clinical significance. Considerable progress has been made in the understanding of the changes responsible for morbidity in the context of microenvironment impairment associated with genital hair removal. In the context of skin barrier changes in microbiota, hair removal may lead to possible infections, especially when activities such as sexual intercourse are taking place where Herpes type 2, Human Papilloma Virus and Molluscum contagiosum may play a role. Determining the precise microbiota changes due to this practice and its role in general microenvironment changes, represents an important clinical and scientific challenge, since overall knowledge does not consider the possible side effects of this common practice, and future recommendations may be developed in order to maintain female skin microbioma balance.