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Personal Hygiene and Vulvovaginitis in Prepubertal Children

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Personal hygiene and vulvovaginitis in prepubertal children

Fatıma Cemek, Dursun Odabaş, Ünal Şenel, A. Tuba Kocaman

PII: S1083-3188(15)00262-4
DOI: 10.1016/j.jpag.2015.07.002
Reference: PEDADO 1875

To appear in: Journal of Pediatric and Adolescent Gynecology

Received Date: 27 November 2014

Revised Date: 12 June 2015
Accepted Date: 10 July 2015

Please cite this article as: Cemek F, Odabaş D, Şenel Ü, Kocaman AT, Personal hygiene and
vulvovaginitis in prepubertal children, Journal of Pediatric and Adolescent Gynecology (2015), doi:
10.1016/j.jpag.2015.07.002.

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Original article

Personal hygiene and vulvovaginitis in prepubertal children

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Running title: Vulvovaginitis in prepubertal girls

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Fatıma Cemek1,*, Dursun Odabaş2, Ünal Şenel3, A. Tuba Kocaman3

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1
Department of Pediatrics, Basaksehir State Hospital, Istanbul, Turkey
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2
Department of Pediatrics, Konya Training and Research Hospital, Konya, Turkey

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Department of Bioengineering, Faculty of Chem. and Met. Eng., Yıldız Technical University,
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Istanbul, Turkey,
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*
Correspondence:
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Dr. Fatıma Cemek

Department of Pediatrics

Basaksehir State Hospital, Istanbul, Turkey

Tel: 0202 383 46 32 Fax: 0212 383 46 25;

E-mail: [email protected]
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Abstract.

Objectives: To determine and compare clinical and microbiological features of vulvovaginitis

in prepubertal girls.

Background: Vulvovaginitis is the most common gynecological problem of childhood.

Methods: This study involves forty-five girls from 2-12 (5.38±2.9) years old; and twenty-six

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girls from 3-12 (5.72±3.1) years old as a control group. Anamnesis and physical examination

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were followed by vaginal smear, urine culture and stool analyses from both groups, and the

personal hygiene status and education level of the mother were determined.

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Results: The most common symptoms among the patients were vaginal discharge (44.4%),

vulvar erythema (37.8%), and vaginal itch (24.4%). Microorganisms, isolated from vaginal

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smears, were detected in 48.9% of the patients. Escherichia coli was shown in the urine
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culture of three patients with vulvovaginitis (6.70%). In microscopic stool analysis parasites

were detected (45.9%). We found some relevant personal hygiene factors, such as wiping
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back to front (42.9%), cleaning by herself after defecation (89.3%), using toilet paper (60.7%)
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and wet wipes (21.4%), having bath by standing (14.3%) and by sitting (46.4%), among
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patients. The questionnaire also showed that the children wear tight clothing (35.7%).

Conclusion: Our findings suggest that vulvovaginitis in prepubertal girls is related not only to
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microorganisms but also poor personal hygiene, the educational status of mothers and specific

irritants.
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Key words: Prepubertal girls, vaginal discharge, vulvovaginitis, personal hygiene

Introduction
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Although the actual incidence is unknown, vulvovaginitis is considered to be the most

common gynecological problem in children and adolescents. Many factors can contribute to

inflammation in the genital area. These factors include introitus less protected by arrangement

of the labia majora, irritation of the vaginal mucosa and low estrogen concentration leaving

the patient susceptible to infection, exposure to irritants (bubble bath), poor hygiene and

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infection by specific pathogens. If symptoms such as vaginal discharge, dysuria,

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inflammation, itching and vulvar erythema are present, it is a case of vulvovaginitis (1-4).

The proximity of the anus and vagina can cause contamination by fecal bacteria. Also,

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prepubertal girls lack protective labial fat pads and pubic hair. In addition, one effect of

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estrogen in puberty is to thicken the vaginal mucosa and thus reduce the incidence of potential
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infections and vaginitis (2-7).

Approximately 75% cases of vaginitis in prepuberty are non-specific vaginitis (7). In

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cases of non-specific vaginitis, Coliform bacteria, Escherichia coli, Enterococci, anaerobic

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Diphtheroids and microorganisms such as bacteria that suggest fecal contamination are the
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most common microorganisms. Many scientists think that inadequate hygiene and tight

clothing (nylon underwear, tights and plastic-coated paper diapers) may have a role in the
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development of non-specific vaginitis. Another common factor is exposure to irritants such as

perfumed cleaning supplies in laundry and bathing, as well as soap (vigorously rubbing the
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genital area with soap). Thus, mildly irritating chemicals deposited at the entrance of the
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vagina cause chemical vaginitis / irritant vaginitis. Then, super-infection with local

microorganisms can develop (8-10).

The aim of this study is to determine and compare the clinical and microbiological features of

vulvovaginitis and to clarify the contribution of clinical and environmental factors and

infection to the aetiology of vulvovaginitis in prepubertal girls.

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Materials and methods

This study was approved by The Human Research Ethics Committee at the Yuzuncu

Yıl University Medical School and conducted in accordance with the Helsinki Declaration.

Parents were informed about the study, and informed written consent was obtained from each

before the start of the study.

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Patients who presented to the children's health and disease clinic in the faculty of

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medicine research and training hospital were admitted to this study. Forty-five girls who were

beyond the diaper stage and who presented with complaints such as redness in the genital

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area, pain, burning, tenderness, itching, and vaginal discharge were diagnosed with

vulvovaginitis and admitted as a patient group. Girls aged 2-12 years at prepubertal status

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Tanner stage I with absence of secondary sexual characteristics, and showing typical
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complaints and symptoms of vulvovaginitis, were enrolled in the study.
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The control group was randomly selected for this study. Girls included in the control

group were of prepubertal age and at Tanner stage I. The twenty-six girls had no
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gynecological complaints, no history of sexual abuse and no systemic antibiotic therapy.

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The families of the children included in this study were informed about the study. The

required permissions were obtained for the examination and laboratory tests. The detailed
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histories of individuals in both groups were taken and clinical information and laboratory
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findings were recorded. The urine, vaginal cultures and stool samples were collected carefully
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from children.

Precautions were taken in the prepubertal girls to prevent contamination of the urine

with vaginal discharge. When urine was collected from small children who could not control

their bladder sphincter, special sterile containers were used. Any contact with the container’s

interior walls was avoided. A midstream sample was the appropriate specimen for a urine

culture: urine was collected after the first brief miction was discarded and before the miction
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was completed. The container was immediately sent to the laboratory for analysis. The

samples were inoculated onto 5% sheep blood-brain heart infusion agar (DIFCO-USA), and

eosin methylene blue agar (DIFCO) medium in the microbiology laboratory. Pathogen

identification and antimicrobial susceptibility tests were examined using Sceptor panels

(Becton-Dickinson, USA).

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Stool samples were collected from all the asymptomatic girls and the symptomatic

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girls. After being placed into stool containers, the samples were examined by direct

microscopy in the parasitology laboratory. In the early morning of three consecutive days, a

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tape test for pinworms was taken from the perineal area of every child with anal itching,

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spread on a slide, and examined under a microscope.
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The vaginal cultures were taken by establishing with the child and the child’s family

good relations and trust for the examinations and investigations. Then the patient was laid on
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the examination table with legs open in the supine position. In the physical examination,
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without use of auxiliary tools like speculum and otoscope, the child’s prepubertal status, skin
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disease, type of stream, and the condition of the vulva and vagina were determined. The

assistance of child’s mother was provided during this process. The swab cultures were taken
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to detect ureaplasma and mycoplasma using specially prepared cotton-tipped sterile, wooden

swabs as a transport medium. The resulting samples were immediately sent to the
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microbiology laboratory for cultivation.

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The data obtained from the patient and control groups were compared. Statistical

analysis was performed with SPSS ver. 20.0. Chi square test was used to compare categorical

variables and Student t test was applied for continuous variables of the treatment groups. For

statistical significance p value of 0.05 was accepted. The average of the data and standard

deviation of patients and control subjects were shown as X ± SD.

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Results

The patient group was composed of forty-five girls from 2-12 years who complained

of vaginal discharge; the control group was composed of twenty-six girls from 3-12 years.

The mean age of children belonging to the patient group was 5.38±2.9 years, whereas in the

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control group this value was 5.72±3.1 years. A statistically significant difference was not

determined between the ages of patient and control groups included in this study (p>0.05).

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Clinical symptoms of patients who were diagnosed with vulvovaginitis are shown in Table 1.

Microorganisms isolated from the cultures are summarized in Table 2. The stool microscopy

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results of stool samples obtained from patients and control groups are shown in Table 3.

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Giardia intestinalis was detected in six children (13.3%) in the patient group and two children
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(7.7%) in the control group. Blastocystis hominis was determined in 3 (6.7%) diseased

children and two children (7.7%) in the control group. Enterobius vermicularis and Ascaris
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lumbricoides, were found in 10 children (22.2%) and one (2.2%) child respectively in the

patients group, whereas these parasites were not found in the control group. Trichuris
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trichiura and iodamoeba butschlii were not detected in the patient group. However, it was
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seen in one child (3.8%) in the control group. The educational status of the children’s mothers
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is shown in detail in Table 4. Hygiene information on patients whose cultures contained

microorganisms are shown in Table 5. Microorganisms were detected in vagina and/or urine
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cultures of 10 girls (35.7 %) who use tight underwear and tights, in 12 girls (42.9 %) who
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clean themselves from the back to the front, in 25 children (89.3 %) who clean themselves

after the toilet, in 4 children (14.3 %) who have a bath while standing, in 13 children (46.4 %)

who have a bath while sitting, in 6 children (21.4 %) who have a bath in a bathtub-basin, in 6

children (21.4 %) who use wet wipes and in 17 children (60.7 %) who use toilet paper.

Discussion
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Prepubertal girls are anatomically, physiologically, and behaviorally exposed to an

increased risk of developing vulvovaginitis. Vaginal discharge is the most common

gynecological complaint in prepubertal girls. Vulvovaginal inflammation is seen in 40 to 50%

of patients who are admitted to the pediatric clinic (5-7). The families and children have

difficulty in expressing discomfort because of undue fear and anxiety caused by society’s

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apprehensions about privacy, by traditional upbringing and by ignorance about the disease.

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The most common complaints of patients are vaginal discharge, vulvar infection signs

(redness, itching, and burning) and fusion of labia minora (3,4,11,12). Piippo et al. detected

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32% vaginal discharge, 21% itching, 22% burning-pain, 13% genital redness, 10% bleeding,

29% urinary symptoms, 3% sensibility, and 7% pain symptoms in 68 prepubertal girls with

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vulvar symptoms (13). In a study conducted in Spain, the most common symptoms of
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vulvovaginitis such as discharge, itching, and dysuria were determined in 74 girls between the
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ages of 2 and 12 (14). In our study, the most common signs and symptoms detected in patients

with vulvovaginitis were: 44.4% vaginal discharge, 24.4% vaginal itching, 37.8% vulvar
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erythema, 33.3% dysuria, 6.3% perineal pain-burning during urination, 13.3% enuresis, 2.1%
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encopresis, 35.6% anal itching.

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Such pathogenic microorganisms as β-hemolytic streptococci, H. influenzae, and, S.

pneumoniae are frequently responsible for vulvovaginal infections in children (5, 15-17).
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Sexually transmitted infections such as Neisseria gonorrheae and Chlamydia trachomatis are
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important causes of vulvovaginitis following child sexual abuse, and screening of these

infections should be undertaken in all children evaluated for possible sexual abuse (17-19).

Some researchers have determined that many bacteria such as coliforms and

streptococci constitute mixed infections in vulvovaginitis in prepubertal girls. Also, cheesy

vaginal discharge is seen in vaginal candidiasis. Generally, infection is facilitated by use of

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antibiotics in patients with diabetes mellitus and increased moisture and heat in the perineal

region caused by tight clothing (5-7, 20).

In our study, Mycoplasma hominis and Ureaplasma were examined because of being

member of colonization and inducing vulvovaginitis. We detected Ureaplasma urealyticum

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colonization only in one patient, six years old.

75% of women are subject to vulvovaginal candidiasis at least once during their

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lifetime (20, 21). Candida is usually not isolated in prepubertal girls, but it may be found in

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girls with predisposing factors, such as a recent course of antibiotics, diabetes or the wearing

of diapers (7, 16). Basic complaints are itchiness, sensitivity and vaginal discharge forming a

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yellow-white curd. We detected only one Candida infection in the patients group. This
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patient, who attends the pediatric nephrology unit, used prophylactic antibiotics at low doses

following diagnosis of recurrent urinary tract infection and enuresis.

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In our study, prepubertal girls whose ages were from 2-12 were included in the patient
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group. This group of children is not sexually active. No sign or symptom of sexual abuse was
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detected in their physical examination or history. For this reason, we did not perform any

culture for microorganisms of sexually transmitted diseases. In our study, microorganisms

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including Streptococcus bovis D-II (6.7%), Enterococcus faecalis D (4.4%), E. coli (4.4%),

Non A-Non B hemolytic Streptococcus (4.4%), Diphtheroid bacilli (8.9%), S. epidermidis

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(2.2%), Ruminococcus productus (6.7%), Candida spp. (2.2%), Actinomyces israelii (6.7%),
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Ureaplasma urealyticum (2.2%) were isolated from cultures of patients with vulvovaginitis.

Recently, many studies have emphasized the importance of checking for foreign

bodies in the etiology of vaginal discharge in prepubertal girls. The main clinical symptoms of

a vaginal foreign body are vaginal bleeding, bloody spotting in underwear and a foul-smelling

discharge. The researchers emphasize that this cause is rare but it should be considered in the
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presence of ongoing bloody discharge in girls who are considered to have an infection. The

most common foreign body is toilet paper. After removal of the foreign body, the

recommended treatment is sitz baths and application of local estrogen cream (22-24). In our

study, a foreign body was not considered in any of the cases because of the duration and

character of discharge.

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Enterobius vermicularis is a common etiologic factor in vulvovaginitis. Increased

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itching of perianal/perineal region at nights, crowded and poor hygiene conditions should

make us consider infestation with E. vermicularis (16, 23, 25). Yilmaz et al. detected it in two

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prepubertal girls among 27 prepubertal girls in their patient group (26). E. vermicularis was

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found in 32.3% of cases of vulvovaginitis in study by Pierce and Hart, and Williams et al.
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reported it as an etiological factor in 20% of cases of prepubertal vulvovaginitis (27-28). In

our study, E. vermicularis was detected in 10 (22.2%) cases of 45 symptomatic prepubertal

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girls. The high incidence of patients with parasites may be explained by patients’ low

sociocultural level and poor hygiene conditions.

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Many researchers have defined the most common cause of vulvovaginitis as allergic

reaction to bubble bath and given some recommendations to the families of patients about
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allergens and the possible role of hygiene in vulvovaginitis (1,24). All of our patients use soap

in the bathroom, as stated by their families. Use of bubble bath was not detected. Allergic
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vulvovaginitis was not encountered in patients, possibly because patients used only cotton
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underwear and had no exposure to irritant substances such as bubble bath.

In our study, non-infectious vulvovaginitis was detected in approximately 80% of

symptomatic girls. The majority of microorganisms indicated in our study belong to the

normal vaginal and intestinal flora. This finding suggests colonization caused by fecal

contamination due to the proximity of anus and vulva, and fecal contamination due to
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inadequate and incorrect cleaning after using the toilet (back-to-front cleaning). Because

normal vaginal flora isolated from patients’ vaginal cultures responded to conservative

treatment in 2-4 weeks, the etiology of the vulvovaginitis in these cases is thought not to

derive from a specific infectious pathogen.

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In the present study, a similar flora was isolated both in studied girls and in controls.

However, a statistically significant difference was found in the number of samples with

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positive microbiological findings between symptomatic girls and controls (p<0.05) (Table 2).

Moreover, we found that wearing tight clothing and cleaning from back to the front after

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using the toilet were associated with increased risk of having a positive urine and vaginal

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culture or of having symptoms. In contrast, bathing while standing and using wet wipes to
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clean were associated with decreased risk of infection and symptoms (Table 5).

We determined that, vulvovaginitis not only depends on infectious agents but also
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poor hygiene and improper cleaning (35.7%) (cleaning from back to front), and the cleaning
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habits of girls after toilet by themselves (89.3%). In addition, use of wet wipes (21.4%) and
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toilet paper (60.7%) can contribute to fecal contamination of the vulva and increase the risk of

vulvovaginitis. The bath type was also important; bathing while standing (14.3%) was found
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to be healthier than while sitting (46.4%) or in a basin (21.4%). The use of tight clothing like

tights was another risk factor for vulvovaginitis. Wearing tights and tight clothing (35.7%)
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was determined as an important risk factor for vulvovaginitis in children in our study group.
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We concluded from our research that the mother’s education level was another

important factor for this disease. Mothers of the children with vulvovaginitis and of children

in the control group graduated from primary school or had a lower level of education (57.8%

and 23.1%, respectively) (Table 5). Children of mothers with low educational level do not

receive an adequate level of toilet training or it may be considered that they do not show
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sensitivity to this issue. The results of another study also showed a significant correlation

between bacterial vaginosis and educational status; it was evident that the lack of education

was significantly associated with bacterial vaginosis (p<0.05) (29).

In another study, the most common sources of vaginal irritation and discharge were

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respiratory bacteria which were manually transmitted to the perineum, local irritants induced

by bubble bath or nylon underwear, and fecal contamination induced by poor perineal hygiene

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(1,5,24,30). Indeed, in our study, some of the microorganisms isolated from cultures were

members of the intestinal flora. This indicates the inadequacy of cleaning after toilet.

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Our study had several limitations. We had great difficulties to create the control group

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due to social and cultural perceptions. Therefore, the number of children in the control group
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was relatively small. Moreover, we did not compare vaginal cultures with cultures from the

nasopharynx. At the same time, symptomatic girls treated with antibiotics or other meds. All
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of the patients and the control group improved hygiene habits.

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Conclusion
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Our findings suggest that vulvovaginitis in prepubertal girls is related not only to

microorganisms but also to poor hygiene, educational status of mothers and specific irritants.
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General recommendations should be given about personal hygiene and avoidance of irritants
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to the mothers of girls. A specific pathogen is not isolated in 25-75% of girls with

vulvovaginitis. This may be due to non-specific irritation resulting from the use of bubble

bath, soaps, or shampoos; poor hygiene; tight clothing; or fecal contamination (7).

Nevertheless, the presence of symptoms such as redness, itching or discharge mostly indicates

an infectious etiology. Organisms such as N. gonorrhea, Chlamydia and Trichomonas are the

strongest predictor of sexual abuse in children. The possibility of sexual abuse should always
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be considered when a child presents with genital symptoms. Although Candida is not

common in children, it can be seen in children who use antibiotics. Atrophic vaginitis may be

present in some children with recurrent infections due to reduced resistance of vaginal mucosa

to infection.

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22. Stricker T, Navratil F, Sennhauser FH. Vaginal foreign bodies. J. Paediatr. Child

Health 2004; 40: 205–207.

23. Sanfilippo JS. Vaginal Discharged Time for a Reappraisal. J Pediatr Adolesc

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24. Smith YR, Berman DR, Quint, E.H. Premenarchal Vaginal Discharge: Findings of

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Procedures to Rule out Foreign Bodies. J Pediatr Adolesc Gynecol 2002; 13:227-230.

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25. Romero P, Rodrıguez E, Munoz M et al. Voiding Dysfunction: Another Etiology of

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26. Yilmaz AE, Celik N, Soylu G, Donmez A, Yuksel C. Comparison of clinical and

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27. Pierce AM, Hart CA. Vulvovaginitis causes and management. Arch Dis Childhood
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1991;67:509–12.

28. Williams TS, Callan JP, Owen LG. Vulvar disorders in prepubertal females. Pediatr
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Ann 1986;15:588–605.
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29. Bahram A, Hamid B, Zohre T. Prevalence of Bacterial Vaginosis and Impact of

Genital Hygiene Practices in Non-Pregnant Women OMJ. 2009;24, 288-293.

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30. Hansen MT, Sanchez VT, Eyster K, Hansen, KA. Streptococcus pyogenes Pharyngeal

Colonization Resulting in Recurrent, Prepubertal Vulvovaginitis. J Pediatr Adolesc

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Gynecol 2007; 20: 315-317.

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Table 1. Clinical symptoms of the patients with vulvovaginitis

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Prepubertal group
Average age 5.38 years
(range 2–12 years)

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Clinical Symptoms (%)
(n = 45)
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Vaginal discharge 20 44.4

Watery discharge from mouth 18 40.0

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Vulvar erythema 17 37.8

Anal itching 16 35.6

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Dysuria 15 33.3
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Odor in discharge 14 31.1

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Vaginal itching 11 24.4

Abdominal pain 12 26.7

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Parasite history 12 26.7

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History of urinary tract infection 9 20.0

Vaginitis treatment received 5 11.1

Enuresis 6 13.3

Perineal pain-burning during urination 3 6.3

Encopresis 1 2.1
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Table 2. Microorganisms isolated from the cultures of girls with vulvovaginitis and in
controls

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Microorganisms Patient Control

The vaginal swab culture n (%) n (%) p-value

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Diphtheroid bacilli 4 (8.9) 1 (3.8) p<0.05
Streptococcus bovis D-II 3 (6.7) 0 p<0.05
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Ruminococcusproductus 3 (6.7) 0 p<0.05

Actinomycesisraelii 3 (6.7) 0 p<0.05
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Enterococcus faecalis D 2 (4.4) 1 (3.8) p>0.05

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Escherichia coli 2 (4.4) 1 (3.8) p>0.05

Non A- Non B hemolytic Streptococcus 2 (4.4) 0 p<0.05
Staphylococcus epidermitis 1 (2.2) 1 (3.8) p>0.05
EP

Candida spp. 1 (2.2) 0 p>0.05

Ureaplasmaurealyticum 1 (2.2) 0 p>0.05
C

Urine culture
Escherichia coli 3 (6.7) 0 p<0.05
AC
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RI
Table 3. Stool microscopy findings in girls with vulvovaginitis and control

SC
Parasites Patient group Control group p-value
n (%) n (%)

U
Enterobiusvermicularis 10 (22.2) 0 p<0.05
AN
Giardia intestinalis 6 (13.3) 2 (7.7) p<0.05
Blastocystishominis 3 (6.7) 2 (7.7) p>0.05
Ascarislumbricoides 1 (2.2) 0 p>0.05
M

Trichurustrichura 0 1 (3.8) p>0.05

Iodamoebabutschlii 0 1 (3.8) p>0.05
D
TE
C EP
AC
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Table 4. Educational status of mothers of patient and control girls

SC
Educational status of mothers Patient group Control group p-value
n (%) n (%)

U
Illiterate 4 (8.9) 1 (3.8) p<0.05
AN
Graduated from primary school 20 (44.4) 4 (15.4) p<0.05
M

Graduated from high school 7 (15.6) 8 (30.8) p<0.05

D

Graduated from college 4 (8.9) 7 (26.9) p<0.05

TE
C EP
AC
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Table 5. Hygiene information of study groups

RI
Symptomatic

SC
patients Control
(n=45) (n=26) p-value
n (%) n (%)

U
Narrow clothing, use of tight AN 21 (46.7) 5 (19.2) p<0.05

Cleaning from back to the front 22 (48.9) 3 (11.5) p<0.05

Those who clean by 35 (77.8) 15 (57.7) p>0.05

themselves after toilet
M

Those who bathe while 7 (15.6) 14 (53.8) p<0.05

standing
D

Those who bathe while sitting 28 (62.2) 10 (38.5) p>0.05

TE
EP

Those who use wet wipes 9 (20.0) 11 (42.3) p<0.05

Those who use toilet paper 42 (93.3) 22 (84.6) p>0.05

C
AC

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