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R E S E A R C H A R T I C L E Open Access
Association between unhygienic menstrual
management practices and prevalence of
lower reproductive tract infections: a
hospital-based cross-sectional study in
Odisha, India
Belen Torondel
1
, Shalini Sinha
2
, Jyoti Ranjan Mohanty
2
, Tapoja Swain
2
, Pranati Sahoo
2
, Bijaya Panda
3
, Arati Nayak
3
,
Mary Bara
4
, Bibiana Bilung
4
, Oliver Cumming
1
, Pinaki Panigrahi
5
and Padmalaya Das
2*
Abstract
Background: The extent to which reproductive tract infections (RTIs) are associated with poor menstrual hygiene
management (MHM) practices has not been extensively studied. We aimed to determine whether poor menstrual
hygiene practices were associated with three common infections of the lower reproductive tract; Bacterial vaginosis
(BV), Candida, and Trichomonas vaginalis (TV).
Methods: Non-pregnant women of reproductive age (18–45 years) and attending one of two hospitals in Odisha,
India, between April 2015 and February 2016 were recruited for the study. A standardized questionnaire was used
to collect information on: MHM practices, clinical symptoms for the three infections, and socio-economic and
demographic information. Specimens from posterior vaginal fornix were collected using swabs for diagnosis of BV,
Candida and TV infection.
Results: A total of 558 women were recruited for the study of whom 62.4% were diagnosed with at least one of the
three tested infections and 52% presented with one or more RTI symptoms. BV was the most prevalent infection (41%),
followed by Candida infection (34%) and TV infection (5.6%). After adjustment for potentially confounding factors,
women diagnosed with Candida infection were more likely to use reusable absorbent material (aPRR = 1.54, 95%CI
1.2–2.0) and practice lower frequency of personal washing (aPRR = 1.34, 95%CI 1.07–1.7). Women with BV were more
likely to practice personal washing less frequently (aPRR =1.25, 95%CI 1.0–1.5), change absorbent material outside a
toilet facility (aPRR = 1.21, 95%CI 1.0–1.48) whilst a higher frequency of absorbent material changing was protective
(aPRR = 0.56, 95%CI 0.4–0.75). No studied factors were found to be associated with TV infection. In addition, among
women reusing absorbent material, Candida but not BV or TV - infection was more frequent who dried their pads
inside their houses and who stored the cloth hidden in the toilet compartment.
Conclusion: The results of our study add to growing number of studies which demonstrate a strong and consistent
association between poor menstrual hygiene practices and higher prevalence of lower RTIs.
Keywords: Menstrual hygiene management, Bacterial vaginosis, Candidiasis, Trichomonas vaginalis,Reproductivetract
infections
* Correspondence: pdas@aiph.ac.in
2
School of Life Sciences, AIPH University, Bhubaneswar, Odisha, India
Full list of author information is available at the end of the article
© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Torondel et al. BMC Infectious Diseases (2018) 18:473
https://doi.org/10.1186/s12879-018-3384-2
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Introduction
Menstrual hygiene management (MHM) practices vary
by socio-cultural context, educational background and
economic status, and there is wide variation in MHM
practices between and within countries [1,2]. MHM is
characterized by practices such as the type of absorbent
material used and the frequency changed, associated
body washing, the methods of washing, drying and stor-
ing reusable pads as well as other contextual factors,
such as the location of menstruation-related changing
and washing practices. These practices can be influenced
by water, sanitation and hygiene (WASH) facilities at the
household level, and the quality of, and access to, these
facilities varies significantly between and within coun-
tries [3]. MHM practices can be unhygienic and incon-
venient, particularly in resource-constrained settings,
with poor WASH access [4], and have been found to be
associated with different reproductive tract infections
{BV, and vulvo-vaginal candidiasis (VVC)} [4] and with
psychosocial stress outcomes [5].
Reproductive Tract Infections (RTIs) are a major pub-
lic health concern worldwide and are particularly com-
mon in low-income settings [6,7]. The prevalence of
RTIs and sexually transmitted infection (STIs) in women
aged 15–44 years in Odisha was 35.2% in 2002–2004 [8].
Another study from the state of West Bengal, India, has
reported that girls with higher socioeconomic status
generally had both safer MHM practices and fewer
gynecological problems [9]. The most common lower re-
productive tract infections are bacterial vaginosis (BV),
vulvo-vaginal candidiasis (VVC), and Trichomonas vagi-
nalis (TV) [10]. BV, the most common RTI, is character-
ized by an alteration in the vaginal microbiome with a
decline in Lactobacillus colonization and an overgrowth
of facultative anaerobic bacteria. Whilst vaginal inflam-
mation is usually absent in BV, it is the most serious risk
factor for women of reproductive age because of its as-
sociation with adverse pregnancy outcomes such as pre-
term birth [11,12], acquisition of sexually transmitted
infections [13], and the development of pelvic inflamma-
tory disease (PID) [14,15]. Candida infection is the sec-
ond most common RTI and VVC affects up to 75% of
reproductive-age women at least once [16]. Candida in-
fection can be asymptomatic and is thus often referred
to as colonization. VVC, the disease state of Candida in-
fection, is diagnosed by observing Candida species in
presence of local signs and symptoms of inflammation
[17]. TV infection is the most prevalent STI worldwide
[18]. TV infection can lead to reproductive complica-
tions such as pelvic inflammatory disease, tubal factor
infertility, pregnancy loss, premature membrane rupture,
preterm delivery, low birth weight [18].
The clinical signs and symptoms of these infections
overlap to a large extent, though the etiologies are quite
different. Common clinical symptoms include vaginal
discharge, dyspareunia, itching and burning sensation.
However, the poor sensitivity and specificity of individ-
ual clinical symptoms, and the poor performance of
standard laboratory tests in many settings, make the
accurate clinical diagnosis of these infections difficult
[19]. In addition, a significant proportion of genital in-
fections are asymptomatic such that laboratory testing is
required to diagnose and identify the specific cause.
Most studies assessing an association between MHM
and RTI have used self-reported symptoms to measure
outcomes which are likely biased [4]. When assessing
MHM practices, most published studies have focused on
absorbents, either comparing the type of absorbent used
(e.g. reusable vs. disposable pads) or, in fewer cases, wash-
ing, drying and storing methods for cloths used for ab-
sorption or other personal hygiene practices [4,20,21].
In a recent case-control study in Odisha, India, it was
observed that women of menstruating age with urinary
tract infections (UTI) and BV were more likely using re-
usable absorbent pads than using disposable pads [22].
Both UTI and BV were also associated with a lack of a
private space for changing, cleaning and washing during
menstruation [22]. In that study, BV and UTIs were not
detected in a significant proportion of women with vagi-
nal symptoms suggesting that other urogenital infections
may be responsible for these symptoms. Only one study
has explored the association of VVC and TV infection
with MHM practices, reporting that the use of saris for
menstrual absorbent protection was safer than rags
washed in river and dried at home [6]. However, no other
MHM practices were explored in that study. In this study
we address this gap by assessing the association of differ-
ent MHM practices among women of reproductive age in
Odisha with the risk of three common infections of the
lower reproductive tract; Bacterial vaginosis (BV), Can-
dida, and Trichomonas vaginalis (TV).
Methods
Study design and study population
This was a cross-sectional study that surveyed women
attending the Obstetrics and Gynecology (O&G) Out-
Patient Department (OPD) of two public hospitals in
Odisha state, India: Capital Hospital, Bhubaneswar;
and, Ispat General Hospital (IGH), Rourkela. Capital
Hospital is a government hospital with approximately
700 beds specializing in Obstetrics and Gynaecology,
and Family Welfare which caters to the urban and
peri-urban population of Bhubaneswar city as well as
adjoining rural areas. Almost all health care services
are provided free of cost and the majority of patients
attending Capital hospital are from the financially dis-
advantaged groups specifically from the urban and peri
urban slums and rural areas IGH, Rourkela is managed
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by the Steel Authority of India Limited and provides
free treatment for its employees and their dependents
and treatment for the general public at a subsidized
cost. The hospital is situated in a District inhabited pre-
dominantly by a tribal population, a large proportion of
the patients attending the hospital are from tribal pop-
ulations. The study population in Rourkela is therefore,
covers a broad spectrum of socio-demographic status.
The patient recruitment was done from April 2015 to
February 2016.
Non-pregnant women of reproductive age (18–
45 years) attending the O&G OPD with vaginal symp-
toms (vaginal discharge, itching, burning, dyspareunia,
with lower abdominal pain, and lower back pain), or
attending the Family Welfare Department (FWD) for
contraceptives, such as intra-uterine devices (IUD) were
eligible for enrolment. We excluded all women meeting
one or more of the following criteria: menstruating dur-
ing the clinic visit, had a hysterectomy, taken a course of
antibiotics during the previous three weeks, used oral
contraceptive pills in the previous three months, had
diabetes mellitus, were HIV positive, or had any severe
medical disorders requiring immediate referral to a
higher level of health care.
Data collection
After identification by the treating doctor, all potential
study participants underwent an informed consent
process in the local language (Odia) and those choosing
to participate provided written consent. The participants
were informed that they would be tested for RTI and
that their results would be provided free of cost and
confidentially. Trained female interviewers administered
a questionnaire collecting information about potential
risk factors for the three infections. The examined risk
factors were selected using a pre-specified conceptual
framework with three groups of risk factors: socio-eco-
nomic characteristics, MHM practices (related with
menstrual absorbent material and body hygiene), and
WASH access variables (access to water and sanitation
resources for practicing safe MHM) (Fig. 1). This frame-
work was already used by the authors in other related
work, as it captures aspects of the working definition of
MHM by the Joint Monitoring Program of the WHO
and UNICEF in 2012 (defining MHM as: Women and
adolescent girls using a clean menstrual management
material to absorb blood that can be changed in privacy
as often as necessary for the duration of the menstruation
period, using soap and water for washing the body as
Sociodemographic
Characteristics
(Age, marital status,
religion,education,
occupation,economic
situation)
Reproductive tract infections
Menstrual hygiene
practices
(Type of
absorbent,frequency and
place of absorbent
change, type of body
hygiene washing and
frequency of washing
during menstruation)
Household enabling
environment
(Access of latrine at
home, water source
location)
Fig. 1 Conceptual framework of risk factors. A conceptual framework with three groups of risk factors: sociodemographic characteristics, MHM
practices and WASH access variables
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required, and having access to facilities to dispose the
used menstrual management materials) and also other
important risk factors related to the RTI identified in the
literature. We used a questionnaire developed and tested
previously by our team [22]. Information on socioeco-
nomic factors included age, marital status, religion, edu-
cation, occupation, number of family member and
monthly income. Information on MHM practices in-
cluded the type of menstrual absorbent used, individual
hygiene habits, and domestic water and sanitation condi-
tions. Questions on the use of absorbents included: the
type of absorbent (reusable/disposable), the type of ma-
terial used in reusable absorbents, frequency and place
of change absorbent. In the case of reusable absorbents,
information on the method of washing, drying, pack-
aging, and storing were also collected. Information on
water and sanitation conditions in their households, in-
clude information about access to latrine and place
where the main water source is located. Clinical symp-
toms related to vaginal discharge (its quantity, smell,
colour, and consistency), burning or itching of the geni-
talia, and the presence of ulcers at vulva and labia, vesi-
cles, papules were collected (Additional file 1).
Collection of vaginal samples
A speculum examination of the vagina and cervix was
done by a trained O&G specialist to assess the presence
of cervical erythema, bleeding, inflammation, with or
without discharge, and ulcers at cervix. Vaginal speci-
mens from the posterior vaginal fornix were collected
using four BD BBL swabs (BD, Maryland, USA). The
first swab was used for Gram staining to diagnose BV,
the second swab was used to determine the presence of
Candida, the third swab was used for DNA extraction
for diagnosis of TV by nucleic acid amplification test,
and the fourth swab was stored for future studies. After
labelling, all materials (slides and swabs) were trans-
ported immediately to a local laboratory for preservation
and subsequent diagnosis.
Diagnosis of BV, TV, and Candida infection
BV was diagnosed using Nugent’s laboratory diagnostic
criteria [23] and a Nugent score (NS) between 0 and 10
was generated using the Nugent criteria. A NS of 0–3
was interpreted as normal or negative for BV, a score of
4–10 as intermediate/abnormal for BV or positive for
BV. Presence of TV was identified by nucleic acid amp-
lification tests [24]anddiagnosticPCRwasusedto
ascertain TV infection. Lastly, AlbiQuick™rapid test
(HARDY Diagnostic, CA, USA) was used for identifica-
tion of Candida albicans as per manufacturer’sinstruc-
tions. (More details for diagnosis of the three infections
in Additional file 2).
Data handling and statistical analysis
All data were double-entered into Epi Info 7 software
(Epi info, Centers for Disease Control and Prevention
(CDC), Atlanta, USA) and analyzed using Stata 11.0
(StataCorp, Stata Statistical Software: Release 11. 2011,
StataCorp LP: College Station, Texas, USA). Pearson χ2
tests were used for initial examination of the association
between individual exposures and each of the four of
outcomes of interest (BV, Candida Infection, TV and
having at least one infection). Among the participant-
subgroup reporting use of reusable pads, we explored
whether different washing, drying and storing practices
were associated with the three studied infections. To es-
timate the prevalence rate ratios (PRR) and adjusted
prevalence rate ratios (aPRR), and the associated 95%
confidence intervals (CIs) for factors in relation to each
of the four outcomes we used Poisson survival regres-
sion models.
Potential risk factors for the three infections were ex-
amined using a pre-specified conceptual framework
with three groups of risk factors: socio-demographic
characteristics, MHM practices (related with menstrual
absorbent material and body hygiene), and WASH ac-
cess variables (access to water and sanitation resources
for practicing safe MHM) (Fig. 1). Analysis was done
using a hierarchical approach. Age and education were
retained in all final models as a priori potential con-
founding factors. Other variables were selected for in-
clusion based on stepwise elimination of variables
associated (P< 0.1) in univariate analysis with the out-
comes of interest. Owing to the collinearity of MHM
practices, the effect of each practice on the risk of
infection was evaluated in separate multivariable
models adjusted for age, and education and by the
other variables of interest from univariate model. Po-
tential interacting variables were evaluated by including
an interaction term in the regression model which was
retained if judged statistically significant (P< 0.05) by
likelihood-ratio test.
Results
Of 860 reproductive age women who visited the gynaecol-
ogy OPD of the two hospitals during the study period 558
were enrolled in the study, 106 did not consent to partici-
pate and a further 196 were excluded according to our
criteria (Fig. 2). Among enrolled women50.5% of women
had at least one RTI symptom (data not shown). 29% of
infected women reported that the symptoms motivating
attendance at the clinic were recurrent, but only 30 out of
101 changed their MHM practices and only 17 changed
the type of absorbents (the majority of them using dispos-
able ones when interviewed) as a result of symptoms
(Data not shown). Having abnormal vaginal discharge was
the most frequently reported symptom (36.6%), followed
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by the feeling of burning or itching in the genitalia (27.9%)
and presence of genital sores (8.9%) (data not shown).
62.4% were diagnosed with at least one of the three tested
infections (1.3% had all three infections, 15.8% had two
infections and 45.3% had only one infection). BV was the
most prevalent infection (41%), followed by Candida
(34%) and TV (5.6%) (Table 1).
The median age of participants was 31 (range 18–45),
and 85.3% of women were married and most identified
as Hindu (96.4%). 15.4% of women had no formal
education, 42% had attained 12th grade (12 years of
education) or higher education. Table 1shows the
socioeconomic characteristics of study participants by
the three infections. A significant difference in the edu-
cation status (P< 0.006) between those with Candida
and those without was observed, while other demo-
graphic and socio-economic variables didn’tshowany
significant difference among this group or any of the
other infections.
Univariate analysis showed that certain MHM prac-
tices were associated with certain infections (Table 2).
Women with BV or Candida infections were more likely
to use reusable cloths more frequently than those with-
out these infections (P< 0.014 and < 0.001, respectively).
However, there was no observed difference by type of
reusable material (Table 2). Similarly, women with BV or
Candida infections were more likely to use reusable
cloths versus disposable pads, to change their absorbents
somewhere other than in a toilet facility, and to wash
less frequently during menstruation. Women changing
absorbents less frequently were more likely to have a BV
infection but not a Candida infection. TV infection was
not associated with any of the tested variables, and ac-
cess to sanitation facilities or water at the household
level was not associated with any of the three infections.
We used multivariable analysis to assess the associ-
ation between MHM variables and the three outcomes
of interest whilst controlling for potential confounding
Number of women of reproductive age (18-45 years) visited OG-OPD at Capital
Hospital, Bhubaneswar and Ispat General Hospital, Rourkela, Odisha, India during
the period of study: 860
Refused consent: 106
Excluded from the study: 196
(Diabetes, HIV infection,
antibiotic use or oral
contraceptives use)
Number of women recruited for the study: 558
Questionnaire administered and vaginal samples collected: 558
Uninfected: 210
Without bacterial vaginosis (BV),
Candidiasis,
Trichomonas vaginalis (TV)
Infected: 348
With bacterial vaginosis (BV),
Candidiasis,
Trichomonas vaginalis (TV)
BV: 134 C : 119 BV+C:64 TV+BV: 24 BV+C+TV: 7
Single infections: 253 Co-infections: 95
Diagnosis
Bacterial vaginosis (BV) : Nugent Scoring,
Candidiasis : AlbiQuickTM rapid test
Trichomonas vaginalis (TV) : PCR
Fig. 2 Schematic diagram of recruitment of participants. Schematic diagram of recruitment of participants at Capital Hospital, Bhubaneswar and
Ispat General Hospital, Rourkela, Odisha, India
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 5 of 12
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factors. Reusable cloths were found to strongly associ-
ated with Candida infection (aPRR = 1.54, 95%CI 1.2–
2.0), weakly associated with BV infection (aPRR =1.23,
95%CI 1.0–1.54) and not associated with TV infection
(Table 3). Changing the absorbent in a location other
than in a toilet facility was associated with a higher risk of
BV (aPRR =1.21, 95%CI 1.0–1.48). Women who washed
themselves less often during menstruation had a higher
risk of BV and Candida infection (aPRR =1.25, 95%CI 1.0–
1.55, aPRR =1.34, 95%CI 1.07–1.7, respectively) but not
for TV. In the BV confirmed group, women who chan-
ged their absorbent material more frequently (twice or
more) presented with reduced rates of infections com-
pared with women who changed only once per day
Table 1 Socioeconomic characteristic of women participating in the study according to infection status Data are expressed in no (%) of
women
Exposures With BV
(N= 229)
Without BV
(N= 329)
P-value With Candidiasis
(N= 190)
Without Candidiasis
(N = 368)
P-value With TV
(N= 31)
Without TV
(N= 527)
P-value
Age
18–25 years 63 (27.51) 100 (30.40) 0.758 59 (31.05) 104 (28.26) 0.069 7 (22.58) 156 (29.60) 0.468
26–35 years 89 (38.86) 124 (37.69) 81 (42.63) 132 (35.87) 15 (48.39) 198 (37.57)
36–45 years 77 (33.62) 105 (31.91) 50 (26.32) 132 (35.87) 9 (29.03) 173 (32.83)
Marital status
Never married 23 (10.04) 52 (15.81) 0.146 28 (14.74) 47 (12.77) 0.137 1(3.23) 74 (14.04) 0.177
Married 203(88.65) 273 (82.98) 162 (85.26) 314 (85.33) 30 (96.77) 446 (84.63)
Divorcee& widow 3 (1.31) 4 (1.22) 0 7 (1.90) 0 7 (1.33)
What is your religion
Hindu 222(96.94) 316 (96.05) 0.098 183 (96.32) 355 (96.47) 0.524 31 (100.00) 507 (96.20) 0.543
Muslim 7 (3.06) 7 (2.13) 6 (3.16) 8 (2.17) 0 14 (2.66)
Christian 0 6 (1.82) 1 (0.53) 5 (1.36) 0 6 (1.14)
What is your caste or tribe
Scheduled caste (SC) 41 (18.47) 47 (14.87) 0.250 22 (12.02) 66 (18.59) 0.067 5 (16.13) 83 (16.37) 0.667
Scheduled tribe (ST) 6 (2.70) 10 (3.16) 4 (2.19) 12 (3.38) 0 16 (3.16)
Other backward caste (OBC) 127 (57.21) 168 (53.16) 114 (62.30) 181 (50.99) 16 (51.61) 279 (55.03)
Other Caste 48 (21.62) 91 (28.80) 43 (23.50) 96 (27.04) 10 (32.26) 129 (25.44)
Education
No formal education 40 (17.47) 46 (13.98) 0.266 40 (21.05) 46 (12.50) 0.006 7 (22.58) 79 (14.99) 0.235
5th –10th grade 102 (44.54) 137 (41.64) 85 (44.74) 154 (41.85) 9 (29.03) 230 (43.64)
12th grade or higher 87 (37.99) 146 (44.38) 65 (34.21) 168 (45.65) 15 (48.39) 218 (41.37)
What is your occupation
Employed 30 (13.10) 52 (15.81) 0.351 26 (13.68) 56 (15.22) 0.642 4 (12.90) 78 (14.80) 0.534
Housewife 179 (78.17) 238 (72.34) 141 (74.21) 276 (75.00) 26 (83.87) 391 (74.19)
Student 15 (6.55) 33 (10.03) 20 (10.53) 28 (7.61) 1 (3.23) 47 (8.92)
Other 5 (2.18) 6 (1.82) 3 (1.58) 8 (2.17) 0 11 (2.09)
How many family members in hh
3 or less 47 (20.52) 66 (20.06) 0.712 44 (23.16) 69 (18.75) 0.470 7 (22.58) 106 (20.11) 0.379
4–5 119 (51.97) 162 (49.24) 92 (48.42) 189 (51.36) 12 (38.71) 269 (51.04)
More than 5 63 (27.51) 101 (30.70) 54 (28.42) 110 (29.89) 12 (38.71) 152 (28.84)
Economic status (monthly income)
< 5000.00 30 (13.10) 35 (10.64) 0.427 26 (13.68) 39 (10.60) 0.607 5 (16.13) 60 (11.39) 0.776
5000.00 –10,000 65 (28.38) 114 (34.64) 59 (31.05) 120 (32.61) 11 (35.48) 168 (31.88)
> 10,000.00 103 (44.98) 136 (41.34) 77 (40.53) 162 (44.02) 11 (35.48) 228 (43.26)
Don’t know 31 (13.54) 44 (13.37) 28 (14.74) 47 (12.77) 4 (12.90) 71 (13.47)
P-value determined by Pearson’s chi-square (χ
2
) test. (hh = household)
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(aPRR = 0.75, 95%CI 0.6–0.93, aPRR =0.56, 95%CI 0.4–
0.75, respectively).
In order to explore if these MHM practices and other
exposure factors were also associated with at least one in-
fection, we performed univariate and multivariate analysis
between the same exposure variables and the new infected
outcome group (Table 3). Analysis of the aggregated infec-
tion outcome (one or more of any infection) showed a
similar pattern in the adjusted multivariate analysis with
significant association between at least one infection and
Table 2 Different menstrual hygiene management practices and WASH access variables of women participating in the study
according to infection status
Exposures With BV
(N = 229)
Without BV
(N = 329)
P-value With Candidiasis
(N = 190)
Without Candidiasis
(N = 368)
P-value With TV
(N = 31)
Without TV
(N = 527)
P-value
MHM practices
Absorbent material
Disposable sanitary pads 99 (43.23) 177 (53.80) 0.014 70 (36.84) 206 (55.98) 0.001 12
(38.71)
264 (50.09) 0.218
Reusable cloths 130
(56.77)
152 (46.20) 120 (63.16) 162 (44.02) 19
(61.29)
263 (49.91)
Type of reusable material use
Old cotton fabric 61 (46.92) 84 (55.26) 0.162 62 (51.67) 83 (51.23) 0.943 9 (47.37) 136 (51.71) 0.715
Old silk/nylon fabric 69 (53.08) 68 (44.74) 58 (48.33) 79 (48.77) 10
(52.63)
127 (48.29)
Frequency of change of absorbent
Once a day 69 (30.13) 60 (18.24) 44 (23.16) 85 (23.10) 0.869 7 (22.58) 122 (23.15) 0.653
Twice a day 110
(48.03)
156 (47.42) 0.001 88 (46.32) 178 (48.37) 17
(54.84)
249 (47.25)
Three times a day or more 50 (21.83) 113 (34.35) 58 (30.53) 105 (28.53) 7 (22.58) 156 (29.60)
Place of change of absorbent
In a toilet facility 130
(56.77)
218 (66.26) 0.023 112 (58.95) 236 (64.13) 0.231 20
(64.52)
328 (62.24) 0.799
Outside a toilet facility 99 (43.23) 111 (33.74) 78 (41.05) 132 (35.87) 11
(35.48)
199 (37.76)
What type of washing do you practice during menstruation
Only vaginal wash 45 (19.65) 58 (17.63) 0.545 43 (22.63) 60 (16.30) 0.068 5 (16.13) 98 (18.60) 0.731
Bath of full body 184
(80.35)
271 (82.37) 147 (77.37) 308 (83.70) 26
(83.87)
429 (81.40)
Frequency of washing during menstruation
Twice or more per day 96 (41.92) 166 (50.46) 0.047 77 (40.53) 185 (50.27) 0.029 15
(48.39)
247 (46.87) 0.869
Once a day 133
(58.08)
163 (49.54) 113 (59.47) 183 (49.73) 16
(51.61)
280 (53.13)
WASH Access variables
Do you have a latrine at home?
Yes 186 (81.2) 265(80.6) 0.84 162 (85.3) 289 (78.5) 0.056 25 (80.7) 426
(80.8%)
0.97
No 43 (18.8) 64 (19.4) 28 (14.7) 79 (21.5) 6 (19.3) 101
(19.2%)
Where is the water source located?
In the house 155 (67.7) 211 (64.1) 0.14 122 (64.2) 244 (66.3) 0.74 20 (64.5) 346 (65.7) 0.64
In the yard 34 (14.9) 42 (12.8) 24 (12.6) 52 (14.1) 6 (19.4) 70 (13.3)
At relatives/neighbor house or
yard
2 (3.65) 2 (0.87) 6 (3.2) 8 (2.2) 0 (0) 14 (2.7)
At a public location 38 (16.6) 64 (19.4) 38 (20) 64 (17.4) 5 (16.1) 97 (18.4)
Data are expressed in no (%) of women. P-value determined by Pearson’s chi-square (χ
2
) test
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 7 of 12
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
reusable absorbents (aPRR = 1.35, 95%CI 1.17–1.56),
non-access to a toilet facility for changing the pads (aPRR
= 1.16, 95%CI 1.02–1.31) and lower frequency of
self-washing and cleaning during menstrual cycle (aPRR =
1.21, 95%CI 1.06–1.38). Higher frequency of change of ab-
sorbents was protective of infections (aPRR = 0.72, 95%CI
0.61–0.86).
Use of reusable pads was correlated with other prac-
tices that plausibly influence the risk of RTI which
required further investigation to assess what aspects of
reusable pad use might explain the higher observed risk
among users. In a sub-group of women who reported
using reusable cloths (n= 282), we analyzed the inde-
pendent association of the method of washing, the place
of washing, the place of drying, the method of packing
for storage, and the place of storage of the reusable pads
on different infections (Table 4). Almost all women
washed the reusable menstrual cloths in soap and water
Table 3 Multivariable table with crude and adjusted PRR for each disease model
Risk Factors BV Unadjusted BV Adjusted Candidiasis
Unadjusted
Candididasis
Adjusted
TV
Unadjusted
TV Adjusted Infected
Unadjusted
Infected
Adjusted
PRR (95%CI) PRR(95%CI) PRR (95%CI) PRR (95%CI) PRR(95%CI) PRR (95%CI) PRR(95%CI) PRR(95%CI)
Absorbent material
Disposable 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Reusable 1.28 (1.1–1.6) 1.23(1.0–1.54) 1.67(1.3–2.1) 1.54(1.21–2.0) 1.55(0.8–3.1) 1.78(0.81–3.9) 1.38(1.2–1.6) 1.35 (1.17–1.56)
Frequency of change of absorbent
Once a day 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Twice a day 0.77 (0.6–0.9) 0.75(0.6–0.93) 0.96(0.7–1.3) 0.97(0.7–1.27) 1.17(0.5–2.8) 1.12(0.47–2.7) 0.81 (0.7–0.9) 0.79 (0.60–0.9)
More than twice a
day
0.57 (0.4–0.8) 0.56(0.4–0.75) 1.04(0.8–1.4) 1.08(0.78–1.5) 0.79(0.3–2.2) 0.74(0.26–2.1) 0.74 (0.6–0.9) 0.72 (0.61–0.86)
Place of change absorbent
In a toilet facility 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Outside a toilet
facility
1.26 (1.03–1.53) 1.21(1.0–1.48) 1.15 (0.91–1.45) 1.09(0.8–1.3) 0.91(0.4–1.8) 0.81(0.4–1.64) 1.24(1.19–1.4) 1.16 (1.02–1.31)
Frequency of washing during menstruation
Twice or more per
day
1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0
Once a day 1.22 (1.0–1.5) 1.25(1.0–1.55) 1.29(1.0–1.6) 1.34(1.07–1.7) 0.94(0.5–1.9) 1.09(0.53–2.3) 1.18(1.0–1.4) 1.21(1.06–1.38)
PRR Prevalence rate ratio, CI confidence interval
Table 4 Multivariable table among women who use reusable cloth comparing the PRR of different MHM practices
Risk Factors BV
Unadjusted
BV Adjusted Candidiasis
Unadjusted
Candidiasis
Adjusted
TV Unadjusted TV Adjusted
PRR (95% CI) PRR (95% CI) PRR (95% CI) PRR (95% CI) PRR (95% CI) PRR (95% CI)
Place to wash absorbent
Inside the toilet stall 1.0 1.0 1.0 1.0 1.0 1.0
At the tube well or yard 1.04(0.81–1.34) 1.01 (0.76–1.34) 0.80 (0.61–1.07) 0.86 (0.64–1.16) 1.39 (0.58–3.33) 2.30 (0.80–6.56)
After washing, how did you dry the cloth
Dry it in the Sun/open space 1.0 1.0 1.0 1.0 1.0 1.0
Dry it inside the house 1.15(0.89–1.48) 1.07(0.82–1.39) 1.89(1.41–2.55) 1.78(1.34–2.38) 2.13(0.83–5.47) 1.91(0.68–5.32)
How do you store the cloth for use next time
Wrapped in polythene 1.0 1.0 1.0 1.0 1.0 1.0
Wrapped in another material 1.01(0.76–1.35) 1.04(0.76–1.42) 0.83(0.59–1.16) 0.86(0.62–1.20) 0.33(0.79–1.42) 0.28(0.07–1.10)
Where did you store the cloth for use next time
Within the cupboard in the changing room 1.0 1.0 1.0 1.0 1.0 1.0
In the toilet 1.10(0.85–1.42) 1.11(0.85–1.43) 1.98(1.50–2.61) 1.96(1.49–2.57) 0.63(0.24–1.61) 0.54(0.21–1.38)
PRR Prevalence rate ratio, CI confidence interval
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 8 of 12
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
(data not shown) and there was no difference in risk of
at least one infection by place of washing nor method of
packing for storage of pads. However, significant differ-
ences in Candida infection were associated with the
place of drying and the place of storage of the cloths.
Women who dried their reusable menstrual absorbent
inside their house and women who kept the stored cloth
hidden in the toilet compartment were more likely to
have Candida infections compared with women who
dried them in the sun or open space (aPRR = 1.78,
95%CI 1.34–2.38) or who kept stored within cupboard
in the changing room (aPRR = 1.96, 95%CI 1.49–2.57).
Discussion
Among the women studied, the RTI prevalence was
62.4% with BV the most common infection (41%) and
abnormal vaginal discharge the most commonly re-
ported RTI symptom. These results are slightly higher
than those observed in the District Level Household
Survey - Reproductive & Child Health (DLHS-RCH)
(2002–4) survey which reported a 35.2% prevalence of
RTI/STIs in Odisha or the ones reported in another dis-
trict of Odisha (39.2%) [25]. This difference may be due
to the use of syndromic diagnosis of RTI/STI cases or
because our study was done in an outpatient hospital
setting where attending women have health problems.
However, the frequencies of these infections are similar
to those reported in other Indian studies [26,27]. Infec-
tious causes of vaginal discharge were observed in
51.75% women with BV 26.25%, Candidiasis 15.25%,
Trichomoniasis 12.3%, and mixed infections 5.5% [28].
The current study supports the hypothesis that certain
MHM practices are associated with a higher risk of
lower reproductive tract infections. Women using re-
usable absorbent pads were more likely to have Candida
infection and BV than women using disposable pads.
This effect remains statistically significant for Candida in-
fection, but not for BV, after adjustment for potential con-
founding factors. A similar lack of association with BV
was observed in a previous study by our team [22]and
also in an intervention study conducted in Kenya which
showed that distribution of disposable sanitary pads
among school girls did not reduce the risk of BV [29,30].
The place where women normally change their absorb-
ent material was also associated with BV after adjusting
for confounders (changing inside a toilet facility was found
to be protective for these infections). Similar findings with
BV were observed in our previously hospital based study
[22]. The current study cannot ascertain whether this as-
sociation is causal, but it suggests that having a secure,
comfortable, and hygienic place where women can prac-
tice MHM without stress and with access to water is im-
portant. This finding is supported by another community
level related study that we conducted in Odisha, which
showed that RTI self-reported symptoms were less com-
mon in women using a latrine for defecation versus open
defecation [31].
Interestingly, higher education was found to be protect-
ive only for Candida infection after adjustment for con-
founding (data not shown). Many different studies have
showed that with education, people are better prepared to
prevent disease and use health services effectively [22,32,
33] but the reasons why this factor only affects Candida
infection and not BV or TV are unknown.
More frequent changing of absorbents and regular
body washing during menstruation was associated with a
lower risk of BV which was not observed in our previous
study in the same setting [22]. The difference could be
due to the different diagnostic criteria used for BV in
this study, whilst the earlier study used Amsel’s clinical
criteria, this study used a more sensitive laboratory-
based Nugent’s criteria for diagnosis of BV. We are not
sure about the mechanism how these exposures are
responsible for BV, but it can be presumed that accumu-
lation of blood in the vagina for a prolonged period of
time may influence the vaginal ecosystem. The similar
findings in the Kenyan study that girls given disposable
sanitary pads tend to share them with others, and they
use their remaining pads for a longer duration of time,
adds plausibility to this hypothesis [30]. BV is caused by
an imbalance of vaginal microbiota and the composition
of vaginal microflora can be influenced by several fac-
tors, including ethnicity [34], sexual activity [35], and
host immune response [36], especially the local vaginal
mucosal response. In addition, it has been observed that
the rectal microflora can serve as a reservoir for
colonization of the vaginal ecosystem [37]. Therefore, it
is logical to assume that MHM practices may influence
the risk of vaginal infections. Another recent cross-sec-
tional study in India, showed an association between
lower frequency of genitalia washing associated with
higher self-reported symptoms of itching and pustules in
the genitalia [38].
Unhygienic MHM practices may create abnormally
moist conditions in the vulvo-vaginal area, which may
promote opportunistic infections such as Candida. Once
infected, removal of Candida from the clothes may be
difficult in absence of adequate cleaning and drying. In
this study, whilst both BV and Candida infection were
associated with several unhygienic MHM practices, TV
infection was not. This could be due to the generally low
prevalence of this infection among this population [39]
but may also be due to the fact that TV is primarily trans-
mitted through sexual contact. The intervention study
mentioned above, showed that the distribution of men-
strual cups or sanitary pads was associated with a lower
prevalence of STIs (C. trachomatis and TV, in particular).
The authors hypothesized this may have prevented STIs
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 9 of 12
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
as girls in the study population had previously reported
having sex to obtain money to buy MHM materials [30].
There are several limitations to our study. Firstly, this
was a hospital-based study and socio-economic, educa-
tion, and WASH characteristics risk factors may differ
from the wider population. Only women attending the
Obstetrics and Gynecology departments consented to
participate in the study, and to provide vaginal swabs,
such that our findings may not be representative of
either the wider population attending other sections of
the hospital and, again, limiting the generalizability of
our findings to the wider population. Secondly, this is a
cross-sectional observational study and so we cannot
infer causality based on the observed associations be-
tween MHM practices and health outcomes. Although
we adjusted for a range of potential confounders, it is
likely that there is residual confounding in our results.
Furthermore, we did not collect data on, nor therefore
adjust for, other possibly important factors, such as sex-
ual practices or other infections. The Candida culture
was able to detect only Candida albicans but no
non-albican species. There is a possibility that other
forms of Candida were not detected.
Despite these limitations, this is the first study, to our
knowledge, to collect detailed information on individual
MHM practices linked to individual laboratory confirmed
lower RTI. The strengths of our work include: a large sam-
ple size with power to test associations between MHM prac-
tices and individual RTIs; the use of validated laboratory
methods with external quality controls to diagnose RTI;
and, lastly, the use of exclusively female doctors and inter-
viewers in the study to facilitate participation in the study.
In India, and globally, there has been significant inter-
est in recent years around the issue of safe MHM, and
much discussion around the inclusion of MHM in the
post-2015 sustainable development goals [40]. One inter-
vention that has been advocated is the provision of dis-
posable pads [41] but many limitations have been
identified. Commercially available, disposable pads are
often too expensive for poor communities [42,43] and
the promotion of disposable pads alone is unlikely to
fully address the health and other problems associated
with poor MHM. Beyond the prohibitive cost, miscon-
ceptions exist that disposable pads possess high absorb-
ing capacity leading to reduced frequency of change, and
accumulation of blood over a longer period of time. Fi-
nally, safe disposal of commercial pads is a challenge,
which has not been addressed in many countries [44].
Reusable materials are still used widely and, for them
to be hygienic, safe accompanying hygienic practices are
required. This can be a great challenge in some settings
such as high density urban settlements where private
space for such practices is limited and in low income
rural areas where the water supply is limited.
Whilst this study aimed to assess the risk presented by
certain MHM practices for the health of women, it is
important to recognize that access to safe, affordable
and appropriate MHM is as much an issue of social just-
ice as it one of public health [33,40]. Whilst our study
suggests that certain MHM practices contribute to the
RTI disease burden, the justification for supporting all
girls and women to manage their menstruation with
safety, dignity, and comfort must extend beyond this
public health rationale. Our study does though provide
important insights as to which aspects of MHM might
be considered for prioritization in national and global
policy concerning MHM.
Conclusion
In conclusion, the results of our study demonstrate a
strong association between poor MHM practices and two
lower RTIs: BV and Candida albicans infection. Our find-
ings support global calls for a dual focus on the provision
of appropriate absorbent materials as well as ensuring that
environmental conditions that enable associated hygiene
including washing and drying of pads can be practiced
with safety and dignity by women. Future research efforts
in this area should seek to measure whether and, to what
extent, such interventions reduce the risk of RTI through
well-conceived and well-designed intervention studies.
Additional files
Additional file 1: Variable table with Definitions (Table that present all
the variables measured in the study and their definitions). (DOC 62 kb)
Additional file 2: Diagnosis of BV, TV, and Candida infection. Detail
explanation about laboratory methods used to diagnosed the studied
infections [45,46]. (DOCX 12 kb)
Additional file 3: Strobe checklist for Cross-sectional studies (Strobe
checklist requested from reviewers. It is not referred in the text, but it is
added as Additional file 3). (DOC 97 kb)
Abbreviations
aPRR: Adjusted prevalence rate ratios; BV: Bacterial vaginosis; CI: Confidence
interval; FWD: Family Welfare Department; IUD: Intra-uterine devices;
MHM: Menstrual hygiene management; OPD: Out-patient department;
PID: Pelvic inflammatory disease; PRR: Prevalence rate ratios; RTI: Reproductive
tract infection; STI: Sexually transmitted infection; TV: Trichomonas vaginalis;
UTI: Urinary tract infections; VVC: Vulvo-vaginal candidiasis
Acknowledgements
We would like to thank Prof Jane Carlton for providing TV positive isolates.
We would like to express our appreciation for the support from study
participants, and hospital nurses for assisting in this project.
Funding
This work was made possible with UK aid from the Department for
International Development (DFID), as part of the SHARE research
programme, and support from the Water Supply and Sanitation Council
(WSSCC). However, the views expressed do not necessarily reflect DFID’s
official policies or the policies of WSSCC. The funding agencies had no
involvement in study design, data collection, data analysis, and data
interpretation.
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 10 of 12
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Availability of data and materials
The datasets used and/or analyzed during the current study are available
from the corresponding author on reasonable request.
Authors’contributions
PD, BT and PP were involved in conceptualizing the manuscript. BT and PD
designed the study and data collection instruments. PD managed and
coordinated the study. PD, SS, JRM, PS and TS did the data collection and
laboratory work. BP and AN are the gynecologists responsible for
recruitment of cases and collection of vaginal samples at Capital Hospital,
and MB and BB at IGH, Rourkela. BT and PD conducted data analysis. BT and
PD wrote the manuscript. OC reviewed the manuscript critically for
important intellectual content. All authors had intellectual input during the
study period and contributed to redrafting the manuscript.
Ethics approval and consent to participate
The study was approved by the Institutional Review Board of Asian Institute
of Public health (AIPH) [ERC/No: 2013–03], Ispat General Hospital, Rourkela
[Regd No: ECR/369/Inst/OR/2013], and the Ethical Committee of Government
of Odisha [No: 237/SHRMU]. The study was also approved by the Ethics
Committee of the London School of Hygiene and Tropical Medicine [LSHTM
ethics ref.: 6520]. Only those women who provided written informed
consent to participate in the study were included.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in published
maps and institutional affiliations.
Author details
1
Department of Disease Control, London School of Hygiene and Tropical
Medicine, London, UK.
2
School of Life Sciences, AIPH University,
Bhubaneswar, Odisha, India.
3
Department of Obstetrics and Gynaecology,
Capital Hospital, Bhubaneswar, Odisha, India.
4
Department of Obstetrics and
Gynaecology, Ispat General Hospital, Rourkela, Odisha, India.
5
Department of
Epidemiology and Pediatrics, Center for Global Health and Development,
college of Public Health, University of Nebraska Medical Center, Omaha, USA.
Received: 14 November 2017 Accepted: 13 September 2018
References
1. Baisley K, Changalucha J, Weiss HA, Mugeye K, Everett D, Hambleton I, et al.
Bacterial vaginosis in female facility workers in North-Western Tanzania:
prevalence and risk factors. Sex Transm Infect. 2009;85:370–5.
2. Aniebue UU, Aniebue PN, Nwankwo TO. The impact of pre-menarcheal
training on menstrual practices and hygiene of Nigerian school girls. Pan
Afr Med J. 2009;2:9.
3. Marni S, Sahin M, Paloubis L, Truong M, Sinden J. WASH in schools
empowers girls’education: proceedings of the menstrual hygiene
Management in Schools Virtual Conference 2015, United Nations Children’s
fund and Columbia University. In: New York; 2016.
4. Sumpter C, Torondel B. A systematic review of the health and social effects
of menstrual hygiene management. PLoS One. 2013;8:e62004.
5. Hulland KR, Chase RP, Caruso BA, Swain R, Biswal B, Sahoo KC,
Panigrahi P, Dreibelbis R. Sanitation, stress, and life stage: a
systematic data collection study among women in Odisha, India. PLoS
One. 2015;10(11):e0141883.
6. Wasserheit JN, Harris JR, Chakraborty J, Kay BA, Mason KJ. Reproductive tract
infections in a family planning population in rural Bangladesh. Stud Fam
Plan. 1989;20(2):69–80.
7. Bhatti LI, Fikree FF. Health-seeking behavior of Karachi women with
reproductive tract infections. Soc Sci Med. 2002;54(1):105–17.
8. Desai GS, Patel R. Incidence of reproductive tract infections and sexually
transmitted diseases in India: levels and differentials. J Fam Welf. 2011;57:48–60.
9. Mishra S, Dasgupta D, Ray S. 2016. A study on the relationship of
sociocultural characteristics, menstrual hygiene practices and gynaecological
problems among adolescent girls in eastern India. Int J Adolesc Med Health.
2016;29(5):27.
10. Mitchell H. Vaginal discharge - causes, diagnosis, and treatment. BMJ. 2004;
328(7451):1306–8.
11. Nelson DB, Bellamy S, Nachamkin I, Ness RB, Macones GA, Allen-Taylor
L. First trimester bacterial vaginosis, individual microorganism levels,
and risk of second trimester pregnancy loss among urban women.
Fertil Steril. 2007;88(5):1396–403.
12. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al.
Association between bacterial vaginosis and preterm delivery of a low-birth-
weight infant. N Engl J Med. 1995;333(26):1737–42.
13. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. Bacterial
vaginosis is a strong predictor of Neisseria gonorrhoeae and chlamydia
trachomatis infection. Clin Infect Dis. 2003;36(5):663–8.
14. Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, Rice P, Richter
HE. A cluster analysis of bacterial vaginosis—associated microflora and
pelvic inflammatory disease. Am J Epidemiol. 2005;162(6):585–90.
15. Hillier SL, Kiviat NB, Hawes SE, Hasselquist MB, Hanssen PW, Eschenbach DA,
Holmes KK. Role of bacterial vaginosis associated microorganisms in
endometritis. Am J Obstet Gynecol. 1996;175(2):435–41.
16. Sobel JD, Faro S, Force RW, Foxman B, Ledger WJ, Nyirjesy PR, Reed BD,
Summers PR. Vulvovaginal candidiasis: epidemiologic, diagnostic, and
therapeutic considerations. Am J Obstet Gynecol. 1998;178(2):203–11.
17. Sobel JD. Vulvovaginal candidosis. Lancet. 2007;369(9577):1961–71.
18. Fichorova RN. Impact of T. vaginalis infection on innate immune responses
and reproductive outcome. J Reprod Immunol. 2009;83(1–2):185–9.
19. Anderson MR, Klink K, Cohrssen A. Evaluation of vaginal complaints. JAMA.
2004;291(11):1368–79.
20. Bhatia JC, Cleland J. Self-reported symptoms of gynecological morbidity
and their treatment in South India. Stud Fam Plan. 1995;26(4):203–16.
21. Narayan K, Srinivasa D, Pelto P, Veerammal S. Puberty rituals reproductive
knowledge and health of adolescent schoolgirls in South India. Asia Pac
Popul J. 2001;16:225–38.
22. Das P, Baker KK, Dutta A, Swain T, Sahoo S, Das BS, Panda B, Nayak A, Bara
M, Bilung B, Mishra PR, Panigrahi P, Cairncross S, Torondel B. Menstrual
hygiene practices, WASH access and the risk of urogenital infection in
women from Odisha, India. PLoS One. 2015;10(6):e0130777.
23. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis
is improved by a standardized method of gram stain interpretation. J Clin
Microbiol. 1991;29:297–301.
24. Conrad M, Zubacova Z, Dunn AL, Upcroft J, Sullivan AS, Tachezy J, Carlton
JM. Microsatellite polymorphism in the sexually transmitted human
pathogen trichomonas vaginalis indicates a genetically diverse parasite. Mol
Biochem Parasitol. 2011;175(1):30–8.
25. Panda S, Bebarrta S, Parida S, Panigrahi O. Prevalence of RTI/STI among
women of reproductive age group in district Sundergarh. Orissa Indian
Journal of Practicing Doctor. 2007;4(1):1–5.
26. Nagarkar A, Mashkar P. A systematic review on the prevalence and
utilization of health care services for reproductive tract infections/
sexually transmitted infections: evidence from India. Indian J Sex
Transm Dis. 2015;36(1):18–25.
27. Sood S, Mohanty S, Kapil A, Tolosa J, Mittal S. In pouch TV culture for
detection of Trichomonas vaginalis. Indian J Med Res. 2007;125:567–71.
28. Sivaranjini R, Jaisankar TJ, Thappa DM, Kumari R, Chandrasekhar L, Malathi
M, Parija SC, Habeebullah S. Spectrum of vaginal discharge in a tertiary care
setting. Trop Parasitol. 2013;3(2):135–9.
29. Juma J, Nyothach E, Laserson KF, Oduor C, Arita L, Ouma C, Oruko K, Omoto
J, Mason L, Alexander KT, Fields B, Onyango C, Phillips-Howard PA.
Examining the safety of menstrual cups among rural primary school girls in
western Kenya: observational studies nested in a randomised controlled
feasibility study. BMJ Open. 2017;7(4):e015429.
30. Phillips-Howard PA, Nyothach E, Ter Kuile FO, Omoto J, Wang D, Zeh C,
Onyango C, Mason L, Alexander KT, Odhiambo FO, Eleveld A, Mohammed
A, van Eijk AM, Edwards RT, Vulule J, Faragher B, Laserson KF. Menstrual
cups and sanitary pads to reduce school attrition, and sexually transmitted
and reproductive tract infections: a cluster randomised controlled feasibility
study in rural western Kenya. BMJ Open. 2016;6(11):e013229.
31. Baker KK, Padhi B, Torondel B, Das P, Dutta A, Sahoo KC, Das B, Dreibelbis R,
Caruso B, Freeman MC, Sager L. From menarche to menopause: a
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 11 of 12
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
population-based assessment of water, sanitation, and hygiene risk factors
for reproductive tract infection symptoms over life stages in rural girls and
women in India. PLoS One. 2017;12(12):e0188234.
32. Garg R, Goyal S, Gupta S. India moves towards menstrual hygiene:
subsidized sanitary napkins for rural adolescent girls issues and challenges.
Matern Child Health J. 2012;16(4):767–74.
33. Sommer M, Hirsch JS, Nathanson C, Parker RG. Comfortably, safely, and
without shame: defining menstrual hygiene management as a public health
issue. Am J Public Health. 2015;105(7):1302–11.
34. NessRB,KipKE,SoperDE,StammCA,RiceP,RichterHE.Variabilityof
bacterial vaginosis over 6- to 12-month intervals. Sex Transm Dis. 2006;
33(6):381–5.
35. Fethers KA, Fairley CK, Morton A, Hocking JS, Hopkins C, Kennedy LJ, Fehler
G, Bradshaw CS. Early sexual experiences and risk factors for bacterial
vaginosis. J Infect Dis. 2009;200(11):1662–70.
36. Witkin SS, Linhares IM, Giraldo P, Ledger WJ. An altered immunity
hypothesis for the development of symptomatic bacterial vaginosis. Clin
Infect Dis. 2007;44(4):554–7.
37. Aila NAE, Tency I, Claeys G, Verstraelen H, Saerens B, Santiago GLS, Backer
ED, Cools P, Temmerman M, Verhelst R, Vaneechoutte M. Identification and
genotyping of bacteria from paired vaginal and rectal samples from
pregnant women indicates similarity between vaginal and rectal microflora.
BMC Infect Dis. 2009;9:167.
38. Mathiyalagen P, Peramasamy B, Vasudevan K, Basu M, Cherian J, Sundar B. A
descriptive cross-sectional study on menstrual hygiene and perceived
reproductive morbidity among adolescent girls in a union territory, India. J
Family Med Prim Care. 2017;6(2):360.
39. Preethi V, Mandal J, Halder A, Parija SC. Trichomoniasis: An update. Trop
Parasitol. 2011;1(2):73–5.
40. Sommer M, Caruso BA, Sahin M, Calderon T, Cavill S, Mahon T, Phillips-
Howard PA. A time for global action: addressing girls’menstrual hygiene
management needs in schools. PLoS Med. 2016;13(2):e1001962.
41. Montgomery P, Ryus CR, Dolan CS, Dopson S, Scott LM. Sanitary pad
interventions for gir ls' education in Ghana: a pilot study. PLoS One.
2012;7:e48274.
42. Crofts T, Fisher J. Menstrual hygiene in Ugandan schools: an investigation of
low-cost sanitary pads. J Water Sanit Hyg Dev. 2012;2:50–8.
43. Garg R, Goyal S, Gupta S. India moves towards menstrual hygiene:
subsidized sanitary napkins for rural adolescent girls—issues and challenges.
Matern Child Health J. 2012;16(4):767–74.
44. Sommer M, Kjellén M, Pensulo C. Girls' and women's unmet needs for
menstrual hygiene management (MHM): The interactions between MHM
and sanitation systems in low-income countries. J Water Sanit Hyg Dev.
2013;3(3):283–97.
45. Kengne P, Veas F, Vidal N, Rey JL, Cuny G. Trichomonas vagnialis: repeated
DNA target for highly sensitive and specific polymerase chain reaction
diagnosis. Cell Mol Biol. 1994;40(6):819–31.
46. Simpson P, Higgins G, Qiao M, Waddell R, Kok T. Real-time PCRs for
detection of trichomonas vaginalis b-tubulin and 18S rRNA genes in female
genital specimens. J Med Microbiol. 2007;56:772–7.
Torondel et al. BMC Infectious Diseases (2018) 18:473 Page 12 of 12
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