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OJHAS Vol. 6, Issue
2: (2007 Apr-Jun) |
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Trichomonas
vaginalis infection in human immunodeficiency virus-seropositive
Nigerian women: The public health significance. |
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Chigozie Jesse Uneke, Department
of Medical Microbiology, Faculty of Clinical Medicine, Ebonyi
State University, PMB 053, Abakaliki, Nigeria Moses Nnaemeka Alo, Department of Medical
Laboratory Science, Faculty of Health Sciences and Technology, Ebonyi
State University, PMB 053, Abakaliki, Nigeria. Ogbonnaya Ogbu, Department
of Applied Microbiology, Faculty of Applied and Natural Sciences, Ebonyi State University, PMB
053, Abakaliki, Nigeria. Duhu Clifford Ugwuoru, Department of Medical Microbiology,
Faculty of Clinical Medicine, Ebonyi State University, PMB
053, Abakaliki, Nigeria. |
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Address For Correspondence |
C.J. Uneke, Department
of Medical Microbiology, Faculty of Clinical Medicine, Ebonyi
State University, PMB 053, Abakaliki, Nigeria
E-mail:
unekecj@yahoo.com
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Uneke CJ, Alo MN, Ogbu O, Ugwuoru DC. Trichomonas
vaginalis infection in human immunodeficiency virus-seropositive
Nigerian women: The public health significance
Online J Health Allied Scs. 2007;2:3 |
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Submitted Jan 10, 2007; Accepted:
Nov 6, 2007; Published: Nov 10, 2007 |
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Abstract: |
Evidence from
the biology and epidemiology of Trichomonas
vaginalis suggests that this protozoan parasite may play an important
role in human immunodeficiency virus (HIV) transmission dynamics, especially
where heterosexual behaviour and a high prevalence of HIV obtain. The
prevalence of T. vaginalis was evaluated among HIV-seropositive
Nigerian women, in an anonymous, unlinked, cross-sectional survey. Of
the total of 250 HIV-seropositive women studied using the wet mount
preparations from high vaginal swab (HVS) and urine specimens, the presence
of T. vaginalis was demonstrated in 61(24.4%) of the HVS specimens
and 57(22.8%) of the urine specimens. The highest prevalence of T.
vaginalis infection (32.6%) was recorded among individuals in the
26-30 years age category and the lowest (18.8%) among the age categories
20-25 years and above 40 years. Since the coinfection of T.
vaginalis and HIV has public health implications for HIV prevention
as it confirms the practice of unprotected sex, educational efforts
must be aimed at sexually active persons and high risk groups and are
best focused upon the use of barrier precautions, particularly condom
use.
Key Words:
Trichomonas vaginalis, HIV, Women, Prevalence |
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Trichomonas
vaginalis is a sexually transmitted parasitic protozoan known to
be responsible for an estimated 180 million new infections per year,
making it the most prevalent nonviral sexually transmitted pathogen
worldwide.(1,2) It can also be transmitted to neonates during
passage through an infected birth canal, but the infection is usually
asymptomatic and self limited.(3) Although
T. vaginalis infection is frequently asymptomatic in adults,
it can cause urethritis in men and vaginitis in women. Symptomatic women
with trichomoniasis usually complain of vaginal discharge, vulvovaginal
soreness, and/or irritation. Dysuria and dyspareunia are also common.(1,4) The infection has also been associated with an increase in adverse
outcomes of pregnancy. Complications of trichomonal vaginitis that have
been reported include premature rupture of membranes, premature labour,
low birth weight, and post-abortion or post-hysterectomy infection.(4-6) Trichomoniasis has neither been the focus of intensive study
nor of active control programs in the sub-Saharan Africa, including
Nigeria, and this neglect is likely a function of the relatively mild
nature of the disease.(7)
However available evidence suggests that T. vaginalis may play
a critical and under-recognized role in amplifying human immunodeficiency
virus (HIV) transmission and, in some circumstances, may have
a major impact on the epidemic dynamics of HIV infection and the acquired
immunodeficiency syndrome (AIDS) in the sub-Saharan Africa.(8-10)
The Sub-Saharan Africa remains by far the worst-affected region by the
global HIV/AIDS epidemic, with 25.4 million people living with HIV (Just
under two thirds, i.e. 64% of all people living with HIV).(11)
The HIV/AIDS epidemic is affecting the females most severely in
the sub-Saharan Africa, with women and girls making up almost 57% of
adults living with HIV, largely because heterosexual sex is a dominant
mode of HIV transmission in the region.(11) In Nigeria, the first AIDS
case was reported in 1986, and since then, the epidemic has rapidly
grown and has extended beyond the commonly classified high risk group
and is now common in the general population with the adult prevalence
of 5% in 2003.(12) The life expectancy in Nigeria increased
from 45 years in 1963 to 53 years in 1990 and was estimated to have
dropped to 51 years in year 2002, largely due to the AIDS epidemic.(12) It is well established that when the prevalence of AIDS reaches
1% of the adult population, the epidemic will become difficult to constrain
or reverse unless drastic and effective measures are taken.(13) Nevertheless,
understanding the role of other sexually transmitted diseases (STDs)
including trichomoniasis, in the transmission of HIV, the role of STDs
in progression of HIV disease, and the role of HIV infection in alterations
of natural history, diagnosis, or response to therapy of STDs is critical
to the development of optimal strategies for HIV control.(14)
In many parts of the sub-Saharan Africa including Nigeria, there is
paucity of information on the interrelationships between Trichomoniasis
and HIV infection among women of child-bearing age. In this report,
we present the findings of a hospital-based study on T. vaginalis
infection among Nigerian women with HIV-infection. The public health
significance of results is discussed as it affects the health care delivery
system and the control of HIV infection in Nigeria and other parts of
the sub-Saharan Africa.
Study Area
The study location
was Abakaliki the capital city of Ebonyi State, South-eastern Nigeria.
The Federal Medical Centre (FMC), one of the largest health institutions
and a major referral centre for HIV screening and confirmation in Abakaliki,
was used for the study. Sex trade is a prominent phenomenon in many
parts of the city, particularly the low income areas where many operational
brothels with commercial sex workers (CSWs) are present and usually
receive high patronage from men of uniform services from the police
barrack and the military cantonment both located in the city. Heterosexual
intercourse is the predominant sexual behaviour in the area and the
prevalence of HIV infection among women attending ante-natal clinics
(ANCs) in the area was 4.6%.(15)
Study Population
/Sampling Technique
Female patients who were confirmed HIV-seropositive by western blot
(WB) technique using the BIO-RAD NEW LAV-BLOT I kits (Bio-Rad Novapath
Diagnostic Group US.), at FMC Abakaliki, from January 2003 to December
2004 were considered for the study. Prior to the WB assay, some of the
subjects had a positive HIV test result as determined by HIV Tri Line
Test ELISA kits (Biosystem INC, Austria), at the FMC Abakaliki,
while others tested positive to HIV infection elsewhere and were referred
to the hospital for confirmatory test. Individuals who had indeterminate
WB results and those who declined participation were excluded from the
study. All the patients were at the hospital to seek medical attention.
The study protocol was approved by the Department of Medical Microbiology,
Faculty of Clinical Medicine, Ebonyi State University Abakaliki-Nigeria.
Approval was also obtained from the authorities of the FMC. The approval
was on the agreement that patient anonymity must be maintained, good
laboratory practice/quality control ensured, and that every finding
would be treated with utmost confidentiality and for the purpose of
this research only. All work was performed according to the international
guidelines for human experimentation in clinical research.
The study was thus, an anonymous, unlinked, cross-sectional survey and
following informed consent 250 HIV-seropositive women were enrolled
into the study. High vaginal swab (HVS) and urine samples were obtained
from each woman. Each patient was given a sterile cotton-tipped swab
and instructed to insert the swab into the vagina and to swab the vaginal
wall. A sterile universal specimen container was also given to each
patient for the collection of first-voided urine (about 10ml). Both
HVS and urine samples were analysed for T. vaginalis infection.
The age of each subject was obtained by interview, other socio-demographic
information could not be obtained due to the general reluctance of the
participants to disclose such information mainly for fear of stigmatization.
Laboratory
Analysis
Microscopic examination of wet mount preparations of the HVS and the
urine samples was done as described previously.(16,17) Briefly, each
swab was placed in 1.5 ml of sterile phosphate-buffered saline (PBS),
pH 7.2. The resulting suspension was used to produce a wet mount for
direct microscopic examination. Centrifugation was performed at 37°
C for 5 min at 2,000 rpm, on each urine sample. The sediment was used
to make a smear on a microscope slide, stained with Giemsa at pH 6.8
for 25 minutes and observed under the microscope. Trichomoniasis was
defined as T. vaginalis infection confirmed through direct microscopy.
Statistical
Analysis
Differences in proportion were evaluated using the chi-square test.
Statistical significant was achieved if P
< 0.05.
Of the total of 250 HIV seropositive women studied, laboratory analysis
indicated the presence of T. vaginalis in 61 (24.4%, 95% CI.,
19.1-29.7%) of the HVS specimens and 57(22.8%, 95% CI., 18.0-28.0) of
the urine specimens (table 1). T. vaginalis was found in the
HVS specimen of each individual whose urine sample had the parasite.
T. vaginalis was not found in the urine samples of five women who
had the parasite in their HVS specimen. The highest prevalence of
T. vaginalis infection (32.6%, 95% CI., 19.1-46.1%) was recorded
among individuals in the 26-30 years age category, followed by those
of the 31-35 years age group (29.2%, 95% CI., 18.1-40.3%). The lowest
prevalence of T. vaginalis infection (18.8%) was observed among
the women of age categories 20-25 years (95% CI., 5.3-32.3%) and
above 40 years (95% CI., 7.7-29.9%) as indicated in table 2. Statistically,
no significant difference was observed in the association between
T. vaginalis infection and age (χ2
=4.42, df=4, P<0.05).
Table 1. Comparison of diagnostic
methods for T. vaginalis using HVS and urine specimens among
HIV-infected Nigerian women. |
Specimen |
Number examined |
Number positive |
Percentage positive |
95% Confidence
interval |
HVS |
250 |
61 |
24.4 |
19.1-29.7 |
Urine |
250 |
57 |
22.8 |
18.0-28.0 |
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Table 2. Age-related prevalence
of T. vaginalis infection among HIV-infected Nigerian
women. |
Age (years) |
Number examined |
Number positive |
Percentage positive |
95% Confidence interval |
20-25 |
32 |
6 |
18.8 |
5.3-32.3 |
26-30 |
46 |
15 |
32.6 |
19.1-46.1 |
31-35 |
65 |
19 |
29.2 |
18.1-40.3 |
35-40 |
59 |
12 |
20.3 |
10.0-30.6 |
>40 |
48 |
9 |
18.8 |
7.7-29.9 |
Total |
250 |
61 |
24.4 |
19.1-29.7 |
The findings of this study suggest that in Nigeria where heterosexual behaviour predominates, T. vaginalis infection may be a frequent
occurrence among Nigerian women with HIV infection. The T. vaginalis
infection prevalence of 24.4% observed in this study is comparatively
higher than those recorded among HIV-seropositive women in Kinshasa,
Zaire (1.9%), (8) Congo (18.6%), (18)
and parts of the USA such as Missouri (11.0%) (19), Rhode Island
(12%) (20), and California (17.4%).(21) However, the prevalence
rates of T. vaginalis infection among HIV-infected Ivorian women
(27%)(9) and among HIV-infected women in New Orleans, USA (36%) (22),
were higher than what we observed in this study.
The coinfection of T. vaginalis and HIV has public health implications
for HIV prevention as it confirms the practice of unprotected sex, a
habit common in many settings in the sub-Saharan Africa, including Nigeria.(11,12) Although it has not been unequivocally established whether trichomoniasis is a risk
factor for HIV transmission or just a marker for
high-risk heterosexual activity (8), findings in a recent study from
the Centers for Disease Control and Prevention, Atlanta, USA, indicated that coincubation
of T. vaginalis isolates with acutely HIV-1-infected peripheral
blood mononuclear cells enhanced HIV-1 replication.(23) Two mechanisms
which have identified that could contribute to the epidemiologic association
of trichomoniasis with the sexual transmission of HIV-1 were (i)
T. vaginalis disruption of urogenital epithelial monolayers could
facilitate passage of HIV-1 to underlying layers, and (ii) activation
of local immune cells by T. vaginalis in the presence of infectious
HIV-1 might lead to increased viral replication.(23)
Hence the need for more vigilant efforts in the diagnosis and treatment
of T. vaginalis in women and also in men cannot be overstated,
especially in countries where heterosexual behaviour predominates, and
a high prevalence of HIV obtains, as in the sub-Saharan Africa.
Although the prevalence of T. vaginalis infection observed
in this study may be considered to be relatively high, with the HVS
specimens recording slightly higher rate than the urine specimens, the
possibility of underestimation of the prevalence may not be ruled out.
While a positive wet mount is diagnostic, a negative wet mount does
not necessarily exclude trichomoniasis.(24)
Moreover microscopic examination of wet mount preparations has
a sensitivity of approximately 60%.(25)
The wet mount and rarely the culture method are the techniques
used for routine T. vaginalis diagnosis in most settings in Nigeria
as in other parts of the sub-Saharan Africa. Although the wet mount is
only 35 to 80% sensitive compared with culture (26),
the sensitivity of culture when compared with polymerase chain reaction
(PCR) has been estimated to be 70%.(16)
Such highly sensitive PCR and related techniques are neither routinely
used nor readily available for T. vaginalis in Nigeria and in
other parts of the sub-Saharan Africa. This is because sophisticated
equipment must be available, is costly to purchase and maintain, and
must be located near clean water and a reliable supply of electricity.
The validity of the results obtained by these techniques strongly depends
on the skills of the technicians, and their interpretation requires
skills training and supervision. These conditions are often lacking
in sub-Saharan Africa, at least in district-level hospitals.(27)
The use of suboptimal laboratory methods for routine T. vaginalis
diagnosis could have far-reaching public health implication as regards
HIV transmission dynamics. Substantial under-diagnosis of the infection
is a major consequence and since most patients with T. vaginalis
infection are asymptomatic or mildly symptomatic, they are likely to
continue to remain sexually active in spite of infection. It
is well established that T. vaginalis typically elicits an aggressive
local cellular immune response with inflammation of the vaginal epithelium
and exocervix with evidence of punctate hemorrhages.(7,25) In
the event of HIV infection, greater numbers of both free virus and viral-infected
white blood cells may increase the probability of HIV exposure and transmission
by T. vaginalis-infected women.(21) Therefore, HIV-infected
women who develop trichomoniasis are likely to be an important source
of continuing HIV transmission and characterizing such individuals can
assist in the targeting of prevention efforts.
It is thus suggested that
careful clinical examination and selective use of wet-mount examination
together with wider use of more sensitive tests for subclinical infection,
such as culture or direct immunofluorescent staining of vaginal fluid,
could lead to improved detection and control of T. vaginalis
infection.(26)
In this study, age-related prevalence of T. vaginalis infection
indicated the highest occurrence among the HIV-infected women of 26-35
years old, which is in conformity with the observation made in a
similar study in Los Angeles.(21) The reason for this was unclear in
the present study and besides, there was no significant difference in
the association between T. vaginalis infection and age (P<
0.05), as was also observed in an earlier study in Alabama, USA.(17)
Our inability
to obtain sufficient socio-demographic data from subjects is a major draw back
to this study. Also our study population size may not be an adequate
representation of the general Nigeria population because the study was conducted
in the south-eastern region which is only one of the six geo-political zones in
the country. These limitations may have affected adequate interpretation of the
public health implications of the findings. Further studies incorporating
detailed socio-demographic parameters as well as larger study population size
are advocated.
In conclusion, the need for providing proper counselling and education
on sexual behaviour and genital hygiene besides treatment to control
and prevent these infections is advocated. Since HIV and T. vaginalis
are primarily spread as sexually transmissible diseases, the educational
efforts must be aimed at sexually active persons and high risk groups
and must be explicit regarding the behaviours that lead to the spread
of both HIV and T. vaginalis. A significant number of both boys
and girls become sexually active as teenagers and must be included in
prevention strategies. Given that the level of promiscuity will often
be difficult to modify within a population as is commonly the case in
Nigeria, then educational campaigns are best focused upon the use of
barrier precautions, particularly condom use.
- Rein MF.
Trichomonas vaginalis. In
Principles and Practices of Infectious Diseases, eds Mandell
GL, Bennet JE & Dolin R (eds). Churchill Livingston. New York: 1995. pp. 2493–
2497.
- Petrin D, Dalgaty K, Bhatt
R,Garber G. Clinical and microbiological aspects of Trichomonas
vaginalis. Clin Microbiol Rev. 1998;11:300–317.
- Danesh IS, Stephen JM, Gorbach
J. Neonatal Trichomonas vaginalis
infection. J Emerg Med. 1995;13:51– 54.
- Sobel JD. Vaginitis.
NEJM. 1996;337:1896–1903.
- Coth MF, Pastorek JG, Nugent
RP, et al. Trichomonas vaginalis
associated with low birth weight
and preterm delivery. Sex Transm Dis. 1997;24:353–360.
- Soper DE, Bump RC, Hurt
WG. Bacterial vaginosis and trichomoniasis vaginitis are risk factors
for cuff cellulitis after abdominal hysterectomy. Am J Obstetr
Gynecol. 1990;163:1016–1021.
- Wolner-Hanssen P, Krieger
J, Stevens CE. Clinical manifestations of vaginal trichomoniasis.
JAMA. 1989;261:571-576.
- Laga M, Manoka A, Kivuvu M et al. Non-ulcerative sexually transmitted
diseases as risk factors
for HIV-1 transmission in women: results from a cohort study. AIDS.
1993;7:95-102.
- Ghys PD, Diallo MO, Ettiegne-Traore
V et al. Genital ulcers associated with human immunodeficiency
virus-related immunosuppression in female sex workers in Abidjan, Ivory Coast.
J Infect Dis. 1995;172:1371-1374.
- ter Muelen J, Mgaya HN,
Chang-Claude J et al. Risk factors for HIV infection in gynaecological
inpatients in Dar Es Salaam, Tanzania, 1988-1990. East Afr Med
J. 1992;69:688-692.
- World Health Organization
(WHO). AIDS epidemic update. UNAIDS/WHO; Geneva.
2004.
- Federal Ministry of Health
Nigeria (FMHN). National HIV/AIDS and
Reproductive Health Survey. Abuja. 2003.
- UNAIDS. 2004 Report on
the global AIDS epidemic. UNAIDS;
Geneva. 2004.
- Wasserheit JN.
Epidemiological synergy. Interrelationships between human
immunodeficiency virus infection and other sexually transmitted diseases.
Sex Transm Dis.1992;19:1-77.
- Federal Ministry of Health
Nigeria (FMHN). Technical report on 2003 National HIV/Syphilis Sentinel Survey
among pregnant women attending antenatal
clinics in Nigeria. FMHN; Abuja. 2004.
- Madico G, Quinn TC, Rompalo A
et al. Diagnosis of Trichomonas vaginalis infection
by PCR using vaginal swab samples. J Clin Microbiol. 1998;36:3205-3210.
- Schwebke JR, Morgan SC, Pinson GB.
Validity of self-obtained vaginal specimens for
diagnosis of trichomoniasis. J Clin Microbiol. 1997;35:1618-1619.
- Sutton MY, Sternberg M, Nsuami M
et al. Trichomoniasis in pregnant human immunodeficiency
virus-infected and human immunodeficiency virus-uninfected Congolese
women: prevalence, risk factors, and association with low birth weight.
Am
J Obstetr Gynecol.
1999;181:656-562.
- Bersoff-Matcha SJ, Horgan MM,
Fraser VJ, Mundy LM, Stoner BP. Sexually transmitted disease acquisition among women infected with human immunodeficiency
virus type 1. Journal of Infectious Diseases,
1998;178:1174-1177.
- Cu-Uvin S, Hogan JW, Warren D
et al. Prevalence of lower genital tract infections
among human immunodeficiency virus (HIV)-seropositive and high-risk
HIV- seronegative women. HIV Epidemiology Research Study Group.
Clin
Infect Dis. 1999;29:1145-1150.
- Sorvillo F, Kovacs A, Kerndt P
et al. Risk factors for trichomoniasis among women
with human immunodeficiency virus (HIV) infection at a public clinic
in Los Angeles
County, California: implications for HIV prevention.
Am
J Trop Med Hyg. 1998;58:495-500.
- Niccolai LM, Kopicko JJ, Kassie A
et al. Incidence and predictors of reinfection with Trichomonas vaginalis in HIV-infected women. Sex
Transm Dis. 2000;27:284-288.
- Guenthner PC, Secor WE, Dezzutti CS.
Trichomonas vaginalis-induced epithelial
monolayer disruption and human immunodeficiency virus type 1 (HIV-1)
replication:
implications for the sexual transmission of HIV-1. Infect Immunol.
2005;73:4155-4160.
- Wiese W, Patel SR, Patel SC
et al. A meta-analysis of the Papanicolaou smear and
wet mount for the diagnosis of vaginal trichomoniasis.
Am J Med.
2000;108:301-308.
- Fouts AC, Kraus SJ. Trichomonas vaginalis: reevaluation of
its clinical presentation
and laboratory diagnosis. J Infect Dis.
1980;141:137–143.
- Krieger JN, Tam MR, Stevens
CE et al. Diagnosis of trichomoniasis: comparison of conventional
wet-mount examination with cytologic studies, cultures, and
monoclonal antibody staining of direct specimens. JAMA. 1988;259:1223–1227.
- Rouet F, Ekouevi DK, Inwoley
A et al. Field Evaluation of a Rapid Human
Immunodeficiency Virus (HIV) Serial Serologic Testing Algorithm for
Diagnosis and
Differentiation of HIV Type 1 (HIV-1), HIV-2, and Dual HIV-1– HIV-2
Infections in West
African Pregnant Women. J Clin Microbiol.
2004;42:4147–4153.
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