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Trichomonas vaginalis in Sub-Saharan Africa: occurrence and diagnostic approaches for the male partner

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26 www.smltsa.org.za | ISSN 1011 5528
Volume 27 No. 1 | June 2013
Medical Technology SA

Before the turn of the century, the World Health Organisation
(WHO) reported that amongst the set of curable sexually trans-
mitted infections (STI’s), there was an estimated 340 million
new cases annually amongst which, Trichomonas vaginalis was
recognised as the most common, with an overwhelming inci-
dence of approximately 174 million reported cases.[1] In 2010,
it was estimated that 32 million individuals suffering from tri-
chomoniasis were localised to Sub-Saharan Africa.[2]
Developing countries face the challenge of increasing rates
in the transmission of microorganisms causing asymptomatic
STI’s. Influential factors that have led to an increase in STI’s
amongst populations of developing countries have been identi-
fied as a combination of behavioural, socio-demographic and
economic. Inadequate health facilities[3], a lack of education[4],
alcohol and drug abuse, as well as multiple sexual partners[5]
have been recognised as significant contributing factors to the
increasing rate of trichomoniasis.[6] An additional cause behind
the increased rate of STI’s, specifically within South Africa, is
the common phenomenon of migration by men from rural to
urban areas for employment.[7] Male migrant workers have been
shown to have high levels of contact with sex workers, as well
as a greater number of casual sexual partners.[8] Over a three
year period, 50% of the male subjects attending the Steve Biko
Academic Hospital, Johannesburg, for an Assisted Reproduc-
tive Technology programme had semen samples which showed
significant levels of positive bacterial cultures.[9] In a study
which observed the occurrence of sexually transmitted bacteria
amongst 367 black South African men, it was shown that al-
most half of the subjects presented urine samples that displayed
infectious microorganisms.[10] Amongst African populations, T.
vaginalis is one of the top four most common bacteria identi-
fied in both male and female subjects which include; Candida
albicans, Neisseria gonorrhoea and Chlamydia trachomatis.[11]

T. vaginalis is an extracellular flagellated protozoan that can be
found in both the male and female urogenital tracts, whereby
it primarily infects the squamous epithelium. Trichomonal
cytopathogenicity has been recognised as a causative factor
behind nongonococcal urethritis and prostatitis in male sub-
jects.[12] The organism is localised to the genitourinary system
and the pathogen has been found in practically all sites of the
genitourinary systems in both sexes infected with T. vaginalis.[13]
Despite the fact that the clinical implications of trichomoniasis
in sexually active women are well known, the significance of
the pathogen T. vaginalis for the male partner is still relatively
uncertain.[14] Infection in the female is a causative factor behind
a number of conditions which include: pelvic inflammatory dis-
ease, cervicitis, urethritis, vaginitis as well as adverse pregnancy
outcomes and preterm delivery.[15, 16, 17] Bacterial colonisation of
the male genital tract (MGT) can result in a variety of clinical
manifestations such as; painful ejaculation, testicular sensitivity
and urethral discharge.[18] It is furthermore regarded as a con-
tributor of male factor infertility.[19] However, infection with T.
vaginalis complicates the diagnostic and treatment approach as
it presents asymptomatically in male subjects. A study which
isolated females with trichomoniasis and examined the sexual
partner’s urine and semen samples, showed that an overwhelm-
ing 72% of the men also tested positive for T. vaginalis despite
the fact that the majority showed no symptoms of the urethral
pathogens.[20]

A link between trichomoniasis and the subsequent increased
risk for human immunodeficiency virus (HIV) infection has
sparked an increased focus on T. vaginalis.[21] With focus on the
infection and HIV amongst high risk population groups in Sub-
Saharan Africa, a bidirectional relationship has been shown to
exist.[22, 23] Research into the management of urethritis amongst
Malawian men showed that treatment of trichomoniasis with
metronidazole resulted in a decrease in the viral shedding of
HIV ribonucleic acid in semen samples.[24] Concomitant treat-
ment of sexual partners with metronidazole offers an avenue
of decreasing the transmission rate of the STI.[13] Considering
that trichomoniasis is asymptomatic, the need for an efficient
screening method in male partners is crucial in the public health
sector.[25] The efficacy of this approach was demonstrated by a
study in Tanzania, which showed that with rapid and aggressive
STI treatment intervention, a decrease in the transmission rate
of HIV was observed.[26] With Sub-Saharan Africa’s distressing
Peer reviewed 
Trichomonas vaginalis in Sub-Saharan africa: occurrence
and diagnoStic approacheS for the male partner
(BSc, HSc, MSc) |  (BSc, HSc, MSc, MBA, PhD)
Division of Medical Physiology, Faculty of Health Sciences, Stellenbosch University, Tygerberg, South Africa
Corresponding author: Margot Flint | email: mf@sun.ac.za | +(27) 72 122 2111

The article aims to focus on trichomoniasis as to highlight the prevalence of this sexually transmitted infection (STI) within Sub-
Saharan Africa, and to introduce an alternative means of diagnosing the infection. Globally, trichomoniasis is the STI with the
highest burden in resource limited countries such as those in Sub-Saharan Africa; however, it is also the most common curable
condition. With challenges faced particularly in the context of South Africa’s public health sector, the implementation of affordable
and rapid point-of-care diagnostic tests could allow for a more effective strategy in recognising asymptomatic STI’s, where labora-
tory infrastructure is lacking.

Trichomonas vaginalis; trichomoniasis; sexually transmitted infections; human immunodeficiency virus; South Africa.
ISSN 1011 5528 | www.smltsa.org.za 27
Volume 27 No. 1 | June 2013
Medical Technology SA
increase in HIV, the identification and management of STI’s
has been postulated as the most effective means of slowing the
transmission rate.[27]

Over the past 150 years, the most common diagnostic method
employed for the identification of aerobic and microaerophilic
bacterial pathogens present in the MGT remains semen cul-
tures.[28, 29] The classification of semen samples as positive for
specific bacterial species is defined with a culture of >1 x 103
colony forming units/millilitre.[30] Agar plates which have been
utilised in studying bacterial species in semen include; MacCo-
nkey agar, blood agar, chocolate agar and Thayer Martin agar.
[31] Culture media, in particular the Diamonds’ medium deemed
the “gold standard”[13], has been considered as the reference
testing for T. vaginalis.[32] However, shortcomings in the tradi-
tional culture process have been recognised, which has led to
the development of enhanced methods of detecting bacterial
pathogens in the MGT.[29] A variety of techniques have since
been developed, for example: direct fluorescent antibody assay
(DFA), enzyme-linked immunoabsorbent assay (ELISA), nucleic
acid amplification test (NAAT) with polymerase chain reaction
(PCR), dot-immunobinding assay (DIBA) and the agglutination
test (AT).[33] With the application of sensitive molecular assays
amongst a group of asymptomatic men seeking fertility as-
sessment, a study showed an unpredicted high occurrence of
pathogens in the semen samples that were analysed.[34] Based
on past research reports such as the above, it is recognised that
there is a necessity for further investigations into more reliable,
inexpensive and convenient diagnostic approaches.
Diagnostic kits
The increasing focus on the pathogen’s involvement in the trans-
mission of HIV[35] and conditions such as perinatal morbidity
and preterm labour in the female subject[36, 37], led to the devel-
opment of more reliable, inexpensive and convenient diagnostic
tests which include: the InPouch® TV (BioMed Diagnostics), as
well as the immunochromatographic XenoStrip-Tv™ (Xenotope
Diagnostics). Research into the efficacy and sensitivity of the
XenoStrip-Tv™ has promoted the kit as a valuable approach
to identify possible trichomoniasis in settings whereby there
is a lack of resources and a need for “rapid point-of care” for
patients.[38, 39] These commercially available diagnostic kits offer
a minimally invasive manner in which to test for T. vaginalis as
urine can replace a urethral swab as the medium.[40] A study
which investigated the stability of T. vaginalis deoxyribonucleic
acid (DNA) for molecular testing when the urine samples were
exposed to varying time delays, showed that the DNA remained
stable over a period of 3 days when stored at 4°C[41], demon-
strating the relative stability of the DNA of the bacteria.
Molecular techniques
The use of PCR in comparison to cultures has been shown to
be significantly more sensitive as a diagnostic approach.[42] To
circumvent the time- and labour-intensive use of cultures to
diagnose a patient with a specific STI, PCR kits were devised
which utilize DNA hybridisation. The use of NAAT is an ex-
tremely sensitive and effective means of diagnosing infection
on several different clinical specimens.[13] It allows for an ELISA-
like system to detect the amplified plasmid DNA particular to a
pathogen.[43] This diagnostic alternative has been proven to have
a high sensitivity (92.7%) and specificity (88.6%) for detecting
T. vaginalis in urine samples from male subjects.[44] The advanta-
geous element to the use of PCR’s to detect the presence of a
cell is the sensitivity of the test, whereby a single nucleated cell
can be detected from a medium allowing for an efficient and
reliable test for possible pathogens.[45]

Despite a decrease in the incident rate in African populations[46,
47], South Africa still remains a populace with a high incident
rate of STI’s.[35] In resource-poor regions, the absence of labora-
tory diagnostic services furthers the predicament of the negative
impacts of STI’s.[3] It has been noted that the absence of routine
screening of patients for STI’s is a fundamental reason.[48] This
highlights the significant need for a logistical and user-friendly
approach to decrease the rate of STI contamination between
partners[9] which may also circumvent the related complica-
tions such as compromised fertility.[48] Within the South African
context, the predominant racial group of black and coloured
citizens also represent the sector of the population that are con-
strained by financial and other limitations which don’t allow for
easy access to health facilities.[48]

Despite comprehensive global studies on the incidence and
effects of STI’s, South Africa remains a country with a consider-
ably low number of studies and publications, highlighting the
need to urgently address the concern.[9] With the findings that
T. vaginalis facilitates the sexual transmission of HIV, a need
has arisen for a rapid and cost-effective detection method to
circumvent an increase in the infection rate in resource-limited
settings. As the STI is commonly asymptomatic amongst males,
there is a need for a reassessment of the identification of the
pathogen to decrease the transmission rate between partners.

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... Sub-Sahara Africa (SSA) is burdened with a high incidence of parasitic infections, including schistosomiasis, trypanosomiasis, trichomoniasis, and leishmaniasis [1][2][3]. Currently, there is a rapid widespread development of resistance to prescription drugs for these parasitic neglected tropical diseases (pNTDs) [4][5][6][7][8]. The available number of drugs for treatment is exceptionally low and each of these has been under prescription for periods of no less than 30 years [9]. ...
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This paper will review the significance of results obtained by DNA amplification methods performed on clinical materials for the detection of bacterial pathogens. They will be compared with conventional culture, antigen detection or serological methods with respect to speed, sensitivity and specificity. PCR has provided promising results in the identification of Bordetella pertussis, Chlamydia pneumoniae, Legionella pneumophila, Streptococcus pneumoniae, Mycoplasma pneumoniae and the various pathogroups of diarrheagenic Escherichia coli. PCR and LCR have also shown encouraging results when used in the diagnosis of sexually transmitted diseases caused by Chlamydia trachomatis. In patients with Lyme disease, the sensitivity of PCR is still insufficient, when compared to serological methods. Here PCR is an adjunct in the diagnosis and no substitute for clinical judgement and serology. PCR applications for the detection of bacterial pathogens in clinical materials have also proved to be both problematic and challenging. Problems in using the PCR include determining the optimal target selection, quantifying the sample volume necessary for analysis, determining a standard for sample preparation, and optimizing amplification reactions. There are also difficulties with PCR inhibitors present in the clinical material and with monitoring the performance of the technique. PCR results are highly reliable and reproducible between laboratories when standardized reagents and protocols are used. An important step in this direction is the commercial availability of PCR kits. Such kits also simplify the handling of PCR, thus requiring less technical expertise, and allowing broader use for diagnosis. In the near future, additional studies must provide a correlation between PCR results and conventional methods with larger numbers of samples. Moreover, as a final evaluation, PCR detection methods must prove their benefit with respect to clinical management.
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Microorganisms associated with genito-urinary tract infections are often difficult to detect due to limitations associated with culture techniques. We have applied PCR-based detection of clinical isolates to complex sample matrices. Clinical isolates of Chlamydia trachomatis, Escherichia coli, Proteus vulgaris and Pseudomonas aeruginosa were grown, diluted and used to spike human urine and human semen. The urine and semen samples were centrifuged and the bacterial pellet was kept. A lysis buffer containing proteinase K, 8-methoxypsoralen and lauryl alcohol polyether was exposed to UV light to remove the bacterial DNA in the proteinase K, and was added to the bacterial pellet. After digestion, the proteinase K was destroyed and the lysates were subjected to 35 cycles of 16S rDNA amplification using a hot-starts technique and two primer pairs specific for eubacterial 16S rDNA: 8FPL-806R and 515FPL-13B. After amplification, the amplicons were cloned and sequenced to confirm amplification of the bacteria used to spiked the samples. We were able to detect as few as 105 bacteria per ml of urine or semen. Thirty unspiked semen samples were tested by PCR, and 17 were positive, including 10 samples negative by routine culture. The amplicons were cloned and sequenced for four PCR-positive/culture-negative semen samples: the 16S rDNA sequences obtained were mainly from strict anaerobes, including Prevotella spp. and Peptostrep-tococcus spp. Some 16S rDNA sequences were obtained that did not match any other 16S rDNA sequences available in various nucleic acid databases. Half of 14 unspiked urine sample tested were positive by PCR, including four samples negative by routine culture. Amplicons were cloned and sequenced for one urine sample showing only Lactobacillus spp. by routine culture, and sequences from Bacteroides ureolyticus, Clostridium spp., Corynebacterium urealyticum, Peptostrep-tococcus spp., and Lactobacillus acidophilus were found. These methods have great promise for the rapid detection of viable, but non-culturable bacteria in semen and urine. We are currently applying this technique for the detection of bacteria associated with idiopathic inflammatory conditions.
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Trichomonas vaginalis (T. vaginalis) is the most common nonviral sexually transmitted infection in the world. Despite the coexisting global epidemics of T. vaginalis and HIV, little attention has focused on the emerging evidence that T. vaginalis increases susceptibility to, and potentially transmission of, HIV. We evaluated T. vaginalis infection in the context of a multisite, randomized controlled trial amongst women in South Africa and Zimbabwe, to determine first, if risk of HIV acquisition was increased among women recently infected with T. vaginalis, and second, if risk of T. vaginalis acquisition was increased among women infected with HIV. After controlling for potential confounders, participants infected with T. vaginalis were more likely to test positive for HIV at their following visit, compared to participants uninfected with T. vaginalis (adjusted hazard ratio = 2.05; 95% CI, 1.05-4.02). Similarly, HIV-positive participants were twice as likely to have acquired T. vaginalis infection at the following visit, compared to HIV-negative participants (adjusted hazard ratio = 2.12; 95% CI, 1.35-3.32). We found an increased risk of both HIV acquisition associated with T. vaginalis infection and risk of T. vaginalis acquisition associated with HIV infection. This bidirectional relationship represents a potentially important factor in sustaining the HIV epidemic in populations where T. vaginalis is endemic.
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The temporal relationship between cervical infection with Trichomonas vaginalis (TV) or human papillomavirus (HPV) and the incidence rate of cervical intraepithelial neoplasia grade three (CIN III) was examined in a cohort of 43,016 Norwegian women. From 1980 to 1989, a cervico-vaginal infection from TV and HPV was diagnosed cytologically in 988 and 678 women, respectively. During the 181,240 person-years of observation, 440 cases of CIN III/cervical cancer developed. The age-adjusted incidence rates (IR) of CIN III were 225 per 100,000 person-years among women with no cytologic evidence of infection, 459 among women with TV infection, and 729 among women with HPV infection. A multiple regression model yielded a relative rate (RR) of CIN III of 2.1 (95 percent confidence interval [CI] = 1.3-3.4) among women with TV infection and 3.5 (CI = 1.9-6.6) among women with HPV infection, compared with women with neither infection. As CIN can be misclassified as HPV infection, the entry Pap-smears of 10 women with HPV infection who later developed CIN III were re-examined. Excluding the four discordant cases with the corresponding person-years decreased the RR of CIN III to 2.1 (CI = 0.9-4.8). Our report demonstrates the limitations of studies that rely only on cytologic detection of HPV infection. Nevertheless, the results support the hypothesis that HPV is a causal factor for CIN III lesions, and also display an association between TV infection and cervical neoplasia.
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Although the prostate gland is believed to serve as a parasite reservoir in trichomoniasis in men, and clinical association of trichomonads with prostatitis is common, there has been, to our knowledge, no unequivocal demonstration of Trichomonas vaginalis within the prostate gland. Using established immunoperoxidase procedures, we have positively identified trichomonads in the prostatic urethra, glandular lumina, submucosa, and stroma. Foci of nonspecific acute and chronic inflammation, as well as intraepithelial vacuolization, were associated with the infection. The finding of trichomonads within and beneath glandular epithelium necessitates reevaluation of the traditional view of T vaginalis as a strictly surface-dwelling organism.