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Female Circumcision and HIV Infection in Tanzania: for Better or for Worse?

Authors:
Rebecca Stallings at Missouri State University
Rebecca Stallings
Statisticus Consultoris
Statisticus Consultoris
Statisticus Consultoris
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Emilian Karugendo
Emilian Karugendo
Emilian Karugendo
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Female Circumcision and
HIV Infection in Tanzania:
for Better or for Worse?
Rebecca Y. Stallings,
χ
2
Statisticus Consultoris, USA and
Emilian Karugendo,
National Bureau of Statistics,
Tanzania
Data Source
This analysis and its findings are
derived from the 2003-04 Tanzania
HIV/AIDS Indicator Survey (the THIS),
which is currently available for public
use. The first author received
permission from the National Bureau of
Statistics in Tanzania to conduct this
work prior to the official release of the
data set to the public.
Introduction
Female circumcision, also referred to
as female genital cutting (FGC) and
female genital mutilation (FGM), is
most prevalent in Africa. The practice
has been linked to obstetrical and
gynecological problems in addition to
mental and physical trauma that may
result from the more severe forms of
the procedure and has hence been
widely condemned for both ethical and
health reasons by the World Health
Organization and other entities
involved with Human Rights.
(continued)
WHO has defined 4 types of circumcision:
I. Clitoridectomy
II. Excision (cutting of both the clitoris and
part or all of the labia minora)
III. Infibulation (cutting of all external
genitalia with stitching of the vaginal
opening)
IV. Other less radical forms including
pricking and piercing
It has been estimated that 80-85% of female
circumcision is either type I or II.
K.E.Kun proposed 4 hypothetical
mechanisms by which female
circumcision could result in an
elevated risk of HIV infection
(ref. K.E.Kun, 1997, Intl J Gynecology
and Obstetrics)
I.
Female circumcision
Infection/scarring
Partial/complete occlusion of the vagina
Greater risk of inflammation/bleeding during
intercourse
Disruption of the genital epithelium/exposure
to blood/penile abrasions which have been
reported to enhance risk of HIV infection
II.
Female circumcision
Painful/difficult vaginal penetration
Increased practice of anal
intercourse, which has been
shown to enhance the efficiency
of HIV transmission
III.
Female circumcision
Higher incidence of obstructed
labor and tearing
Hemorrhage
Higher risk of blood transfusion;
blood supply may not be optimally
screened for HIV
IV.
Use of unsterilized instruments to
perform the female circumcision
procedure
Exposure to blood contaminated by
the virus
(continued)
While WHO and the International Federation
of Gynecology and Obstetrics publicly
postulated that female circumcision might be
a risk factor for HIV infection as long ago as
1992, very little research has been published
to date examining this relationship.
In light of the alarming spread of HIV among
females in a number of African countries
where female circumcision continues to be
practiced, the dearth of work on this question
is somewhat perplexing.
Prior Studies
3 published studies were identified which
looked at the association between female
circumcision and HIV infection;
All 3 studies were conducted in the
Kilimanjaro region of Tanzania
•S.E.Msuya et al, 2002, Tropical Medicine
and Intl Health
0.64 [95% CI = 0.26<RR<1.57]; N=379
•S.H.Kapiga et al, 2002, JAIDS
1.29 [95% CI =0.88<RR<1.90];N=312
•E.Klouman et al, 2005, Tropical Medicine
and Intl Health
1.19 [95% CI=0.45<RR<3.16];N=392
Tanzania HIV/AIDS Indicator Survey
• All protocols were reviewed and given ethical
clearance by the National Institute for Medical
Research (NIMR)
• A nationally representative probability sample
of households was selected, excluding
Zanzibar, which had recently been similarly
surveyed
• Data collection took place from December
2003-March 2004 and was conducted by
trained interviewers, all of whom were nurses
from the Ministry of Health
(continued)
• Participants aged 15-49 were
interviewed and asked to give informed
consent for the collection of capillary
blood by finger-prick for HIV testing
• All participants were offered free VCT at
their closest center regardless of their
consent
• For participants consenting to the
procedure, a set of unique barcoded
labels was used to provide an
anonymous link
(Continued)
• HIV testing was conducted at the
national reference laboratory at
Muhimbili University College of Health
Sciences
• Cleaned questionnaire data was
anonymously linked to results from the
HIV testing using the barcodes after the
destruction of the end pages of the
questionnaires
Response Rates
Households selected: 6901
…interviewed 6499
…response rate 98.5%
Eligible women 7154
…interviewed 6863
…response rate 95.9%
…interview & HIV test result 6061
…response rate for both 84.7%
Distribution of reported female
circumcision
• The highest reported rates of female
circumcision were found in the Northern
regions of Tanzania bordering Kenya, and in
the regions directly south of those, ranging
from 20% in Iringa to 73% in Manyara. These
adjacent regions hence form a central belt
from North to South.
• Other than in the capital city of Dar es
Salaam (7%), the rate did not exceed 3%
elsewhere in the country
• Ethnicity was not collected but may explain
the regional clustering wrt female
circumcision rates.
Age at time of circumcison, type of
procedure, and practitioner
• Age at time of circumcision, type of procedure,
and practitioner were not collected in the 2003-
04 THIS, but were included in the 1996 DHS
• 74% of women in 1996 who self-reported
having been circumcised said that the
procedure was performed by a “circumcision
practitioner” (91% in Lake zone)
• Doctors or trained nurses/midwives were most
frequently reported by women in the Northern
Highlands (6.9%)
• The next 2 slides show distributions of age and
type by zone
Age at circumcision by zone
0
10
20
30
40
50
60
70
0-5 yrs 6-10 yrs 11-15 yrs 16+ yrs miss/dk
Coastal N Highlands Lake Central S Highlands
Type of procedure by zone
0
10
20
30
40
50
60
70
80
90
clitoridectomy
excision
infibulation
Coastal N Highlands Lake Central S Highlands
Distribution of female HIV infection
• HIV infection among women aged 15-44
ranged from 2.0-15.2% by region
• Among the 10 (of 21) regions with the highest
reported female circumcision rates (>=20%),
only 4 were among the 10 regions with the
highest female HIV infection rates
• The regions with female HIV infection rates
>10% were Mbeya, Iringa, Dar es Salaam,
and Pwani
Potential confounders available and
examined
Demographic characteristics
•Region
• Household wealth index
•Age
• Educational attainment
• Occupation
• Time in current residence
• Religion
(continued)
Marriage and sexual activity
• Age at sexual debut
• Age when began cohabiting
• Currently married or living with partner
• Number of wives of husband/partner
• Lifetime sex partners
• Sex partners in last 12 months
• Use of alcohol during recent sexual liasons
• Ability to say “no” to having sex with recent
partners
(continued)
Symptoms of sexually transmitted
diseases
• Genital sore or ulcer in last 12 months
• Bad smelling abnormal discharge in last
12 months
Potential exposure to contaminated blood
• Any injection in last 12 months
• Any blood transfusion in last 12 months
Methods
•The χ
2
test of association was used to
examine the bivariate relationships between
potential HIV risk factors with both
circumcision and HIV serostatus
• Logistic regression was used to reduce the
model to those factors remaining statistically
significantly associated with HIV serostatus
and to adjust circumcision status for those
factors
• All analyses were performed using the latest
version of the Statistical Analysis System
(SAS)
Results
The crude relative risk of HIV
infection among women reporting
to have been circumcised versus
not circumcised was
0.51 [95% CI =0.38<RR<0.70]
The power (1 – ß) to detect this
difference is 99%
Logistic Regression Models
• Each variable that was statistically significant in the
simple bivariate analyses was added to a separate
simple logistic regression model to predict HIV
serostatus, together with circumcision status
• Additional logistic models were run which
combined those variables which remained
significant in their individual models, together with
circumcision status
• Models were further restricted to include only those
women who had ever been sexually active
• A final model was selected in which all variables
remain statistically significant
Final Logistic Regression Model
n=5284 ever sexually active women
(continued on following slides)
0.880.410.60Circumsized
3.771.282.20Genital ulcer
in last 12
mos
UL 95% CILL 95% CIOR estimateEffect
(continued)
UL 95% CILL 95% CIOR estimateEffect
Regional
zone
1.00Central (ref).
2.250.721.27Northern
highlands
2.070.691.19Coastal
1.590.480.87Southern
5.091.632.88Southern
highlands
1.730.560.99Lake
(continued)
UL 95% CILL 95% CIOR estimateEffect
6.152.784.135th
(highest)
4.862.253.314th
2.761.211.833rd
2.050.861.332nd
1.001st
(lowest)
HH wealth
index
quintile
(continued)
UL 95% CILL 95% CIOR estimateEffect
3.250.811.6245-49
4.891.402.6240-44
5.121.562.8235-39
7.202.304.0730-34
4.561.462.5825-29
3.631.172.0620-24
1.0015-19 (ref.)
Age (years)
(continued)
UL 95% CILL 95% CIOR estimateEffect
6.871.763.476-10
4.892.173.265
5.282.233.434
3.591.802.543
3.081.642.252
1.001 (ref.)
Lifetime sex
partners
(continued)
UL 95% CILL 95% CIOR estimateEffect
5.212.003.23In 2+ prior
unions
4.812.653.57In 1 prior
union
2.501.331.82In 2+
union
2.241.041.53Never in
union
1.00In 1st
union (ref.)
Union
status
Discussion
• The surprising and perplexing significant
inverse association between reported female
circumcision and HIV seropositivity remained
highly statistically significant in the final
logistic regression model, despite the
presence of other significant potential
confounders, namely, geographic zone,
household wealth index, woman´s age,
lifetime sex partners, and current/past union
status
• Some additional analyses were undertaken
using those women for whom a male partner
was interviewed and could be linked (n=2305)
Couples analysis (male x female)
UL 95% CILL 95% CIRR estimate
that both
partners are
+ for the
factor
Factor
examined
19.96.911.7Genital
ulcer
9.03.35.4Abnormal
discharge
10.35.07.1Circum-
cised
15.88.511.6HIV
positive
Muslim women are more likely
than other women to be married
to a partner of the same religion
90.5 82 75.2 68.4
0
20
40
60
80
100
Muslim Catholic Protestant None
Percent of women married to partner of
same religion
Relative Risk of HIV infection for the
Female Partner by circumcision status
UL 95% CILL 95% CIRR estimateComparison
made
1.420.660.97Male circ
vs neither
0.960.310.55Both circ
vs neither
0.970.330.56Both circ
vs male
only
Discussion continued
• The couples analysis also suggests a
protective effect, real or not, of female
circumcision
• There are several important risk factors which
were not collected in the 2003-04 THIS which
might be explanatory confounders of this
perplexing conundrum, including ethnic
group, age at time of circumcision and type of
circumcision
• In 6 of the 10 regions with the highest female
circumcision rates, the HIV seroprevalence
among males is <5%, and is <3% in 3 of
them. In such cases, a lower transmission
risk may be an explanatory confounder.
Conclusions
• The surprising and perplexing
significant inverse association between
reported female circumcision and HIV
seropositivity has not been explained by
other variables available and examined
in these analyses
• As no biological mechanism seems
plausible, we conclude that it is due to
irreducible confounding
• Anthropological insights on female
circumcision as practiced in Tanzania
may shed light on this conundrum
Recommendations
• Similar analyses are needed
from other countries to
determine if this association
holds elsewhere.
• It is an understatement to say
that further research is
warranted.
Thank you for your attention !
... Moreover, Langerhans cells occur in the clitoris, the labia and in other parts of both male and female genitals, and no one is talking of removing these in the name of HIV prevention (Dowsett and Couch 2007). Indeed, A lowered risk of HIV infection among [5297] circumcised women has been reported (Stallings and Karugendo 2005). Why weren't trials also undertaken into the alleged HIV-preventive efficacy of female circumcision (FC) to test how randomly allocating women to immediate vs. delayed FC groups could "benefit" women by showing that FC is an effective HIV preventive measure? ...
Critique of African RCTs into Male Circumcision and HIV Sexual Transmission
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Full-text available
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On the basis of three seriously flawed sub-Saharan African rand-omized clinical trials into female-to-male (FTM) sexual transmission of HIV, in 2007 WHO/UNAIDS recommended circumcision (MC) of millions of African men as an HIV preventive measure, despite the trials being compromised by irrational motivated reasoning, inadequate equipoise, selection bias, inadequate blinding, problematic randomization, trials stopped early with exaggerated treat-ment effects, and failure to investigate non-sexual transmission. Several questions remain unanswered. Why were the trials carried out in countries where more intact men were HIV+ than in those where more circumcised men were HIV+? Why were men sampled from specific ethnic subgroups? Why were so many men lost to follow-up? Why did men in the intervention group receive additional counsel-ling on safe sex practices? The absolute reduction in HIV transmission associ-ated with MC was only 1.3 % (without even adjusting for known sources of error bias). Relativereduction was reported as 60 %, but after correction for lead-time bias alone averaged 49 %. In a related Ugandan RCT into male-to-female (MTF) transmission, there was a 61 % relative increase (6 % absolute increase) in HIV infection among female partners of circumcised men, some of whom were not informed that their male partners were HIV+ (also some of the men were not informed by the researchers that they were HIV+). It appears that the number of circumcisions needed to infect a woman (Number Needed to Harm) was 16.7, with one woman becoming infected for every 17 circumcisions performed. As the trial was stopped early for “futility,” the increase in HIV infections was not statistically significant, although clinically significant. In the Kenyan trial, MC was associated with at least four new incident infections. Since MC diverts resources from known preventive measures and increases risk-taking behaviors, any long-term benefit in reducing HIV transmission remains dubious.
View
... As it happens, defenders of FGM in some countries actually do cite such "health benefits" as "a lower risk of vaginal cancer … less nervous anxiety, fewer infections from microbes gathering under the hood of the clitoris, and protection against herpes and genital ulcers" (Svoboda & Darby, 2008). Jarringly, at least one study conducted by Western researchers has shown a link between "female circumcision" and a reduced prevalence of HIV-a result that the authors, both experienced statisticians, characterized as a "significant and perplexing inverse association between reported female circumcision and HIV seropositivity" (Stallings & Karugendo, 2005). Be that as it may, we can take the thought experiment one step further. ...
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In January 2015, Sir James Munby, President of the Family Division, reached a landmark decision about female genital mutilation ("FGM") in the context of British law. Munby argued that the least severe forms of FGM as defined by the World Health Organization constituted "significant harms" in the eyes of the law. Since the most common forms of male circumcision are physically more invasive than the most minor forms of FGM, then, according to Munby, male circumcision must also constitute "significant harm." In order to rescue the legal distinction between these two types of non-therapeutic genital alteration carried out on minors, however, Munby appealed to (among other things) the fact that male circumcision is regarded as a "religious practice" for some groups, whereas FGM is "merely" a "cultural practice," and thus deserving of less legal protection. In this commentary, drawing on the recent work of other scholars, I argue that the supposed distinction between "religious" and "cultural" cannot be used to justify differential legal treatment of male and female forms of non-therapeutic genital alteration, nor can the supposed difference regarding "health benefits" that are sometimes attributed to male circumcision.
View
... Perhaps it is good to indicate how the practice could contribute to the current global agenda of fighting ills such as HIV/AIDS and state of moral decadence (Kang'ethe & Khayundi, 2014). In tandem with male circumcision, the practices are believed to have an impact on behavioural change that is necessary to tame the tide of the HIV/AIDS and sexually transmitted diseases especially in African countries south of Sahara (Ramphele, 2008;Kang'ethe & Khayundi, 2014;Yount & Abraham 2007, Stallings & Karugendo, 2005. Perhaps this is because the rites are supposed to be accompanied by a lot of lessons and counselling. ...
Reconceptualising and Locating the Succinct Niche of the Practice of Female Circumcision Rite in Africa: A Literature Review
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Advisedly and visionary, cultures need to be examined, and re-examined holistically to avoid unwarranted and skewed judgement against them, especially from the outsiders. Regrettably, subjective and dishonest treatment of African cultures especially by the west and some African elites have cost Africans their cultures, almost leading to their demise. It is critical, therefore, that a new dawn is ushered in to effectuate and reclaim cultural revival, cultural renaissance, cultural autonomy and emancipation that will reposition cultures such as female circumcision in their rightful niche. This article aims to reconceptualise and locate the cultural of female circumcision in its rightful niche. The article has used a review of literature methodology. Findings indicate that: the culture of female circumcision has immense social capital that could be used to facilitate behavioural change and therefore address social ills such as HIV/AIDS and moral decadence; It needs to be respected by reconceptualising it a new by referring it as female genital operation or surgery; discard retrogressive terminologies such as FGM/C/ torture etc; needs to be understood from “insider’ lenses as opposed to the “outsider” lenses. The article recommends to the governments of Africa to respect the rite and lift the ban; allow people to enjoy their cultural rights; facilitate the removal of retrogressive issues surrounding the rite such as clinical hazards or mishaps; carry out holistic research on the rite to determine its positive and negative aspects. DOI: 10.5901/mjss.2014.v5n27p1335
View
... Moreover, Langerhans cells occur in the clitoris, the labia and in other parts of both male and female genitals, and no one is talking of removing these in the name of HIV prevention (Dowsett and Couch 2007). Indeed, A lowered risk of HIV infection among [5297] circumcised women has been reported (Stallings and Karugendo 2005). Why weren't trials also undertaken into the alleged HIV-preventive efficacy of female circumcision (FC) to test how randomly allocating women to immediate vs. delayed FC groups could "benefit" women by showing that FC is an effective HIV preventive measure? ...
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Chapter
Full-text available
  • Jun 2013
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View
... Although it is not deemed ethically possible to study female circumcision by means of a RCT, a large Tanzanian study, which controlled for confounding variables, found that this practice reduced HIV transmission. 32 Biologically the explanation for this is probably the same as for male circumcision. ...
View
... 25 Moreover, at least one study by Western scientists has shown a link between "female circumcision" and reduced transmission of HIV -a result that the authors, both experienced statisticians, characterized as a "significant and perplexing inverse association between reported female circumcision and HIV seropositivity." 99 The thought experiment can be taken a step further. With respect to causal plausibility, it is often argued that the biological mechanism through which the foreskin in males becomes a vector for HIV transmission (although the details are somewhat contentious) 101,102 is the presence of Langerhans cells in the inner mucosa of the foreskin. ...
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View
... 72 Indeed, "[a] lowered risk of HIV infection among [5,297] circumcised women" has even been reported. 73 Why weren't trials also undertaken into the alleged HIV-preventive efficacy of female circumcision to test how randomly allocating women to immediate versus delayed female circumcision groups could "benefit" women by showing that female circumcision is an effective HIV preventive measure? ...
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View
Associations between female genital mutilation/cutting and HIV: a review of the evidence
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  • Sep 2019
Apart from its known association with short- and long-term adverse physical, psychological, and sexual sequelae, female genital mutilation/cutting (FGM/C) could be associated with increased susceptibility to HIV. Some experts propose that FGM/C increases risk of genital trauma and bleeding. Given the known protective effect for men of male circumcision against HIV and that, in some communities, male circumcision and FGM/C are thought of as “equivalent” or parallel procedures, there is an obvious need to more accurately determine the effects of FGM/C on HIV infection risk in women. This article reviewed current evidence of associations between FGM/C and HIV, drawing on evidence from peer-reviewed as well as grey literature. All studies evaluated were observational. This review investigated associations between FGM/C and HIV, not a causal relationship, and observational studies therefore sufficed. The final review included 14 studies from several African countries. The strength of the evidence overall was determined to be of low to moderate quality by Department for International Development criteria: conceptual framing, openness and transparency, cogency, appropriateness and rigour, validity, reliability, and cultural sensitivity. Findings were inconsistent: four studies found no association between FGM/C and HIV, six found a negative association, two found a positive association, and two found an indirect association. Many of the studies had significant deficiencies including insufficient statistical power, inadequate adjustment for potential confounders, and measurement of FGM/C status by self-reporting alone. The available evidence did not conclusively demonstrate the anticipated association between FGM/C and HIV. This review revealed the need for stronger study designs and outlines some considerations for future research.
View
Do the Benefits of Male Circumcision Outweigh the Risks? A Critique of the Proposed CDC Guidelines
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The Centers for Disease Control and Prevention (CDC) have announced a set of provisional guidelines concerning male circumcision, in which they suggest that the benefits of the surgery outweigh the risks. I offer a critique of the CDC position. Among other concerns, I suggest that the CDC relies more heavily than is warranted on studies from Sub-Saharan Africa that neither translate well to North American populations nor to circumcisions performed before an age of sexual debut; that it employs an inadequate conception of risk in its benefit vs. risk analysis; that it fails to consider the anatomy and functions of the penile prepuce (i.e., the part of the penis that is removed by circumcision); that it underestimates the adverse consequences associated with circumcision by focusing on short-term surgical complications rather than long-term harms; that it portrays both the risks and benefits of circumcision in a misleading manner, thereby undermining the possibility of obtaining informed consent; that it evinces a superficial and selective analysis of the literature on sexual outcomes associated with circumcision; and that it gives less attention than is desirable to ethical issues surrounding autonomy and bodily integrity. I conclude that circumcision before an age of consent is not an appropriate health-promotion strategy.
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Male and Female Circumcision Associated With Prevalent HIV Infection in Virgins and Adolescents in Kenya, Lesotho, and Tanzania
Article
Remarkable proportions of self-reported virgins and adolescents in eastern and southern Africa are infected with HIV, yet non-sexual routes of transmission have not been systematically investigated in such persons. Many observers in this region have recognized the potential for HIV transmission through unhygienic circumcision procedures. We assessed the relation between male and female circumcision (genital cutting) and prevalent HIV infection in Kenyan, Lesothoan, and Tanzanian virgins and adolescents. We analyzed data from recent cross-sectional national probability sample surveys of adolescents and adults in households, focusing on populations in which circumcision was common and usually occurred in puberty or later. Circumcised male and female virgins were substantially more likely to be HIV infected than uncircumcised virgins (Kenyan females: 3.2% vs. 1.4%, odds ratio [OR] = 2.38; Kenyan males: 1.8% vs. 0%, OR undefined; Lesothoan males: 6.1% vs. 1.9%, OR 3.36; Tanzanian males: 2.9% vs. 1.0%, OR 2.99; weighted mean phi correlation = 0.07, 95% confidence interval, 0.03 to 0.11). Among adolescents, regardless of sexual experience, circumcision was just as strongly associated with prevalent HIV infection. However, uncircumcised adults were more likely to be HIV positive than circumcised adults. Self-reported sexual experience was independently related to HIV infection in adolescent Kenyan females, but was unrelated to HIV infection in adolescent Kenyan, Lesothoan, and Tanzanian males. HIV transmission may occur through circumcision-related blood exposures in eastern and southern Africa.
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