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AIDS PATIENT CARE and STDs

Volume 24, Number 8, 2010


ª Mary Ann Liebert, Inc.
DOI: 10.1089/apc.2010.0082

Relations Between Circumcision Status,


Sexually Transmitted Infection History,
and HIV Serostatus Among a National Sample
of Men Who Have Sex with Men in the United States

Kristen Jozkowski, M.S.,1,2 Joshua G. Rosenberger, M.P.H.,1–3 Vanessa Schick, Ph.D.,1,2


Debby Herbenick, Ph.D.,1,2 David S. Novak, M.S.W.,4 and Michael Reece, Ph.D., M.P.H.1,2

Abstract

Circumcision’s potential link to HIV/sexually transmitted infections (STI) has been at the center of recent global
public health debates. However, data related to circumcision and sexual health remain limited, with most
research focused on heterosexual men. This study sought to assess behavioral differences among a large sample
of circumcised and noncircumcised men who have sex with men (MSM) in the United States. Data were
collected from 26,257 U.S. MSM through an online survey. Measures included circumcision status, health in-
dicators, HIV/STI screening and diagnosis, sexual behaviors, and condom use. Bivariate and regression analyses
were conducted to determine differences between HIV/STI status, sexual behaviors, and condom use among
circumcised and noncircumcised men. Circumcision status did not significantly predict HIV testing ( p > 0.05), or
HIV serostatus ( p > 0.05), and there were no significant differences based on circumcision status for most STI
diagnosis [syphilis, gonorrhea, chlamydia, human papilloma virus (HPV)]. Being noncircumcised was predictive
of herpes-2 diagnosis, however, condom use mediated this relationship. These data provide one of the first large
national assessments of circumcision among MSM. While being noncircumcised did not increase the likelihood
of HIV and most STI infections, results indicated that circumcision was associated with higher rates of condom
use, suggesting that those who promote condoms among MSM may need to better understand condom-related
behaviors and attitudes among noncircumcised men to enhance the extent to which they are willing to use
condoms consistently.

Introduction searchers have found that circumcision acts as a protective


factor against some STIs including syphilis and gonorrhea.1,2
Halperin and Baily5 found that men who were circumcised
C ircumcision’s potential link to HIV and sexually
transmitted infection (STI) prevention has been at the
center of recent global public health debates. Approximately
were two to eight times less likely to become infected with
HIV, while Weiss et al.6 found that among men in sub-
one quarter of men worldwide have been circumcised for Saharan Africa, circumcision was associated with a reduction
various reasons including religion, culture, medical reasons in risk of risk of HIV infection.
and/or parental/nonmedical preference,1 yet researchers are However, although some researchers recommend circum-
divided in terms of gauging the potential benefits and risks cision as an HIV prevention strategy,6 others have been less
of recommending the procedure as a mechanism to prevent confident. According to a meta-analysis conducted by Van
HIV and STIs.2-4 Howe,4 of the 29 articles examined, circumcised men were at
Data from several studies have identified a higher preva- increased risk for both HIV acquisition and transmission
lence of HIV among men who were not circumcised compared to uncircumcised men, leading the author to sug-
compared to those who were circumcised.3–6 In addition, re- gest that routine circumcision as a means to prevent HIV

1
Center for Sexual Health Promotion, 2Department of Applied Health Science, Indiana University, Bloomington, Indiana.
3
Division of Adolescent Medicine, Indiana University, Indianapolis, Indiana.
4
Online Buddies, Inc., Cambridge, Massachusetts.

465
466 JOZKOWSKI ET AL.

infection would be unfounded. Similarly, Baily et al.3 reported ceeded to the study questionnaire; most participants took
no difference among circumcised and uncircumcised men approximately 20 min to complete the questionnaire. Com-
with regard to STI histories and Cook and colleagues2 re- pensation for participation included the opportunity to re-
ported mixed findings; in their study uncircumcised men had ceive an electronic coupon valued at $10 that could be
an increased likelihood of syphilis and gonorrhea infection yet redeemed for merchandise from an affiliate of the site from
had a decreased likelihood of genital warts, and no associa- which men were recruited.
tions existed between circumcision status and genital herpes, The recruitment message remained in each individual’s
chlamydia, or nongonococcal urethritis. electronic mailbox for a period of 7 days, after which time any
Among studies that have discussed the efficacy of cir- unopened e-mails were automatically removed. A total of
cumcision in protecting against HIV transmission among 127,489 individuals opened the recruitment email and 43,477
men, most tend to focus on transmission via heterosexual (34.1%) of these men clicked on the link to the study website.
sex.7 Vaginal intercourse may present differences with regard Of those viewing the study information and consent form,
to disease transmission and circumcision status compared to 26,257 (60.4%) consented to and subsequently participated in
anal intercourse due to the differences between vaginal and the study. All study protocols were reviewed and approved
anal mucosa ( J. Sanchez, unpublished data). Limited research by Institutional Review Board at the academic institution of
exists highlighting circumcision as an HIV prevention tech- the authors.
nique among MSM. According to Millett and colleagues,8
there was no relationship among circumcision status and Main outcome measures
self-reports of STIs among a sample of 1,154 black and 1,091 Participants completed items related to sociodemographics,
Latino MSM nor did a meta-analysis of 15 studies, examining circumcision status, health status, health-related behaviors,
circumcision and HIV/STI rates, find any sufficient evidence and sexual behaviors.
to support findings that circumcision provides a protective
effect against HIV/STI infection.9 Sociodemographics. Measures included those related to
While there seems to be inconclusive findings regarding the a participant’s age, sexual orientation, race/ethnicity, and
risks and benefits of circumcision, previous research tends level of education completed. Participants also responded to
to focus on STI status and/or diagnosis. Little research has items related to their relationship and current sexual rela-
examined the differences among circumcised and uncir- tionship status.
cumcised men with respect to sexual behavior. One study
indicated that some behavioral characteristics such as en- Circumcision status. Measures included a single item,
gaging in sexual activity the last time they spent a night away asking men to respond to the question, ‘‘Are you circum-
from home, ever having used a condom, or having used a cised?’’ with one of the following response options: no, yes, or
condom during last intercourse did not differ among cir- no response.
cumcised and uncircumcised men.3 Furthermore, Buchbinder
and colleagues10 found no relationship between unprotected Health status. Measures included those related to physi-
insertive anal intercourse and circumcision, nor was circum- cal and mental quality of life using the four-item Healthy Days
cision associated with a reduction in HIV infection in men Core Module from the Centers for Disease Control and Pre-
who engaged in protective receptive anal sex and unprotected vention (CDC) health-related quality of life measure (HRQOL-
insertive anal sex. 4),12 a widely validated set of survey measures used to assess
While MSM in the United States continue to be dis- a person’s sense of well-being.13–18 In addition, we assessed
proportionally impacted by HIV and STIs, data from large history of participation in testicular self-examinations, pro-
populations of men related to circumcision status and sexual vider-administered (general physical examination) examina-
health behaviors remains limited, inconclusive,1,2,4 and most tions, and HIV and other STI screenings and diagnoses
research available tends to be heterosexually focused.7 The (including HIV, chlamydia, gonorrhea, syphilis, HPV, or her-
current study sought to assess behavioral differences among pes within the past 2 years).
a large, fairly representative sample of circumcised and
noncircumcised MSM in the United States. Sexual behaviors. Participants were asked to indicate
whether or not they had engaged in specific sexual behaviors
Methods with men within the past month, past 3 months, past year,
more than a year ago, or never. Behaviors included receptive
Participant recruitment and data collection
and insertive anal intercourse, and performing and receiving
This study was conducted via a participatory effort with an oral sex. Sexual behaviors were summed across participants.
Internet-based networking site for men who seek sexual or
social interactions with other men. An electronic recruitment Condom behaviors. Participants were asked to indicate
message was sent via e-mail to all individuals residing in the the number of times they used a condom during the past ten
United States who had an account with the website at the time times they engaged in insertive anal intercourse, and the
of the study ( July 2009). The recruitment e-mail provided number of times their partner used a condom during the past
a brief description of the study, its incentives, and included a ten times they engaged in receptive anal intercourse.19 Con-
link to the study website. Previous research has found that dom use variables were created for insertive behaviors, (top,
Internet-based convenience samples are useful tools to better when the participant used a condom during insertive sex) and
understand understudied issues and/or for collecting data receptive behaviors (bottom, when the participants’ partner
from hard-to-reach populations, such as gay men who seek wore a condom during receptive anal intercourse). These
sex partners via the Internet.11 Interested individuals pro- items were treated as a continuous variables from using a
CIRCUMCISION STATUS, STI HISTORY, AND HIV SEROSTATUS 467

condom 0 of 10 times to using a condom 10 of the 10 times including general health, physically unhealthy days (t(24,260) ¼
during the past 10 sexual acts. 0.75), mentally unhealthy days (t(24,374) ¼ 0.098) and activity
limited days (t(24,238) ¼ 0.65) there were no significant differ-
Data analyses ences based on quality of life on any of the measures for those
individuals who were circumcised compared to those who were
The overall sample was narrowed further to include (1)
not ( p > 0.05).
only men who indicated that they currently have at least one
When looking at general assessments of non-disease related
male sexual partner (eliminating 334, 1.3%, participants from
health issues, there were no differences based on circumcision
the sample) and (2) men who responded to the item related to
status for getting a physical exam (w2(25,113) ¼ 0.175, p > 0.05),
circumcision status (removing an additional 764, 2.9%, men
however, groups were significantly different based on cir-
from the sample) . The final sample utilized for these analyses
cumcision status for conducting a testicular self-examination
included 25,159 men. All analyses were conducted using
(w2(25,103) ¼ 41.345, p < 0.001), with noncircumcised men
PAWS version 17.0 (SPSS Inc., Chicago, IL). Descriptive ana-
having been more likely to conduct a testicular self-examination
lyses were conducted to present participant characteristics
in the last month.
including demographics, health behaviors, and sexual be-
haviors. Bivariate analyses including independent sample
Sexual behaviors and condom use
t-tests, and a series of w2 and Mann-Whitney U tests were
calculated to compare demographic differences between men Circumcision status was predictive of men’s engagement in
who had been circumcised and men who had not. In addition, sexual behavior in the past month ( p < 0.001) with circum-
logistic regression analyses with adjusted odds ratios (ad- cised men being more likely to have engaged in sexual be-
justed for age, race, education, and relationship status) were havior (oral and anal sex) within the past month, compared to
conducted to determine if circumcision was a predictor of uncircumcised men (odds ratio [OR] ¼ 0.882, p < 0.001).
HIV/STI testing behaviors and HIV/STI serostatus. Multiple At the bivariate level, there were no differences based on
regression analyses were conducted to determine if circum- circumcision status for condom use during insertive anal sex
cision status was a predictor of condom use behaviors. Baron (t(17,554) ¼ 0.897, p > 0.05) and partner’s use of a condom
and Kenny’s20 suggested methods were used for testing me- during receptive anal sex (t(16,299) ¼ 1.908, p > 0.05).
diators between circumcision and herpes diagnosis. Sobel’s However, when circumcision was entered into a multivariate
test was also used to test for partial mediation. model, controlling for age, race, relationship status, and ed-
ucation level, circumcision status was predictive of men’s
Results condom use behaviors during both insertive and receptive
anal sex ( p < 0.05).
Participant characteristics
Upon further exploration of condom use behaviors, results
Of the 25,159 men who had participated in the current indicate that about one fifth of men used a condom 10 of 10
study, 21,312 (82.1%) indicated that they were circumcised times they engaged in anal sex (insertive, 23.3%; receptive,
whereas 3,847 (14.8%) indicated that they were not circum- 23.9%), %), while one third reported using a condom zero 0 of
cised. 10 times or never using a condom (32.2%; receptive, 33.9%) for
Table 1 provides a summary of the main demographics both insertive and receptive sexual behaviors. Nearly one half
from the entire sample and a comparison of men based on of the men in this sample fell into the range of using a condom
circumcision status. For the entire sample, age was diverse, 1 of 10 times to 9 of 10 times out of the past 10 acts of anal sex
although most participants tended to be 30 years of age or (insertive, 44.5%; receptive, 42.2%).
older (n ¼ 16,905; 69.0%), and circumcision rates were highest
among Caucasian participants (n ¼ 18472; 86.9%), followed STI testing and diagnosis
by African Americans (n ¼ 815; 77.5%) and Latinos (n ¼ 896;
Participant’s history of getting tested for HIV did not sig-
46.2%). Most participants had received some college educa-
nificantly differ based on circumcision status, however, group
tion or higher (87.4%), identified as white (n ¼ 21,295, 81.9%),
differences did exist for STI testing ( p < 0.01) in the last year,
and self-identified as homosexual/gay (n ¼ 21,162; 81.4%). In
with men who were circumcised reporting higher rates of STI
terms of relationship status, a majority of men indicated that
testing. Among those participants who reported having pre-
they were not currently dating anyone (n ¼ 14,625; 56.2%),
viously been diagnosed with any STI or HIV, no differences
although most (n ¼ 20, 900; 83.7%) were currently sexually
existed with the exception of herpes, which was more likely in
active. Comparison of circumcised and noncircumcised men
men who were not circumcised (Table 2).
based on demographic characteristics, indicated that differ-
Logistic regressions were conducted to determine if cir-
ences existed with regard to age, race, education, and rela-
cumcision status was predictive of having been diagnosed
tionship status.
with an STI or HIV in the past 2 years (Table 3), when con-
trolling for age, racial status, education level, and relationship
Circumcision status and general health
status. Results indicate that circumcision status was not pre-
The sample was healthy overall, with the majority of men dictive of HIV/STI diagnoses, exclusive of herpes. Because
indicating their general health to be very good to excellent group differences at the bivariate level existed for STI testing
(71.2%). Overall, based upon the CDC (CDC, 2003) guide- and at the multivariate level for condom use, these variables
lines19 which designate ‘‘good’’ health as under 14 unhealthy were entered in the logistic regression model as potential
days per month, participants reported a relatively low num- mediators using Baron and Kenny’s four-step test of media-
ber of physically, mentally or activity limited days (M ¼ 1.73– tion.21 Both STI testing and condom use met Baron and
4.46, SD ¼ 4.55–7.35). Using the HRQOL health outcomes Kenny’s first three criteria. When STI testing was entered into
468 JOZKOWSKI ET AL.

Table 1. Participant Characteristics and Circumcision Status (n ¼ 25,159)

Circumcision status

Total sample Yes No

Characteristics n % 21,097 3803 p

Age (n ¼ 24,900) <0.001


18–23 3560 14.2 2851 80.1 709 19.9
24–29 4435 17.6 3666 82.7 769 17.3
30–39 5762 22.9 4935 85.6 827 14.4
40–49 6970 27.7 6122 87.8 848 12.2
50–59 3318 13.2 2868 86.4 450 13.6
60 þ 855 3.4 655 76.6 200 23.4
Education (n ¼ 25,104) 0.02
High school or less 2817 11.3 2316 82.2 501 17.8
Some college or associates degree 8485 33.7 7157 84.3 1328 15.7
Bachelors degree 8112 32.2 6976 86.0 1136 14.0
Masters degree 3826 15.2 3245 84.8 581 15.2
Professional 1625 6.5 1374 84.6 251 15.4
Other 239 0.9 199 83.3 40 16.7
Race/ethnicity (n ¼ 25,028) <0.001
Black 1014 4.0 815 80.4 199 19.6
White 20650 82.1 18472 89.5 2178 10.5
Hispanic/Latino 1857 7.4 896 48.2 961 51.8
Asian/pacific islander 729 2.9 426 58.4 303 41.6
Other 777 3.1 599 77.1 178 22.9
Sexual orientation (n ¼ 25,112) 0.087
Homosexual/gay 20542 81.6 17435 84.9 3107 15.1
Bisexual 3927 15.6 3317 84.5 610 15.5
Heterosexual/straight 126 0.5 115 91.3 11 8.7
Relationship status (n ¼ 25,099) <0.001
In a relationship: 5 years 4767 18.9 4153 87.1 614 12.7
In a relationship: 1–5 years 2658 10.6 2252 84.7 406 15.3
In a relationship: 1 year or less 2044 8.1 1672 81.8 352 18.2
Currently dating more than one person 1439 5.7 1209 84.0 230 16.0
Not currently dating anyone 14105 56.1 11892 84.3 2213 15.7
Current sexual relationship (n ¼ 24,999) 0.08
In a monogamous sexual relationship 4643 18.5 3923 84.5 720 15.5
Sexual relationships with more than one person 6025 23.9 5120 85.0 905 15.0
Sexually active but not in a sexual relationship 10232 40.7 8757 85.6 1475 14.4
Not sexually active with another person 4099 16.3 3381 82.5 718 17.5

the model, the relationship from circumcision to herpes findings support claims made by the American Pediatric
was significantly reduced, indicating partial mediation Association and other organizations, that there is not enough
( p < 0.01). substantial evidence to indicate the necessity of recommend-
Additionally, when condom use was entered into the ing neonatal circumcision as a preventive procedure to protect
model, it emerged as a significant predictor of herpes diag- against future STI or HIV infection.18
nosis ( p < 0.05) while circumcision status dropped out of the Unlike previous research, the current study examined
model ( p > 0.05), indicating full mediation. sexual and condom-use behaviors among MSM based on
circumcision status. Most of the men in this sample, regardless
of circumcision status were currently sexually active with a
Discussion
partner, however, circumcised men were more likely to en-
This study provides data of one of the first, large national gage in a higher frequency of sexual behavior (any oral or anal
assessments of associations between circumcision status, sex) in the past month or three months. Furthermore, 65.1% of
sexual behaviors, and STI screening and diagnosis among circumcised men indicated they were currently having sex
MSM in the United States. Study participants were fairly with more than one person, potentially increasing their like-
representative of national rates of the MSM population which lihood for STI exposure.
are weighted toward metropolitan areas. Consistent with In addition, being circumcised was associated with higher
previous studies,3,4 results from this study suggest that cir- rates of never using a condom whereas not being circumcised
cumcision status (being circumcised) shows no protective was associated with higher rates of always using a condom.
factors for most STIs (chlamydia, HPV, syphilis) or HIV, as These findings suggest that those who promote condoms
diagnoses are not significantly different across groups. Such among MSM may need to better understand condom-related
CIRCUMCISION STATUS, STI HISTORY, AND HIV SEROSTATUS 469

Table 2. w2 and Mann-Whitney U

Circumcision status

Yes No

Health variable n % n % w2

21,312 84.7 3847 15.3


Physical examination in last year 15,531 73.0 2784 72.7 0.175
Testicular examination in last month 9412 44.2 1909 49.9 41.345a
STD test in last year 9224 43.5 1575 41.2 7.127b
Positive syphilis diagnosis (2 year) 936 4.4 170 4.5 0.028
Positive gonorrhea diagnosis (2 year) 1009 4.8 193 5.1 0.713
Chlamydia diagnosis (2 year) 886 4.2 165 4.4 0.220
HPV (2 year) 911 4.4 153 4.1 0.555
Herpes (2 year) 878 4.2 187 5.0 4.987a
HIV test 18697 88.3 3330 87.2 3.348
HIV positive 3012 14.3 543 14.3 0.009
Sexual behavior (any oral, or anal sex) in past month 12300 59.1 2094 56.3 10.983b

Circumcision status

Yes No

Condom Use & Health Variables n % n % Mann-Whitney U

Health status 1.081 (ns)


Excellent 5990 28.1 1125 29.2
Very good 9653 45.3 1706 44.3
Good 4830 22.7 873 22.7
Fair 745 3.5 127 3.3
Poor 79 0.4 13 0.3

STD, sexually transmitted disease; HPV, human papilloma virus; ns, not significant.
a
p < 0.01 level; bp < 0.05 level.

behaviors and attitudes among both circumcised and non- never using a condom. In addition, 43.4% of men reported
circumcised men to enhance the extent to which all MSM are using a condom between 1 and 9 times out of the past 10
willing to use condoms consistently. Future research should instances of intercourse, indicating a range of inconsistency in
potentially explore better understanding this discrepancy in condom use behaviors. While this measure of condom use
condom use behavior based on circumcision status. may not be optimal, as it is quantified in such a wide range, it
Similar to findings of condom use among heterosexual does provide an important insight for researchers studying
men,19 for both circumcised and uncircumcised men, condom condom use. Previous research regarding condom use often
use behaviors were inconsistent as just over 20% (23.6%) re- asks participants about condom use in terms of a dichoto-
ported always using a condom for insertive and receptive mous (yes/no) variable. Given that nearly half the sample
behaviors and approximately one third (33.1%) reported reported condom use somewhere within the range of 1 to 9 of

Table 3. Logistic Regression (Control for Race/Ethnicity, Age, and Education)

Outcome variable B SE ExpB Wald statistic

Positive syphilis diagnosis (2 year) 0.001 0.087 1.001 0.000


Positive gonorrhea diagnosis (2 year) 0.077 0.082 0.926 0.868
Chlamydia diagnosis (2 year) 0.05 0.088 0.951 0.325
HPV (2 year) 0.086 0.091 1.090 0.893
Herpes (2 year) 0.186 0.084 0.831 4.875b
HIV test 0.062 0.055 1.064 1.292
HIV positive 0.041 0.052 0.959 0.640
Herpes with condom use mediator 0.168 0.086 0.845 3.791
Condom use (top) 0.196 0.053 0.822 13.485a
Condom use (bottom) 0.133 0.054 0.876 5.974b
Sexual behavior (any oral or anal sex) in past month 0.126 0.037 0.882 12.272a
a
p < 0.01 level.
b
p < 0.05 level.
HPV, human papilloma virus.
470 JOZKOWSKI ET AL.

the previous 10 sexual encounters, measuring condom use for HIV prevention in the United States. PLOS Medicine
with a dichotomous (yes/no) variable may not be appropriate 2007;4:1162–1166.
in all situations especially if the intent is to asses individual 8. Millett G, Ding H, Lauby J, et al. Circumcision status and
HIV/STI risk on a longer term basis (e.g., to assess condom HIV infection among black and Latino men who have sex
use in the last week). In addition, a ‘‘yes’’ response to a with men in 3 US cities. AIDS 2007;46:643–650.
question about whether or not a condom was used in a sexual 9. Millett G, Flores S, Marks G, et al. Circumcision status and
encounter may include individuals who used a condom for risk of HIV and sexually transmitted infections among men
part of the time, but did not use it the entire time penetration who have sex with men: A meta- analysis. JAMA 2008;14:
was occurring. Researchers and clinicians should make efforts 1674–1684.
10. Buchbinder S, Vittinghoff E, Heagert P, et al. Sexual Risk,
to be more accurate in terms of the realization and concep-
nitrite, inhalant use, and lack of circumcision associated with
tualization of the variation in this behavior. More clearly
HIV seoconversions in men who have sex with men. AIDS
worded questions, taking into account contextual and situa-
2005;39:82–89.
tional factors, regarding condom use should be considered in 11. Carballo-Dieguez A, Miner M, Dolezal C, Rosser B, Jacoby S.
order to gain the most accurate information from research Sexual negotiation, HIV-status disclosure, and sexual risk
participants or patients about their condom use behaviors. behavior among Latino men who use the Internet to seek sex
While this study represents an exploration of health be- with other men. Arch Sex Behav 2006;5:473–481.
haviors and STI diagnoses based on circumcision status 12. Centers for Disease Control and Prevention. Measuring
among a large sample of MSM from all states in the United healthy days. Atlanta, GA: Centers for Disease Control and
States, it remains limited by the extent to which the sample is Prevention; 2000.
one of convenience, as challenges remain with establishing 13. Centers for Disease and Control Prevention. Health-related
true nationally representative samples of MSM for research. quality of life among persons with epilepsy—Texas 1998.
Furthermore, data were collected on the Internet and only MMWR 2001;50:24–26.
from members of a single Internet-based site, yet this method 14. Centers for Disease Control and Prevention. State differ-
of recruitment was purposive and closely resembles national ences in reported Healthy Days among adults—United
representations of MSM in the United States. States, 1993–1996. MMWR 1998;47:239–244.
In addition, because this study was not specifically de- 15. Centers for Disease Control and Prevention. Community
signed to examine circumcision, future large scale research indicators of health- related quality of life—United States,
should take a more in-depth approach to understanding im- 1993–1997. MMWR 2000;49:281–285.
portant issues associated with circumcision and condom use, 16. Andresen E, Catlin T, Wyrwich K, Jackson-Thompson
including pleasure and satisfaction. J. Retest reliability of surveillance questions on health related
quality of life. J Epidemiol Community Health 2003;57:
339–343.
Author Disclosure Statement
17. Moriarty D, Zack M, Kobau R. The Centers for Disease
No competing financial interests exist. Control and Prevention’s Healthy Days Measures—Popu-
lation tracking of perceived physical and mental health over
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