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The Program Cost and Cost-Effectiveness of Screening Men for Chlamydia to Prevent Pelvic Inflammatory Disease in Women

Gift, Thomas L. PhD*; Gaydos, Charlotte A. PhD; Kent, Charlotte K. PhD; Marrazzo, Jeanne M. MD, MPH§; Rietmeijer, Cornelis A. MD, PhD; Schillinger, Julia A. MD, MSc*; Dunne, Eileen F. MD, MPH*

doi: 10.1097/OLQ.0b013e31818b64ac

Background: Because men transmit Chlamydia trachomatis to women, screening men to prevent pelvic inflammatory disease in women may be a viable strategy. However, the cost-effectiveness of this approach requires careful assessment.

Methods: Data from a demonstration project and longitudinal study that examined screening men for chlamydia were applied to a compartment-based transmission model to estimate the cost-effectiveness of screening men for chlamydia compared with alternative interventions, including expanded screening of women and combining disease investigation specialist–provided partner notification with screening. Cases of pelvic inflammatory disease and quality-adjusted life years lost were the primary outcome measures. A male screening program that screened 1% of men in the population annually was modeled.

Results: A program targeting high-risk men for screening (those with a larger number of partners in the previous year than the general population and a higher chlamydia prevalence) was cost saving compared with using equivalent program dollars to expand screening of lower-risk women. Combining partner notification with male screening was more effective than screening men alone. In sensitivity analyses, the male program was not always cost saving but averaged $10,520 per quality-adjusted life year saved over expanded screening of women.

Conclusions: Screening men can be a cost-effective alternative to screening women, but the men screened must have a relatively high prevalence compared with the women to whom screening would be expanded (under baseline assumptions, the prevalence in screened men was 86% higher than that of screened women). These modeling results suggest that programs targeting venues that have access to high-risk men can be effective tools in chlamydia prevention.

A compartmental transmission model was created using data from a male chlamydia screening study to examine the cost-effectiveness of screening men for chlamydia. Screening high-risk men was a cost-effective alternative to screening lower-risk women.

From the *Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; †Division of Infectious Diseases, Department of Medicine, Johns Hopkins University, Baltimore, Maryland; ‡San Francisco Department of Public Health, San Francisco, California; §Department of Medicine, University of Washington School of Medicine, Seattle, Washington; and ∥Denver Public Health Department, Denver, Colorado.

The authors thank Harrell Chesson, PhD, for many helpful suggestions regarding model construction and critical review of the manuscript.

Correspondence: Thomas L. Gift, PhD, Centers for Disease Control and Prevention, 1600 Clifton Rd. NE, MS E-80, Atlanta, GA 30333. E-mail:

Received for publication May 14, 2008, and accepted August 19, 2008.

CHLAMYDIA IS THE MOST COMMONLY reported disease in the United States, with over 3 million cases estimated to occur annually.1–3 The sequelae of chlamydial infection in women include pelvic inflammatory disease (PID), which in turn can lead to chronic pelvic pain, ectopic pregnancy, and infertility.4 Because chlamydial infection in women is often asymptomatic, and because the sequelae of untreated infection can be serious and costly, numerous organizations recommend annual chlamydia screening of sexually active women 25 years of age or younger (the age group in which chlamydia prevalence is highest).5–7 However, similar recommendations do not generally exist for men. Therefore, most infections identified and treated in men are a result of syndromic management or diagnostic testing of symptomatic men. As with women, asymptomatic infection is common in men.8 However, the sequelae of chlamydial infection in men (primarily epididymitis) are less common and less costly to treat than those in women.8,9

Because men transmit Chlamydia trachomatis to women, screening men to prevent PID in women may be a viable strategy. Men diagnosed with chlamydia can be instructed to refer their partners for treatment (an approach commonly called partner referral), or they can be interviewed by a disease intervention specialist (DIS) who will elicit the names of partners and contact information for them, then inform the partners directly to seek treatment [this is commonly referred to as partner notification (PN)]. Another approach to partner treatment is to make some provision for their partners to receive treatment without visiting a provider (typically referred to as expedited partner therapy).10 Although these interventions can lead to increased treatment in women and treating men for chlamydia can theoretically lead to reduced infection rates in women by reduced transmission, direct evidence that the burden of disease in women falls when men are screened has been lacking.11 This lack of evidence has left STD prevention programs with little guidance to inform approaches to screening men for chlamydia. Mathematical models that have examined the impact of screening men in comparison with screening women have generally shown that screening men is either less cost-effective than screening women11–13 or that it is relatively costly in terms of cost per quality-adjusted life year (QALY) saved.14 Many studies examining the cost-effectiveness of screening men have considered only the relative cost-effectiveness of different male screening approaches, without comparing the cost-effectiveness of screening men with the cost-effectiveness of screening women. Well-constructed transmission models have typically assumed that male screening programs would be broad based and that the men screened would have chlamydia prevalence equal to that of men in the general population. What has not been thoroughly examined is the cost-effectiveness of a relatively small male chlamydia screening program targeted at high-risk men. A review of the literature on the cost-effectiveness of screening men for chlamydia is published in this issue that describes 29 cost and cost-effectiveness studies in more detail, detailing assumptions each study made regarding setting, prevalence, number of partners, and screening strategies considered for analysis.15

To examine the impact on men and their female partners of screening men for chlamydia, a multisite demonstration project and longitudinal study of repeat chlamydial infection was launched in 4 US cities in 2001.16 Over 23,000 men were screened in Baltimore, MD; Denver, CO; San Francisco, CA; and Seattle, WA. As a part of this study, we collected data enabling us to undertake a cost-effectiveness analysis to examine the feasibility and economic and public health value of screening men for chlamydia.

Because screening women for chlamydial infection is the most obvious alternative use of resources that would be used for screening men, we compared the male screening program with an expanded screening program for women.

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Between 2001 and 2003, men in 4 US cities were screened for chlamydia in a variety of venues including correctional institutions, school clinics, community-based organizations, adolescent primary care, drug treatment centers, and street outreach settings. Men provided urine specimens for testing by a ligase chain reaction (LCx, Abbott Labs, Abbott Park, IL), polymerase chain reaction (AMPLICOR, Roche Molecular Systems, Somerville, NJ), or strand displacement amplification (BDProbeTec ET, Becton, Dickinson and Company, Sparks, MD) assay. After a positive test result for C. trachomatis, men were recalled for treatment and interviewed by a DIS, who then attempted to document treatment for female sex partners that the men had had within 60 days of testing. If treatment could not be documented, the DIS sought to locate the female sex partners and to refer them for treatment.16

Research staff at each site collected time-motion data on the amount of labor time involved in conducting screenings in a sampling of venues. Data were collected at adult and juvenile detention facilities, school sites (health clinics and a health fair), community-based organizations, and a drug treatment center. Researchers measured the time necessary for preparing for screening, travel to and from the venue (when relevant), and specimen collection and preparation. Researchers at 2 sites (Baltimore and Denver) also recorded the amount of time associated with PN, which consisted of the time required to notify the sex partners of infected men of their exposure to chlamydia and refer them for treatment.

Additional data used in the cost-effectiveness analysis came from a cohort study that was part of this project and is described in this issue.17 Other data came from the literature. From the cohort study we obtained information on the number of partners in the 60 days before screening, the number of partners in the follow-up period after testing, the number of men testing positive for C. trachomatis, the number treated, and the number reinfected during the follow-up period. A questionnaire administered to female partners provided data on partner treatment rates because of DIS notification and because of other reasons, including being directly notified by her infected male partner because the woman developed symptoms of chlamydial infection, or because the woman tested positive in a screening visit. We used literature values for test sensitivity and specificity, the likelihood of sequelae in cases of untreated chlamydial infection in men and women, and costs for testing, treatment, and sequelae. We also used literature estimates of patient time and travel costs to account for lost productivity costs associated with visits for testing and treatment by the men and their partners. We estimated lost wages by calculating the average wage plus 25% for fringe benefits.18 We used these data to determine the program cost of the intervention, including all costs that were incurred by the program, including testing, treatment, and partner notification.

To facilitate the cost-effectiveness analysis, we also constructed a dynamic compartment-based model to estimate the impact of screening men for chlamydia on their current and future female partners using screening of women alone with partner referral as a baseline, using Berkeley Madonna, version 8.3.9 (Robert I. Macey and George F. Oster, Berkeley, CA) and Microsoft Excel, version 2003 (Microsoft Corporation, Redmond, WA). We used data from the 4-city male screening study for baseline values for the variables, but sought to create a model that would be applicable to a variety of locations that would have circumstances similar to those modeled. We assumed the screening would occur in a hypothetical population of 100,000 persons 15 to 34 years of age, with equal numbers of men and women. Although screening guidelines for women typically extend only to age 25 or 26 years in the absence of other risk factors, some individual programs have guidance calling for screening in women over age 25, and available data suggest that routine screening above age 25 years of age frequently occurs.19 The population was assumed to consist of 2 sexual risk stratifications for each sex, based on the rate of partner change (high and low). As a baseline, we assumed that 35% of women, or 17,500, were screened annually. This intervention is referred to as “women” in the results tables. We modeled a limited, venue-based male screening program that would screen 1% of the men in the population, or 500 annually, as an adjunct to the existing program of screening women (in the tables, this combined approach is denoted “women and men”). Additional intervention alternatives that were modeled included adding PN [for partners of women only (“women with PN”), partners of men only (“women and men, PN for men”), and partners of both sexes (“women and men, PN for both”)], and expanding screening of women in lieu of screening men (“expand women”). Finally, we examined a potential expansion of male screening to 3% of the men in the population annually, holding the number of women screened at 35% (“women and expand men, PN for men”). The model's structure was similar to previously published examples.13,20,21

To estimate the impact of PN, we used study data on the percentage of partners for whom locating information was provided, and of those partners, the percentage that were found and treated as a result of PN. Complete details of the cost-effectiveness model are provided in the Appendix.

We used QALYs lost and cases of PID in women as our primary outcome measures, but also tracked cases of acute chlamydia treated and prevented in men and women for each of the options we considered. We calculated QALYs lost because of chlamydial infection and sequelae using estimates of the likelihood of various sequelae of chlamydial infection and PID and their health utility impact that have been published previously.9,22,23 We used a societal perspective for the dynamic cost-effectiveness model. We included costs for staff, testing, treatment, and travel, including costs for PN and partner treatment, sequelae costs and lost productivity costs for screened men and women and their partners. The time frame for the model was 5 years, and the analytic horizon extended up to 20 years after development of PID to incorporate QALY losses because of PID sequelae (Appendix). Therefore, the costs and outcomes shown in the results tables indicate the cost of conducting the interventions over a 5-year period, and include the lifetime costs associated with cases of chlamydia incurred during that 5-year period for each intervention. When presenting cost-effectiveness results, we considered for exclusion interventions dominated under either strong dominance or extended dominance. Strong dominance was defined as an intervention having higher net societal cost than the next most effective intervention, and extended dominance was defined by an intervention having a higher incremental cost-effectiveness ratio than the next most effective intervention.24

We conducted 1- and 2-way sensitivity analyses on key variables to examine the robustness of our findings and to estimate the impact of our results in settings with different prevalences, screening costs, or screening coverage in the population as a whole and in each risk class. We also performed a multiway sensitivity analysis using Latin hypercube sampling, which is a form of Monte Carlo sampling that is computationally more efficient than a sensitivity analysis that computes every possible combination of variable values.25 We assumed a uniform distribution for all variables sampled. We performed 2 sets of 50 simulations, using societal-perspective costs.

Cases of chlamydia, sequelae, QALYs, and costs that developed in the years after initiation of the male or expanded female screening program were discounted at 3% per year, although this discount rate was also varied in sensitivity analysis. All costs were adjusted to 2006 dollars using the Medical Care component of the consumer price index for all urban consumers.26

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Table 1 shows the parameters and variables used in the cost-effectiveness analysis, their baseline values, and sources. Cost of specimen collection varied by venue. The cost varied because the amount of staff time, number of staff persons involved in specimen collection, and wage cost for involved staff varied. The amount of staff time for specimen collection in opportunistic venues is shown in Table 2, and all costs used in the analysis are shown in Table 3.







The baseline values in Table 1 produced an equilibrium chlamydia prevalence in the model population of 2.9% in women and 2.3% in men before any screening intervention; under the baseline intervention of “women,” the equilibrium prevalence of chlamydia declined to 2.4% in women and 2.1% in men. The men screened under “women and men” had a prescreening prevalence of 5.4%, or 86% higher than that of the women who were screened. Using the test performance parameters in Table 1, the test positivity of the men screened was 6.0%, compared with 3.4% for the women screened.

The discounted program cost of screening men under “women and men” was approximately $55,400 over the 5-year period, or $11,080 per year (calculations not shown). This was approximately equal to the net program cost of screening an additional 510 women per year for the simulated alternative of “expand women.” Complete results for all intervention alternatives are shown in Table 4, ranked in order of increasing effectiveness in terms of preventing lost QALYs (or equivalently, increasing QALYs saved). The order was the same when placing in order the interventions in terms of decreasing cases of PID in women, and the rank order of the interventions would also have been the same if the outcome were chlamydial infections prevented (in either women alone or women and men combined). Table 5 shows the cost-effectiveness results after removing “women with PN” and “women and men,” “PN for both,” which were dominated under extended dominance. We did not remove “expand women,” even though it was strongly dominated, because it is the most obvious alternative use of resources that might be used for male screening. Similarly, we did not remove “women and men,” even though it was dominated via extended dominance by “women and men,” “PN for men” because some programs may not be equipped to offer PN for patients diagnosed with chlamydia, even though it may be cost-effective to do so.





In univariate sensitivity analysis, we first varied the proportion of screened men who were from the high partner change group, which changed the positivity in screened men. “Men and women” saved more discounted QALYs than “expand women” as long as the positivity in the screened men exceeded 4.3%. This corresponded to less than 9% of the screened men coming from the high partner change group (compared with 17% at baseline and 5% in the general population). Although screening men with a positivity of 4.3% was as effective in saving discounted QALYs as expanded screening of women with a positivity of 3.4%, it was more costly. To achieve equivalence in discounted total societal cost with “expand women,” the positivity in screened men would have to be 4.7% (Fig. 1).

Fig. 1

Fig. 1

When varying male test cost, the net societal cost of “women and men” was lower than that of “expand women” unless the male testing cost exceeded $27.50 per male tested. However, male testing cost never exceeded $20,600 per QALY saved over that of “expand women,” which was the incremental cost per QALY when test cost equaled $37.52, the top of the sensitivity analysis range. When the probability of PID in women infected with chlamydia was varied, the net societal cost of “men and women” was lower than that of “expand women” unless the probability of PID in women with chlamydia was less than 8%. However, “women and men” saved more QALYs than “expand women” across the entire range of PID probabilities, costing $210 per QALY saved over that of “expand women” when the probability of PID in women infected with chlamydia was 5%.

For the multiway sensitivity analysis, we varied the variables shown with ranges in Tables 1, 3 simultaneously to compare the cost and QALYs saved of “women and men” with “expand women” (Fig. 2). Positive numbers in the figure indicate that “women and men” was higher in cost or saved more QALYs than “expand Women;” negative numbers indicate the reverse. The average cost difference of the 100 iterations was +$41,300 in cost and +3.93 QALYs saved, indicating that the average incremental cost-effectiveness ratio for “women and men” compared with “expand women” was $10,520 per QALY saved.

Fig. 2

Fig. 2

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The 4-city male chlamydia screening study showed that it is possible to find and screen high-risk men in many venues. Surveillance data and a literature review by Rietmeijer et al. in this issue shows that in a number of settings, principally, detention facilities prevalences are consistently high.3,27 We show that it is possible to screen men in such venues at modest cost per specimen collected. The data collected during PN activities show that PN can be an effective adjunct to screening men, but in the transmission model, most of the reduction in disease in women came from detection and treatment of infection in men, rather than through PN. Most settings lack the resources to undertake PN for partners of patients diagnosed with chlamydia.28 Providing PN for partners of screened men might be more feasible given the relatively small male screening program envisaged by this analysis, but even if PN cannot be provided, our modeling results suggest that screening men for chlamydia can still have a beneficial impact on women.

Screening young women and women with risk factors is an obvious use of chlamydia prevention dollars, because surveillance data and research studies consistently show that these women have the highest prevalence of chlamydia among women.29,30 Less data are published on the prevalence in older women, but what data exist indicate that the prevalence among older women, such as those 30 years of age or older, is much lower than that of younger women.

Screening men for chlamydia is a viable intervention alternative to increasing screening of women if high-risk men (those with high numbers of partners and high chlamydia prevalence compared with the general population of men) can be found; the relative benefit of screening men over screening women from the general population diminishes when the prevalence among screened men declines toward the population average. Similarly, the advantage of screening men diminishes if a group of unscreened women has a chlamydia prevalence that is the same as or even somewhat less than that of the men who are being considered for screening. However, in many instances, men with high chlamydia rates are relatively easily identified–correctional settings are an obvious possibility, and one in which specimens can usually be obtained relatively inexpensively. Another readily accessible population with high chlamydia rates is male military recruits.27,31

The cost advantage of screening high-risk men is impacted by the cost of specimen collection. This suggests that the most advantageous venues for screening high-risk men are those in which men are already receiving a health screening, as they are at jail intake, or in another setting where specimens can be obtained at low cost. Screening men was cost saving compared with expanded screening of women at the baseline because the program cost of the 2 intervention alternatives was equal, and screening men saved more QALYs. The multiway sensitivity analysis suggests that societal-perspective cost savings cannot be assumed to prevail in all instances when screening roughly equivalent numbers of men and women as an add-on to an existing program of screening women. The net societal cost of screening high-risk men averaged about $41,300 over the 5-year period, or $8260 per year, but consistently saved more QALYs than a program slightly expanding screening of women from the general population. The average incremental cost per QALY gained by screening high-risk men was $10,520, which would put it among the most cost-effective preventive interventions recently examined in a systematic review.32

When varying the parameters of the model, the program costs of the 2 interventions will not necessarily be equivalent. The salient finding from the sensitivity analysis is that screening a limited number of high-risk men was found to be consistently more effective in saving QALYs than screening an equivalent number of women from the general population, and that the average cost per QALY of screening the men was in a range typically considered to be cost-effective.

Our findings and the transmission model we used are subject to limitations. First, infection and reinfection were random events controlled for by only 2 factors: population prevalence and rate of partner change. We did not model partnerships explicitly, so treated patients with untreated partners were not more likely to be reinfected than patients whose partners were successfully treated (however, we did control for the likelihood that partners of infected patients were more likely to be infected). Modeling of specific partnerships is not readily accomplished by compartmental models. However, reinfection had no impact on the model that was distinct from an initial infection. Partner treatment did reduce incident infections in the opposite sex generally, but the impact was not modeled by partnership. We did not examine interventions that call for repeat screening of women or men testing positive, although such screening is suggested.6 Second, because individuals in the population were not tracked, we did not account for the possibility that a given partner might be named by more than 1 diagnosed patient; this could have led to an overestimation of the effectiveness of PN. Third, the limitations inherent in any modeling exercise apply to this one, as well: they are simplifications of reality and may not capture important characteristics of transmission. The baseline values for the parameters in Table 1 were selected to be consistent with the literature and to yield an equilibrium prevalence that represents the true prevalence of chlamydia in the population for men and women. The intervention of “women” at baseline yielded postintervention equilibrium chlamydia prevalences in men (2.1%) and women (2.4%) that are close to those found in a nationally representative survey for the same age groups (2.0% in men and 2.5% in women).30

Another population-based model has suggested that screening additional women averts more adverse outcomes of chlamydial infection than screening men.11 However, it assumed population-wide age-based screening of men as an alternative to population-wide age-based screening of women. Our modeling results also show that screening women would likely be more effective than screening men if a broad-based male screening program were undertaken. However, when the prevalence among screened men substantially exceeds that of the additional women who would otherwise be screened, screening the men can be the best approach. In our model, the baseline prevalence of screened men was nearly twice that of women (86% higher). In numerous settings, such a prevalence difference might exist: For example, in California family planning clinics in 2006, the chlamydia positivity was 2.0% for women 30 or older versus 6.4% in women 15 to 24 years (these data are from the Infertility Prevention Program, which targets young, sexually active women under 26 for screening).29 The median chlamydia positivity reported in 2006 among men entering correctional facilities in California was 5.5%.29 If the alternative use of male chlamydia screening funds would go to increase screening among women 30 years of age or older, our findings indicate that screening the men at jail intake would be cost-effective.

In most areas of the US, male screening will likely be an intervention that will only be adopted or implemented to a limited degree. Chlamydia screening rates among young women are low; therefore, screening women will remain the priority.33,34

However, within those limits, targeted screening of high-risk men can play a role in chlamydia prevention.

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        Each person was classified as susceptible (uninfected), exposed (incubating), infected (symptomatically or asymptomatically), or suffering sequelae (PID or epididymitis). The model is depicted in Figure 1. After infection, persons were assumed to progress through an incubation period to either symptomatic or asymptomatic infection. Chlamydial infections were assumed to either resolve spontaneously (if unscreened and asymptomatic) or through infected persons seeking treatment on their own (if unscreened and symptomatic).

        Fig. 3

        Fig. 3

        We modeled a representative population, and categorized people based on sex and rate of sex partner change only (we excluded differences in race and age). The population was closed, with no entry or exit, because of the relatively short time horizon. Estimates for the rate of partner change in the population and the per-partnership rate of chlamydia transmission were taken from the literature. We used data provided by men screened in 4 cities for the rates of partner change among the men screened (ci,j, Table 1), proportion of treated men interviewed by DIS (ηi), proportion of partners in the last 60 days (PNI) elicited by DIS (πi,j), proportion of elicited partners located and notified (f), and return rates for treatment (ri,j). For the equivalent female PN program, we used either the same values as for the men or values from the literature (Table 1). For partner notification, we assumed a 10-day lag between index patient screening and partner notification, assuming the partners were locatable at all.

        TABLE 6

        TABLE 6

        See Table 1 for variable definitions. In the notation below, S = susceptible (uninfected), E = exposed, A = asymptomatically infected, X = symptomatically infected, SQ = sequelae, λ = force of infection, ρ = the sexual mixing coefficient, PN = infected patients treated through PN, SP = infected sex partners, RFA and RFX = recovery from infection if asymptomatic or symptomatic, respectively. In the subscript notation below and in Table 1, i = sex (1,2); j = sexual activity level (1,2 based on low, high); k = sexual activity level of partner (1,2 based on low, high). An accent sign (eg, i') denotes values different from the one under consideration (eg, when i = 1, i' = 2).

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        The expression for RFX is the same as that for RFA, except that dxi is substituted for dai and PNXij is substituted for PNAij. Sequelae in women (SQ2j) can be either symptomatic or asymptomatic; for modeling purposes the only difference between the 2 is duration (dsq). The sequelae state was modeled as a simplified transition from infection back to susceptibility, in which persons would test negative for chlamydia, but not be immediately susceptible to reinfection. If the sequelae state were instead modeled as one in which persons would test positive, the results in Tables 3a and 3b would change minimally (less than 1%), leaving the ordinal ranking of screening options and dominance unchanged (results available from the authors upon request). The degree of assortative mixing between rate of partner change groups is controlled by equation 13 and the modeling assumption that the number of sex acts for each rate of partner change group balances between men and women.21 When j = k, Δjk = 1; when jk, Δjk = 0. Given this, if ε = 1 then mixing is fully assortative, meaning low-rate persons always choose other low-rate persons as sex partners; if ε = 0, then mixing is completely random and the partner change groups of sex partners are based on the total partnerships in the population.21 We calculated QALYs by applying published health utility measures to symptomatic chlamydial infections and sequelae, and assumed that sequelae of PID developed at previously estimated rates.9,22,23 These health utility measures, the onset delay (where relevant) and the duration for which they were incurred are shown in Table 1a.

        We started the model with 1 infected human in the high partner change group and allowed the system to come to an equilibrium prevalence for men and women, then applied the various intervention alternatives. In the absence of screening, the overall prevalence of chlamydia in women was 2.9% in women and 2.3% in men; under the baseline intervention of screening 35% of women, the equilibrium prevalence of chlamydia was 2.4% in women and 2.1% in men, which is close to that found in a population-based survey.30

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