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FORUM
 INNOVATIVE RESPONSES FOR PREVENTING
   HIV TRANSMISSION: THE PROTECTIVE
       VALUE OF POPULATION-WIDE
    INTERRUPTIONS OF RISK ACTIVITY
                                            Justin O Parkhurst, BSE, MPhil (Oxford), DPhil (Oxford)
                         Health Policy Unit, London School of Hygiene and Tropical Medicine, Keepel Street, London, UK
                                                      Alan Whiteside, MA, DEcon
                  Director, HEARD (Health Economics and HIV/AIDS Research Division), University of KwaZulu-Natal, Durban




 Concurrent partnering contributes to high HIV prevalence. This is in part due to the natural history of the virus.
 After transmission, an individual’s viral load spikes in a period of ‘acute infection’ during which they are highly
 infectious.1,2 Models estimate that around 10 - 45% of HIV acquisition arises from sex with an individual in the
 acute infection period.3

 If everyone in a population abstained from high-risk sex for a given period of time, in theory the viral loads of all
 recent seroconverters should pass through the acute infection period. When risk behaviour resumed there would
 be almost no individuals in the high-viraemic phase, thereby reducing infectivity, and HIV incidence would fall.
 Recurring population-wide shifts in risk behaviour are not unheard of. Many, in fact, occur as part of existing
 religious observances. The month of Ramadan in Muslim communities is perhaps one of the most obvious cases.
 Ramadan sees significant behaviour changes. In addition to fasting from sunrise to sunset, observant individu-
 als abstain from coitus during daylight hours.4 There is anecdotal evidence that risky sexual behaviours are also
 significantly reduced over this period. In Indonesia, for instance, it was reported that research with sex workers
 was not possible during Ramadan because people ‘abstained from sex from one end of the month to the other
 … Many sex workers returned to home villages during this time.’5

 This article argues that a population-wide interruption of risk behaviour for a set period of time could reduce
 HIV incidence and make a significant contribution to prevention efforts. It calls for mathematical modelling of
 periodic risk behaviour interruptions, as well as encouragement of policy interventions to develop campaigns of
 this nature. A policy response, such as a ‘safe sex/no sex’ campaign in a cohesive population, deserves serious
 consideration as an HIV prevention intervention. In some contexts, periods of abstinence from risk behaviour
 could also be linked to existing religious practices to provide policy options.


                        THE ARGUMENT                                              discourages the consumption of alcohol and homosex-
                                                                                  ual sex. All these factors may help explain the lower
There are scientific reasons to believe that popula-
                                                                                  levels of seroprevalence in countries with large Muslim
tion-wide periods of risk reduction could be effective.
                                                                                  populations.10 Norms and patterns of sexual behaviour
Additionally there is evidence to suggest that sexual
                                                                                  may also be quite different in observant Muslim com-
behaviours, including periods of abstinence, driven by
                                                                                  munities compared with other groups. Indonesia, for
religious reasons, may have kept the prevalence low in
                                                                                  instance, has a low national prevalence rate, estimated
Muslim countries. According to UNAIDS only one coun-
                                                                                  to only be around 0.2%, but Papua province has a ma-
try in North Africa and the Middle East region (Sudan)
                                                                                  jority Christian population and an HIV prevalence of
had an HIV prevalence over 0.2%. In South and South-
                                                                                  2.4%, over 10 times the national rate.11
East Asia, predominantly Muslim countries such as Pa-
kistan, Bangladesh and Indonesia show similarly low
                                                                                  There are, however, cases where HIV prevalence ap-
HIV prevalences, typically below 0.2%.6 There are seri-
                                                                                  pears to be unusually low in Muslim areas, even given
ous challenges in attributing cause, however. The prac-
                                                                                  high levels of risk activity. In Dhaka, Bangladesh, for
tice of male circumcision is near universal, and is highly
                                                                                  instance, HIV prevalence apparently remains low de-
protective against men acquiring HIV.7-9 While Islam
                                                                                  spite common risk behaviours of injection drug use
permits polygamy, it prohibits sex outside marriage and
                                                                                  and commercial sex.12 So while confounding makes it
T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E                                                               A P R I L   2 0 1 0   19
hard to attribute the protection derived from Ramadan                                                            DISCUSSION
      practices of abstinence, there is scientific plausibility
                                                                                          A population-wide ‘month off’ from risk behaviour
      for considering it as an intervention.
                                                                                          may help to interrupt the spread of HIV by allowing
                                                                                          the acute infection period to pass and the HIV viral
      A potential intervention would be an aggressive na-
                                                                                          load to fall before risk activity is resumed. The month
      tional campaign to ensure that everyone who is sexu-
                                                                                          of Ramadan may provide one example of this that has
      ally active in a population either commit to 100% con-
                                                                                          unknowingly been protective for Muslim societies.
      dom use or refrain for sexual intercourse over a period
      of a month or longer. This would be a national cam-
                                                                                          We investigated whether there were other opportuni-
      paign with buy-in from leadership at every level, from
                                                                                          ties for abstinence from particular practices similar to
      the President (or King) through church and business
                                                                                          Ramadan through a review of major world religions.
      down to local community leaders. It could be trialled
                                                                                          We did not find examples of sustained population-
      best in small homogeneous populations, and indeed
                                                                                          wide abstinence from sexual activity outside of Islamic
      the National Emergency Response Council on HIV/AIDS
                                                                                          societies. Small groups might do so, however, such as
      (NERCHA) in Swaziland has been considering it (per-
                                                                                          the Marange Apostolic sect in Zimbabwe’s Manicaland,
      sonal communication with author AW). There is also
                                                                                          who were found to abstain from sex during Passover
      evidence from Mozambique that a 2-month ‘cooling
                                                                                          (and also found to have lower prevalence of HIV than
      off’ period during which people would abstain from
                                                                                          surrounding populations).14,15 However, many religions
      starting any new sexual relationships would be feasible
                                                                                          do incorporate some form of abstinence or asceticism
      and acceptable.13
                                                                                          – whether it is the Christian Lenten restrictions for 40
                                                                                          days,4 the Hindu Brahmacharya practices (where some
                        TESTING AND VALIDATION                                            young men restrict sexual activity16 ), or Buddhist gen-
      Avenues can be explored to test or validate the idea that                           eral notions of self-restraint including life-long dietary
      population-wide interruptions in risk behaviour would                               restrictions. What is critical about periods such as Lent
      slow the spread of HIV. On a theoretical level, ideally                             and Ramadan, however, is that they provide clear, ex-
      we feel that this should be further explored through                                tended time periods into which a campaign promoting
      mathematical modelling and estimation exercises.                                    abstinence from sexual risk behaviour might be incor-
      Such exercises could predict how a population-wide                                  porated.
      abstinence campaign might reduce infections, both in
      the month of abstinence and over the course of a year                               While converting people to a religion is not a reason-
      through reduction in average viral loads when risk ac-                              able public health strategy, these insights do raise the
      tivity resumes. However, models may require some ad-                                possibility of campaigns to regularly, if only tempo-
      ditional survey data to inform their parameters.                                    rarily, reduce risk behaviour across a population. The
                                                                                          World Health Organization, for instance, has promoted
      In practice, an experimental trial would be impossible                              ‘tobacco-free’ days.17 In this vein, key HIV risk behav-
      and unethical (abstinence is known to be protective on                              iours can be targeted in populations. A ‘safe sex/no sex’
      its own), nor would it be feasible to control some groups                           campaign for a limited period of time may be a reason-
      when such a wide-scale mobilisation effort might be                                 able public health intervention strategy to attempt in
      needed to promote the behaviour change. However,                                    some settings.
      discussions are under way to actually attempt inter-
      ruptions in risk behaviour in this manner, and these                                In hyper-epidemic countries in particular, policy mak-
      must be observed with sufficient evaluation research                                ers, populations and politicians are open to new ideas
      to be built in. Risk behaviours can be assessed before,                             to address the epidemic. Prevalence rates and incidence
      during and after the intervention period to assess the                              rates are at unacceptably high levels and to be success-
      impact they may have had. This can be done with sur-                                ful interventions take time and require long-term be-
      veys as well as in-depth investigation of particular                                haviour change. The ‘safe sex/no sex’ campaign has the
      groups to help avoid respondent bias. A campaign for                                advantage of requiring a one-off short-term adaption,
      a month of ‘safe sex/no sex’ would also produce eas-                                being relatively cheap, having nation-building quali-
      ily verifiable data with regard to adherence, evidenced                             ties, and not carrying stigma. Finally, many elements
      in the number of births occurring nine months after                                 can be easily monitored.
      the campaign. Finally, in theory, the average HIV viral
      load in the population could also be monitored before,                              While universal permanent abstinence from sex work
      during and after the period of abstinence to see how                                may be impossible to achieve, a month of ‘no commer-
      much it impacted on infectiousness, and to get better                               cial sex’ or ‘no new partners’ might be more possible
      estimates of effectiveness in practice over modelling                               in some populations in which sex work appears to be
      efficacy calculations. However, this might require very                             a driving influence on spread (mining communities in
      large sample sizes to show significant results.                                     southern Africa, for instance18 ). Permanent monogamy
                                                                                          may be a challenging long-term goal for some, but a

20   A P R I L   2 0 1 0                                                             T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E    
                                                                                                                                                                          
                                                                                                                                                                         
‘month of monogamy’ might be a useful starting point.                                       9. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A.
                                                                                               Randomized, controlled intervention trial of male circumcision for reduction of
It has rarely been attempted to put such ideas into                                            HIV infection risk: the ANRS 1265 trial. PLoS Med 2005; 2: 0001-0011.
                                                                                           10. Gray P. HIV and Islam: is HIV prevalence lower among Muslims? Soc Sci Med
practice, but they may reap significant benefits for HIV                                       2004; 58: 1751-1756.
prevention.                                                                                11. Statistics Indonesia (BPS), ORC Macro. Indonesia Demographic and Health Survey
                                                                                               2007. Calverton, Md: BPS and Macro International, 2008.
                                                                                           12. Foss AM, Watts CH, Vickerman P, et al. Could the CARE-SHAKTI intervention
REFERENCES                                                                                     for injecting drug users be maintaining the low HIV prevalence in Dhaka,
 1. Chin J. The AIDS Pandemic: The Collision of Epidemiology with Political Correctness.       Bangladesh? Addiction 2006; 102: 114-125.
    Oxford: Radcliffe Publishing, 2007.                                                    13. Halperin D, Cipriano E, Senda R, et al. A two-month national 'cooling-off' period?:
 2. Halperin DT, Epstein H. Concurrent sexual partnerships help to explain Africa's            Acceptability of an intensive behavior change campaign to reduce acute HIV
    high HIV prevalence: implications for prevention. Lancet 2004; 364: 4-6.                   infection in Mozambique. Presentation at the HIV Acute Infection Meeting,
 3. Wawer MJ, Gray RH, Sewankambo NK, et al. Rates of HIV-1 transmission per                   Boston, 22 - 23 September, 2009.
    coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191:     14. Gregson S, Ndlovu J, Mlilo M, Dauka E. Fluctuations in sexual activity, the validity
    1403-1409.                                                                                 of sexual behaviour estimates for short time-intervals, and HIV intervention
 4. Ryan FT. The Sacred Art of Fasting: Preparing to Practice. Woodstock, VT: SkyLight         evaluation in rural Zimbabwe. J Sex Res 2001; 2: 180-181.
    Paths Publishing, 2005.                                                                15. Gregson S, Zhuwau T, Anderson RM, Chandiwana SK. Apostles and zionists: the
 5. Pisani E. The Wisdom of Whores: Bureaucrats, Brothels, and the Business of AIDS.           influence of religion on demographic change in rural Zimbabwe. Popul Stud 1999;
    London: Granta Books, 2008.                                                                53: 179-193.
 6. UNAIDS. Report on the Global HIV/AIDS Epidemic. Geneva: UNAIDS, 2008.                  16. Alter JS. Celibacy, sexuality, and the transformation of gender into nationalism in
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    men in Rakai, Uganda: a randomised trial. Lancet 2007; 369: 657-666.                   17. World Health Organization. Showing the Truth, Saving Lives: The Case for
 8. Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in              Pictoral Health Warnings. Geneva: WHO, 2009.
    young men in Kisumu, Kenya: a randomised controlled trial. Lancet 2007; 369:           18. Campbell C. 'Letting Them Die': Why HIV/AIDS Prevention Programmes Fail.
    643-656.                                                                                   Oxford: James Currey, 2003.




T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E                                                               A P R I L   2 0 1 0                   21

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Innovative Responses for preventing HIV transmission: The protective value of population-wide interruptions of risk activity

  • 1. FORUM INNOVATIVE RESPONSES FOR PREVENTING HIV TRANSMISSION: THE PROTECTIVE VALUE OF POPULATION-WIDE INTERRUPTIONS OF RISK ACTIVITY Justin O Parkhurst, BSE, MPhil (Oxford), DPhil (Oxford) Health Policy Unit, London School of Hygiene and Tropical Medicine, Keepel Street, London, UK Alan Whiteside, MA, DEcon Director, HEARD (Health Economics and HIV/AIDS Research Division), University of KwaZulu-Natal, Durban Concurrent partnering contributes to high HIV prevalence. This is in part due to the natural history of the virus. After transmission, an individual’s viral load spikes in a period of ‘acute infection’ during which they are highly infectious.1,2 Models estimate that around 10 - 45% of HIV acquisition arises from sex with an individual in the acute infection period.3 If everyone in a population abstained from high-risk sex for a given period of time, in theory the viral loads of all recent seroconverters should pass through the acute infection period. When risk behaviour resumed there would be almost no individuals in the high-viraemic phase, thereby reducing infectivity, and HIV incidence would fall. Recurring population-wide shifts in risk behaviour are not unheard of. Many, in fact, occur as part of existing religious observances. The month of Ramadan in Muslim communities is perhaps one of the most obvious cases. Ramadan sees significant behaviour changes. In addition to fasting from sunrise to sunset, observant individu- als abstain from coitus during daylight hours.4 There is anecdotal evidence that risky sexual behaviours are also significantly reduced over this period. In Indonesia, for instance, it was reported that research with sex workers was not possible during Ramadan because people ‘abstained from sex from one end of the month to the other … Many sex workers returned to home villages during this time.’5 This article argues that a population-wide interruption of risk behaviour for a set period of time could reduce HIV incidence and make a significant contribution to prevention efforts. It calls for mathematical modelling of periodic risk behaviour interruptions, as well as encouragement of policy interventions to develop campaigns of this nature. A policy response, such as a ‘safe sex/no sex’ campaign in a cohesive population, deserves serious consideration as an HIV prevention intervention. In some contexts, periods of abstinence from risk behaviour could also be linked to existing religious practices to provide policy options. THE ARGUMENT discourages the consumption of alcohol and homosex- ual sex. All these factors may help explain the lower There are scientific reasons to believe that popula- levels of seroprevalence in countries with large Muslim tion-wide periods of risk reduction could be effective. populations.10 Norms and patterns of sexual behaviour Additionally there is evidence to suggest that sexual may also be quite different in observant Muslim com- behaviours, including periods of abstinence, driven by munities compared with other groups. Indonesia, for religious reasons, may have kept the prevalence low in instance, has a low national prevalence rate, estimated Muslim countries. According to UNAIDS only one coun- to only be around 0.2%, but Papua province has a ma- try in North Africa and the Middle East region (Sudan) jority Christian population and an HIV prevalence of had an HIV prevalence over 0.2%. In South and South- 2.4%, over 10 times the national rate.11 East Asia, predominantly Muslim countries such as Pa- kistan, Bangladesh and Indonesia show similarly low There are, however, cases where HIV prevalence ap- HIV prevalences, typically below 0.2%.6 There are seri- pears to be unusually low in Muslim areas, even given ous challenges in attributing cause, however. The prac- high levels of risk activity. In Dhaka, Bangladesh, for tice of male circumcision is near universal, and is highly instance, HIV prevalence apparently remains low de- protective against men acquiring HIV.7-9 While Islam spite common risk behaviours of injection drug use permits polygamy, it prohibits sex outside marriage and and commercial sex.12 So while confounding makes it T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E                                                               A P R I L   2 0 1 0 19
  • 2. hard to attribute the protection derived from Ramadan DISCUSSION practices of abstinence, there is scientific plausibility A population-wide ‘month off’ from risk behaviour for considering it as an intervention. may help to interrupt the spread of HIV by allowing the acute infection period to pass and the HIV viral A potential intervention would be an aggressive na- load to fall before risk activity is resumed. The month tional campaign to ensure that everyone who is sexu- of Ramadan may provide one example of this that has ally active in a population either commit to 100% con- unknowingly been protective for Muslim societies. dom use or refrain for sexual intercourse over a period of a month or longer. This would be a national cam- We investigated whether there were other opportuni- paign with buy-in from leadership at every level, from ties for abstinence from particular practices similar to the President (or King) through church and business Ramadan through a review of major world religions. down to local community leaders. It could be trialled We did not find examples of sustained population- best in small homogeneous populations, and indeed wide abstinence from sexual activity outside of Islamic the National Emergency Response Council on HIV/AIDS societies. Small groups might do so, however, such as (NERCHA) in Swaziland has been considering it (per- the Marange Apostolic sect in Zimbabwe’s Manicaland, sonal communication with author AW). There is also who were found to abstain from sex during Passover evidence from Mozambique that a 2-month ‘cooling (and also found to have lower prevalence of HIV than off’ period during which people would abstain from surrounding populations).14,15 However, many religions starting any new sexual relationships would be feasible do incorporate some form of abstinence or asceticism and acceptable.13 – whether it is the Christian Lenten restrictions for 40 days,4 the Hindu Brahmacharya practices (where some TESTING AND VALIDATION young men restrict sexual activity16 ), or Buddhist gen- Avenues can be explored to test or validate the idea that eral notions of self-restraint including life-long dietary population-wide interruptions in risk behaviour would restrictions. What is critical about periods such as Lent slow the spread of HIV. On a theoretical level, ideally and Ramadan, however, is that they provide clear, ex- we feel that this should be further explored through tended time periods into which a campaign promoting mathematical modelling and estimation exercises. abstinence from sexual risk behaviour might be incor- Such exercises could predict how a population-wide porated. abstinence campaign might reduce infections, both in the month of abstinence and over the course of a year While converting people to a religion is not a reason- through reduction in average viral loads when risk ac- able public health strategy, these insights do raise the tivity resumes. However, models may require some ad- possibility of campaigns to regularly, if only tempo- ditional survey data to inform their parameters. rarily, reduce risk behaviour across a population. The World Health Organization, for instance, has promoted In practice, an experimental trial would be impossible ‘tobacco-free’ days.17 In this vein, key HIV risk behav- and unethical (abstinence is known to be protective on iours can be targeted in populations. A ‘safe sex/no sex’ its own), nor would it be feasible to control some groups campaign for a limited period of time may be a reason- when such a wide-scale mobilisation effort might be able public health intervention strategy to attempt in needed to promote the behaviour change. However, some settings. discussions are under way to actually attempt inter- ruptions in risk behaviour in this manner, and these In hyper-epidemic countries in particular, policy mak- must be observed with sufficient evaluation research ers, populations and politicians are open to new ideas to be built in. Risk behaviours can be assessed before, to address the epidemic. Prevalence rates and incidence during and after the intervention period to assess the rates are at unacceptably high levels and to be success- impact they may have had. This can be done with sur- ful interventions take time and require long-term be- veys as well as in-depth investigation of particular haviour change. The ‘safe sex/no sex’ campaign has the groups to help avoid respondent bias. A campaign for advantage of requiring a one-off short-term adaption, a month of ‘safe sex/no sex’ would also produce eas- being relatively cheap, having nation-building quali- ily verifiable data with regard to adherence, evidenced ties, and not carrying stigma. Finally, many elements in the number of births occurring nine months after can be easily monitored. the campaign. Finally, in theory, the average HIV viral load in the population could also be monitored before, While universal permanent abstinence from sex work during and after the period of abstinence to see how may be impossible to achieve, a month of ‘no commer- much it impacted on infectiousness, and to get better cial sex’ or ‘no new partners’ might be more possible estimates of effectiveness in practice over modelling in some populations in which sex work appears to be efficacy calculations. However, this might require very a driving influence on spread (mining communities in large sample sizes to show significant results. southern Africa, for instance18 ). Permanent monogamy may be a challenging long-term goal for some, but a 20 A P R I L   2 0 1 0                                                             T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E          
  • 3. ‘month of monogamy’ might be a useful starting point. 9. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A. Randomized, controlled intervention trial of male circumcision for reduction of It has rarely been attempted to put such ideas into HIV infection risk: the ANRS 1265 trial. PLoS Med 2005; 2: 0001-0011. 10. Gray P. HIV and Islam: is HIV prevalence lower among Muslims? Soc Sci Med practice, but they may reap significant benefits for HIV 2004; 58: 1751-1756. prevention. 11. Statistics Indonesia (BPS), ORC Macro. Indonesia Demographic and Health Survey 2007. Calverton, Md: BPS and Macro International, 2008. 12. Foss AM, Watts CH, Vickerman P, et al. Could the CARE-SHAKTI intervention REFERENCES for injecting drug users be maintaining the low HIV prevalence in Dhaka, 1. Chin J. The AIDS Pandemic: The Collision of Epidemiology with Political Correctness. Bangladesh? Addiction 2006; 102: 114-125. Oxford: Radcliffe Publishing, 2007. 13. Halperin D, Cipriano E, Senda R, et al. A two-month national 'cooling-off' period?: 2. Halperin DT, Epstein H. Concurrent sexual partnerships help to explain Africa's Acceptability of an intensive behavior change campaign to reduce acute HIV high HIV prevalence: implications for prevention. Lancet 2004; 364: 4-6. infection in Mozambique. Presentation at the HIV Acute Infection Meeting, 3. Wawer MJ, Gray RH, Sewankambo NK, et al. Rates of HIV-1 transmission per Boston, 22 - 23 September, 2009. coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191: 14. Gregson S, Ndlovu J, Mlilo M, Dauka E. Fluctuations in sexual activity, the validity 1403-1409. of sexual behaviour estimates for short time-intervals, and HIV intervention 4. Ryan FT. The Sacred Art of Fasting: Preparing to Practice. Woodstock, VT: SkyLight evaluation in rural Zimbabwe. J Sex Res 2001; 2: 180-181. Paths Publishing, 2005. 15. Gregson S, Zhuwau T, Anderson RM, Chandiwana SK. Apostles and zionists: the 5. Pisani E. The Wisdom of Whores: Bureaucrats, Brothels, and the Business of AIDS. influence of religion on demographic change in rural Zimbabwe. Popul Stud 1999; London: Granta Books, 2008. 53: 179-193. 6. UNAIDS. Report on the Global HIV/AIDS Epidemic. Geneva: UNAIDS, 2008. 16. Alter JS. Celibacy, sexuality, and the transformation of gender into nationalism in 7. Gray RH, Kigozi G, Serwadda D, et al. Male circumcision for HIV prevention in North India. The Journal of Asian Studies 1994; 53: 45-66. men in Rakai, Uganda: a randomised trial. Lancet 2007; 369: 657-666. 17. World Health Organization. Showing the Truth, Saving Lives: The Case for 8. Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in Pictoral Health Warnings. Geneva: WHO, 2009. young men in Kisumu, Kenya: a randomised controlled trial. Lancet 2007; 369: 18. Campbell C. 'Letting Them Die': Why HIV/AIDS Prevention Programmes Fail. 643-656. Oxford: James Currey, 2003. T H E  S O U T H E R N  A F R I C A N  J O U R N A L  O F  H I V  M E D I C I N E                                                               A P R I L   2 0 1 0 21