Knowledge of specific HIV transmission modes in relation to HIV infection in Mozambique

Background: In prior research, Africans who knew about blood-borne risks were modestly less likely to be HIV-infected than those who were not aware of such risks. Objectives/Methods: I examined the association between knowledge of specific HIV transmission modes and prevalent HIV infection with data from the 2009 Mozambique AIDS Indicator Survey. Results: Respondents displayed high awareness of blood exposures and vaginal sex as modes of HIV transmission. However, only about half of respondents were aware of anal sex as a way HIV can be transmitted. After adjustments for demographics and sexual behaviors, respondents who knew that HIV could spread by contact with infected blood or by sharing injection needles or razor blades were less likely to be infected than those who did not know about these risks. Respondents who knew about sexual risks were as, or more, likely to be HIV infected as those who did not know about sexual risks. Also, children of HIV-uninfected mothers were less likely to be infected if their mothers were aware of blood-borne HIV risks than if their mothers were unaware. Conclusion: HIV education campaigns in Mozambique and elsewhere in sub-Saharan Africa should include a focus on risks from blood exposures and anal sex.


Introduction
A wide variety of blood exposures is independently associated with incident and prevalent HIV infection in sub-Saharan Africa [1][2][3][4][5][6][7][8][9] . Anal sex has also been repeatedly associated with HIV infection in heterosexual Africans 10-15 , with some exceptions 16,17 . Knowledge of blood-borne HIV risks varies markedly across the region, with awareness much higher in West, central and East Africa than in Southern Africa 18 . This geographic variation in knowledge corresponds closely to differences in HIV prevalence, such that countries in which many people know about blood-borne risks have much lower HIV prevalence than countries in which few know about these risks. Although HIV education campaigns in West, central and East Africa have included a focus on blood-borne risks, campaigns in Southern Africa have not, likely leading to deficits in Southern Africans' knowledge. At the individual level, persons who know about blood-borne risks are modestly less likely to be HIV-infected than those who are not aware of such risks, independent of demographics and sexual behaviors 18 .
In contrast, belief in condom use as a strategy for avoiding HIV infection is positively associated with HIV infection at both the individual and national levels in sub-Saharan Africa 18 . That is, those who believe condoms are an effective strategy for preventing HIV transmission are more likely to be HIV-infected than those who do not believe condom use protects against HIV, independent of demographics and sexual behaviors.
Although long assumed to be rare, anal sex is not uncommon in sub-Saharan Africa, as modest to large proportions of heterosexual men and women report engaging in it [10][11][12][13][14][15][19][20][21][22][23][24][25][26][27] . Research based on nonprobability samples suggests that many Africans are unaware that anal sex is a significant risk for HIV transmission. While 87% of young adult Nigerians in one study knew anal sex is an HIV risk 28 , only 54% of men in Cape Town, South Africa in 1999 19 and 29% of adolescents in a Western Cape (South Africa) township with very high HIV prevalence shared that perception 26 . Some South African women in a qualitative study explained the lack of risk involved with anal sex 29 . Moreover, Kenyan prostitutes viewed vaginal sex as equally or more risky than anal sex 21 . Throughout the last 13 years, researchers have noted that HIV education campaigns targeting heterosexuals in sub-Saharan Africa lack warnings about the risk of anal sex 10,15,19,23,24,27,30 .
In this paper, I report on the relationship between knowledge of HIV transmission routes and prevalent HIV infection in Mozambique, a country with high HIV prevalence not included in prior analyses. I analyzed data from the 2009 Mozamibique AIDS Indicator Survey (AIS), a special version of the Demographic and Health Surveys (DHS) conducted in poor countries. I included respondents' data in analysis if they reported never having been tested previously for HIV and also reported awareness of HIV/AIDS. HIV counseling may, in some places, involve education about blood-borne and sexual risks 32 , which may confound the relationship between knowledge and serostatus 33 . Respondents who did not report awareness of HIV/AIDS were not asked about ways that it could be transmitted. Ninety-seven percent of female respondents and 99% of male respondents reported they had heard of HIV/AIDS.
Respondents who reported awareness of HIV/AIDS were asked whether it was possible to transmit HIV through each of several types of direct and indirect interpersonal contact. I focused on knowledge of four types of contact: sharing injection needles/blades; contact with infected blood; unprotected vaginal sex (i.e., vaginal sex without a condom); and unprotected anal sex. I coded "don't know" responses to these questions as "no".
For the analyses of mother's knowledge and child's serostatus, I included biological mother-child pairs in which the mother was HIV-uninfected, to eliminate confounding by vertical transmission.

Mozambique Demographic and Health Survey (DHS) data
In the 2003 Mozambique DHS, the household participation rate was 95%, and 91% of eligible women (age 15-49 years) and 81% of eligible men (age 15-64 years) participated 34 . Women were recruited as respondents from all households, but men were recruited as respondents only from one-third of households. Respondents did not provide blood specimens for HIV testing. The 2003 Mozambique DHS data and documentation are also available at http://www.measuredhs.com.
As I did with the AIS data, I included respondents' data in analysis if they reported never having been tested previously for HIV and also reported awareness of HIV/AIDS. Ninety-seven percent of female respondents and 99% of male respondents in the 2003 DHS reported they had heard of HIV/AIDS.
Respondents who reported awareness of HIV/AIDS were asked "Do you know how you can avoid HIV/AIDS?" Those answering affirmatively were then asked "How can you prevent HIV/AIDS?" Interviewers encouraged and recorded multiple responses, and responses were coded by DHS staff. To compare with the 2009 Mozambique AIS and other DHS, I focused on two measures: whether a respondent had a response that was coded as "only use sterilized syringes/needles" and "always use a condom". I coded "don't know" responses to the open-ended question as "no" for each of these measures.

Statistical analysis
With the 2009 Mozambique AIS data, I computed crossclassifications, odds ratios, and the associated 95% confidence intervals (CI) for the relationships between each knowledge measure and prevalent HIV infection, separately for women and men. To examine the associations further, I calculated the odds ratios, with HIV status as the dependent variable and a knowledge measure as the independent variable, adjusted for age (in whole years), urban/rural residence, number of whole years of education, wealth (in quintiles), reported number of sex partners in the prior 12 months, and whether the respondent reported having had a sexually transmitted disease in the prior 12 months. In addition, I calculated adjusted odds ratios (AORs) in the manner just described but adjusting for each of the three other knowledge measures as well. I also computed the Pearson ( Online search of HIV prevention education efforts focused on blood-borne risks In July of 2011, I sought evidence of public HIV education campaigns focused on blood-borne risks in Mozambique by searching two online databases: the Google search engine and the Media/Materials Clearinghouse. For the Google search, I used the key words "Mozambique", "HIV", and "razor". I examined the resources identified until I found 30 consecutive resources to be irrelevant (for a total 320 resources examined). I repeated this search in September of 2011 at the Google's Mozambican site, with the equivalent key words in Portuguese: "Moçambique", "VIH," and "lâmina" (290 resources examined). I also extended this search by adding, in turn, the names of the 14 HIV prevention programs and campaigns mentioned in the AIS questionnaire (for questions about respondents' familiarity with the programs and campaigns) 31 . My Google search was not exhaustive, especially given the limited scope induced by the key word "razor". However, the razor blade is perhaps the most ubiquitous sharp instrument involving possible blood exposure in daily life in Mozambique. Any public education campaign about blood-borne HIV risks that excludes explicit mention of razor blades is probably superficial or very narrow. For the Media/Materials Clearinghouse search, I inspected all materials pertaining to Mozambique. I also examined any sources related to Mozambique that I had found in an earlier search of the US National Library of Medicine Gateway 18 .

Results
In the 2009 Mozambique AIS, over 90% of respondents reported that HIV could spread through shared needles/razors and nearly 80% reported that HIV could be spread through contact with infected blood ( Table 1). Approximately 90% of women and men reported vaginal sex as an HIV transmission route. In contrast, only 48% of women and 58% of men thought that HIV could spread through anal sex.
Before adjustments for demographics and sexual behavior variables, respondents who believed that HIV spread through vaginal or anal sex were more likely to be infected than those who did not believe HIV spread in that way (Table 1). In unadjusted analyses, respondents who reported that HIV could be transmitted through blood contact or reusing sharps were about as likely to be infected as respondents who did not think HIV was transmitted in that way.
Urban residence, education, and wealth were moderately positively associated with knowledge of blood-borne HIV risks (results not shown), and these same factors were positively related to HIV infection as well 31 . Consequently, the AORs between the knowledge measures and HIV infection in (Table 2 and Table 3) provide better estimates of the relationship between the knowledge measures and HIV infection.
After adjustments for demographic factors and sexual behavior variables, the measures of knowledge of blood-borne risks become inversely related to HIV infection. That is, respondents who reported that HIV can spread through shared needles/razors and blood contact were less likely to be infected than those who reported that HIV does not spread through such means, once demographics and sexual behaviors were held constant. The adjustments for potential confounders also caused the positive associations for knowledge of vaginal sex risk in women and knowledge of anal sex risk in men to disappear. However, the adjusted associations for knowledge of anal sex risk in women and knowledge of vaginal sex risk in men remained meaningfully positive. In particular, men who believed HIV spreads through vaginal sex were almost twice as likely to be infected as men who did not believe this (Table 3). The adjusted odds ratios for knowledge of shared needles/razors as transmission risks are generally similar to those for knowledge of avoiding shared razors as an HIV prevention strategy in four other countries in Southern Africa (Table 2 and Table 3). The adjusted associations for knowledge of vaginal sex risk also approximate those for knowledge of condoms as a prevention strategy from the other Southern African countries.
The blood-borne risk knowledge measures correlated moderately with each other (r = 0.26-0.29) as did the sexual risk knowledge measures (r = 0.23-0.29). The associations between one bloodborne risk knowledge measure and one sexual risk knowledge measure were weaker (r = 0.12-0.23). Nonetheless, when all four knowledge measures were included in analysis together (last column in (Table 2 and Table 3), the associations between each knowledge measure and HIV infection were almost the same as when the knowledge measures were analyzed separately.
HIV uninfected mothers' knowledge of blood-borne HIV risks was also inversely related to their children's HIV status. Children whose mothers knew that contact with blood is an HIV risk were less likely to be infected (0.4%; 11/2511) than children whose mothers did not know about this risk (1.2%; 7/591; OR 0.37, 95% CI 0.14-0.95).
There was no online evidence of public HIV education campaigns that focused on blood-borne transmission risks in Mozambique. Some participants in a face-to-face community HIV education program that was implemented in Mozambique credited the program with informing them about some blood-borne risks 35,36 . However, none of the descriptions of the program at the program's website (http://www.steppingstonesfeedback.org) or elsewhere online indicate that this topic is formally covered in the program.

Discussion
Adult Mozambicans displayed very high awareness of some blood exposures and vaginal sex as modes of HIV transmission when directly asked about such contact in the 2009 Mozambique AIDS Indicator Survey. However, only a little more than half of respondents were aware of anal sex as a way HIV can be transmitted. After adjustments for demographics and sexual behaviors, knowledge of blood-borne risks was inversely associated with prevalent HIV infection. That is, respondents who knew that HIV could spread by contact with infected blood or by sharing injection needles or razor blades were less likely to be infected than those who did not know about these risks. Knowledge of sexual risks was negligibly to   Instead, these results indicate that Southern Africans are typically aware of a variety of blood-borne HIV risks (including shared needles and razors that might not involve large or visible blood contamination), but only when specifically prompted.
Interestingly, observed levels of Southern Africans' knowledge of sexual risks differ relatively little based on measurement approach. In the aforementioned studies, the proportions of respondents aware of sexual HIV transmission risks tended to be only slightly less when measured with recall methods than recognition methods. The difference between the proportion of 2003 Mozambique DHS respondents who recalled "always use a condom" as a prevention strategy (62%) and the proportion of 2009 Mozambique AIS respondents who recognized vaginal sex as a transmission mode (92%) is somewhat larger, although this could be due to increases over time in Mozambicans' perceptions of vaginal sex as a risk.
The discrepancy between observed levels of knowledge of bloodborne HIV risks based on recall and recognition measurement reveals that blood-borne risks are not salient in the minds of Southern Africans. In 2011, Class interviewed 23 HIV infected adults and 26 parents or other caretakers of HIV infected children in Maputo, Mozambique (Deena Class, personal communications, July 11, 2011, August 27, 2011, and September 29, 2011. Nearly all of Class' respondents noted blood-borne transmission as one mode of HIV spread. However, none of the adults attributed their infections to a blood exposure. Five of the infected children had seronegative biological mothers, indicating that these children had acquired their infections horizontally. Remarkably, only one of these mothers suspected blood-borne transmission for her child. Furthermore, none of these five mothers were told by their healthcare providers how their children might have been infected. In another study, Zimbabwean youth almost universally recognized the potential for HIV transmission through shared razors, yet ranked the avoidance of sharing razors as the least effective strategy for preventing HIV in comparison to strategies focused on sexual exposures and behaviors not known to protect against infection (avoiding deep kissing and washing hands) 43 . Similarly, Kenyans in Nyanza province grossly underestimated how long HIV can survive on a blood-contaminated razor blade or inside a blood-contaminated needle or syringe 44 . Thus, many Africans may recognize blood-borne HIV transmission as a theoretical possibility, but regard it as unlikely in practice.
Such apparent misunderstandings of blood-borne HIV transmission are not surprising given the lack of public education about bloodborne risks in sub-Saharan Africa. Just as in other African countries 18 , efforts to educate Mozambican traditional healers about hygienic practices began decades ago 45,46 and continue to this day 47,48 .
There was also at least one attempt to educate barbers about bloodborne risks in the early 1990s 49 . However, I found no good evidence that public HIV education campaigns in Mozambique have in the past focused on blood-borne risks to any meaningful extent. Furthermore, as in other Southern African countries 18 , large recent and current public HIV education campaigns in Mozambique exclude mention of blood-borne risks 50,51 (see also: One Love Regional Campaign -Southern Africa, and Center for Communication Programs). Indeed, Class' Mozambican respondents who noted bloodborne transmission as one mode of HIV spread said they learned of these risks informally, not from HIV education campaigns, health care providers, or public health sources (Deena Class, personal communication, September 29, 2011).
Mozambicans' awareness of anal sex as a transmission risk was much lower than their awareness of vaginal sex as a risk, even though the actual risk from anal sex is much higher. Contrary to my expectation, knowledge of anal sex risk was not associated with lower rate of HIV infection. It is unclear why this is so. Further investigation of the perceived risk of anal sex (e.g., whether risk differs for men and women) and whether respondents engage in anal sex might help clarify this result.
Beliefs in vaginal sex as an HIV transmission risk and condom use as an HIV prevention strategy 18 are associated with a higher likelihood of HIV infection in Mozambique and elsewhere in sub-Saharan Africa. This is consistent with the lack of association between condom use in vaginal sex and incident HIV infection 14,52,53 . Condom use itself may even make people more vulnerable to infection by reducing mucosal exposure to HIV and thus hindering the development of alloimmunity against HIV 54,55 .
To determine the modes of transmission of HIV in sub-Saharan Africa with confidence, researchers must assess blood and sexual exposures comprehensively in incident HIV cases and controls, trace their contacts corresponding to such exposures, and sequence the DNA in infected persons' HIV isolates [56][57][58] . In the meantime, HIV education campaigns in Mozambique and other poor countries should focus on blood-borne and anal sex transmission risks comprehensively and emphasize strategies for avoiding these dangers 59-61 .

Competing interests
No relevant competing interests declared.

Grant information
The author(s) declared that no grants were involved in supporting this work.

Current Referee Status:
Referee 02 August 2012 Referee Report: This is an interesting article. However, I am sure there are some sections where readers would like to have some more information e.g. how the adjustments for demographic and sexual behaviors were performed.

I have read this submission. I believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.
No competing interests were disclosed. a) The literature is quoted selectively and issues are oversimplified.
The paper states that blood exposure is important but does not state that the preponderance of studies show that sexual exposure is by far the most common mode of HIV transmission.
For example it doesn't reference articles such as: Unsafe injections and transmission of HIV-1 in sub-Saharan Africa. The global burden of disease attributable to contaminated injections given in health care settings.
Quantifying HIV-1 transmission due to contaminated injections.
The paper seems to claim that knowledge about blood borne infections account for the regional differences in HIV prevalence. A single citation (a paper by the same author) for this claim is provided. Other possibilities are not discussed such as: Understanding the differences between contrasting HIV epidemics in east and west Africa: results from a simulation model of the Four Cities Study Ecological and individual level analysis of risk factors for HIV infection in four urban populations in sub-Saharan Africa with different levels of HIV infection.
The paper also implies that condoms are not protective against HIV. Again this is not what the preponderance of studies shows: Condom effectiveness in reducing heterosexual HIV transmission.
The author also notes the reference as evidence for the lack of an association Allen S et al. (2003) between condoms and HIV incidence but the study found that incident HIV infection was found in 5.4% of testing intervals when discordant couples had unprotected sex and in 2.6% of testing intervals when the discordant couples did not have unprotected sex.
b) The interpretation of the results are not always supported by the data in the paper: The Author states: "After adjustments for demographic factors and sexual behavior variables, the measures of knowledge of blood-borne risks become inversely related to HIV infection. That is, respondents who reported that HIV can spread through shared needles/razors and blood contact were less likely to be infected than those who reported that HIV does not spread through such means, once demographics and sexual behaviors ". were held constant However, it is unclear how the author reaches this conclusion. The OR for the above relationships are about 0.9 and the confidence intervals are wide. This is not evidence of a relationship.
The author also states: And finally; The OR for men's understanding of vaginal sex is close to being statistically significant.

c) The paper's conclusion is not supported:
The author claims that: "HIV education campaigns in Mozambique and elsewhere in sub-Saharan Africa should include a focus on risks from blood exposures and anal sex." However, the data in the paper doesn't suggest that this is called for, and even if the data were supportive of the need to do this, there are opportunity costs associated with doing so. What should health workers or health educators not do to create time and money for this change in message?
Is the title appropriate for the content of the article? Yes Is the abstract a suitable summary of the article? No (see above) Is the article well constructed and clear? No (see above) Is there adequate analysis, including information on how the data were analyzed (e.g. programs, code, stats etc.)? There is no information on how the author decided that some results were important Are the conclusions sensible and balanced? No (see above).
Have any potential biases or competing interests been disclosed? Yes I have read this submission. I believe that I have an appropriate level of expertise to state that I do not consider it to be of an acceptable scientific standard, for reasons outlined above.
No competing interests were disclosed. Livesley states that "the preponderance of studies show that sexual exposure is by far the most common mode of HIV transmission" and criticizes me for not citing three articles that he thinks support this view. However, there is no solid empirical evidence that vaginal sex is the dominant mode of HIV transmission in sub-Saharan Africa, because studies with designs rigorous enough to determine modes of transmission have not yet been conducted. In the last paragraph of the current article, I wrote "to determine the modes of transmission of HIV in sub-Saharan Africa with confidence, researchers must assess blood and sexual exposures comprehensively in incident confidence, researchers must assess blood and sexual exposures comprehensively in incident HIV cases and controls, trace their contacts corresponding to such exposures, and sequence the DNA in infected persons' HIV isolates56 57 58." My colleagues and I have published this plea dozens of times in the last nine years, and no other researchers have attempted to conduct the necessary research. Simply stating that vaginal sex is the dominant mode of transmission, or wishing it to be the case, does not make it so; rather, in science, strong empirical evidence must be presented to support a claim. My colleagues and I carried out a study in Calabar, Nigeria in which we assessed blood and sexual exposures fairly comprehensively in incident HIV cases and controls ( reported results from modeling exercises on the share of HIV infections that may et al. be due to unhygienic medical injections (just one of many blood exposures encountered by Africans). I and others disagree with many of the assumptions and parameter estimates used and emphasized in their simulations (because they are at odds with empirical data). Their models also lack several key risk components of unhygienic injection practices. I refrain from a detailed technical critique of these studies here. Crucially, neither modeling exercise produced an estimate of the share of HIV transmission due to vaginal sex. Furthermore, modelers have not been able to simulate HIV epidemics that resemble African epidemics with parameter estimates derived from empirical data on Africans' vaginal sex behavior ( . results cannot be used as an estimate of the protective et al effect of condom use during vaginal sex in sub-Saharan Africa or elsewhere. The protective effect of condom use during anal sex, though, has been well-established in other research.
Livesley questions my description of adjusted odds ratios of 0.81 to 0.95 for the association between knowledge of blood-borne HIV risks and prevalent HIV infection as indicating an inverse relationship. By definition, odds ratios under 1.0 reflect inverse or negative relationships. The adjusted odds ratios were in the inverse direction for two different measures of knowledge of blood-borne HIV risks and for both women and men. The confidence intervals for these odds ratios do include 1.0. However, the consistency of the association across measures and sample subgroups, and similarity in magnitude of the association to similar associations in neighboring and nearby countries mean that it is warranted to describe the relationship as inverse.
Livesley criticizes me for characterizing the adjusted odds ratios between knowledge of anal sex and HIV infection in women (AOR = 1.18) and knowledge of vaginal sex and HIV infection in men (AOR = 1.85) as "meaningfully positive." In this context, I intended "meaningfully positive" to refer to associations that were mild to moderate in magnitude. Livesley also correctly noted that "the OR for men's understanding of vaginal sex is close to being statistically significant." This result means that Mozambican men who believed that HIV can be transmitted through vaginal sex without a condom were twice as likely to be infected with HIV as men who did not believe vaginal sex was a risk.
Livesley argues that the results in my article do not suggest that HIV education programs in sub-Saharan Africa should include a focus on blood-borne risks and anal sex. The results show that Mozambican adults who were unaware of blood-borne transmission were at increased risk for HIV infection, and that children of uninfected mothers who were unaware of blood-borne transmission were at much increased risk for HIV infection. Almost half of Mozambican adults did not know anal sex was an HIV transmission risk. In my opinion, these findings justify including a focus on blood-borne risks and anal sex in HIV education efforts.
Livesley further wonders how such topics could be incorporated in HIV prevention and education programming. Successful examples abound. As I discussed in my 2011 article, there is a "heavy emphasis on avoiding blood-borne risks in HIV education programs for primary school students in rich countries [69,70], travelers to poor (especially African) countries [71][72][73], and employees of the United Nations working in poor countries [74,75]" (p. 194). Most of these educational efforts have