Social and Behavioral Determinants of Sexually Transmitted Disease: Scientific and Technologic Advances, Demography, and the Global Political Economy

THIS IS A GREAT HONOR and a very humbling experience. I am very grateful to all who made this moment possible—to the American STD Association, to the selection committee, to those who nominated me, and to the whole field of sexually transmitted disease (STD) epidemiology and prevention. I am particularly grateful to King Holmes, Ward Cates, and Russ Alexander for their heavy duty mentoring throughout, but especially during the early years. Mentoring me was slightly different than mentoring a Harvard- or Yale-trained MD. I had to be taught how to speak and write in English; I had to be taught STD and epidemiology. I had to be introduced to the American culture, the medical culture, the Centers for Disease Control and Prevention culture, the public health culture; and I badly needed self-confidence enhancing behavioral interventions. My mentors have been extremely patient with me. However, it takes a village to make a career (Fig. 1). I have learned and received support from so many individuals; some directly, some indirectly; some thought they were learning from me while they taught me. Some thought they were receiving support from me while they supported me. I cherish each of them and am very grateful to all.Fig. 1: It Takes a Village.Often the Parran Lecture is a description of the recipients’ series of accomplishments. Alternatively, it can be the description of one recent achievement. When I look back on my career up to this point, what I find remarkable is not what I have done, but rather, what I have observed happen in the field; so much has changed since 1978. Robert Frost had said, “How many things have to happen to you before something occurs to you?” In what follows, I describe some thoughts that occur to me based on developments in science, technology, demography, and the global political economy at this point in time. One relevant scientific contribution is the argument by Duncan Watts and colleagues that population structure is relevant to the spread of infectious disease, and traditional mathematical models have understated the role of nonhomogeneous mixing in populations with geographic and social structure.1 The recently proposed geographic and network models do incorporate various aspects of interaction structure among individuals, but these complex models have low tractability and general conclusions are notoriously difficult to draw from them. Watts and colleagues introduce a class of metapopulation models. They assume homogeneous mixing within local contexts. They also assume local contexts are embedded in a nested hierarchy of successively larger domains. The movement of individuals between contexts is modeled through transport parameters and disease spreads stochastically. This model successfully reproduces aspects of real epidemics, including extreme size variation and temporal heterogeneity, which have been difficult to reproduce with the traditional compartment models as well as recent network models. The results of this work also suggest that when epidemics do occur, the basic reproduction number Ro may bear little relation to their final size. The large variations in epidemic size and the resurgence behavior derive not from average statistics like Ro, but from rare, stochastic events in which the epidemic escapes from currently infected contexts into newly susceptible populations. Individuals introduce disease to previously uninfected groups. Thus, stochasticity is important not only at the outset of an epidemic, but throughout its entire progress. As suggested earlier by Bailey,2 global epidemics should be considered as many smaller epidemics occurring in different subpopulations; most transmission occurs at the subpopulation level; broader spread depends on mixing between subpopulations. The final size and duration of the epidemic are highly sensitive to the structure of the population through which it spreads even when the basic reproductive number is held constant. Conversely, similar distributions of epidemic size can correspond to very different values of Ro. The details of this multiscale hierarchical metapopulation model will probably evolve and improve in the future. The model is not yet developed for sexually transmitted infections. This model has important implications for future directions in the social and behavioral aspects of STD epidemiology and prevention. Some of the questions we may pursue in the future include: What are the sexually relevant meta population structures? What is the structure of sexual segregation? What parameters define the boundaries around sexual links or subpopulations within which there is random sexual mixing? How do sexually relevant metapopulation structures vary across societies with high and low incidence and prevalence of STDs? In addition to transportation, which is relevant to the spread of all infections, what are sexually relevant mechanisms that establish contact across hierarchically located subpopulations in a metapopulation? Some examples come to mind—bathhouses, conventions, “dogging” as practiced in the United Kingdom, Internet-based sex partner recruitment and group sex. Finally, what are the determinants of these mechanisms? What are the big events or slow developments that change these mechanisms—either suddenly and radically or slowly and fundamentally? Some work has already been done in the STD field on these issues3–5 Further focus on a systematically developed research agenda along these lines may be helpful. There are other relevant scientific developments. Norman R. Brown6 at the University of Alberta in Calgary has been doing some interesting work on cognitive processes involved in the organization of experiential knowledge and the generation of numeric estimates. His work is highly relevant to ours particularly as we collect data on histories of sexual behavior, STD diagnoses, numbers of partners, sexual practices, and condom use. More specifically, Brown has conducted research on the multiple strategies people use in estimating event frequency and the factors that affect strategy choice. His findings suggest that men approximate and therefore overestimate their number of sex partners, whereas women enumerate and therefore underestimate their number of partners. Brown has also done work on the cognitive processes of population estimation, subjective geography, autobiographic memory, and event dating. The work on event frequency, autobiographic memory, and event dating have particular relevance to the construction of interview schedules and survey instruments in STD work; perhaps, we should follow this line of research carefully in the future. Another very interesting and highly relevant development, particularly in the past 2 years, involves the advances in neurobiology enabled by functional magnetic resonance imaging (FMRI) and position emission tomography (PET) technologies. Multidisciplinary research (including neuroscience, anthropology, and social psychology) has focused on neurophysiological systems that relate to love using MRI technologies. Lucy Brown, Arthur Aron, and Helen Fisher’s findings (among others)7,8 indicate that romantic love may have more to do with motivation, reward, and generalized drive aspects of human behavior than with emotions or the sex drive. Subjects in the early stages of romantic love relationships showed intense activity in the reward and motivation regions of the brain, which are rich with dopamine. The researchers conclude that sex and romantic love involve quite different brain systems. This finding is counterintuitive and raises questions. For decades, sexual behavior has been conceptualized as composed of premarital, marital, extramarital, and nonmarital sex. All along, it has been implicitly assumed that love and marriage were the counterfactual and sex outside of marriage the deviation, the exception. Is it possible that neurobiology and neuron endocrinology are going to turn this conceptual scheme inside out in the new millennium? The same research also revealed that in several brain areas, the strength of neural activity declined with the length of romance. The MRI images indicated more activity in the ventral pallidum portion of the basal ganglia in people with longer romantic relationships—the region where receptors for the hormone vasopressin (rather than dopamine) are, vasopressin being the hormone associated with attachment. Neurobiology of love includes processes that critically involve oxytocin, vasopressin, dopamine, and serotonergic signaling.8 A senior member of this research team—Helen Fisher—distinguishes 3 primary drives that evolved for reproduction: the sex drive, romantic love, and long-term attachment—each with its associated hormones and chemical neurotransmitters in the brain: oxytocin, dopamine, and vasopressin. Fisher’s latest work shows that men and women who have been rejected by a romantic partner show increased activity in areas of the brain that link to anxiety, obsessive/compulsive behaviors, high-risk decision-making, muscle pain, and anger management. She links these findings to the crosscultural phenomena of stalking, homicide, suicide, and clinical depression as well as abandonment rage.9 Others, including Lieberman, and colleagues from UCLA have studied the effects of rejection on the brain, particularly on the prefrontal cortex and the cingulate located in the center of the brain.10 The work on the biologic effects of rejection may have important implications for mechanisms underlying concurrent partnerships and short gaps between partnerships; the resolution and establishment of sex partnerships; and the sexual and health behaviors of marginalized populations, whether they are racial–ethnic minorities, those with incarceration histories, or men who have sex with men (MSM) in a context of homophobia. Other work in neuroendocrinology may also be relevant to behaviors of marginalized individuals. It appears that stressors can trigger a search for pleasure, proximity, and closeness—promoting the rebalancing of altered physiological and psychologic states.11 Considerable volumes of work in psychoneuroendocrinology deal with differences between men and women. Functional sex-related differences have been reported in brain correlates of emotional processing, facial processing, working memory, auditory and language processing; in the relation between stress and memory; and in the brain correlates of sexual arousal. There are also many anatomic differences between the brains of men and women. In this context, work by Larry Cahill,12 a neurobiologist at the University of California at Irvine, is particularly interesting. Cahill has shown that neural mechanisms underlying emotionally influenced explicit recall of emotionally arousing events are different in men and women, particularly in relation to the hemispheric involvement of the human amygdala. Cahill showed, using PET scans, that even in a resting state, men’s and women’s brains are wired differently. Many brain areas that communicate with the amygdala in men are engaged with and respond to the external environment and the right hemisphere amygdala is more active. In women, the brain areas that communicate with the amygdala control the internal environment and the left hemisphere amygdala is more active. These findings may have implications for our interactions with our target populations and research subjects as we communicate with them for data collection, risk assessment, or behavioral intervention purposes. The take-home message in this literature is that the brain seems to be hard-wired in relation to many behaviors related to STD, but the causes of the hard wiring are not necessarily or purely biologic. The environment and behaviors have great impact on the hard wiring of the brain and can effectively change it. Evolutionary psychology, which used to be known as sociobiology, has made remarkable contributions to our understanding of sexuality. This work has focused on a number of subjects, including men’s and women’s mating preferences; sex differences in ideal number of sex partners over a lifetime; sex differences in likelihood of agreeing to have sexual intercourse; sex differences in desirable partner characteristics; and desirable characteristics of short- and long-term mates. When asked how many sex partners they would like to have over a given period of time, men report more partners than women.13 When asked if they would agree to have sexual intercourse with an attractive member of the opposite sex, they have known for varying lengths of time, men were only slightly disinclined to have intercourse with a woman they had known for just 1 hour; it is very unlikely that a woman would have sex with a man she has known for only this length of time. Men and women look for the same characteristics in long-term partners such as kindness, understanding, intelligence, personality, adaptability, and creativity. On the other hand, men were apparently more prepared to have casual sex with a partner of much lower intelligence than themselves compared with women. Evolutionary psychology suggests that short-term mates are selected on the basis of physical characteristics, whereas long-term mates are selected on the basis of psychologic characteristics. Men’s and women’s sexual strategies have evolved to enhance their reproductive success and inclusive fitness. Thus, women try to find men who will transfer resources to their offspring; “health” and “paternal investment” or “good provider” “good genes” are attributes they look for in men. Men, on the other hand, try to find women who promise rapid production of offspring and a disinclination to mate with other men; “health” “fertility” and “faithfulness” are desirable attributes in women. Interestingly, it may be beneficial from an evolutionary point of view for a woman to marry a “good provider” but mate with a man with “good genes.” Many songs in the popular culture refer to this particular scenario. Evolutionary psychology also focuses on “jealousy” as a potential evolved coping mechanism for lack of commitment and on power and status behaviors in men because these may act as signals to females that the male has “good provider” attributes. Finally, based on evolutionary psychology, features men rate as attractive in a woman include symmetric face and body, full lips, small noses and a waist to hip ratio of approximately 0.7.13 Although macrolevel propositions of evolutionary psychology have met widespread acceptance, many of its more specific hypotheses have been challenged. Evidence of great overlaps between men and women and major variation within sexes about many sexual behavior parameters suggest that at the present moment, there are many unknowns in this domain. However, they are exciting and, perhaps, highly relevant unknowns. Over the past 2 decades, evolutionary biology, evolutionary physiology, and biochemistry have also made remarkable advances. Just like evolutionary psychology, each of these disciplines has defined the key to understanding human sexuality as the recognition that it is an issue in evolution. Animals’, plants’, and humans’ physiological and biochemical characteristics adapt to certain lifestyles and evolve in response to environmental conditions. Evolved sexual strategies are dependent on both ecologic parameters and the parameters of a species’ biology and both sets of these parameters vary among species. In his 1997 book, Why is Sex Fun?, Jared Diamond described normal human sexuality as having well-defined features.14 These include long-term sexual partnerships, coparenting, proximity to the sexual partnerships of others, private sex, concealed ovulation, extended female receptivity, sex for fun, and female menopause. On a different but related note, the emerging field of epigenetics focuses on single nutrients, toxins, behaviors, or environmental exposures that can silence or a its in The environmental a chemical change in the or brain that a group of the group to the control of a and may silence or the the its of This is Thus, we are longer to whether or environment has a impact on our development, or They are or can through biochemical that whether at or can be from one generation to the and behaviors have a impact on in the where this of neurobiology and evolutionary psychology, both of which point to the of hard wiring and but at the same the important effects of environment and behavior on biology and the brain, in our understanding of human sexual behavior in the In what follows, I sexual behaviors and their global political the most known data sexual behaviors is the that the of to men and women who have had sexual intercourse has from the of indicate from to for women and to for men between and from the support the results from the of However, these are not in with some other For in very recent compared in sexual behaviors in the United and over the of the and in of and sex and partnerships in both In many the were have reported similar for the general population of Helen Ward and colleagues reported that the rate of sex with women had over the of the in the United compared data from and 2 and in reported frequency of sex and colleagues asked about in group sex events in their of a network based of and other in and high in group sex having sex in group sex and having sex at these The in these findings suggests that may be sexual their sexual and their number of partners. than number of partners over over the past or past of which would be by the and of sexual at number of sex partners sexually from the Sex showed that have more sex partners sexually This finding for all from the of showed that the and number of sex partners sexually were for the the around the and the number of sex partners sexually also with The in all these was remarkable a great the number of partners sexually reported by is an are more sexually with more people when they are However, the data suggest that there is a period in the number of sex partners sexually between and the are observed in all groups. 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