Lucia F O'Sullivan, Kimberly D Hearn
Rates of genital tract infections are currently at their highest levels in the USA and many other Western countries.1 Women in all societies have higher rates of sexually transmitted diseases than men, primarily because infections are more easily transmitted from men to women, especially young women.2 Moreover, greater proportions of women tend to be asymptomatic when infected and thus go undiagnosed and untreated. They are also more likely to experience severe health complications from infection. It is increasingly clear that female sexual dysfunction can occur secondary to medical problems (see Chapters 7.1—7.6 and 16.3-16.9 of this volume), such as urinary tract infections, sexually transmitted diseases, and human immunodeficiency virus infection.3-6 In this chapter, we summarize the current body of knowledge regarding sexual function and urinary tract infections, sexually transmitted diseases, and human immunodeficiency virus infection, in relation to disorders of desire, arousal, orgasm, and sexual pain. We then provide some treatment guidelines for health-care professionals interested in promoting sexual health among women.
Psychosocial and relational context
The Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV), of the American Psychiatric Association requires that a diagnosis of female sexual dysfunction be given if the disturbance “causes marked distress” and “interpersonal difficulty” (see Chapter 9.1). This criterion is particularly pertinent to women because, with relatively few exceptions, emotional and relational dynamics take on the most profound significance in diagnosing and treating urinary tract infections, sexually transmitted diseases, and human immunodeficiency virus infection and concomitant sexual dysfunctions. Although urinary tract infections appear to have more benign effects on female sexual dysfunction, women report considerable shame and degradation from diagnoses of sexually transmitted diseases, particularly human immunodeficiency virus.7,8 This connection between infections and female sexual dysfunction is related to the close associations with often socially undesirable activities and public or private acknowledgement of violations of societal expectations of sexual conduct. Furthermore, women are more susceptible to the repressive effects of such social constraints on sexuality than men.9 Women may be at risk of emotional, physical, or verbal abuse in their primary relationships upon disclosure of their infection or breakup once infection is discovered10,11 (see Chapter 3.4). Generally, women across societies tend to be penalized more severely on the basis of their sexual conduct and reproductive capacity than men, and so women suffer greater stigma and abuse as a result of infection10,11 (see Chapters 3.1-3.3).
Depression, shame, relationship conflict, and medical illness upon disclosure of infection within a relationship may make sexual interactions distressing and uncomfortable, leading at times to a diagnosis of sexual dysfunction.6 Emotional and relational issues significantly affect sexual arousal.12 Self-esteem, body image, and the quality of the relationship with a partner affect a woman’s ability to respond sexually.12 However, as key elements in the diagnosis of female sexual dysfunction are the persistent personal distress or interpersonal difficulties associated with these infections, the diagnosis of female sexual dysfunction is not appropriate in cases where disturbances occur inconsistently13 (see Chapters 9.2-9.5). For example, transient pain from intercourse during an outbreak of genital ulcers or a temporary aversion to sexual intercourse during peak infection with a bacterial sexually transmitted disease would not in themselves warrant a diagnosis of female sexual dysfunction.
Urinary tract infections
Urinary tract infection is one of the most common bacterial infections encountered in clinical practice in Western countries. In the USA, an estimated 34% of adults (20 or older) report at least one lifetime occurrence of urinary tract infection.14 Urinary tract infections are more common among women than among men (with a ratio of men to women of 1:3.9), although prevalence in elderly women and men is similar.15 Presentation can include different forms of cystitis, pyelonephritis, and urethral syndrome, with the most common complaints being dysuria and flank or back pain.16 Although there are a number of potential causes of urinary tract infection in women, risk factors include sexual intercourse, use of spermicidal products, and diaphragm use.17 For adolescents, urinary tract infections are frequently used as markers for sexual activity.18 Among older women, obstructing lesions, estrogen deficiency, and antibiotic exposure are more common causes.15 Uropathogenic Escherichia coli is the causative agent in the majority of cases. The urinary tract is armed with several specialized defenses against bacterial colonization, including glycosamines, low pH, and salts and urea that eliminate bacteria.19 However, significant proportions of patients have recurrent urinary tract infections, possibly linked to a persistent quiescent bacterial reservoir that establishes itself within the bacterial mucosa.20
One-third of women with an initial urinary tract infection have a recurrence, a third of these within the first 6 months.21 These women are believed to have an increased susceptibility to vaginal colonization with uropathogens, with a greater propensity for uropathogenic coliforms to adhere to uroepithelial cells.17 New approaches to prevent current urinary tract infection include the use of probiotics and vaccines. However, in a study of the E. coli urinary isolates from men with female partners suffering from urinary tract infection, urinary isolates were identical to the E. coli found in the urine or vagina of their sex partners.22 In fact, E. coli that caused urinary tract infection was nine times more likely than other E. coli to be shared by sex partners. Moreover, sharing was twice as likely if the couple had engaged in oral sex. Because sexual abstinence is unlikely among most women, particularly for those in an established sexual relationship, some place themselves at risk of recurrent infection. For women presenting a first urinary tract infection by E. coli, vaginal intercourse increased the risk of a second urinary tract infection with both a different and same uropathogen, as did using a diaphragm, cervical cap, and spermicide.23 These findings emphasize the importance of considering the context of sexual interactions and/or involving sexual partners and/or in developing a treatment plan.
Women experiencing urinary tract infections frequently experience dysuria, which is pain, burning, or discomfort on urination. They are likely to avoid sex before and during the treatment of a urinary tract infection because of severe discomfort or pain. Treatment typically comprises administration of antibiotics, though estrogen replacement therapy has been used in the past for postmenopausal women.24 Fortunately, treatment is typically rapid and highly effective. Intercourse while infected is often avoided at the recommendation of health-care providers until treatment is completed and because pelvic thrusting during sexual intercourse causes dyspareunia,12 potentially leading to an aversion to sexual experiences25 and strife between sexual partners. Educating and testing the patient and her partner or partners may go far to fortify treatment efforts and forestall the development of a chronic sexual dysfunction.
Sexually transmitted diseases
Clinical trial research on links between sexually transmitted diseases and female sexual dysfunction is in the earliest stages or nonexistent. There is some suggestion of links between sexually transmitted disease infection and sexual aversion disorder, which involves the persistent or recurrent phobic aversion to and avoidance of sexual contact with a partner.13 Sexual pain disorders may also be a logical link with sexually transmitted disease infection. Although there are a large number of asymptomatic cases, the most commonly presented symptoms among women with sexually transmitted diseases include lower abdominal pain, abnormal vaginal discharge, pain during sexual intercourse, painful micturition, vaginal itching, and genital ulcers. Each of these symptoms has clear implications for female sexual dysfunction, as described below.
For simplicity, sexually transmitted diseases can be classified as bacterial infections (gonorrhea, chlamydia, syphilis, and chancroid) and viral infections [herpes simplex virus (HSV), human papillomavirus, hepatitis B virus, and human immunodeficiency virus]. We briefly consider each of these in the sections below in terms of links to female sexual dysfunction. We consider the case of human immunodeficiency virus separately.
Rates of gonorrheal infection in the USA are the highest of all industrialized countries. Approximately 650000 cases occur each year.1 Rates declined steadily from the mid-1970s to 1990s, but increased again from 1997 through today. Infection is caused by the bacterium Neisseria gonorrhoeae and can lead to infection of the urethra, cervix, rectum, and throat. It invades epithelial cells, leaving the genital tract prone to infection by opportunistic aerobic and anaerobic bacteria.26 This sexually transmitted disease has an equal estimated male to female ratio.27 Gonorrhea is a major cause of pelvic inflammatory disease, infertility, and ectopic pregnancy among women. It also facilitates human immunodeficiency virus transmission.1 Although most infected women are asymptomatic, symptoms for women may include unusual vaginal discharge, painful and urgent urination, pain and bleeding during and after intercourse, and abdominal and pelvic pain. All of these symptoms can disrupt women’s sexual functioning.
Chlamydia is the most commonly reported infectious disease in the USA, with three million cases each year.28 It is caused by the bacterium Chlamydia trachomatis. Pathogenesis may be linked to a host cell-mediated immune response to a chlamydial heat- shock protein.26 From 1987 through 2002, the reported rate of chlamydial infection among women increased from 78.5 cases per 100000 to 455.5,29 though, probably as a result of improved screening and testing procedures. Reported 1995 rates reflected a male to female ratio for chlamydia infection of 1:5.6.2 Although easily treated with antibiotics, 75% of cases among women present no symptoms, and so the majority of these are left untreated.1 Clinical manifestations may be related to particular serovars: in one review, women who reported abdominal pain and/or dyspareunia were more often infected with serovar F.30 Forty per cent of women with untreated chlamydia develop pelvic inflammatory disease, with 20% of these women becoming infertile. Symptoms of chlamydia may include unusual vaginal discharge, bleeding after intercourse, abdominal pain, and dysuria. Chlamydia is also associated with ectopic pregnancy, inflamed rectum, and chronic pelvic pain,31 which can produce serious medical and psychologic consequences for women and their partners, and again disrupt sexual functioning.
Syphilis is a genital ulcerative disease caused by the bacterium Treponema pallidum, which appears to act by invading the intercellular junctions of endothelial cells. Rates of syphilis are at their lowest since 1941 (2.4 per 100000 population), although occasional spikes in recent years have been noted in association with human immunodeficiency virus coinfection among men.1 The male to female ratio is currently 3.5:1. Untreated syphilis can lead to cardiovascular and neurologic diseases, blindness, death, and perinatal death in 40% of cases among pregnant women. Syphilis is easily misdiagnosed because chancres in the primary stages may be painless and overlooked by the infected individual. Secondary syphilis involves a host of symptoms that may disappear and reappear over the first 2 years of the disease, including rash, fever, fatigue, hair loss, and swollen lymph glands. Early stages of infection are unlikely to interfere significantly with sexual function, especially if undiagnosed; however, later stages produce serious physical complications that must be treated medically to ensure survival.
Chancroid is caused by infection with the bacterium Haemophilus ducreyi, which produces a hemolysin implicated in the invasion of epithelial cells.32 Periodic outbreaks of chancroid have occurred in the USA, although this form of sexually transmitted disease is relatively rare outside of tropical and subtropical countries. In 1995, there were only seven new cases.14 Infection begins with the appearance of painful sores on the genitals and is sometimes accompanied by swelling of lymph nodes in the groin.14 Among women, symptoms are typically limited to painful urination or defecation, painful intercourse, rectal bleeding, or vaginal discharge. Chancroid lesions are sometimes mistaken for genital ulcers from herpes simplex virus or syphilis infection, and, like these infections, are associated with increased risk of human immunodeficiency virus infection unless treated.33 These symptoms, coupled with the distress of a chancroid outbreak, can interfere with sexual functioning.
As a family of infections, viral forms are the most serious in many respects, as they are treatable, but not curable. For sexually active individuals, there are almost no established methods of prevention beyond the condom, which is far less effective with viral forms than with bacterial forms of sexually transmitted diseases.34 It is important to note that, although condoms are the best-known means of preventing infection with sexually transmitted diseases, other than total abstinence, use requires the cooperation of the male partner. Yet, the majority of men report resisting its use,35 and studies consistently reveal incomplete or inaccurate use throughout intercourse,36 reducing its prophylactic utility.
Herpes simplex virus
Genital herpes-herpes simplex virus type two (herpes simplex virus 2) infects one million people in the USA each year, most often adolescents and young adults.1 After the patient recovers from the primary infection, the virus remains latent in sensory ganglia of the peripheral nervous system37 and can cause disease by reactivation.38 This disease can be fatal among newborns and those with human immunodeficiency virus.1 Although approximately 25% of US women and 20% of US men test positive for herpes, less than 10% of those infected are aware that they are infected.1 Like the bacterial infections, herpes simplex virus can make the patient more susceptible to human immunodeficiency virus infection, and it makes human immunodeficiency virus- infected individuals more infectious to those not yet infected - an issue of particular importance in serodiscordant couples. Prompt treatment can abort painful genital herpes simplex virus reactivation episodes, once individuals learn to recognize the onset of symptoms.39 Superficial pain from genital herpes outbreaks12 and the stigma attached to this infection40 (which is considerable) may contribute to the development of female sexual dysfunction. In particular, individuals report strained relationship dynamics when partners have to abstain from sexual interactions during periodic outbreaks.41
In 1999, 5.5 million people in the USA acquired human papillomavirus,1 making it the most common sexually transmitted disease in the country. Recent Centers for Disease Control and Prevention research found that 72% of adolescent women at a public, sexually transmitted disease clinic had high-risk human papillomavirus strains;42 these strains have caused considerable concern because of their links to cervical cancer.43,44 Human papillomavirus sometimes causes genital warts, but in many cases is asymptomatic. Genital warts can be treated and cured, but subclinical human papillomavirus infection is much more common and is incurable at this time. Human papillomaviruses are intraepithelial pathogens.45 They induce benign lesions on mucocutaneous surfaces that are chronic persistent growths, some of which may progress to malignancy. Infection with human papillomavirus is strongly associated with experience of vulvar vestibulitis syndrome, a disorder characterized by extreme vaginal pain and pain during intercourse.46
Hepatitis B virus
The incidence rate of acute hepatitis B in 2001 was 2.8/100000 in the population, with a male to female ratio of 1.8:1/ Unlike the other sexually transmitted diseases, infection is likely to occur through means other than sexual contact; most cases of hepatitis B virus infection are acquired through intravenous drug use. It remains one of the most serious forms of sexually transmitted diseases, however. Although the pathogenesis of this virus remains unclear, infection with hepatitis B virus is clearly implicated in liver pathogenesis. Death from chronic liver disease occurs in 15-25% of infected persons. In addition, chronic hepatitis B virus infection has a high risk of hepatocellular carcinoma.47 Although a vaccine is available, there are a number of barriers to its uptake, including low awareness of its availability, high cost, and few recommendations for its use by health-care providers.48 Approximately 30% of infected persons have no symptoms, although symptoms can include jaundice, fatigue, abdominal pain, joint pain, nausea, and vomiting.1 Implications for female sexual dysfunction relate most directly to the seriousness of medical complications associated with infection.
Human immunodeficiency virus
Organic causes of sexual dysfunctions are generally temporary and easily treatable, compared with psychologic causes such as intrapersonal and interpersonal conflict. However, human immunodeficiency virus represents a notable exception by virtue of being a chronic infection that may lead to acquired immune deficiency syndrome, and which until the recent advent of antiretroviral treatment programs meant the eventual death of the infected person. The reduction in acquired immune deficiency syndrome rates due to advances in treatment has led many to conclude mistakenly that human immunodeficiency virus rates are also drastically reduced. In fact, rates of human immunodeficiency virus infection have been steadily increasing, especially among women.49 For example, in a prospective study of human immunodeficiency virus serodiscordant couples, women were 17.5 times more likely to seroconvert than comparably exposed seronegative men.50 Use of highly active antiretroviral therapy has led to an increase in the pool of surviving human immunodeficiency virus-infected individuals.51 With unprotected sexual intercourse between women and men the predominant mode of transmission,52 the implications for the field of sexual health cannot be understated.
Infection occurs when human immunodeficiency virus binds to the T-lymphocyte surface antigen CD4 and enters the cell.53 Viral RNA undergoes reverse transcription, which produces double-stranded viral DNA that is then incorporated into the host DNA. Viral replication results in a reduced CD4 count and eventual defeat of the individual’s immune system. Today, infection with human immunodeficiency virus requires close medical supervision and often complicated treatment regimens that may help to extend the life of an individual indefinitely. Not all people infected with human immunodeficiency virus, however, have access to these treatments or adhere properly to them if available (introducing the possibility of the emergence of resistant strains54). Oddly, despite widespread media coverage and educational programs associated with the onset of the human immunodeficiency virus epidemic, most individuals believe that they personally are at little to no risk of infection or are reluctant to be tested, in large part because of the emotional impact of the diagnosis.55
There are important links between the broader family of sexually transmitted diseases and human immunodeficiency virus. Risk of infection by human immunodeficiency virus and other sexually transmitted diseases increases as the number of sexual partners and frequency of unprotected sex increase. Sexually transmitted diseases also place women at greater risk of human immunodeficiency virus infection than men.56 In a study comparing human immunodeficiency virus-positive and human immunodeficiency virus-negative women, those infected with human immunodeficiency virus were more likely to report a history of other types of sexually transmitted diseases.57 Both human immunodeficiency virus status and CD4 lymphocyte count were associated with evidence of genital ulcers, genital warts, and vaginal candidiasis. Moreover, CD4 lymphocyte depletion was closely related to chronic viral infections.
As with studies of other types of sexually transmitted diseases, clinical trial research and reports on the medical management of infection and sexual dysfunction center almost exclusively on men.58
Studies directly assessing relationships between human immunodeficiency virus infection and sexual dysfunction are relatively rare, and those that exist typically do not include women.59 However, there are notably more studies than those addressing other sexually transmitted diseases. The most common sexual dysfunctions in women generally (loss of desire, anorgasm, and dyspareunia) are also the most common among human immunodeficiency virus-infected women.58,60-62 Hypoactive sexual desire disorder emerged as the most prevalent psychiatric diagnosis in a study of human immunodeficiency virus-seropositive women.63 The symptoms were not a subset of mood or anxiety disorders, and most described significant negative effects on their quality of life and intimate relationships. Moreover, candidal and herpetic vulvovaginitis is common among infected women, as is pelvic inflammatory disease, leading to deep dyspareunia, and thus further avoidance of sexual intimacy. Human immunodeficiency virus-positive women may also have altered body image, as a result either of weight loss or redistribution of fat associated with lipodystrophy, or of the fatigue, wasting, and pain that are associated with advanced stages of the disease.58
Psychologic distress (e.g., depression, anxiety) secondary to the infection may exacerbate sexual dysfunction64 (see Chapter 16.2). Newly diagnosed individuals cite a decrease in sexual interest and avoidance of sexual intimacy for fear of transmitting human immunodeficiency virus to their sexual partners.65 Sexual dysfunction that is associated with medication regimens for acquired immune deficiency syndrome and/or depression may also occur. Several researchers have reported that the use of protease inhibitors is associated with a decrease in sexual desire and arousal.61,62,66 For example, in a study of 904 human immunodeficiency virus-positive women and men receiving antiretroviral therapy, 29% of the women in the sample reported a decrease in sexual interest.62 The reported decrease in sexual interest was significantly higher in those individuals whose treatment included protease inhibitors than in those not receiving protease inhibitors. Declining sexual interest was also associated with symptomatic versus asymptomatic human immunodeficiency virus infection.
Because of the high rates of genital tract infections among women, inquiries about female sexual health should be integrated into routine gynecologic care. Although women infected with urinary tract infections, sexually transmitted diseases, and possibly human immunodeficiency virus may present with gynecologic, urologic, or obstetric issues, there are often clear psychologic and relational implications in the forefront of these diagnoses. The psychologic and interpersonal domains may interact with the physical and biologic to hinder early diagnosis and intervention while complicating treatment options, compliance, and ultimately prognosis.
Although female sexual disorders are broadly conceptualized to encompass disorders of desire, arousal, or orgasm, as well as pain, many women present special concerns that center on problems of experience and expression of passion, communication, nongenital touching, and affection.67 These should be considered integral components of the female sexual function evaluation, as should an individual’s experience of her sexuality, self-esteem, and body image.3 Women presenting common symptoms relating to genital tract infections, namely, vaginal discharge, genital lesions, and abdominal or pelvic pain, are probably first seen at primary health care and family planning clinics. Although the clinical picture and pathology of these infections are well known, the profound impact of these diseases on women’s sexual health, and ultimately their physical and psychologic well-being, especially their self- and sexual selfesteem, needs further investigation.
To improve women’s sexual health, physicians should receive formal training in sexual functioning to become competent in the first-level medical diagnosis of both gynecologic problems and female sexual dysfunction, and in developing treatment and prevention protocols. This approach should include obtaining a complete patient history, conducting a physical examination, applying treatment, providing education, and offering appropriate referrals.68 If possible, a comprehensive evaluation of both the woman and her sexual partner or partners should be conducted before formulating a treatment plan,69 as long as this puts the woman’s safety at no risk. Ideally, a comprehensive approach involving education and reassurance in a collaboration between physician and therapist would help provide a complete treatment addressing both the medical and psychosocial consequences of infection.12,70
1. Centers for Disease Control and Prevention (CDC). Tracking the Hidden Epidemics 2000: Trends in STDs in the United States (accessed 30 April 2004 at www.cdc.gov/nchstp/od/news/).
2. Aral SO, Gorbach PM. Sexually transmitted infections. In GM Wingood, RJ DiClemente, eds. Handbook of Women’s Sexual and Reproductive Health. New York: Kluwer Academic/Plenum, 2002: 255-79.
3. Goldstein I. Female sexual arousal disorder: new insights. Int J Impot Res 2000;12(Suppl 4): S152-7.
4. Berman LA, Berman JR, Chhabra S et al. Novel approaches to female sexual dysfunction. Expert Opin Investig Drugs 2001; 10: 85-95.
5. Morley JE, Kaiser FE. Female sexuality. Med Clin North Am 2003; 87: 1077-90.
6. Shifren JL. The role of androgens in female sexual dysfunction. Mayo Clin Proc 2004; 79(Suppl 4): S19-24.
7. Lee RS, Kochman A, Sikkeman KJ. Internalized stigma among people living with HIV-AIDS. AIDSBehav 2002; 6: 309-19.
8. Rotheram-Borus M. Variations in perceived pain with emotional distress and social identity in AIDS. AIDS Patient Care STDS 2000; 14: 659-65.
9. Bancroft J. The medicalization of female sexual dysfunction: the need for caution. Arch Sex Behav 2002; 31: 451-5.
10. El-Bassel N, Gilbert L, Rajah V et al. Fear and violence: raising the HIV stakes. AIDS Educ Prev 2000; 12: 154-70.
11. El-Bassel N, Witte SS, Gilbert L et al. HIV prevention for intimate couples: a relationship-based model. Fam Sys Health 2001; 19: 379-95.
12. Berman JR, Bassuk J. Physiology and pathophysiology of female sexual function and dysfunction. WoMhlUoL 2002; 20: 111-18.
13. Basson R, Berman J, Burnett A et al. Report of the International Consensus Development Conference on female sexual dysfunction: definitions and classifications. J Urol 2000; 163: 888-93.
14. NIH. Health matters: STDs. Issued by the National Institute of Allergy and Infectious Disease (accessed 22 April 2004 at www.niaid.nih.gov/factsheets/stdother.htm).
15. Harrington RD, Hooton TM. Urinary tract infection risk factors and gender. J Gend Specif Med 2000; 3: 27-34.
16. Abrahamsson K, Hansson S, Jodal U et al. Staphylococcus sapro- phyticus urinary tract infections in children. Eur J Pediatr 1993; 152: 69-71.
17. Hooton TM. Recurrent urinary tract infections in women. Int J Antimicrob Agents 2001; 17: 259-68.
18. Weir M, Brien J. Adolescent urinary tract infections. Adoles Med State Art Rev 2000; 11: 293-313.
19. Kucheria R, Sheerin NS, Dasgupta P et al. Urinary tract infections: advances and new therapies. BJU Int 2004; 93: 690-1.
20. Mulvey MA, Joel SD, Hultgren SJ. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 2001; 69: 81-90.
21. McLaughlin SP, Carson CC. Urinary tract infections in women. Med Clin North Am 2004; 88: 417-29.
22. Foxman B, Manning SD, Tallman P et al. Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. AmJEpdmo 2002; 156: 1133-40.
23. Foxman B, Gillespie B, Koopman J et al. Risk factors for second urinary tract infections among college women. Am J Epidemiol 2000; 151: 1194-1205.
24. Stapleton A, Stamm WE. Prevention of urinary tract infection. Infect Dis Clin North Am 1997; 11: 719-33.
25. Arcos B. Female sexual function and response. J Am Osteopath Assoc 2004; 104(Suppl 1): S16-20.
26 Mann SN, Smith JR, Barton SE. Pelvic inflammatory disease. IntJ STD AIDS 1996; 7: 315-21.
27. Aral SO, Holmes KK. Social and behavioral determinants of the epidemiology of STDs: industrialized and developing countries. In Holmes KK, Sparling PF, Mardh PH et al. , eds. Sexually Transmitted Diseases. New York: McGraw-Hill, 1999: 39-76.
28. Cates W. Estimates of the incidence and prevalence of sexually transmitted diseases in the United States. Sex Transm Dis 1999; 26(Suppl 4): S2-7.
29. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2002 Supplement Report: Chlamydia Prevalence Monitoring Project. Division of STD Prevention, October 2003.
30. Geisler WM, Suchland RJ, Whittington WL et al. The relationship of serovar to clinical manifestations of urogenital Chlamydia trachomatis infection. SexTmnmDis. 2003; 30: 160-5.
31. Cohen CR, Brunham RC. Pathogenesis of Chlamydia-induced pelvic inflammatory disease. SexTran^mInfect 1999; 75: 21-4.
32. Wood GE, Dutro SM, Totten PA. Target cell range of Haemophilus ducreyi hemolysin and its involvement in invasion of human epithelial cells. Infect Immun 1999; 67: 3740-9.
33. Lewis DA. Chancroid: from clinical practice to basic science. AIDS Patient Care STDs 2000; 14: 19-36.
34. Wilson TE, Jaccard J, Levinson RA et al. Testing for HIV and other sexually transmitted diseases: implications for risk behavior in women. Health Psychol 1996; 15: 252-60.
35. VanOss Marin B, Tschann JM, Gomez CA et al. Self-efficacy to use condoms in unmarried Latino adults. Am J Community Psychol 1998; 26: 53-71.
36. Lee DJ, Clarke J. Cover it up or cool it? Sexual intercourse during therapy for bacterial sexually transmitted infections - a discussion for evidence for efficacy of condom use preventing transmission during an acute bacterial STI. Int J STD AIDS 2004; 15: 285-8.
37. Blondeau JM, Embil JA, McFarlane ES. Herpes simplex virus infections in male and female mice following pinna inoculation: responses to primary infection and artificially induced recurrent disease. JMedViol 1989; 29: 320-6.
38. Steiner I, Kennedy PG. Herpes simplex virus latent infection in the nervous system. J Neurovirol 1995; 1: 19-29.
39. Strand A, Patel R, Wulf HC et al. Aborted genital herpes simplex virus lesions: findings from a randomized controlled trial with valaciclovir. S^xTran^nJ^[e£t 2002; 78: 435-9.
40. Lee JD, Craft, EA. Protecting one’s self from a stigmatized disease ... once one has it. DeSOSlBehOX 2002; 23: 267-99.
41. Mirotznik J, Shapiro RD, Steinhart JE et al. Genital herpes: an investigation of its attitudinal and behavioral correlates. J Sex Res 1987; 23: 266-72.
42. Samoff E. Incidence, clearance and persistence of HPV in a cohort of female adolescents. Paper presented at the 2004 National STD Prevention Conference, March, 2004.
43. Phillips Z, Johnson S, Avis M et al. Human papillomavirus and the value of screening: young women’s knowledge of cervical cancer. Health Educ Res 2003; 18: 318-28.
44. Waller J, McCaffery KJ, Forrest S et al. Human papillomavirus and cervical cancer: issues for biobehavioral and psychosocial research. AnnBehavMed 2004; 27: 68-79.
45. Stanley M, Coleman N, Chambers M. The host response to lesions induced by human papillomvirus. Ciba Found Symp 1994; 187: 21-32.
46. Sarma AV, Foxman B, Bayirli B et al. Epidemiology of vulvar vestibulitis syndrome: an exploratory case-control study. Sex Transm Infect 1999; 75: 320-6.
47. He QY, Lau GK, Zhou Y et al. Serum biomarkers of hepatitis B virus infected liver inflammation: a proteomic study. Proteomics 2003; 3: 666-74.
48. Ganguly R, Banerji M. Hepatitis B virus infection and vaccine acceptance among university students. Am J Health Behav 2000;
49. UNAIDS. 2004 Report on the global AIDS epidemic. Geneva: Joint United Nations Program on HIV/AIDS, July 2004.
50. Padian N, Shiboski S, Jewell N. Female-to-male transmission of human immunodeficiency virus. JAMA 1991; 266: 1664-7.
51. Palella FJ, Delaney KM, Moorman AC. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998; 338: 853-60.
52. World Health Organization. The World Health Report 2004 - Changing History. Geneva: World Health Organization, May 2004 (accessed 22 June 2004 at www.who.int/whr).
53. Lee LK, Dinneen MD, Ahmad S. The urologist and the patient infected with human immunodeficiency virus or with acquired immunodeficiency syndrome. BJU International 2001; 88: 500-10.
54. Leigh Brown AJ, Frost SD, Mathews WC et al. Transmission fitness of drug-resistant human immunodeficiency virus and the prevalence of resistance in the antiretroviral-treated population. J Infect Dis 2003; 187: 683-6.
55. Steinbrook R. The AIDS epidemic in 2004. N Engl J Med 2004: 351: 115-17.
56. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75: 3-17.
57. Greenblatt RM, Bacchetti P, Barkan S et al. Lower genital tract infections among HIV-infected and high-risk uninfected women: findings of the Women’s Interagency HIV Study (WIHS). Sex Transm Dis 1999; 26: 143-51.
58. Hijazi L, Nandwani R, Kell P. Medical management of sexual difficulties in HIV-positive individuals. Int J STD AIDS 2002; 13: 587-92.
59. Collazos J, Martinez E, Mayo J et al. Sexual dysfunction in HIV- infected patients treated with highly active antiretroviral therapy. JAçquiiJmmu£e.DeÊ£SnàL 2002; 31: 322-6.
60. Brown GR, Kendall S, Ledsky R. Sexual dysfunction in HIV- seropositive women without AIDS. J Psychol Human Sex 1995; 7:73- 97.
61. Nusbaum MRH, Hamilton C, Lenahan P. Chronic illness and sexual functioning. Am Fam Physician 2003; 67: 347-54.
62. Schrooten W, Colebeunders R, Youle M et al. Sexual dysfunction associated with protease inhibitor containing highly active antiretroviral treatment. AIDS 2001; 15: 1019-23.
63. Brown GR, Rundell JR. A prospective study of psychiatric aspects of early HIV disease in women. Gen Hosp Psychiatry 1993; 15: 139-47.
64. Anastasiadis AG, Davis AR, Ghafar MA et al. The epidemiology and definition of female sexual disorders. World J Urol 2002; 20: 74- 8.
65. Green G. The reproductive careers of a cohort of men and women following HIV-positive diagnosis. J Biosoc Sci 1994; 26: 409-15.
66. Martinez E, Collazos J, Mayo J et al. Sexual dysfunction with protease inhibitors. Lancet 1999; 353: 810-11.
67. Leiblum SR. Definition and classification of female sexual disorders. Int J Impot Res 1998; 10(Suppl 2): S104-6.
68. Phillips NA. Female sexual dysfunction: evaluation and treatment. Am Fam Physician 2000; 62: 127-36.
69 Leiblum SR, Weigel, M. Psychotherapeutic interventions for treating female sexual dysfunction. World J Urol 2002; 20: 127-36.
70. Berman JR, Goldstein I. Female sexual dysfunction. Urol Clin North Am 2001; 28: 405-16.