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Sexually Transmitted Diseases:
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The History of Nongonococcal Urethritis: Thomas Parran Award Lecture

TAYLOR‐ROBINSON, DAVID

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From the MRC STD Research Group, The Jefferiss Wing, Imperial College School of Medicine at St Mary's, London, United Kingdom

Correspondence: David Taylor‐Robinson, MRC STD Research Group, The Jefferiss Wing, Imperial College School of Medicine at St Mary's, London W2 1NY, United Kingdom.

IT IS A GREAT HONOR to be invited to New Orleans to receive the Thomas Parran Award of the American Venereal Disease Association. I am particularly appreciative because I am not a native of the United States, although I have made many visits and spent sabbatical periods in this country. Indeed, it is here in the 1960s that I first began to work on sexually transmitted organisms and, in an indirect way, on nongonococcal urethritis (NGU), a subject pursued ever since and, hence, the reason for my discussion of the disease.

Thomas Parran, who lived from 1892 to 1968, was an epidemiologist who joined the United States Public Health Service in 1917 and was Surgeon General of this organization from 1936 to 1948. It was his dedicated efforts that were instrumental in bringing about the control of syphilis in the United States which, after the first World War and in the 1920s and 1930s, had escalated to become a major public health problem. In comparison, NGU paled into insignificance, although during the lifetime of Thomas Parran there were a number of landmark events in our understanding of this disease.

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Early History of NGU

Gonorrhea simplex was distinguished from Gonorrhea virulenta in the 18th century, an indication that even at that time there was an appreciation of the existence of two different sorts of disease. However, it was not until after 1879, the time when Neisser discovered the gonococcus, that the term “urethritis non‐gonorrhoica” was coined.1 In 1904, Ludwig Waelsch described mild nongonococcal urethritis and said it was difficult to cure,2 a clinical comment well appreciated to this day. The first event in understanding the microbial etiology of NGU may be traced back to 1903 when Neisser, who was interested in doing experimental work on syphilis in monkeys, made an expedition to Java. He took with him Ludwig Halberstaedter and Stanislaus von Prowazek who, not much to Neisser's liking, inoculated the eyes of orangutans with trachoma material and found that they developed conjunctival inclusions.3 Later, similar inclusions recognized as being caused by an infectious agent, which was at first named Chlamydozoa, were found in what is now a familiar triad, namely the conjunctiva of infants, the cervix of mothers, and the urethral scrapings from male partners with NGU, or in what was called, at that time, Waelsch urethritis. In the 1930s and later, Philip Thygeson and others in the United States confirmed the baby—mother—NGU relationship.4 In the United Kingdom in the 1940s, Arthur Harkness, a venereologist working at a urological center in London and a contemporary of Thomas Parran, undertook a comprehensive reappraisal of NGU which, embodied in a monograph published in 1950,5 reawakened interest in the condition. His observations confirmed that chlamydial organisms had an important role although, of course, they had not yet been isolated and Harkness did not have the techniques that became available later to look at this relationship.

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Further Work on Chlamydia trachomatis

It was, in fact, 1957 when T'ang and colleagues6 in China reported that they had isolated chlamydial agents in embryonated hen eggs. This set in motion a chain of events in the detection of Chlamydia trachomatis, as the agent became known, which have now culminated in the development and use of the ligase chain reaction for diagnosis,7 a diagnosis not only of chlamydial infection in NGU but, perhaps even more important, in diseases in women. The journey from embryonated egg to the ligase chain reaction has embraced an enormous amount of work involving tissue cell culture, enzyme immunoassay, fluorescence, and molecular techniques.8 It is to be hoped that the promise of and expectations for the ligase chain reaction assay will be realized fully. At the same time, the current wave of enthusiasm for molecular techniques and the appreciation that cell culture is far less sensitive than most have realized should not lead to denigration of the latter technique, for it has been the bedrock on which most of our understanding of chlamydial infection in NGU and other conditions has been based.

My introduction to the topic of NGU, although I did not think about it in this way at the time, came in the early 1960s, during a sabbatical in the United States in Robert Chanock's Laboratory of Infectious Diseases at the National Institutes of Health. Here, I became familiar with the ureaplasmas9 that, at the time, were called T‐strains. In late 1965, after returning to the United Kingdom, I began to collaborate with Eric Dunlop at the London Hospital who, with Barrie Jones, had been the first to isolate C. trachomatis from men with NGU.10 As in other developed countries, in the United Kingdom in the 1970s and 1980s, the number of cases of NGU increased dramatically, always outstripping cases of Gonorrhea, until a peak was achieved about 1986–1987 followed apparently by a decline.11 My own group became involved in detecting chlamydial infections in the early 1970s and subsequently have undertaken numerous studies12–25 (Table 1) on patients with NGU attending genitourinary medicine clinics at Watford, Central Middlesex, and St. Mary's hospitals. The proportion of NGU patients who have had a chlamydial infection has varied from 31% to 49%, but overall it has been approximately 40% and has not decreased (Table 1). This is not in accord with the findings at another genitourinary medicine clinic in London where the proportion of individuals with chlamydial NGU has declined.26 The reason(s) for the discrepancy are not clear. What is clear, however, is that at both these clinics, as at others, there is a large segment of NGU that appears to be nonchlamydial, that is, it is larger in homosexual than in heterosexual men,27 and there has been controversy and doubt about its etiology. Although the evidence implicating C. trachomatis organisms as a cause of NGU seems to be overwhelming,28–31 recovery of the organisms from a patient does not necessarily mean that they are the cause, despite the fact that there is hardly ever any thought to the contrary. Furthermore, failure to recover C. trachomatis organisms does not necessarily mean that the disease is nonchlamydial, although to extend this notion to the point of never looking for alternatives would seem to be obtuse. This has not been the case, and outside a minor role for Trichomonas vaginalis, yeasts, and herpes simplex virus,29–31 attention has been paid to Ureaplasma urealyticum, and more recently to Mycoplasma genitalium and the bacteria involved in bacterial vaginosis.

Table 1
Table 1
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The Role of Ureaplasma urealyticum Organisms

As mentioned earlier, these organisms were at one time called T‐strains by Maurice Shepard, who isolated them in the United States in the early 1950s from men with or without NGU.32 This terminology was used because the organisms produced very small colonies on agar (T means tiny) compared with the much larger “fried‐egg”‐type colonies produced by other mycoplasmas. Only later, when the T‐strains or T‐mycoplasmas as they were also called, were found to be unique in metabolizing urea,9 were they ascribed to the genus and species U. urealyticum33 and called ureaplasmas trivially. Results of some of the earlier studies indicated that ureaplasmas occurred in men with NGU more often than in men without NGU, whereas in other studies no difference was seen between the two groups34; the lack of difference also pertained to a study of men with or without postgonococcal urethritis.35 As a result of the uncertainty about the role of ureaplasmas, I felt that experimental inoculation of the human urethra might be helpful in resolving the issue, and I persuaded my colleague George Csonka to join me in such a venture.36 Thus, in an experiment that was not undertaken lightly, 5 × 104 organisms of a cloned culture of U. urealyticum were inoculated intraurethrally. This was followed by urethral symptoms, the finding of leukocytes in the urine, polymorphonuclear leukocytes in the centrifuged deposit of first‐pass urine samples, and shedding of the organisms. Treatment with minocycline after 6 days resulted in gradual resolution of the symptoms and signs and eradication of the organisms from first‐pass urine samples. One virtue of such a “volunteer” experiment is that there is a fairly clear knowledge of what is being received. On the other hand, there should be caution in not overinterpreting observations based on a small experiment. Furthermore, it is worth reflecting on volunteer experiments in which Mycoplasma hominis, inoculated intranasally and orally, unquestionably caused sore throats with an exudative pharyngitis37; yet, subsequently, this mycoplasma has not been shown to cause sore throats in the wider population.38 It is of added interest, therefore, that ureaplasmas have been shown to cause urethritis in volunteer experiments in Germany40 Furthermore, the intraurethral inoculation of male chimpanzees with ureaplasmas (105 organisms) has resulted in some of them developing urethritis with shedding of the organisms41 and a greater than fourfold antibody response—features that, apart from the latter, responded to tetracycline therapy. Results of studies in which “differential” antibiotics have been given to subjects with NGU14,42 also have been supportive of a role for ureaplasmas in the disease, assuming that the antibiotic in question allows growth only of the ureaplasmas and not of some unknown agent; this, of course, cannot be guaranteed. Overall, however, there is considerable evidence that ureaplasmas are pathogenic, although for what proportion of NGU they might be responsible is unclear and still a matter of speculation. What seems much more clear is that not all cases of NGU are caused by C. trachomatis or U. urealyticum.30 This view is supported by the fact that many men who have NGU from which these microorganisms cannot be recovered still respond to treatment with tetracyclines or erythromycin, suggesting the possible existence of another agent susceptible to such antibiotics.

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The Role of Mycoplasma genitalium

Table 2
Table 2
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Whether spiroplasmas might be involved in causing NGU was a thought I had in the late 1970s. I had looked at discharges from men with NGU in wet preparations microscopically and had wondered whether some motile spiral forms might be such organisms. A spiroplasma is a motile mycoplasma with a helical structure found in plants and insects; Spiroplasma citri was the first to be isolated.43 The possibility of a human counterpart took me to Joseph Tully's laboratory at the National Institutes of Health with urethral specimens from 13 men with acute NGU. These specimens were inoculated into SP4 medium, which had been developed by Tully and colleagues44 for isolating spiroplasmas and was helpful in isolating other mycoplasmas, too. This resulted approximately a month later in an acidic color change in the medium containing two of the specimens. This color change was subculturable, and examination of the medium by electron microscopy revealed flask‐shaped structures45,46 akin, morphologically and in some other respects, to Mycoplasma pneumoniae, one of the established causes of primary atypical pneumonia in humans. The isolate was certainly not a spiroplasma and later it was called M. genitalium.47 Its inoculation intraurethrally into male chimpanzees resulted, as with the ureaplasmas, in development of urethritis in most of them, together with an antibody response.48,49 However, after the original isolation of the mycoplasma from men with NGU, the energetic attempts of several groups failed to repeat the findings, and it was not until the advent of molecular probes50 that further progress was made.51 This became rapid with the use of the polymerase chain reaction. In my group, Helen Palmer and Claire Gilroy developed such a technique,52 as did others.53 In men attending the genitourinary medicine clinic at St. Mary's Hospital, not only was C. trachomatis detected significantly more often in those with NGU than in those without the disease, but, by use of the polymerase chain reaction, M. genitalium was detected significantly more often, too, independently of C. trachomatis.24 Similar observations were made in Denmark,54 and subsequently in Japan,55 France,56,57 and the United States.58 Recently, through collaboration with Shyh Lo (Armed Forces Institute of Pathology, Washington), antibody to M. genitalium, measured by an enzyme‐linked immunosorbent assay technique, has been found significantly more often in men who are mycoplasma polymerase chain reaction‐positive than in those who are not. The evidence that M. genitalium is involved in acute NGU and in other conditions59 is mounting.

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Possible Role of Bacteria Associated With Bacterial Vaginosis

The possible association of bacterial vaginosis (BV) with NGU is worth consideration. In brief, BV is a condition in which lactobacilli that are dominant in the healthy vagina decrease in number, often to the point of disappearance, and several bacterial species that are present normally in small numbers increase, perhaps 1000‐ to 10,000‐fold.60 In this situation, the chance of these organisms gaining access to the male urethra and possibly causing a reaction by virtue of virulence factors is much increased. With this in mind, Frances Keane in my group has been studying disease in couples. So far, of men who had NGU, 31% of their female partners had BV, whereas of men without NGU, only 8% of their partners had BV; the association was a little stronger in chlamydia‐negative couples. Obtaining the male partners of women with BV is much more difficult to achieve, but, again, there appears to be a relationship in that women who suffered from BV were more likely to have a partner with NGU than were those without BV. This is a continuing area of investigation that may be important in explaining the occurrence of NGU in apparently stable relationships and may provide further rationale to that already existing62 for the occasional use of metronidazole in treating NGU that does not respond to tetracycline or erythromycin. Furthermore, because ureaplasmas are to some extent associated with BV, it is interesting to speculate that their association with NGU might be as much through the possible association of BV with NGU as through an independent association.

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Acknowledgments

I would like to thank my colleagues and numerous collaborators over the years who have contributed so much to the studies I have mentioned; without them, I would not be here today. I also thank my family, who have given me so much support over the years. They have also provided a useful break and brought me down to earth when there have been signs of over‐cockiness. In this regard, I recently had a fax from my son, Andrew, in Glasgow. It read “I thought I'd send you this pic, because when I saw it it reminded me of you.” I turned to the cartoon on the next page with trepidation to find the following: The doctor is saying to an old and somewhat deaf man “I need you to give me a urine, blood, semen and stool sample, Mr. Sproggett” and Mr. Sproggett turns to his wife, saying: “What did he just say?” and she retorts, “He told you to leave your underpants at reception.” I have yet to find out whether I am supposed to be the doctor or Mr. Sproggett, although I have my suspicion! It had not occurred to me before that a piece of clothing subjected to modern, highly sensitive molecular techniques might be an extremely good noninvasive sample, not only for the study of NGU, but for other conditions, too. Is it beyond the realm of imagination that the future will see studies of this kind?

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International Journal of Std & AIDS
Genital mycoplasmas, including Mycoplasma genitalium, as sexually transmitted agents
Uuskula, A; Kohl, PK
International Journal of Std & AIDS, 13(2): 79-85.

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Idiopathic Urethritis in Young Men in the United States: Prevalence and Comparison to Infections with Known Sexually Transmitted Pathogens
Wetmore, CM; Manhart, LE; Golden, MR
Journal of Adolescent Health, 45(5): 463-472.
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Drugs
Concurrent gonococcal and chlamydial infection - How best to treat
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Drugs, 59(4): 801-813.

Journal of Clinical Microbiology
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Yoshida, T; Maeda, S; Deguchi, T; Miyazawa, T; Ishiko, HR
Journal of Clinical Microbiology, 41(5): 1850-1855.
10.1128/JCM.41.5.1850-1855.2003
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Clinical Infectious Diseases
Role of Mycoplasma genitalium and Ureaplasma urealyticum in acute and chronic nongonococcal urethritis
Horner, P; Thomas, B; Gilroy, CB; Egger, M; Taylor-Robinson, D
Clinical Infectious Diseases, 32(7): 995-1003.

Lancet
Update on sexually transmitted mycoplasmas
Taylor-Robinson, D; Furr, PM
Lancet, 351(): 12-15.

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Taylor-Robinson, D; Gilroy, CB; Jensen, JS
Venereology-the Interdisciplinary International Journal of Sexual Health, 13(3): 119-127.

Clinics in Geriatric Medicine
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Clinics in Geriatric Medicine, 19(3): 637-+.
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Sexually Transmitted Diseases
Errata

Sexually Transmitted Diseases, 23(2): 170.

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Sexually Transmitted Diseases
Antibodies to Chlamydia trachomatis Heat-Shock Protein 60 kDa and Detection of Mycoplasma genitalium and Ureaplasma urealyticum Are Associated Independently With Chronic Nongonococcal Urethritis
HORNER, P; THOMAS, B; GILROY, C; EGGER, M; MCCLURE, M; TAYLOR-ROBINSON, D
Sexually Transmitted Diseases, 30(2): 129-133.

PDF (179)
Sexually Transmitted Diseases
Association of Ureaplasma urealyticum (Biovar 2) With Nongonococcal Urethritis
Deguchi, T; Yoshida, T; Miyazawa, T; Yasuda, M; Tamaki, M; Ishiko, H; Maeda, S
Sexually Transmitted Diseases, 31(3): 192-195.

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Sexually Transmitted Diseases
Quantitative Detection of Ureaplasma parvum (biovar 1) and Ureaplasma urealyticum (biovar 2) in Urine Specimens from Men With and Without Urethritis by Real-Time Polymerase Chain Reaction
Yoshida, T; Deguchi, T; Meda, S; Kubota, Y; Tamaki, M; Yokoi, S; Yasuda, M; Ishiko, H
Sexually Transmitted Diseases, 34(6): 416-419.
10.1097/01.olq.0000243621.89212.40
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Sexually Transmitted Diseases
Polymerase Chain Reaction-Based Subtyping of Ureaplasma Parvum and Ureaplasma Urealyticum in First-Pass Urine Samples from Men With or Without Urethritis
Yoshida, T; Ishiko, H; Yasuda, M; Takahashi, Y; Nomura, Y; Kubota, Y; Tamaki, M; Maeda, S; Deguchi, T
Sexually Transmitted Diseases, 32(7): 454-457.

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