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.
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.
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.
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. urealyticum 33 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.
The Role of Mycoplasma genitalium
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.
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.
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?
1. Barlow R. Urethritis non-gonorrhoica: eine kritische Studie. Dtsch Arch Klin Med 1899; 66:444–469.
2. Waelsch L. Uber nicht-gonorrhoische Urethritis. Arch Derm Syph Wien 1904; 70:103–124.
3. Halberstaedter L, von Prowazek S. Ueber Zelleinschlüsse parasitärer Natur beim Trachom. Arb K Gesundh Amt 1907; 26:44–47.
4. Thygeson P, Stone W. Epidemiology of inclusion conjunctivitis. Arch Ophthalmol 1942; 27:91–122.
5. Harkness AH. Non-gonococcal urethritis. Edinburgh: Living-stone, 1950; 166–170.
6. T'ang F-F, Chang H-L, Huang Y-T, Wang K-C. Trachoma virus in chick embryo. Natl Med J China 1957; 43:81–86.
7. Chernesky MA, Jang D, Lee H, et al. Diagnosis of Chlamydia trachomatis
infections in men and women by testing firstvoid urine by ligase chain reaction. J Clin Microbiol 1994; 32:2682–2685.
8. Taylor-Robinson D. Laboratory methods for chlamydial infections. J Infect 1992; 25(suppl):61–67.
9. Purcell RH, Taylor-Robinson D, Wong DC, Chanock RM. Color test for the measurement of antibody to T-strain mycoplasmas. J Bact 1966; 92:6–12.
10. Dunlop EMC, Jones BR, Al-Hussaini MK. Genital infection in association with TRIC virus infection of the eye. III. Clinical and other findings: Preliminary report. Br J Vener Dis 1964; 40:33–42.
11. Department of Health (UK). New cases seen at NHS genito-urinary medicine clinics in England: 1991 Annual figures: Summary information from form KC60. DH Statistics Division, 1993.
12. Prentice MJ, Taylor-Robinson D, Csonka GW. Non-specific urethritis: A placebo-controlled trial of minocycline in conjunction with laboratory investigations. Br J Vener Dis 1976; 52:269–275.
13. Taylor-Robinson D, Evans RT, Coufalik ED, et al. Ureaplasma urealyticum
and Mycoplasma hominis
in chlamydial and non-chlamydial nongonococcal urethritis. Br J Vener Dis 1979; 55:30–35.
14. Coufalik ED, Taylor-Robinson D, Csonka GW. Treatment of non-gonococcal urethritis with rifampicin as a means of defining the role of Ureaplasma urealyticum.
Br J Vener Dis 1979; 55:36–43.
15. Ngeow YF, Munday PE, Evans RT, Taylor-Robinson D. Taking cell cultures to the patient in an attempt to improve chlamydial isolation. Br J Vener Dis 1981; 57:44–46.
16. Munday PE, Thomas BJ, Johnson AP, Altman DG, Taylor-Robinson D. Clinical and microbiological study of non-gonococcal urethritis with particular reference to nonchlamydial disease. Br J Vener Dis 1981; 57:327–333.
17. Thomas BJ, Evans RT, Hawkins DA, Taylor-Robinson D. Sensitivity of detecting Chlamydia trachomatis
elementary bodies in smears by use of a fluorescein-labelled monoclonal antibody: Comparison with conventional chlamydial isolation. J. Clin Pathol 1984; 37:812–816.
18. Taylor-Robinson D, Furr PM, Hanna NF. Microbiological and serological study of non-gonococcal urethritis with special reference to Mycoplasma genitalium.
Genitourin Med 1985; 61:319–324.
19. Hawkins DA, Fontaine EAR, Thomas BJ, Boustouller YL, Taylor-Robinson D. The enigma of non-gonococcal urethritis: Role for Bacteroides ureolyticus.
Genitourin Med 1988; 64:10–13.
20. Thomas BJ, Osborn MF, Munday PE, Evans RT, Taylor-Robinson D. A 2-year quantitative assessment of Chlamydia trachomatis
in a sexually transmitted diseases clinic population by the MicroTrak direct smear immunofluorescence test. Int J STD AIDS 1990; 1:264–267.
21. Hay PE, Thomas BJ, Gilchrist C, Palmer HM, Gilroy CB, Taylor-Robinson D. The value of urine samples from men with non-gonococcal urethritis for the detection of Chlamydia trachomatis.
Genitourin Med 1991; 67:124–128.
22. Palmer HM, Gilroy CB, Thomas BJ, Hay PE, Gilchrist C, Taylor-Robinson D. Detection of Chlamydia trachomatis
by the polymerase chain reaction in swabs and urine from men with non-gonococcal urethritis. J Clin Pathol 1991; 44:321–325.
23. Hay PE, Thomas BJ, Gilchrist C, Palmer HM, Gilroy CB, Taylor-Robinson D. A reappraisal of non-gonococcal ure-thritis. Int J STD AIDS 1992; 3:191–195.
24. Hay PE, Thomas BJ, Mackenzie P, Taylor-Robinson D. Detection of Chlamydia trachomatis
in men: Sensitive tests for sensitive urethras. Sex Transm Dis 1992; 20:1–5.
25. Horner PJ, Gilroy CB, Thomas BJ, Naidoo ROM, Taylor-Robinson D. Association of Mycoplasma genitalium
with acute non-gonococcal urethritis. Lancet 1993; 342:582–585.
26. Zelin JM, Robinson AJ, Ridgway GL, Allason-Jones E, Williams P. Chlamydial urethritis in heterosexual men attending a genitourinary medicine clinic: Prevalence, symptoms, condom usage and partner change. Int J STD AIDS 1995; 6:27–30.
27. Bowie WR, Alexander ER, Stimson JB, Floyd JF, Holmes KK. Therapy for nongonococcal urethritis: double-blind randomized comparison of two doses and two durations of minocycline. Ann Intern Med 1981; 95:306–311.
28. Schachter J. Chlamydial infections. N Engl J Med 1978; 298:428–435, 490–495.
29. Bowie WR. Urethritis in males. In: Holmes KK, Mårdh P-A, Sparling PF, et al, eds. Sexually Transmitted Diseases. 2nd ed. New York: McGraw-Hill, 1990; 627–639.
30. Munday PE. Persistent and recurrent non-gonococcal urethritis. In: Taylor-Robinson D, ed. Clinical Problems in Sexually Transmitted Diseases. Dordrecht: Martinus Nijhoff, 1985; 15–35.
31. Hawkins DA, Taylor-Robinson D. Non-gonococcal urethritis in the male. In: Asscher AW, Brumfitt W, eds. Microbial Diseases in Nephrology. Chichester: John Wiley, 1986; 47–67.
32. Shepard MC. The recovery of pleuropneumonia-like organisms from Negro men with and without nongonococcal urethritis. Am J Syph Gonor Vener Dis 1954; 38:113–124.
33. Shepard MC, Lunceford CD, Ford DK, et al. Ureaplasma urealyticum
(gen.nov., sp.nov.): Proposed nomenclature for the human T (T-strain) mycoplasmas. Int J Syst Bact 1974; 24:160–171.
34. Taylor-Robinson D, McCormack WM. Mycoplasmas in human genitourinary infections. In: Tully JG, Whitcomb RF, eds. The Mycoplasmas. Vol. 2. Host-Parasite Relationships. New York: Academic Press, 1979; 307–366.
35. Hare MJ, Dunlop EMC, Taylor-Robinson D. Mycoplasmas and ‘non-specific’ genital infections. III. Post-gonococcal urethritis: A prospective study. Br J Vener Dis 1969; 45:282–286.
36. Taylor-Robinson D, Csonka GW, Prentice MJ. Human intraurethral inoculation of ureaplasmas. Quart J Med 1977; 46:309–326.
37. Mufson MA, Ludwig WM, Purcell RH, Cate TR, Taylor-Robinson D, Chanock RM. Exudative pharyngitis following experimental Mycoplasma hominis
38. Mufson MA. Mycoplasma hominis:
A review of its role as a respiratory tract pathogen of humans. Sex Transm Dis 1983; 10(suppl):335–340.
39. Jansch HH. Pathogenitätsnachweiss für harnstoffsplatende Mycoplasmen im menschlichen Urogenitaltrakt im Selbstver-such. Hautarzt 1972; 23:558.
40. Kawamura N. Experimental studies on genitourinary tract infection caused by Ureaplasma urealyticum.
Sex Transm Dis 1991; 71:21–24.
41. Taylor-Robinson D. Mycoplasmal and mixed infections of the human male urogenital tract and their possible complications. In: Razin S, Barile MF, eds. The Mycoplasmas. Vol. 4. Mycoplasma Pathogenicity. New York: Academic Press, 1985; 27–63.
42. Bowie WR, Alexander ER, Floyd JF, Holmes J, Miller Y, Holmes KK. Differential response of chlamydial and ureaplasma-associated urethritis to sulphafurazole (sulfisoxazole) and aminocyclitols. Lancet 1976; ii:1276–1278.
43. Saglio P, Laflèche D, Bonissol C, Bové JM. Isolation and culture in vitro
of mycoplasma associated with stubborn disease of citrus fruits and their observation with the electron microscope. CR Hebd Seances Acad Sci. Ser D. Sci Natur (Paris) 1971; 272:1387–1390.
44. Tully JG, Rose DL, Whitcomb RF, Wenzel RP. Enhanced isolation of Mycoplasma pneumoniae
from throat washings with a newly modified culture medium. J Infect Dis 1979; 139:478–482.
45. Tully JG, Taylor-Robinson D, Cole RM, Rose DL. A newly discovered mycoplasma in the human urogenital tract. Lancet 1981; i:1288–1291.
46. Taylor-Robinson D, Tully JG, Furr PM, Cole RM, Rose DL, Hanna NF. Urogenital mycoplasma infections of man: A review with observations on a recently discovered mycoplasma. Isr J Med Sci 1981; 17:524–530.
47. Tully JG, Taylor-Robinson D, Rose DL, Cole RM, Bové JM. Mycoplasma genitalium,
a new species from the human urogenital tract. Int J Syst Bact 1983; 33:387–396.
48. Taylor-Robinson D, Tully JG, Barile MF. Urethral infection in male chimpanzees produced experimentally by Mycoplasma genitalium.
Br J Exp Path 1985; 66:95–101.
49. Tully JG, Taylor-Robinson D, Rose DL, Furr PM, Graham CE, Barile MF. Urogenital challenge of primate species with Mycoplasma genitalium
and characteristics of infection induced in chimpanzees. J Infect Dis 1986; 153:1046–1054.
50. Roberts MC, Hooton M, Stamm W, Holmes KK, Kenny GE. DNA probes for the detection of mycoplasmas in genital specimens. Isr J Med Sci 1987; 23:618–620.
51. Hooton TM, Roberts MC, Roberts PL, Holmes KK, Stamm WE, Kenny GE. Prevalence of Mycoplasma genitalium
determined by DNA probe in men with urethritis. Lancet 1988; i:266–268.
52. Palmer HM, Gilroy CB, Furr PM, Taylor-Robinson D. Development and evaluation of the polymerase chain reaction to detect Mycoplasma genitalium.
FEMS Microbiol Letts 1991; 77:199–204.
53. Jensen JS, Uldum SA, Søndergård-Andersen J, Vuust J, Lind K. Polymerase chain reaction for detection of Mycoplasma genitalium
in clinical samples. J Clin Microbiol 1991; 29:46–50.
54. Jensen JS, Orsum R, Dohn B, Uldum S, Worm A-M, Lind K. Mycoplasma genitalium:
A cause of male urethritis? Genitourin Med 1993; 69:265–269.
55. Deguchi T, Komeda H, Yasuda M, et al. Mycoplasma genitalium
in non-gonococcal urethritis. Int J STD AIDS 1995; 6:144–145.
56. Janier M, Lassau F, Casin I, et al. Male urethritis with and without discharge: A clinical and microbiological study. Sex Transm Dis 1995; 22:244–252.
57. Charron A, de Barbeyrac B, Renaudin H, Geniaux M, Bébéar C. Mycoplasma genitalium
as etiological agent of male urethritis in Southwest France. Abstracts of Eleventh Meeting of International Society for STD Research. New Orleans: 1995; 203.
58. Lackey PC, Ennis DM, Cassell GH, Whitley RJ, Hook EW. The etiology of nongonococcal urethritis. Clin Infect Dis 1995; 21(abstr):759.
59. Taylor-Robinson D. The history and role of Mycoplasma genitalium
in sexually transmitted diseases (The Harrison Lecture). Genitourin Med 1995; 71:1–8.
60. Weström L, Evaldson G, Holmes KK, van der Meijden W, Rylander E, Fredriksson B. Taxonomy of vaginosis: Bacterial vaginosis—a definition. In: Mårdh P-A, Taylor-Robinson D, eds. Bacterial Vaginosis. Stockholm: Almqvist and Wiksell International, 1984; 259–260.
61. Taylor-Robinson AW, Borriello SP, Taylor-Robinson D. Identification and preliminary characterization of a cytotoxin isolated from Mobiluncus
spp. Int J Exp Pathol 1993; 74:357–366.
62. Hawkins DA, Fontaine EAR, Thomas BJ, Boustouller YL, Taylor-Robinson D. The enigma of non-gonococcal urethritis: Role for Bacteroides ureolyticus.
Genitourin Med 1988; 64:10–13.