1. health and fitness
2. disease

Clinical Spectrum Of Chlamydia trachomatis Infection
Carolyn Thompson
Introduction
This review outlines the development of our
knowledge of the oculogenital serovars D - K of
Chlamydia trachomatis, with particular reference to
the epidemiology and some of the clinical manifestations.
The word 'chlamydia' is derived from the Latin
word cloak, which aptly describes the organism's
requirement as an obligate intracellular parasite.
Human disease caused by Chlamydia trachomatis
was recognised many thousands of years ago with
the clinical features of trachoma being described in
both Egyptian papyrae and Ancient Chinese civilisation1. The term trachoma was first coined by the
Sicilian physician Pedanius Diascarides in around
the year 60 AD. However, infections due to the
oculogenital serovars such as non-gonococcal
urethritis and neonatal ophthalmia were not recognised as distinct entities until after the identification
of the gonococcus in the late 19th Century.
In 1907 Halberstaedter and Von Prawazek were
the first to visualise intracytoplasmic inclusions of
Chlamydia trachomatis in stained conjunctival scrapings taken from orangutangs which had been
inoculated with human trachomatis material. Very
shortly thereafter similar inclusions were identified
in human material from trachoma cases and in
1909 Linder found inclusions in conjunctival
scrapings taken from infants with neonatal
ophthalmia, the genital tracts of the mothers of the
affected infants and the urethras of the fathers. The
organism itself was first isolated from patients with
lymphogranuloma venereum and later the
trachoma serovars were isolated by inoculation of
embryonated hen's egg yolk sacs in the 1950s.
Because of the lack of technology, the study of
genital chlamydial infections was not actively
pursued and it was not until the development of
cell culture isolation techniques that in 1966
Dunlop demonstrated that approximately a third of
the cases of non-gonococcal urethritis at that time
were due to Chlamydia trachomatis infections2 The
lack of highly sensitive and specific tests have made
the epidemiological study of chlamydial infections
very difficult. In the last 10 years it has become
recognised as the most prevalent sexually
transmitted bacterial
nfection in developed
countries but the true incidence of infection is
difficult to determine for several reasons: the
inadequacies of tests hitherto available and the lack
of availability of universal testing until very
recently; the fact that many infections are
asymptomatic therefore patients do not present for
testing; and the lack of uniformity in reporting by
laboratories. The development of DNA
amplification tests and the ability to test urine
specimens rather than relying on urethral or
endocervical swabs3 will hopefully address some of
these issues.
Prevalence of infection
Data collection in the UK is dependent upon
two different systems. Firstly, the reporting by
GUM clinics on the KC60 returns for England and
Wales and the ISD(D)5 for Scotland, but these do
not reflect infections diagnosed and treated outwith
GUM, for instance by Family Planning,
Gynaecologists or GPs where referral to the GUM
clinic is not made. The second system is by the
voluntary reporting by laboratories of all tests
performed. Unfortunately neither of these systems
is comprehensive.
Overall there has been a slight fall in the rate of
infection analysed by sex and age. The rate of
infection is highest in women in the 16-19 year
band and for men in the 20-25 band4. Trends in
incidence are difficult to interpret: it was only in
1990 that chlamydia had its own individual
diagnostic code in the GUM returns, it previously
having been coded as non-specific genital tract
infection; in 1990 not all clinics had access to
chlamydia testing; many clinics that did have access
to testing only screened selected populations, e.g. a
man presenting with microscopic evidence of a
non-gonococcal urethritis might not have had a
chlamydia test taken as treatment would be given
anyway; over the last eight years the sensitivity of
the diagnostic test used has varied with the change
from culture to antigen detection methods and now
most recently in some centres, DNA amplification
methods. Most prevalence studies have used either
culture or antigen detection methods, which are
likely to be an underestimate of the true extent of
infection. However, it has been demonstrated
repeatedly that being of young age, i.e. teenager or
in early 20s, being unmarried and having had a
new sexual partner in the last year are all independently associated with a higher risk of infection.
Carolyn Thompson
BSc, MB ChB, FRCP(Ed)
Graduated from Edinburgh
Medical School in 1980 and
after completing the preregistration year, spent four years
in General Medicine in
Aberdeen and then West
Lothian. Trained in GUM at
Edinburgh Royal Infirmary,
starting in 1985, becoming a
Consultant in 1990. Currently
working as a single -handed
GUM Consultant in Fife,
Scotland.
Correspondence:
Carolyn Thompson
Consultant in GUM,
Department of GUM,
Victoria Hospital,
Kirkcaldy Hospitals NHS
Trust, Hayfield Road,
Kirkcaldy KY2 5AH
Asymptomatic Infections in Men
Prevalence studies using culture done in the
1970s and 1980s estimated that between 3-5% of
men attending STD clinics had asymptomatic
chlamydial infection of the urethra5, although in
1982 11% of male military recruits in the United
States were found to be chlamydia positive6 and a
similar figure was found in Sweden using culture as
a diagnostic test in 19907. Two recent studies using
DNA amplification techniques found that only 4. 1
% of 704 male military recruits in Austria8 and 5.4%
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3
63
Clinical Spectrum Of Chlamydia trachomatis Infection
of over 5,000 predominantly teenage boys in Seattle9 were positive. This latter study showed that the likelihood of infection
increased with age from under 15 up to 20 years.
In the UK Kudesia10 in 1993 reported the testing of
mid-stream urine specimens found to have sterile pyuria with an
overall prevalence of chlamydial infection of 6%, and 15% in the
30 year and under age group. This study did not test urines
where there was no pyuria, or where bladder pathogens were
found.
Pharyngeal infection has been relatively understudied, but
has been estimated in the past to be approximately 3-6% of the
STD clinic population5 and in Manchester in 1995 was found to
be 2.4%11. Three cases of pharyngeal infection were found, all of
which were asymptomatic. Interestingly, these were only
detected by PCR and, all three cases were culture negative.
Asymptomatic Infections in Women
The prevalence of chlamydial infection in women has been
studied in a variety of groups including those who are pregnant,
those attending Gynaecology or Family Planning Clinics and
college students as well as those attending STD or GUM clinics.
The prevalence has ranged from 3-5% in asymptomatic women
attending Community based clinics to over 20% in women attending STD clinics5. Recent studies using LCR demonstrate
prevalences ranging from 5.6% in Finnish women attending
Family Planning or University Student Health Clinics to 18% of
pregnant women attending routine ante-natal clinics in
Birmingham, USA12 13 14 15. A teenage community survey found a
prevalence of 8.6% in nearly 5,000 young women, and in contrast
to the rates with age in the young men, in women the rate of
infection decreased with age from under 15 up to 20 years9.
Several UK studies have found a prevalence ranging from
2.9% to 12% in asymptomatic women attending for routine
cervical cytology16 17 18 19 20 and 5% to 8% in women requesting a
termination of pregnancy (Thomp son [unpublished])21. Only one
study used LCR which gave quite a relatively low prevalence of
2.5%20 in contrast to previous London data from the 1980s22.
Clinical Manifestations in Men
Urethritis
Although Koch's postulates have not been specifically
fulfilled, persuasive evidence from studies in the 1970s suggest
that chlamydia can be isolated from up to 50% of cases of NGU
in heterosexual men23. Variations in reported prevalence may be
due to a combination of geographical differences, the selection
of study populations and differences in the diagnostic test used.
It has been recognised that the organism can be isolated from
some men where there is no clinical or microscopic evidence of
urethritis. However, many men who are asymptomatic do have
pus cells on examination of a urethral smear. Zelin24 recently
showed that 24% (31/131) of men with non-gonococcal urethritis
were chlamydia culture positive of whom over half were
asymptomatic but only one, i.e. 3% had no evidence of urethritis.
Harry25 however, found that 21.1% (19/90) of GUM attendees
64
found to be chlamydia positive were asymptomatic and with no
evidence of urethritis. With the new generation of more sensitive
tests for the diagnosis of chlamydia it is likely that the proportion
of asymptomatic infections will be seen to increase.
Epididymitis
In the 1950s epididymitis was thought to be largely due to
either gonococcal infection or tuberculosis. As these infections
began to be controlled by appropriate antimicrobial therapy in
the 1960s and 1970s the diagnosis of 'idiopathic epididymitis'
emerged. It was Berger's study in 197826 which demonstrated that
chlamydia could be isolated in the majority of cases of epididymitis in men aged less than 35 years of age whereas coliforms were commonly found in men older than 35. In chlamydial epididymitis there is usually an associated urethritis although
this is generally asymptomatic resulting in the individual not
having previously sought treatment.
Prostatitis
Many workers have tried to implicate chlamydia in the
aetiology of prostatitis but its role remains controversial. In 1981
Nilsson27 reported the recovery of chlamydiae from the
expressed prostatic secretions of 26 men with acute nongonococcal urethritis, all of whom were considered to have
evidence of prostatitis. In the same year, Bruce28 reported
frequent isolation of chlamydiae from the prostatic expressae of
men with non-bacterial prostatitis. However, these studies did not
convincingly demonstrate the presence of chlamydia in the
prostate itself and the definition of prostatitis used was disputed.
Poletti29 in 1985 performed trans-rectal biopsies of the prostate in
30 men with known positive urethral cultures for chlamydia and
the diagnosis of non-bacterial prostatitis (based on prostatic
tenderness or swelling on digital palpation). Chlamydiae were
cultured from a third of these men but it has been suggested that
urethral contamination might have been the source of the
positive cultures. Bruce did a further study30 when he cultured
chlamydia from the expressed prostatic secretions of six men
who had had negative urethral chlamydial cultures. Doble31 in
1989 using ultrasound directed biopsies in order to overcome the
problems of urethral contamination was unable to isolate
chlamydia from any specimen although a chronic inflammatory
reaction was confirmed in the majority of cases. Finally, Krieger32
in 1996 using PCR detected chlamydial DNA in 4/135 prostatic
biopsies. In his study population he specifically excluded
individuals with microscopic evidence of urethritis or other
evidence of infection with gonorrhoea, chlamydia or ureaplasma.
Proctitis
It is well known that Chlamydia trachomatis in the form of
lymphogranuloma venereum (LGV) can cause a severe proctitis
but the oculogenital serovars can also produce a milder proctitis
which may be asymptomatic or produce rectal discomfort with
some bleeding, mucous discharge and diarrhoea. This is
generally a much milder syndrome than the LGV type and
Rompalo in 198633 estimated that it may be responsible for up to
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3
Clinical Spectrum Of Chlamydia trachomatis Infection
5% of cases of proctitis in gay men. To date, there have been no
studies using DNA amplification techniques.
Reiter's syndrome
Benjamin Brodie in 1818 first described the association of
urethral discharge, recurrent joint swellings and conjunctivitis.
However, it was nearly 100 years later, in 1916, when Hans Reiter
described a similar syndrome of arthritis and conjunctivitis in
association with dysentery. The latter’s name has now been
attached to both forms of the syndrome which is also known as
sexually acquired reactive arthritis (SARA). The HLA B27
haplotype is linked with the development of Reiter's and is
thought to increase the risk by tenfold34. SARA has been
strongly associated with chlamydial urethritis although very few
workers have demonstrated the organism in the affected joints.
Keat in 198735 demonstrated elementary bodies in the joint fluid
and synovial biopsies of patients with Reiter's syndrome and
Taylor-Robinson using PCR in 199236 repeated previous work
and found that 6/8 of his stored synovial samples were positive
confirming his previous study. Nikkari37 in 1997 using LCR found
chlamydia in 4/12 synovial fluid specimens although
interestingly, using PCR, the same samples were all negative.
Similarly Poole38 in New Zealand was unable to demonstrate any
evidence of chlamydial infection in ten patients with SARA.
Thus not all studies using synovial fluid have yielded positive
results, but others have demonstrated that synovial tissue is more
likely to yield positive results than synovial fluid.
Clinical Manifestations in Women
Cervicitis
The majority of women with cervical infection are
asymptomatic. It is estimated that about a third will have
symptoms of mucopurulent vaginal discharge or irregular
bleeding due to cervicitis. The presence of chlamydial infection
is associated with the presence of cervical ectopy but whether
this means that ectopy predisposes women to infection by
exposing a greater number of susceptible columnar epithelial
cells, or that ectopy increases the shedding of chlamydia from the
cervix making it more easily detected, or whether the presence
of infection itself may cause the ectopy is unclear.
Bartholinitis
Like the gonococcus, chlamydia can produce infection of the
Bartholin's gland but is a much less frequent cause. In 1978
Davies39 reviewed 30 women with Bartholinitis of whom nine had
chlamydial infection; however, in seven of these there was
concurrent gonococcal infection.
Urethritis
Screening studies within STD clinics suggest that 50% of
women have C. trachomatis in both the urethra and the cervix
and up to 25% may have the organism at only one site implying
that screening of the cervix alone is likely to miss up to a
quarter of all infections. Stamm40 in 1980 recognised chlamydia
as a cause of the dysuria syndrome in young women with sterile
urine; however urethral infection may often be asymptomatic.
Objective signs of infection such as urethral discharge and meatal
erythema are infrequent. Dysuria may be milder and have a
longer incubation often taking between 7-10 days to develop
when compared with a urinary tract infection. In addition there
is usually no associated haematuria or supra-pubic tenderness.
However, microscopy of a urethral smear would usually
demonstrate pus cells. Horner's study41 in 1995 took specimens
from both urethra and cervix in 130 women. Evidence of
chlamydial infection was found by direct fluorescent antibody in
39 women of whom 75% (29/39) were positive at both sites.
Fifteen percent (6/39) were positive in the cervix only and 10%
(4/39) positive only in the urethra. When asked about symptoms,
only one-third of those complaining of dysuria had a urethral
infection and the majority of those with urethral chlamydia
actually had no symptoms. There was little correlation between
symptoms and the presence of urethral infection.
Upper genital tract infection
The study of upper genital tract infection is difficult as there
are no generally accepted criteria for the clinical diagnosis and
laparoscopy is not performed in all cases. In most regions it is not
reportable. Most aetiological studies are based on rates of
isolation from the cervix and not the upper genital tract and
many studies are concerned with only one micro-organism rather
than a combination of infections. Finally, it has become apparent
that there is an epidemic of asymptomatic silent pelvic
inflammatory disease (PID) running parallel to the clinically
overt cases. It was Per Anders Mardh42 in 1981 who first
described two women with salpingitis who had chlamydia
cultured from the uterine aspirate despite negative cervical
cultures. It is now recognised that chlamydial endometritis is a
cause of menorrhagia and late post-partum endometritis in
people with untreated antenatal chlamydial infection43.
Earlier Mardh44 had suggested that a third of cases of PID
were due to chlamydia. He found that 19 of 53 women with
salpingitis had chlamydial infections of the cervix and that of
those with cervical infection, at laparoscopy 6/7 cultured
chlamydia from the fallopian tubes. Studies done in Seattle at
around the same time5 suggested that up to 80% of women with
laparoscopically confirmed salpingitis and/or endometritis have
either chlamydial or gonococcal infections as the cause. Recent
studies from the UK45 21 46 have confirmed chlamydia as a major
aetiological factor in the development of PID and Blackwell's
study21 showed that of those girls found to be chlamydia positive
at the time of termination of pregnancy, nearly two-thirds
developed clinical PID.
Kamwendo47 in Sweden in 1993 screened 200 male contacts
of 196 women admitted to hospital for acute PID. Of the women
found to have chlamydia, 44% of their contacts were also positive
for chlamydia and overall, gonorrhoea, chlamydia and NSU were
demonstrated in 60% of the male partners although the majority
of these were asymptomatic. These data strongly support the
need for routine screening and treatment of the male sexual
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3
65
Clinical Spectrum Of Chlamydia trachomatis Infection
partners of women with acute PID.
In sub-clinical PID, i.e. where there is no abdominal pain but
histological evidence of endometritis, Henry Suchet48 in 1981
found chlamydia in 15% of the fallopian tubes where there was
no evidence of acute salpingitis and 23% of those with salpingitis.
It was recognised in the 1970s that acute PID can have an
adverse effect on fertility and Buchan49 in 1993 reported a large
cohort study comparing 1200 women with PID with over 10,000
controls. He found that the women with PID had nearly a
tenfold risk of future non-specific abdominal pain, a fivefold risk
of gynaecological pain and endometriosis, eightfold risk of future
hysterectomy and a nearly tenfold risk of ectopic pregnancy.
Infertility as an outcome was not examined. In the same year
Hillis50 examined the rates of ectopic pregnancy and infertility in
over 400 women with a past history of PID and demonstrated
that a delay in treatment of between 3-9 days more than doubled
the risk of future impaired fertility and if treatment was delayed
by greater than nine days this was more than tripled (the results
were identical for ectopic pregnancy and infertility when
analysed separately). These two studies provide convincing
evidence of the serious morbidity caused by PID. The fact that
many infections are asymptomatic emphasizes the need for
screening of the younger age groups.
Impact of screening for chlamydial
infection in women
Since the introduction of widespread chlamydial screening in
Sweden, there has been a progressive reduction in admissions for
acute PID from 180 in 1976 to 24 in 199451. The greatest decrease
was seen in the 15-19 year old age group, the obvious conclusion
being that this dramatic fall is as a result of the intensive
screening of young women that occurs in Sweden. This is
reinforced by data from Scholes52 in Seattle where 645 women
were randomly selected and screened for chlamydia and over
1500 controls allocated to 'usual care'. Both cohorts were
followed up for a period of one year after which time the rate of
PID in the unscreened group was more than double (18:8) that
of the screened group.
Perihepatitis
Perihepatitis, otherwise known as the Fitz-Hugh Curtis
Syndrome, was first reported in Spanish in 1920 by Stajano, a
Uruguayan physician, at a meeting in Montevideo53 and went
unrecognised in the English literature. In 1930, Curtis54 described
the presence of 'violin string' adhesions between the liver capsule
and the anterior abdominal wall in women with gross
pathological evidence of previous tubal infections and in 1934,
Fitz-Hugh55, another American, described a local peritonitis of
the anterior liver surface, the diaphragm and anterior abdominal
wall in three patients. The first patient underwent laparotomy
and was found to have a "sprinkled salt" appearance of the liver
from which typical gram negative intracellular diplococci were
visualised. It was originally thought that the syndrome was due
to gonorrhoea but case reports in the 1970s56 57 58 suggested that
there may be an alternative aetiology. Dalaker59 in 1981 reported
66
four cases of PID and perihepatitis confirmed by laparoscopy in
which chlamydia was isolated from the cervix in all four cases
and from the fallopian tubes in two of the four cases. Since then
it has become recognised that only about a third to a half of cases
have coincident gonococcal infection and up to half have chlamydial infections. Wolner-Hanssen60 in 1982 cultured chlamydia
from adhesions around the liver and Van Dongen61 in 1993
described two patients in whom the fibrinous violin string
adhesions were associated with ascites and visualised clearly by
ultrasound.
It is likely that this syndrome is much more common than is
currently clinically recognised, perhaps because patients often
present to Surgical Units. Sweet62 in 1981 reported that upper
quadrant abdominal pain had been reported amongst 12% of
patients with acute salpingitis but it is not clear how many of
these had the severe pleuritic pain which is traditionally
associated with Fitz-Hugh Curtis syndrome. In 199763 a
prospective study of 157 women with a clinical diagnosis of PID
of whom 27 had laparoscopically confirmed perihepatitis and
salpingitis were compared with 46 patients with salpingitis alone.
In this study both current use and history of ever having used the
oral contraceptive pill were both negatively associated with
evidence of perihepatitis and, at laparoscopy, the perihepatitis
group significantly more often had moderate to severe pelvic
adhesions than the salpingitis alone group. In summary the
diagnosis of perihepatitis had been made on the basis of typical
symptoms in up to 20% and on the basis of laparoscopic findings
in 5-15% of women with salpingitis.
Neonatal Infections
As with the gonococcus, vertical transmission from a
cervically infected pregnant woman can infect the baby and this
has been demonstrated in several studies with up to 44% of
neonates developing conjunctivitis and 22% pneumonitis64. It is
assumed that the infant is inoculated with organisms via
passage through the infected cervical secretions and several sites,
i.e. the eye and nasopharynx, rectum and vagina may be seeded
independently. It is also possible that the infant directly aspirates
infected secretions with the first breath and even an infant
delivered by caesarean section may be infected if the membranes
have been ruptured spontaneously prior to delivery.
In 1977 Chandler and Alexander65 demonstrated that 50% of
babies born to infected women had developed conjunctivitis and
67% had evidence of infection by the development of serum
antibody at one year. Similar results were found by Frommell66
who also showed that 11 % developed pneumonia. Taking all
studies together it has been suggested that 60-70% of neonates will
seroconvert64 The biggest study was done by Schachter67 in 1986.
He followed up over a period of five years 131 infants exposed
at birth, but untreated. His transmission rates were lower than
those suggested by other studies, with 18% developing
conjunctivitis and 16% pneumonitis. However, even in this study
60% were found to have seroconverted although, of these, about
a third did not have any documented infection at any particular
site.
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3
Clinical Spectrum Of Chlamydia trachomatis Infection
The prevalence of neonatal infection will only be reduced by
increasing awareness of chlamydial infection amongst adults and
introduction of routine screening especially for high risk groups
during pregnancy.
22. Taylor-Robinson D. Chlamydia trachomatis and sexually transmitted disease. BMJ 1994;
308: 150-1
23. Taylor-Robinson D. Genital chlamydial infections: clinical aspects, diagnosis, treatment and
prevention. In. Recent advances in sexually transmitted diseases and AIDS. Harris JRW,
Forster SM eds. Edinburgh: Churchill Livingstone, 1991; pp 219-262
24. Zelin JM, Robinson AJ, Ridgway GL, Allason-Jones E, Williams P. Chlamydial urethritis in
References
1.
York, 1989
2.
heterosexual men attending a genitourinary medicine clinic: prevalence, symptoms,
Chlamydia. Mardh P-A, Paavonen J, Puolakkainen M. Plenum Medical Book Company, New
condom usage and partner change. Int J STD&AIDS 1995; 6: 27-30
25. Harry TC, Saravanamuttu KM, Rashid S, Shrestha TL. Audit evaluating the value of routine
Dunlop EMC, Harper IA, al-Hussaini MK et al. Relation of TRIC agent to 'nonspecific'
screening of Chlamydia trachomatis urethral infections in men. Int J STD&AIDS 1994; 5:
genital infection. Br J Vener Dis 1966; 42: 77-87
3.
Lee HH, Chernesky MA, Schachter J et al. Diagnosis of Chlamydia trachomatis
374-5
26. Berger RE, Alexander ER, Monda GD, Ansell J, McCormick G, Holmes KK. Chlamydia
genitourinary infection in women by ligase chain reaction assay of urine. Lancet 1995; 345:
213-6
4.
trachomatis as a cause of acute 'idiopathic' epididymitis. N Eng J Med 1978; 298: 301-4
27). Nilsson S, Johannisson G, Lycke E. Isolation of Chlamydia trachomatis from the urethra
Simms 1, Catchpole M, Brugha R et al. Epidemiology of genital Chlamydia trachomatis in
and from prostatic fluid in men with signs and symptoms of acute urethritis. Acta Derm
England and Wales. Genitourin Med 1997; 73: 122-126
5.
Stamm WE, Holmes KK. Chlamydia trachomatis infections of the adult. In. Sexually
Venereol 1981; 61: 456-9
28. Bruce AW, Chadwick P, Willett WS, O'Shaughnessy M. The role of chlamydiae in
Transmitted Diseases. Holmes KK, Mardh P-A, Sparling PF, Wiesner PJ eds. New York:
McGraw Hill, 1990, pp 181-194
6.
Podgore JK, Holmes KK, Alexander ER. Asymptomatic urethral infections due to
Chlamydia trachomatis in male U.S. military personnel. J Infect Dis 1982; 146:828
7.
cells in patients affected by nonacute abacterial prostatitis. J Urol 1985; 134: 691-3
30. Bruce AW, Reid G. Prostatitis associated with Chlamydia trachomatis in 6 patients. J Urol
Larsson S, Ruden A-K, Bygdeman SM. Screening for Chlamydia trachomatis genital
infection in young men in Stockholm. Int J STD&AIDS 1990; 1: 205-6
8.
genitourinary disease. J Urol 1981; 126: 625-9
29. Poletti F, Medici MC, Alinovi A et al. Isolation of Chlamydia trachomatis from the prostatic
1989; 142: 1006-7
3 I. Doble A, Thomas BJ, Walker MM et al. The role of Chlamydia trachomatis in chronic
Stary A, Tomazic-Allen S, Choueiri B, Burczak J, Steyrer K, Lee H. Comparison of DNA
amplification methods for the detection of Chlamydia trachomatis in firstvoid urine from
abacterial prostatitis: a study using ultrasound guided biopsy. J Urol 1989; 141: 332-3
32. Krieger JN, Riley DE, Roberts MC, Berger RE. Prokaryotic DNA sequences in patients
asymptomatic military recruits. Sex Trans Dis 1996; 23: 97-102
9.
Marrazzo JM, White CL, Krekeler B et al. Community-based urine screening for
with chronic idiopathic prostatitis. J Clin Microbiol 1996; 34: 3120-8
33. Rompalo AM, Price CB, Roberts PL, Stamm WE. Potential value of rectal screening
Chlamydia trachomatis with a ligase chain reaction assay. Ann Intern Med 1997; 127: 796803
cultures for Chlamydia trachomatis in homosexual men. J Infect Dis 1986; 153: 888-92
34. Keat AC, Maini RN, Nkwaazi GC, Pegrum GD, Ridgway GL, Scott M Role of Chlamydia
10. Kudesia G, Zadik PM, Ripley M. Chlamydia trachomatis infection in males attending
general practitioners. Genitourin Med 1993: 70: 356
trachomatis and HLA-B27 in sexually acquired reactive arthritis. Br Med J 1978; 1: 605-7
35. Keat A, Thomas B, Dixey J, Osborn M, Sonnex C, Taylor-Robinson D. Chlamydia
11. Jebakumar SPR, Storey C, Lusher M, Nelson J, Goorney B, Haye KR. Value of screening
for oro-pharyngeal Chlamydia trachomatis infection. J Clin Path 1995; 48: 658-61
trachomatis and reactive arthritis: the missing link. Lancet 1987; 1: 72-4
36. Taylor-Robinson D, Gilroy CB, Thomas BJ, Keat ACS. Detection of Chlamydia trachomatis
12. Lan J, Melgers 1, Meijer CJ et al. Prevalence and serovar distribution of asymptomatic
DNA in joints of reactive arthritis patients by polymerase chain reaction. Lancet 1992;
cervical Chlamydia trachomatis infections as determined by highly sensitive PCR. J Clin
Microbiol 1995; 33: 3194-7
340: 81-2
37. Nikkari S, Puolakkainen M, Yli-Kerttula U, Luukkainen R, LehtonenOP, Toivannen P. Ligase
13. 0stergaard L, Moller JK, Anderson B, Olesen F. Diagnosis of urogenital Chlamydia
chain reaction in detection of Chlamydia DNA in synovial fluid cells. Br JRheumatol 1997;
trachomatis infection in women based on mailed samples obtained at home: multipractice
comparative study. BMJ 1996; 313: 1186-9
36: 763-5
38. Poole ES, Highton J, Wilkins RJ, Lamont IL. A search for Chlamydia trachomatis in synovial
14. Paukku M, Puolakkainen M, Apter D, Hirvonen S, Paavonen J. First-void urine testing for
fluids from patients with reactive arthritis using the polymerase chain reaction and antigen
Chlamydia trachomatis by polymerase chain reaction in asymptomatis women. Sex Trans
Dis 1997; 24: 3443-6
detection methods. Br J Rheumatol 1992; 31: 31-4
39. Davies JA, Rees E, Hobson D, Karayiannis P. Isolation of Chlamydia trachomatis from
15. Andrews WW, Lee HH, Roden WJ, Mott CW Detection of genitourinary tract Chlamydia
trachomatis infection in pregnant women by ligase chain reaction assay. Obstet Gynecol
Bartholin's ducts. Br J Vener Dis 1978; 54: 409-13
40. Stamm WE, Wagner KF, Amsel R et al. Causes of the acute urethral syndrome in women.
1997; 89: 556-60
16. Smith JR, Murdoch J, Carrington D et al. Prevalence of Chlamydia trachomatis infection in
N Eng J Med 1980; 303: 409-15
41. Horner PJ, Hay PE, Thomas BJ, Benton AM, Taylor-Robinson D. The role of Chlamydia
women having cervical smear tests. BMJ 1991; 302: 82-4
trachomatis in urethritis and urethral symptoms in women. Int J STD&AIDS 1995; 6: 31-
17. Thompson C, Wallace E. Chlamydia trachomatis Br J Gen Pract 1994; 44: 590-1
18. Hopwood J, Mallinson H. Chlamydia testing in community clinics - a focus for accurate
4
42. Mardh P-A, Moller BR, Ingerslev HJ, Nussler E, Westrom L, Wolner-Hanssen P.
sexual health care. Br J Fam Planning 1995; 21: 87-90
19. Oakeshott P, Kerry S, Hay S, Hay P. Opportunistic screening for chlamydial infection at
Endometritis caused by Chlamydia trachomatis. Br J Vener Dis 198 1; 57: 191-5
43. Wager GP. Puerperal infectious morbidity: Relationship to route of delivery and to
time of cervical smear testing in general practice: prevalence study. BMJ 1998; 316: 351-2
20. Grun L, Tassano-Smith. J, Carder C et al. Comparison of two methods of screening for
antepartum Chlamydia trachomatis infection. Am J Obstet Gynecol 1980; 138: 1028-33
44. Mardh P-A, Ripa T, Svensson L, Westrom L. Chlamydia trachomatis in patients with acute
genital chlamydial infection in women attending in general practice: cross section survey.
BMJ 1997; 315: 226-30
salpingitis. N Eng JMed 1977; 296: 1377-9
45. Stacey CM, Munday PE, Taylor-Robinson D et al. A longitudinal study of pelvic
21. Blackwell AL, Thomas PD, Wareham K, Emery SJ. Health gains from screening for
infection of the lower genital tract in women attending for termination of pregnancy.
inflammatory disease. Br J Obstet Gynaecol 1992; 99: 994-9
46. Bevan CD, Johal BJ, Mumtaz G, Ridgway GL, Siddle NC. Clinical, laparoscopic and
Lancet 1993; 342: 206-10
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3
microbiological findings in acute salpingitis: report on a United Kingdom cohort. Br J
67
Clinical Spectrum Of Chlamydia trachomatis Infection
Obstet Gynaecol 1995; 102: 407-14
Chlamydia trachomatis as possible cause of peritonitis and perihepatitis in young women.
47. Kamwendo K, Johansson E, Moi H, Forslin L, DanieIsson D. Gonorrhea, genital chlamydial
infection, and nonspecific urethritis in male partners of women hospitalised and treated
Br Med J 1978; 1: 1022-4
59. Dalaker K, Gjonness H, Kvile G, Urnes G, Anestad G, Bergan T. Chlamydia trachomatis
for acute pelvic inflammatory disease. Sex Transm Dis 1993; 20: 143-6
as a cause of acute perihepatitis associated with pelvic inflammatory disease. Br J Vener
48. Henry-Suchet J, Catalan F, Loffredo V et al. Chlamydia trachomatis associated with
Dis 198 1; 57: 41-3
chronic inflammation in abdominal specimens from women selected for tuboplasty. Fertil
60. Wolner-Hanssen P, Svensson L, Westrom L, Mardh P-A. Isolation of Chlamydia
Steril 198 1; 36: 599-605
trachomatis from the liver capsule in Fitz-Hugh Curtis Syndrome. N Eng J Med 1982; 306:
49. Buchan H, Vessey M, Goldenacre M, Fairweather J. Morbidity following pelvic
113
inflammatory disease. Br J Obstet Gynaecol 1993; 100: 558-62
6I.
50. Hillis SD, Joesoef R, Marchbanks PA, Wasserheit JN, Cates W, Westrom L. Delayed care
of pelvic inflammatory disease as a risk factor for impaired fertility. Am J Obstet Gynecol
1993; 168: 1503-9
62. Sweet RL, Draper DL, Hadley WK. Etiology of acute salpingitis: Influence of episode
number and duration of symptoms. Obstet Gynecol 1981; 58: 62-8
51. Kamwendo F, Forslin L, Bodin L, Danielsson D. Decreasing incidences of gonorrhea- and
chlamydia-associated acute pelvic inflammatory disease. A 25-year study from an urban
63. Money DM, Hawes SE, Esenbach DA et al. Antibodies to the chlamydial 60 M heat-shock
protein are associated with laparoscopically confirmed perihepatitis. Am J Obstet Gynecol
area of central Sweden. Sex Transm Dis 1996; 23: 384-91
1997; 176: 870-7
52. Scholes D, Stergachis A, Heidrich FE, Andrilla H, Holmes KK, Stamm WE. Prevention of
pelvic inflammatory disease by screening for cervical chlamydial infection. N Eng J Med
64. Harrison HR, Alexander ER. Chlamydial infections in infants and children. In. Sexually
transmitted Diseases. Holmes KK, Mardh P-A, Sparling PF, Wiesner PJ eds. New York:
1996; 334: 1362-6
McGraw Hill, 1990, pp 811-20
53. Stajano C. La reaccion frenica en ginecologica. Semana Med Buenos Aires 1920; 27: 243-8
54. Curtis AH. A cause of adhesions in the right upper quadrant. JAMA 1930; 94: 1221-2
65. Chandler JW, Alexander ER, Pheiffer TA, Wang SP, Holmes KK, English M. Ophthalmia
neonatorum associated with maternal chlamydial infeections. Trans Am Acad Ophthalmol
55. Fitz-Hugh T. Acute gonococcic peritonitis of the right upper quadrant in women. JAMA
1934; 102: 2094-6
Otolaryngol 1977; 83: 302-8
66. frommell GT, Rothenberg R, Wang SP, McIntosh K. Chlamydial infection of mothers and
56. 0nsrud M. Perihepatitt ved salpingitt. J Nor Med Assoc 1979; 33: 1705-6
their infants. J Pediatr 1979; 95: 28-32
57. Husebo OS, Bjerkeseth T, Kalager T. Acute perihepatitis. Acta Chir Scand 1979; 145: 4835
Van Dongen PWJ. Diagnosis of Fitz-Hugh Curtis syndrome by ultrasound. Eur J Obstet
Gynecol Reprod Biol 1993; 50: 159-62
67. Schachter J, Grossman M, Sweet RL, Holt J, Jordan C, Bishop E. Prospective study of
perinatal transmission of Chlamydia trachomatis. JAMA 1986; 255: 3374-7
58. Muller-Schoop JW, Wang SP, Munziger J, Schlapfer HU, Knoblauch M, Amman RW.
68
Rila Publications Ltd • CME BULLETIN Sexually Transmitted Infections & HIV • Volume 2 No.3