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| Journal of the New Zealand Medical Association,
26-November-2004, Vol 117 No 1206
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The development of cervical cytology and colposcopy in
New Zealand: 50 years since the first cytology screening laboratory at
National Women’s Hospital
Ronald Jones, Norman Fitzgerald
Cervical cytologyThe possibilities of gynaecological
cytology were first explored in New Zealand in 1947 by Dr Lindsay Brown, the
first pathologist at Cornwall Hospital (later named the National Women’s
Hospital, NWH) and two obstetric and gynaecological registrars, Drs Norris and
Holmden.1
Dr Jim Norris described and illustrated the findings of 50
cytology cases for his ‘book’—a prerequisite for the
examination of the Royal College of Obstetricians and
Gynaecologists.2 Dr Brown later indicated that
his initial studies did not point to any value in gynaecological
cytology.3
Another Auckland pathologist, Dr Jack Burton, reported
that
‘it
was decided in 1949 that the potentialities of the method (vaginal cytology)
should be investigated from the viewpoint of its local
employment’.4 ‘After a trial run
extending over a few weeks, detailed study was made of 260 smears taken from
over 140 clinic and inpatient cases, mostly from the gynaecology department,
Cornwall Hospital, Auckland’. ‘Malignant neoplasms were diagnosed by
the smear in 32 instances’
A paper by the NWH gynaecologist Mr Jefcoate Harbutt,
titled New Concepts in the Treatment of
Carcinoma of the Cervix, read at the First New Zealand Congress of the
Royal College of Obstetricians and Gynaecologists in 1955, commented that
vaginal smears
‘give
us the opportunity of making a diagnosis in pre-clinical asymptomatic cases and
their value has been substantiated. Mass screening, although acknowledged to be
ideal, has been found to be impractical from the economic viewpoint, but
selective screening of cancer prone patients should be part of the service in
any gynaecological
clinic’5
The advent of Professor Harvey Carey in 1953, the second
postgraduate professor at the NWH, was the catalyst for the development of
cervical cytology in New Zealand. Dr Stephen Williams, Pathologist-in-Charge at
Greenlane Hospital ‘agreed, reluctantly’ to process and examine
500–1000 cytology slides ‘to get Carey off his
back’.3 To his surprise, after about 200
specimens, a smear containing abnormal cells was detected in a symptomless
woman. This convinced Williams that cytology may have something to offer.
In 1958 Carey and Williams reported ‘surprise
positives’ in 2.4% of gynaecological patients and 3% of obstetric
patients.6 The same year, Carey reported to the
Auckland Hospital Board that (during a 3-year cytology survey) 20,000 smears had
been taken, and the lives of 40 women had been saved at a cost of ₤170
each.7
In 1966, Dr Herbert Green reported that in Auckland
‘about 60% of the provinces female population had been
screened’8—this was almost
certainly an over-estimate.
New Zealand’s first cervical cytology screening
laboratory was established at the NWH (Cornwall) in 1954, and according to Green
‘had
a fair start on the rest of New Zealand, Australia, and
Britain’.1 ‘In early years in line
with policy laid down by the British Empire Cancer Campaign and NWH the test was
restricted to women over 30 being examined for gynaecological reasons as opposed
to obstetrical’—‘by 1962 all women were offered
smears’9
The number of smears examined annually by the NWH laboratory
rose from 3250 in 1955 to 28,000 in 1962 and 40,000 in 1976. In 1955, 80 general
practitioners attended a course (sponsored by the Postgraduate School of
Obstetrics and Gynaecology, the Auckland Division of the British Empire Cancer
Campaign, and the NWH) for the early diagnosis of malignant disease, including
the cytology of desquamated cells in the sputum and the cervix. From this time,
smears were sent from all over New Zealand to NWH at a cost of
₤1.10.00—subsequently 15 shillings. Later, community laboratories
were paid 1 guinea to process and report a cervical smear. This fee was
subsequently halved.
In 1955, Dr John Sullivan was appointed
Pathologist-in-Charge at National Women’s Hospital, and in 1957 he studied
cytology with Dr George Wied (a student of Papanicolaou) in Chicago, USA. On his
return to New Zealand, he joined Williams in the cytology laboratory at Cornwall
Hospital. Sullivan was an active participant in the international debate on the
nature of carcinoma in situ (CIS),
commenting in one symposium that ‘the majority, if not all, invasive
cervical cancers are preceded by a preinvasive
stage’.10
From the mid-1950s, cervical cytology became established in
the other main centres. Dr JO Mercer encouraged a microbiology technician, Rani
Parker, to study cytology in the laboratory of Dr Ruth Graham, Buffalo, New York
State, USA. On Parker’s return to New Zealand, the Wellington Cytology
Laboratory was established. Most of the early screeners were former nurses.
Cytology, mainly of sputum and body fluids, commenced at
Christchurch Hospital in 1954. Cervical cytology commenced in 1957 when Dr
Alastair Burry returned following postgraduate training in Britain. Beau
Fitzgerald, a gynaecologist, established a cytology laboratory in the Department
of Obstetrics and Gynaecology in Dunedin in 1955, staining and reporting his own
smears—eight positive smears were reported in the first 1000 smears
taken.
Norman Fitzgerald, a pathologist, initiated a cervical
cytology and non-gynaecological cytology service within the Pathology Department
of the Otago Medical School in 1959. He later spent 2 years of postgraduate
diagnostic cytopathology training at the Johns Hopkins Hospital and University
of Maryland, USA and at the Churchill Hospital in Oxford, England. However,
cytology was not accepted with much enthusiasm by several New Zealand’s
senior pathologists, including Professor D’Ath.
130 doctors attended the first New Zealand Cancer Conference
held at the National Women’s (Cornwall) Hospital in 1959 under the
auspices of the New Zealand Branch of the British Empire Cancer Campaign (with
Dr George Wied, Chicago, USA as the guest speaker).
This served as a catalyst for the wider use of cytology in
New Zealand. It was at this conference that Wied suggested that New Zealand
should start a ‘national cervical screening
programme’,11 an event which did not take
place until the recommendation of the Cervical Cancer Inquiry three decades
later.12
At the 1959 conference, Dr Green, a young academic
obstetrician and gynaecologist is reported as saying:
‘thanks
to modern diagnostic techniques (referring to cervical smears) an increasing
number of cases of cervical cancer (referring to carcinoma
in
situ) are now discovered so early that
100% cures are possible...early cancer found in this way before any clinical
symptoms are present’...
‘treatment
could often consist of simple local surgery instead of removal of the uterus,
because smears taken after treatment would immediately reveal any recurrence of
the disease or incomplete
treatment’13...
‘nationwide
cervical screening for cancer of the cervix had to be kept within the bounds of
practical possibility’, indicating the vast increase in smear numbers and
‘new cases’11...
‘if
undiscovered or left undetected, a third of these ‘cancers’
(referring to CIS) would spread and be more difficult to treat within 9
years’13
This final statement fitted with international opinion that
about one-third of cases of CIS would eventually progress to invasive cancer. By
1966, Green was observing some cases of CIS following a small diagnostic biopsy
alone; striking evidence of his experimental approach to the management of CIS
of the cervix.14,15
In 1962, the College of General Practitioners supported by
the British Empire Cancer Campaign, promoted a national Cervical Smear Research
Survey through 337 doctors.16,17 17,000 women
were screened in the first year. It was noted that since oral contraception was
‘coming into vogue’ the survey was an ‘excellent opportunity
for a long-term study of the influence, which they have upon the incidence of
carcinoma in situ of the cervix’.
Thousands of brochures promoting the campaign were sent to
households all over the Auckland province, addressed ‘To the lady of the
house’. Coincident with the campaign, Professor Carey suggested that the
Thames area be chosen for a pilot community study of cervical cytology
screening. Dr McIndoe reported on the survey in 1964 and
1966.18,19 Dr Baerytz performed a similar
survey in Wanganui.20
The national GP register ceased in 1965 partly due to the
emerging debate of the value of screening following Green’s research.
Darby and Williams reported an ‘audit’ of the progress of the NWH
cytology laboratory in 1965, and commented that ‘with the present limits
of accuracy in the screening of cervical
smears...it seems that a substantial
reduction of incidence of invasive carcinoma could be expected rather than an
elimination of the
condition’.21
In 1976, Green described himself as a long-standing cervical
cytology ‘dissenter’ and a ‘doubting Thomas’, although
his views only became influential after Carey left NWH for Sydney, Australia in
1963.1
According to McIndoe, Carey’s move to Sydney
‘had
the most profound effect on the future development of cervical cytology and
colposcopy in Auckland: not immediately—but the strange ideas of Green and
his influence on the field in New Zealand would have been
controlled3
Green’s scepticism of cervical screening and the
‘premalignant’ nature of carcinoma
in situ had a significant adverse
influence on the development of cytology screening in New Zealand during the
1960s and 1970s. Not only did Green argue in the international scientific
literature that cytology screening did not influence the incidence or mortality
from cervical cancer, but he also vigorously promoted his ‘atypical
viewpoint’ in the New Zealand lay
press.14,22–25
In an article, following a 1970
New Zealand Herald newspaper headline
titled Cancer smear test
‘over-rated’, Green stated
‘in situ cancer is no more likely
to develop into invasive cancer of the cervix than in any other woman of the
same age’.23 In the same article, he
stated that ‘similar microscopic appearances to adult
in situ cancer could be demonstrated in
the infant cervix’.
In 1972, the New Zealand
Herald quoted Green as saying ‘that there was no positive evidence
that cervical smears were a reliable test for
cancer’.24 Following an
Auckland Star newspaper headline
titled Doubts about the wisdom of mass cancer
screening, Green reasserted that in
situ cancer is not a forerunner of invasive cancer; the article then went
on to state ‘Professor Green’s colleagues at National Women’s
do not necessarily agree with his
findings’.25
McIndoe regarded Green’s criticism of cytology in the
lay press as ‘implied questioning of the credibility and integrity of Dr
Williams (cytopathologist) and myself’ and set out in some detail his
response to the criticisms in a memorandum to the Medical Superintendent at
NWH—“It is not reasonable to expect members of the public to
appreciate there is a difference between ‘mass screening’ and
‘cytology as a diagnostic
discipline”.3
Both McIndoe and Williams challenged Green’s views in
the correspondence columns of the New Zealand Medical Journal in
1972.26 Subsequently, Dr JE Giesen, a
Wellington gynaecologist, provided support for McIndoe and Williams: ‘the
time has come for some counter to be made to statements emanating from Auckland
(ie, Green) from time to time to the effect that cervical cytology is of little
value’.27
Giesen’s letter provoked a response from Green
supporting the case for ‘diagnostic’ cytology in cervical cancer
while questioning ‘the wholesale and very expensive screening of
asymptomatic populations with the avowed aim of abolishing death from cervical
cancer’.28 Giesen silenced him with
‘Professor Green is entitled to his opinion, but it must be realised that
the vast majority of world authorities do not share
it’.29
The public and the profession were understandably confused.
On the one hand, the Cancer Society was actively promoting mass cervical
screening while on the other, a senior university professor was publicly stating
that cervical screening was a waste of time. In 1978, Professor Alan Clark from
the Department of Surgery at the Otago Medical School commented on a lay article
by Green and challenged his ‘iconoclastic views’, pointing out that
‘readers might be mistaken if they saw the article as an objective
scientific review simply because it had been written by an
academic’.30
As late as 1981, in a paper
titled Cervical cancer in New Zealand—a
failure of cytology?, Green continued to cast doubt on the
‘progression model,’ and the value of cytology screening in the
control of cervical cancer.31 Graeme Duncan, a
gynaecologist, was an enthusiastic supporter of cervical cytology, introducing
cytology screening of inpatients in the Wellington Hospital, teaching
colposcopy, and orchestrating the New Zealand Colposcopy Society. He also
challenged Green’s opinion on the relationship between cervical cytology
and cervical cancer incidence in New Zealand.32
It is noteworthy that, with the exception of Clark, the only
criticism of Green came from non-academics. It has been suggested that Green (as
Associate Professor and Deputy-Head of the Post Graduate School of Obstetrics
and Gynaecology) ‘had a significant impact on medical opinion and practice
relating to cervical screening’.33
In 1971, Dr Stephen Williams, Pathologist-in-Charge at NWH,
wrote to Dr George Wied in Chicago, USA
‘It
is unfortunate that our colleague (Green) should have developed an almost
obsessional view about the natural history of carcinoma
in
situ of the cervix, and there is no doubt
that his emphatically expressed attitude, coming, as it does from an influential
department, has brought confusion to the local scene.
I
believe that he is sincere, although perhaps bigoted, on this subject. He bases
his conclusions on the statistical interpretations and extrapolations of a
smallish series of cases, the composition of which has been questioned. It
appears that in a number of cases where invasion has clearly followed the
original in
situ diagnosis, he has reviewed the
histology himself (although he is not a trained histopathologist) and has
removed them from his series on the grounds that they were invasive carcinomas
from the outset.
There
is no doubt that he has created a good deal of uncertainty amongst the general
practitioners and medical students. Altogether it is an embarrassing and awkward
development, and one which does not appear to be susceptible to reasoned
argument and
discussion.’34
Obstetricians and gynaecologists were generally not
influenced by Green’s teachings. Occasionally, Green defended his position
on the natural history of carcinoma in
situ and screening with complex mathematical models and data analyses,
described by one critic as being ‘almost
uninterpretable’.22,35
In 1970, a paper by Green, which set out his view that
cytology had not influenced invasive cervical cancer incidence or mortality, was
used as a subject for debate by a number of eminent United States physicians,
and published in Modern Medicine in the
USA, but not in New Zealand.36,37
Green was strongly condemned by some contributors; for
example
‘it
is incomprehensible that in 1970 we are still debating the relationship of
carcinoma in
situ to invasive cancer’ (W
Christopherson); and
‘it
can be stated unequivocally that the Papanicolaou smear has done more to
eradicate invasive cancer of the cervix and lower the death rate from cancer in
women than in any other scientific contribution to date’ (M
Jordan).
None of the distinguished contributors offered any support
to Green, although one contributor generously suggested that Green’s
‘iconoclastic’ views might be considered ‘not proved’.
The correspondence on cervical screening in the
New Zealand Medical Journal in 1985
which among other issues led to the phrase ‘unfortunate experiment’,
illustrates much about Green.
Quoting the 1984 McIndoe et al
paper,(15,38) the Executive Committee (Drs
Duncan, Svensen, and Jones) of the New Zealand Society for Colposcopy and
Cervical Pathology provoked Green with
‘those
who questioned the value of cytology screening and the invasive potential of
intraepithelial neoplasia have now been clearly shown to be
wrong’
Green (again quoting McIndoe et al
1984)15,39 responded with his often-quoted
phrase:
‘invasive
cancer was never properly excluded in making the initial diagnosis of
in
situ cancer, or alternatively,
in
situ cancer was over-diagnosed in making
the final diagnosis of invasion. An
in
situ or invasive cancer is not necessarily
so because McIndoe, McLean, and Jones say so’
Green reiterated that screening had had no effect on
cervical cancer mortality. Professor David Skegg was drawn into the
correspondence, addressing Green’s ‘many misconceptions’, and
including the now well-known phrase ‘unfortunate experiment at National
Women’s Hospital’.40
While Skegg’s letter effectively silenced Green, it
does illustrate how Green unwisely allowed himself to be drawn into the debate
even after the results of his failed experiment had been reported in a leading
international medical journal. At this time, Green received brief support from
two academics, Drs Skrabanek and Jamieson who suggested that ‘listening to
and asking leading questions of a patient is far, far better than screening in
the control of cervical
cancer’.41
By the late 1960s, opportunistic cervical screening was well
established in general practice, obstetrics and gynaecology clinics, and
community clinics such as Family Planning. Questions relating to the
‘smear test’ were raised in Parliament in the early 1970s, although
it has only become a political tool in more recent times. In 1977, the New
Zealand Department of Health published Guidelines on the frequency of screening
based on the recommendations of the Walton Report from
Canada.42
The New Zealand Contraception and Health Study was an
impetus for improvements in the quality of cervical cytology reporting in the
1980s.43 This study was designed to assess
cervical epithelial changes, which might be associated with use of Depo Provera
(depot medroxyprogesterone;Upjohn Co Ltd) as a contraceptive agent compared to
other contraceptive modalities. While the study failed to produce any
significant scientific advances, it did improve the skills of New Zealand
pathologists and technologists, and liaison between the participating
laboratories.
The first meeting of the New Zealand Society of Cytology was
held in the National Women’s Hospital Cytology Laboratory on 30 April
1968, and attended by Dr Stephen Williams (Chairman), Dr John Sullivan
(Treasurer), and Mr Michael Churchouse (Secretary).
The Society continues to serve the dual purposes of
encouraging and providing education and collegiality between cytopathologists
and technologists. From the early 1960s, the NWH laboratory established a
reputation for training in cytology. Indeed, some authorities once considered it
to be the premier cytology training laboratory in
Australasia.44
Initially the only qualification was the USA-based
Cytotechnologist of the International Academy of Cytology. From 1964, training
courses for Technologist Trainees and Laboratory Assistants (the mainstay
workforce of all cytology laboratories) proceeded in parallel, beginning with
the Qualified Technical Assistant (QTA) after 2 years, then leading to the
Qualified Technical Officer (QTO) after 5 years. In addition, Stephen Williams
and Michael Churchouse, who were the driving force behind the training
programme, ran a Correspondence Course for students from Australasia and the
Pacific Islands. Cytology training also occurred in the other major public and
private laboratories.
From 1960, the responsibility for reporting the increasing
numbers of cervical smears mostly fell to the private pathology laboratories in
the main centres. With a few exceptions, the pathologists of the time were
self-taught using the textbooks and atlases of North American experts such as Dr
George Papanicolaou, Dr Ruth Graham, and Dr Leopold Koss. There were varying
degrees of expertise and interest in cytological diagnosis amongst the
pathologists and a general lack of understanding in the academic section of
pathology regarding the value of, and need for, special training in cytological
diagnosis.
Two studies marked the end of this opportunistic screening
era. In 1988, Jones et al estimated that 61% of eligible Auckland women were
being screened during a 3-year interval, with more than half of the women being
overscreened.45 A crude prevalence (CIN 1-3) of
5.3% was reported. The following year the New Zealand Health and Contraceptive
Study reported a crude prevalence of mild dysplasia or worse or worse of 4.3%,
in a population of women under 40 years.43
The emergence of a new generation of doctors led by
Professor David Skegg from Dunedin and the foundation of the New Zealand Society
for Colposcopy and Cervical Pathology in 1981 created a new awareness of the
importance of cervical screening and improved assessment of women with
abnormalities in their smear. The rising incidence of cervical cancer in younger
women prompted a joint Cancer Society and Department of Health working party
chaired by Professor Skegg. They reviewed the evidence for screening and
published their findings in 1985, commenting ‘it is remarkable how little
effort has been made to monitor screening practice in New
Zealand’.46
A follow-up meeting (again sponsored by the Cancer Society
and Department of Health) involving a range of professional and consumer
representatives discussed many of the issues relating to cervical screening and
recommended ‘a national cervical screening programme within 3–4
years’.47
These recommendations were overtaken by events following the
1984 publication of a paper titled The
Invasive Potential of Carcinoma in situ of Cervix (by McIndoe et al)
which described the outcome of a research programme on carcinoma
in situ of the cervix led by Professor
Green at the National Women’s Hospital.15
The events relating to that paper were subsequently published in an
Metro magazine article titled
An Unfortunate Experiment at National Womens
in 1987 by Sandra Coney and Phillida
Bunkle.48
As a result of that
Metro article, the New Zealand
Government initiated a judicial inquiry by Judge Sylvia Cartwright titled
Allegations Concerning the Treatment of
Cervical Cancer at National Women’s
Hospital.12 The inquiry name was a
misnomer since the investigation was into validity of the outcome of the (mis)
management of a group of women with a cancer ‘precursor’ (carcinoma
in situ), as presented in the paper by
McIndoe et al.15
Among the many recommendations of the 1988 report of the
inquiry was that a National Cervical Screening Programme (NCSP) be
established—three decades following Wied’s original suggestion.
Professor Skegg signalled early concern with the NCSP in a
paper titled How not to organise a cervical
screening programme.49 He expressed
concern at the Health Department’s ‘lack of open discussion’
and ‘consultation with health professionals, and with researchers who have
relevant experience’ but who had ‘decided to plan the programme
in-house’.
Skegg suggested that drawbacks can be minimised by careful
design and monitoring of a screening programme. Sadly, a cluster of cervical
cancers in Gisborne highlighted a systemic regional failure in cytology
reporting by a solo practitioner, leading to a further public
inquiry.50 Hopefully this will be the last
public inquiry into cervical cancer in New Zealand.
ColposcopyDr Ernst Navratil (of Graz, Austria)
described the use of colposcopy at a visit to NWH in 1958, thus prompting
Professor Carey to purchase a Zeiss colposcope in 1960.
Dr Bill McIndoe records
‘since
nobody knew how to use this instrument, it was placed in a cupboard and
virtually forgotten about. On my return to the hospital in 1961, I began
experimenting with the instrument, found it quite easy to manage, and was able
to visualise the cervix and take photographs without difficulty. I had no clear
idea of what I was
doing’3
McIndoe spent 4 months with Dr Malcolm Coppleson in Sydney
in late 1963, and stated ‘under his (Dr Coppleson’s) helpful
guidance, I began to appreciate the subtleties of colposcope
diagnosis’.3 Following McIndoe’s
appointment as Colposcopist at NWH in 1964, his only teaching aid was an Atlas
of Colposcopy written in German by Mestwerdt. Thus, for some time, McIndoe used
German terminology to describe his findings. Some years later, a small mobile
‘travelling’ colposcope was purchased by NWH and used by McIndoe in
several North Island towns (Hamilton, Napier, and New Plymouth)—both for
educational and service requirements.
McIndoe was an enthusiastic student of the technique, and a
Foundation Member and regular contributor at the International Federation for
Colposcopy and Cervical Pathology (IFCPC). His early colpophotographs appeared
in international texts. Drs Graeme Duncan (Wellington) Trevor Svensen
(Christchurch) and Ron Jones (Auckland) were responsible for the admission of
New Zealand to the IFCPC in 1981. While Green initially promoted colposcopy for
use in his study of CIS, he had little enthusiasm for the technique.
The early teaching of colposcopy was done on an
apprenticeship basis, principally by McIndoe in Auckland. Elsewhere, it was
largely a matter of having an interest in the technique, attending a 2-day
course, buying a colposcope, and learning by experience. Duncan established the
second New Zealand colposcopy service in 1973, and was seminal in formalising
teaching, with a number of courses in Wellington in the 1980s. Svensen commenced
a colposcopy service in Christchurch in 1978.
Rene Cartier, from Paris, and one of the international
doyens of colposcopy, was a close friend of McIndoe, and he ran three
‘Paris’ courses in New Zealand in the 1980s and early
1990s.
SummaryIt is to be hoped that the lessons
learned from the past half century will be considered by those persons
responsible for the evaluation of future technologies. In a relatively small
country like New Zealand, initiatives in healthcare are often determined by only
a few advocates, usually medical professionals. The beliefs of these individuals
need to be subject to rationale debate and increased reliance placed on sound
evidence-based practice.
Author information:
Ronald W Jones, Clinical Professor of Obstetrics and Gynaecology, National
Women’s Hospital, Auckland; Norman Fitzgerald, Pathologist, Southern
Community Laboratories, Dunedin
Correspondence:
Professor Ronald W Jones,
Gynaecology Service, National Women’s Hospital, Private Bag 92
189, Auckland. Fax: (09) 631 0746; email: DianeA@adhb.govt.nz
References:
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