Early microscopy: history of fine needle aspiration (FNA) with particular reference to goitres
2001; Wiley; Volume: 12; Issue: 1 Linguagem: Inglês
10.1046/j.1365-2303.2001.00276.x
ISSN1365-2303
Autores Tópico(s)History of Medical Practice
ResumoSurgeons of the late 18th and early 19th centuries were accomplished macroscopists. The printed water colour plates of gross disease in Sir Astley Cooper's Illustrations of the Diseases of the Breast (1829)1 almost surpass the colour photography of our day. But they lack any form of reliable microscopy as the compound instruments of that time were flawed. There did exist a group of optical pioneers working in Europe and Great Britain, but Joseph Jackson Lister (father of Lord Lister), together with Thomas Hodgkin,2 by combining two forms of glass objectives and calculating the relevant optical distances, designed a compound microscope largely free of both chromatic and spherical aberration. These optical principles were quickly adopted in Europe but somewhat later in London. Because of this invention, scientific microscopy had begun. Astonishing progress was made in European centres (Paris, Berlin, Breslau, Vienna) thereafter and descriptions of natural and pathological tissue began to appear in the literature. It is widely accepted that the first graphic illustrations of tumour tissue — which would in retrospect be regarded as valid — came from Johannes Müller, a physiologist in Berlin.3 His small volume On the Nature and Structural Characteristics of Cancer, etc., contains many drawings of natural tissue and tumour cells made from scrape smears sent to him by colleagues. The explosion of reliable optics translated into dramatic changes in the definition and understanding of disease epitomized by advances in the 1860s.4 Although contemporary surgeons wrote on the subject of clinical error, particularly in breast lumps, a survey of 66 surgical textbooks (European, British and American) for the whole of the 19th century revealed very few which mentioned the idea of 'biopsy'. There were some indications of the use of puncture by trocars and grooved needles to detect cysts or deeply placed abscesses.5 The earliest report of a needle technique being employed to obtain material for microscopy was by Kün (1847) of Strasbourg.6 He described an exploring needle incorporating a depression at the tip, with cutting edges, for extracting tissue from a subcutaneous tumour. The yield was smeared. A similar technique was probably used by Lebert (1845) whose third volume of Physiologie Pathologique was an 'Atlas of Cells'.7 In London, Paget (St Bartholomew's) and Erichsen (University College Hospital),8 in separate publications, extolled the grooved needle and microscopy for diagnosis, especially for breast diseases. But this style of investigation was limited to very few surgeons. Paget, in addition to his many other gifts, was a superb early microscopist and cytologist. He read French and German so was fully aware of European developments. His descriptions and illustrations in Lectures on Tumours (1853)9 were decades ahead of his time. Contemporary illustrations of grooved needles reveal that they were 'large' in diameter (2–4 mm).10 It is important to understand that these puncture techniques did not involve any form of aspiration. A major problem for microscopists at this time was the absence of suitable stains. However, the decade 1870–1880 and around then witnessed a dramatic change. Tissue stains were discovered and mechanical microtomes so improved that thin, well-stained sections of tissue could be made. These were easier to read than scrape or puncture smears so, by 1890, there was an eclipse of early tissue cytology. The development of needles and syringes in medical practice began in 1853 when Wood (Edinburgh) employed a simple instrument for hypodermic injection of drugs. There were many subsequent modifications but by 1890–1910 there was much technical improvement resulting from the inventions of Luer (Paris 1896) and Record (Berlin 1906).11 Before then, syringe and needle exploration was reported in a minority of surgical texts for relieving pus and fluid, but not for aspiration and microscopy. Wyeth (1892)12 described and illustrated an exploring needle and syringe from which it is evident that the needle size was 'large' (2–3 mm diameter). The dimension of ≤ 1 mm has come to be accepted as the definition of 'thin' or 'fine'. The next event smacks of serendipity, but it is critical in the development of FNA. Captain E.D.W. Greig and Lieutenant A.C.H. Gray were military doctors seconded to the Sleeping Sickness Commission which was investigating trypanosomiasis in Uganda. They employed a hypodermic syringe and needle (size not stated) to aspirate the enlarged cervical nodes of sufferers. From microscopy of the 'node juice' they identified motile trypanosomes. Their findings were reported by a Captain Bruce (later of Brucellosis fame) in a British Medical Journal memorandum in 1904.13 Soon afterwards there were other reports of a similar technique to puncture and diagnose lymph nodes infected by leishmaniasis and secondary syphilis.14 Guthrie (1921),15 from the John Hopkins Hospital favouring a 2-mL Record syringe and a 5-cm long 21 gauge needle (0.8 mm diameter) reported cytological smears on a variety of pathology including Hodgkin's disease. Around this time there were other isolated reports of node puncture.16 Thereafter the extension of FNA (0.8–1.0 mm diameter needles) was pursued by scattered investigators in Europe and South America,17–19 mainly clinicians with a haematological interest. The technique was largely but not exclusively applied to lymphadenopathy. In the mid-1920s there were attempts in New York and Chicago to employ large needle (1.2–3.0 mm) aspiration for a variety of disease sites ranging through lymph nodes,20 prostatic disease and bone tumours.21 This procedure was designed to extract small fragments of tissue for histological, not cytological examination. A far more systematic study evolved at the Memorial Centre, New York in the mid-1920s, resulting from a controversy related to the ethos and practice of biopsy as such. Hayes E. Martin, a young head and neck surgeon, was at odds with James Ewing, the Chief of Pathology and insisted that he required some form of tissue diagnosis in order to advise and manage his patients appropriately. A compromise was reached. Around 1926, employing an 18 gauge (1.2 mm) needle coupled with a 20-mL Record syringe, aspiration biopsy was performed on a variety of neoplasms. The yield was for both histology and cytology. Heat fixed, rapidly stained by haematoxylin and eosin (H & E), smears were made and seminal reports appeared in the early 1930s.22,23 Vast experience was accumulated (approximately 2500 tumours annually) and Stewart,23 the histopathologist, enunciated fundamental principles regarding the philosophy of aspiration biopsy and emphasized the need for close clinical and pathological co-operation. This group was never confident with needle biopsy for the diagnosis of lymph node, thyroid and salivary pathology, but their approach coincided with a fierce controversy both in Great Britain and the USA over the reliability and risks of biopsy in surgical practice. However, needle biopsy continued at the Memorial Centre, but by the 1950s had fallen away for goitres and salivary gland disease. Certainly the overall principle of aspiration biopsy was rejected in the USA until many decades later. Contemporaneous and important study of tissue cytology was progressing at St Thomas' Hospital,24 derived from scrape smears of fresh tissue. Needle aspiration was never performed or even considered. The result was a well-illustrated and careful appraisal of the whole principal of cytodiagnosis and, had Professor Leonard Dudgeon not died in 1938, it is possible that clinical cytology might have advanced in Great Britain ahead of the USA and G.N. Papanicolaou. But it did not. The first half of the 20th century was a 'dark age' for biopsy in general: a review of 50 surgical textbooks (1900–65) detected very few mentions of this subject. There was an exception. Neurosurgeons had early realized the value of large cannula (Dandy, 2 mm diameter) aspiration of brain tumours via a burr hole.25 Tissue fragments were fashioned into wet-fixed smears. This approach remained popular and a comprehensive and well-illustrated monograph appeared in 1997.26 FNA had, through the late 1930s, continued in regions of Europe and into the Second World War period so that articles and comprehensive monographs on a wide range of organ puncture appeared in the 1940–60 era.18,19,27,28 It is important to re-emphasize that many of the involved clinicians were also haematologists. The first edition of Cardozo's monograph and atlas27 covered many needle puncture sites and set down important principles of clinical cytology. In company with others in Europe and South America, his style was the air-dried, methanol fixed, Romanowksky (Giemsa) stained smear. This contrasted significantly with the Memorial group where H & E was favoured. Thyroid puncture and cytology was slow to emerge from the general practice of FNA. For one reason, it was a difficult area of cytodiagnosis. Stewart (1933)23 relating the Memorial experience, had encountered no difficulty in identifying anaplastic thyroid carcinoma, stating: 'But the diagnosis of papillary and follicular tumours vs. active hyperplastic Graves' disease or colloid adenoma has not been consistently possible'. Goitre FNA did, however, develop in three regions. In Uruguay, Piaggio Blanco, Paseyro and colleagues29 reported on both tumour diagnosis and the value of smears to study immunological aspects by a simple precipitin agar gel test on the thyroid aspirate. From Europe the results of goitre FNA emerged from Cracow,30 Paris,31 Marseilles28 and Leiden.27 Developments from Scandinavia were, however, of the utmost and fundamental importance. The Swedish school of aspiration biopsy — known there as ABC — centred upon the Stockholm Karolinska Radiumhemmet Hospital — but not exclusively so. The first publication was by Söderström (1952)32 from Upssala and later Lund. This contribution began in the early 1950s and has been immense in both teaching and influencing clinicians to adopt FNA as an expeditious, cheap, safe and reliable means of diagnosis.33,34 The sheer volume, histopathological correlation, scientific rigour and follow-up information, coupled with superbly illustrated publications within an ethos among the medical profession to allow the technique free reign, explains this notable success. The emphasis was on 'front line' performance. Their practice invented a novel speciality of 'clinical cytologist' who would examine the patient, aspirate the lesion, read the slides and arrange subsequent onward referral.33 The adoption of goitre FNA elsewhere has been both hesitant and intermittent. In Great Britain reports appeared in the late 1970s and early 1980s35 and it has slowly gained in popularity since then. In North America publications from both Canada and USA did much to further FNA as opposed to large needle core biopsy.36,37 But widespread usage has been tempered by well-publicised caveats over excessive reliance on cytodiagnosis.38 Puncture without aspiration was proposed and developed in Paris by Zajdela and colleagues (1987)39 and has received limited support for vascular organs such as thyroid and spleen. Attempts have been made to address the problem of distinguishing follicular lesions of the thyroid by the use of nuclear morphometry;40 but this remains an area of intense controversy. In addition, there have been arguments over the matter of terminology — as yet unresolved — but philosophical and semantic arguments have led to fine needle aspiration (not biopsy) being favoured by the British Society for Clinical Cytology. During the past 20 years the principle of preoperative diagnosis before surgical intervention, particularly for breast, salivary gland and thyroid disease, has gained acceptance; while FNA is also popular in the management of some abdominal, pelvic and soft tissue tumours. But there remains a body of opposition to the principle of FNA cytodiagnosis and its clinical utility. The concept of preoperative atraumatic diagnosis has, however, not been rejected. The emphasis has partially reverted to minute biopsy fragments for histopathology. Some critics favour a fine needle drill instrument for core diagnosis.41 An example of the controversy is seen in the management of breast lumps in general and nonpalpable screening abnormalities in particular. There is continuing debate as to whether FNA cytology or core (2 mm diameter) needle for histology is preferable. The matter may never be settled and practice will depend on personal experience, enthusiasm and prejudice. Orell (1992)42 fears that FNA may fall away because of poor training and professional pressures. Much would be lost in medical and surgical practice if that happened: but the discipline does demand consistently close liaison between enthusiastic clinicians and equally keen cytopathologists for a good reputation to be maintained. In goitres, core biopsy has never become popular and FNA is extensively practised, albeit with some inherent problems and pitfalls. These can be overcome or realized within informed and well audited clinical practice. The position is summarized by the Aberdeen Group as follows: 'Despite its apparent limitations, however, routine aspiration cytology has alerted us to the risk of neoplasia and malignancy in dominant thyroid swellings … . we still consider it the most valuable and only appropriate investigation.'43
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