Trepanning or trephines: a history of bone marrow biopsy

historical review Trepanning or trephines: a history of bone marrow biopsy Liakat A. Parapia Department of Haematology, Bradford Teaching Hospitals N...
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historical review

Trepanning or trephines: a history of bone marrow biopsy Liakat A. Parapia Department of Haematology, Bradford Teaching Hospitals NHS Foundation Trust, Bradford, UK

Summary Trepanning of bone is the oldest known procedure carried out by man and yet it is only in the last 100 years that we have made use of the technique to diagnose and treat haematological disorders. These advances have been made possible by improvements in instruments, techniques, anaesthesia, laboratory processing and the expertise of haematologists to report the specimens. With the advent of immunological markers and molecular biology, the need for quality bone marrow specimens, if anything, has increased. It will be many years before the bone marrow aspiration/trephine procedure is relegated to the annals of history. Keywords: bone marrow, trephine, trepanning, marrow aspiration, history.

Trepanning or trephines A concise history The oldest known procedure carried out on mankind is that of trepanning. Skulls 8000–10 000 years old showing evidence of medical intervention have been found in Europe, Northern Africa, Asia, New Guinea, Tahiti and New Zealand (Fig 1). This extensive distribution has been attributed to Asiatic origins. Many of these ‘patients’ survived as shown by evidence of healing of their bones (Fig 1). In Peru, from where a large amount of information comes, the procedure is likely to have been carried out to relieve headaches, mental illness and to relieve intracranial pressure. Peruvians used sharp knives of obidian, stone and bronze for trephination, as well as bone instruments, bandages, native cotton and other auxiliary items (Bender, 1966). One of the most spectacular operations described by Celsus, the roman physician, was trephination. He recommended it for removal of damaged cranial bones and as a therapeutic measure for relieving headaches. For the excision of small areas

Correspondence: Dr Liakat A. Parapia, Clinical Director, Pathology, Consultant Haematologist, Bradford Teaching Hospitals NHS Foundation Trust, Duckworth Lane, Bradford BD9 6RJ, UK. E-Mail: [email protected]

of bone Celsus described a specialized instrument, a surgical modiolus or crown trephine (Fig 2) (Jackson, 1988). ‘‘The modiolus is a hollow cylindrical iron instrument with its lower edges serrated; in the middle of which a pin was fixed. A small pit is made with the angle of a chisel for the reception of the pin, so that, the pin being fixed, the modiolus when rotated cannot slip; it is then rotated by means of a strap. When a way has been cut by the mediolus the central pin is taken out, and the mediolus worked by itself.’’ (De Medicina VIII, 3; trans. W.G. Spencer) (Jackson, 1988). Crown trephines (Figs 3 and 4) were used as late as the 1700s for therapeutic measures but not for diagnostic use (Jackson, 1988). Similar trephines have continued to be used by surgeons to the present day for therapeutic purposes on the skull (Fig 5). First attempts to obtain a bone marrow sample by surgical trephine for diagnostic reasons were undertaken by Pianese (Italy) in 1903 (Wintrobe, 1985). He punctured the top part of the epiphysis of a femur. He also described a case of anaemia because of bone marrow infiltration by Leishmania as ‘Leishmania Infantum’ (Sebastian, 1999). Ghedini (1908) suggested trephination of the medial part of the epiphysis of femur using a haematological spoon. However, he analysed tibial aspirates after tissue sections rather than marrow aspirates. His technique did not gain wide acceptance. Morris and Falconer (1922) introduced a method for tibial marrow biopsy using a drill like instrument that produced a marrow specimen very similar to that obtained today. Seyfarth (1922) developed a puncture needle for open biopsy of the sternal method at the point between 3rd and 4th ribs. He obtained satisfactory smears, touch preparations, wet preparations and blocks for sectioning. These procedures were carried out without benefit of adequate anaesthesia but gowns and gloves were recommended. In 1927, Anirkin, a Russian physician, obtained bone marrow from the sternum using a lumbar puncture needle. It is noteworthy that Anirkin worked at the same Military Medical Academy of Leningrad as the famous histologist Maximow, the illustrious psychologist Pavlov, and the last Tsar’s physician, Botykin, who is attributed for the first description of viral hepatitis. Anirkin published the results of 103 procedures in the Russian ‘news of surgery’ journal (Anirkin, 1929). No complications were reported. Anirkin claimed that marrow aspiration stimulated marrow activity! Anirkin’s technique was used not

ª 2007 The Author doi:10.1111/j.1365-2141.2007.06749.x Journal Compilation ª 2007 Blackwell Publishing Ltd, British Journal of Haematology, 139, 14–19

Historical Review

Fig 1. Edinburgh Skull, trepanning showing hole in back of skull – (Wellcome Library, London).

Fig 3. The Surgeon’s Mate. Instruments for trephination, including the trephine designed by himself. (Wellcome Library, London, UK).

Fig 2. Two bronze crown trephines and the folding handle used to rotate them Picture courtesy of Romisch-Germanisches Zentralmuseum, Mainz, Germany.

only for haematological disorders but also for the recognition of typhus and tuberculosis. Peabody (1927), carefully prepared sections of curetted tibial marrow from patients with Pernicious anaemia were described. Arjeff (1931) introduced needles with a guard and Grunke (1938) still recommended a short lumbar puncture needle for marrow aspiration with the help of a wooden mallet on the sternum. The report by Custer and Ahlfeldt (1932) included an account of their experience with biopsy of the sternal marrow. A disk of the ventral plate of 1 cm diameter was removed with a trephine, an elaborate operating technique at the time. This report also demonstrated the value of obtaining histological sections and touch preparations of the marrow compared with examining smears. KLIMA NEEDLE-1935 (Fig 6). The needles developed by Klima and Rosegger (1935) have guards. Leitner further

modified the needle with the guard running on a thread. An example of a winged needle is shown in Fig 7. A modern Salah needle with a guard is shown in Fig 8. The later was probably the commonest in use in the late 20th century. Henning and Korth (1934) suggested a cannula with a side opening to facilitate irrigation of the marrow cavity. Their cannula was graduated in centimetres. These authors stated that they could obtain bone marrow by injecting 1 ml of heparin or sodium citrate solution even when simple puncture had failed. They rarely carried out marrow irrigation. Until 1939, many authors felt local anaesthetic was unnecessary (Leitner et al, 1949). Between 1929 and 1938 bone marrow samples were taken from healthy volunteers. Faber, Anirkin’s assistant, published the results of normal bone marrow. It seems probably that the first deaths were reported in 1943 and 1944 following sternal punctures; the sternum was completely punctured and the right side of the heart penetrated. It was then recommended that the sternal puncture needle be driven through the outer plate of the bone by gentle taps from a small hammer (Whitby & Britton, 1946). Turkel and Bethell (1943) described a microtrephine of about 2 mm bore, which could be passed through a hollow introducing

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Historical Review

Fig 4. Tourniquets & Trepanning Medical Instruments Print 1764 (Author’s collection).

Fig 5. A 19th-century crown trephine (Author’s collection).

Fig 7. A winged aspiration needle (Author’s collection).

Fig 8. Salah needle (Author’s collection).

Fig 6. Sternal marrow needle. Klima’s pattern, modified by Leitner (1949) (Author’s collection).

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needle only slightly larger than a marrow aspirating needle. No skin incision was necessary and it could be used on the sternum! The samples obtained were small and fragile.

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Historical Review

Fig 9. Waterfield needle designed for aspiration from the iliac crest (Author’s collection).

Although the pelvis contains 50% of the body’s marrow, it was not until 1950 that the pelvis was suggested as a source of a specimen (Rubinstein, 1950). One assumes that prior to this, either suitable needles were not available or the site not considered. Bierman (1952) first suggested using posterior iliac crest, which is the preferred site for both aspiration and biopsy. The Sacker-Nordin trephine (Sacker & Nordin, 1954), which could safely be used on the iliac crest, provided sufficient material for accurate diagnosis. Waterfield modification iliac crest aspiration is shown in Fig 9. In response to a 5% failure rate in carrying out aspiration biopsies, McFarland and Dameshek (1958) described a technique for trephine biopsy using the Vim-Silverman biopsy needle (Silverman, 1938). These biopsies were carried out in left lateral position from the right iliac crest using local anaesthetic and without incision of the skin. Ellis & Westerman (1964) reported on 1445 cases using a modification of the Vim-Silverman needle between 1959 and 1963. The modified needle contained finger grips, an assembly stylet and an obturator that locked in position, in addition to being larger and sturdier. These biopsies were often carried out in the outpatient department, and 5% were unsatisfactory for analysis. The biopsy was of specific diagnostic value in 11% of cases where an aspirate alone would not have been sufficient. The transilial wide bore needle was designed to obtain ‘transfixing’ or cortex to cortex iliac crest biopsies (Bordier et al, 1964). A commonly used trephine needle in the 1960s/ 1970s was the Gardner’s trephine needle with a serrated end (Fig 10). In 1971 Khosrow Jamshidi, a citizen of Iran, had his patent application published (no. 1252170). The interior diameter of the distal portion was tapered radially towards the cutting tip (Fig 11). This design allowed tissue to freely enter the lumen and avoided crushing of the tissue (Jamshidi & Swaim, 1971). Biopsies taken with an electric drill were performed exclusively from the anterior iliac crest (Burkhardt, 1971). In

Fig 10. Gardner’s trephine needle with serrated end for iliac crest biopsy (Author’s collection).

Fig 11. Jamshidi trephine needle. Photo supplied courtesy of Cardinal Health, Inc. All rights reserved.

Fig 12. Islam trephine needle (Author’s collection).

1988, a patent application was filed for a powered biopsy needle (Parapia et al, 1988, Patent application no. 8817008) that had a replaceable and disposable needle. After market research it was felt that, in view of the excellent nonmechanical biopsy needles available, it should not be introduced. However, Islam (1982) described an improvement whereby sampling error was reduced. The needle (Fig 12), designed to obtain marrow samples from the posterior iliac crests, had 14 side holes in the distal portion of the needle. The proximal end of the needle was fitted with a large metal bar allowing a firm grip and smoother operation (Islam, 1982, 1997).

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Historical Review

Bone marrow morphology Nucleated red cells were first observed in the bone marrow by Neumann (1868). He also discovered the transformation of fatty marrow into red haemopoietic tissue in anaemia. Schilling (1925) showed the importance of the clinical examination of the blood. A microscopic examination of bone tissue in a blood disorder was done in 1846 by John Dalrymple (1804–1852) of Dublin on a patient with multiple myeloma (Sebastian, 1999). The value of morphological examinations of the blood was shown by Ehrlich (1879), who used appropriate staining methods to classify the various blood and bone marrow cells. Pappenheim (1898) built on the findings of Ehrlich (1891) by using Romanowsky eosin and methylene blue, which permitted better cell differentiation. Naegeli (1900) and Schilling (1925) soon began to link up the reactions of the peripheral blood with changes at the site of origin of the red cells. Investigations at first depended on postmortem findings. By the 1940’s the heterogeneity of even the lymphocytes was recognized. More recently, haematological diagnoses have been much enhanced by the addition of flow cytometry and molecular genetics. The modern biopsy needles (Figs 13–15) are very similar to those used in the past. The main areas of progress have been in improving the success rate of acquiring a satisfactory sample with, for example, a Traplok needle. This features ‘forceps’ that capture large undamaged samples. Local, intravenous and general anaesthesia have reduced the amount of pain suffered by the patients undergoing biopsies, but improvements in adequate analgesia continue (Johnson et al, 2007). Marrow needles are rarely used for fluid administration. A modern example is shown in Fig 13. Economical disposable needles will be increasingly available as more suppliers compete for the market. Better accuracy in reporting has made the acquisition of a good quality biopsy almost mandatory. For the foreseeable

Triple- crown cannula tip

Jamshidi marrow acquisition cradle Fig 14. T-handle modern disposable bone marrow biopsy/aspiration needles with triple-crown cannula tip.

Fig 15. Modern disposable Jamshidi marrow aspiration and biopsy needles with specimen retention system. Photo supplied courtesy of Cardinal Health, Inc. All rights reserved.

Fig 13. Modern marrow needle for administering transfusion.

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future there is no prospect of trephine biopsies losing their appeal. It is possible that there may be room for an easier and less painful method of carrying out this procedure, for example the quality of needle biopsies may be further improved to reduce ‘failure’ rates and pain. Hopefully, with modern advances in molecular diagnosis, blood sampling and aspiration biopsy specimens alone may suffice.

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Klima, R. & Rosegger, H. (1935) Zur methodik der diagnostschen sternalpunktion. Klinische Woechenschrift, 14, 541–542. Leitner, S.J. (1949) Bone marrow biopsy, Haematology in the Light of Sternal Puncture (ed. by C. J. C. Britton and E. Neumark ), pp. 5–10. Churchill Ltd, London. McFarland, W. & Dameshek, W. (1958) Biopsy of the bone marrow with the Vim-Silverman needle. Journal of the American Medical Association, 166, 1464–1466. Morris, L.M. & Falconer, E.H. (1922) Intravitum bone marrow studies II. Survey of the clinical field. Archives of Internal Medicine, 30, 490– 506. Neumann, E. (1868) Ueber die Bedeutung des Knochenmarkes fur die Blutbildung. Zentralbl Med Wissensch, 6, 689. Naegeli, O. (1900) Uber rothes Knockenmark und Myeloblasten. Deutsche Medizinische Woechenschrift, 18, 287–290. Pappenheim, A. (1898) Abstammung und Entstehung der rotten Blutzelle. Virchows Archiv (Pathological Anatomy and Histopathology), 151, 80–158. Parapia, L.A., Cox, J. & Brown, G. (July 1988) Powered biopsy needle, British Patent Application No. 8817008.9. Peabody, F.W. (1927) Pathology of bone marrow in pernicious anaemia. American Journal of Pathology, 3, 179–202. Rubinstein, M.A. (1950) The technic and diagnostic value of aspiration of bone marrow from the iliac crest. Annals of Internal Medicine, 32, 1095–1908. Sacker, L.S. & Nordin, B.E.C. (1954) A simple bone biopsy needle. Lancet, I, 347. Schilling, V. (1925) Das Knochenmark als Organ. Deutsche Medizinische Wochenschrift, 51, 261–264, 344–348, 467–469, 516–518, 598– 600. Sebastian, A. (1999) A Dictionary of History of Medicine, Partheon Publishing Group, New York, pp. 137. Seyfarth, C. (1922) Eine einfache methode zur diagnostichen Entnahme von knochenmark beim lebenden. Arch fur Schiffs-und TropenHygiene, Pathologie und therapie exotischer Krankheiten, 26, 337–341. Silverman, I. (1938) A new biopsy needle. American Journal of Surgery, 40, 671–672. Turkel, H. & Bethell, F.H. (1943) Biopsy of the bone marrow performed by a new and simple instrument. Journal of Laboratory and Clinical Medicine, 28, 46–51. Whitby, L.E.H. & Britton, C.J.H. (1946) Disorders of the Blood. J & A. Churchill Ltd, London, pp. 704. Wintrobe, M. (1985) Haematology, the Blossoming of a Science: A Story of Inspiration and Effort. Lea & Febiger, Philadelphia, PA, pp. 58.

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