Gut: first published as 10.1136/gut.30.Spec_No.17 on 1 November 1989. Downloaded from

Gut Festschrift, 1989, 17-21

William Hillary and sprue in the Caribbean: 230 years later

COURTENAY BARTHOLOMEW

Aretaeus from Cappadocchia, which was at that time Caribbean other than Barbados. By now it was part of the Greek Empire and is now part of present thought to be a disease which affected predominantly day Turkey, left us an account of sprue in Chapter European and American expatriates living in the VII of his extant works entitled 'On the Coeliac tropics and sparing the indigenous populations. On Affection'.' This was in the second or third century the other hand studies of native populations in AD and probably refers to coeliac sprue. South India, reported by Baker in 1951,' showed that More than a millenium later, in 1747, an English- tropical sprue was not limited to expatriate residents. man, more specifically a Yorkshireman, migrated to This has been confirmed by other investigators. the Caribbean island of Barbados which had been a In more recent times, another Yorkshireman, British colony since 1627. This Yorkshireman, Dr Christopher Booth, kindled my interest in small William Hillary, came to practice medicine but was bowel disease when I was a student at the Post- also a systematic observer of the weather and its graduate Medical School at Hammersmith in 1963. relationship to disease. He began these observations Obtaining biopsies of small bowel mucosa had been in Ripon in England and resumed them in Barbados. pioneered by Shiner and Crosby and the dissecting

In 1759, he published one of the earliest books in microscope became to the gastroenterologist what copyright. the English medical literature on tropical diarrhoeal the ophthalmoscope was to the ophthalmologist. As disease which occurred more frequently in native we peered through its lenses we enjoyed the slender Barbadians than in white settlers. It carried the beauty of normal finger-like villi, the brain-like con- cumbersome title Observations on the changes of the volutions of patients with the sprue syndrome and the air and the concomitant epidemical diseases in the denuded mosaic mucosa of those with severe coeliac Island of Barbadoes, to which is added a treatise on disease as described by Holmes, Hourihane and the putrid bilious fever, commonly called the yellow Booth.6 http://gut.bmj.com/ fever; and such other diseases as are indigenous or In those early days, Chris Booth would ask his endemical in the West Indian Islands.' This book was students, 'If you had one test, and only one test, to published by Hawes, Clarke, and Collins in London make a diagnosis of coeliac disease, what would you and a copy can still be found in the Barbados choose?'. The answer he expected was 'a small bowel Museum. biopsy'. At that time it was thought that a flat mucosa In 1880, Manson was probably the first to use the was diagnostic of coeliac disease but regarding term 'sprue' for the wasting illness with diarrhoea tropical sprue the situation was less clear. At the 1962 occurring in some tropical countries. Apparently this meeting of the CIBA Foundation Study Group on on September 25, 2021 by guest. Protected is an anglicised version of the Dutch word 'sprouw' Intestinal Biopsy held in honour of Professor C which Ketelaer4 had given to a diarrhoeal disorder Jimenez Diaz, professor of medicine in Madrid,h with aphthous ulceration occurring in Holland and Tom Hendrix of Johns Hopkins, Baltimore, asked which is now believed to be coeliac disease. Vincent Charlotte Andersen of the Royal Childrens Hospital, Ketelaer was a Dutch physician who was rector of the Melbourne, 'Have you seen a flat biopsy in any Gymnasium of Zierikzsee. His treatise, De aapthis patients who do not respond to a gluten free diet?' To nostratibus seu Belgarum Sprouw (concerning native this she replied 'no, so far I have not seen a really flat aphtha or sprue of the Belgians) first appeared in biopsy in any other clinical situation'. Then Cyrus 1669 and was reprinted several times. It gave another Rubin from Seattle commented'. . while experience very clear description of sprue but is differentiated teaches that one cannot be dogmatic about such from the clinically somewhat similar disease occur- matters, at present it would appear that, with the ring in the tropics which was subsequently called exception of tropical sprue, the characteristic lesions 'tropical sprue'. are found only in coeliac disease and idiopathic By the early part of this century, tropical sprue was steatorrhoea'. With the passage of time and tide, also recognised in the Indian subcontinent, in Ceylon however, experience did teach us otherwise. On (Sri Lanka), in South East Asia and in islands of the intestinal biopsies and tropical sprue Booth had this 17 Gut: first published as 10.1136/gut.30.Spec_No.17 on 1 November 1989. Downloaded from

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r , rl i to say, 'In our studies of jejunal biopsies obtained ally determined difference in response to a hypo- http://gut.bmj.com/ from patients with tropical sprue we have never thetical infection. The fact that African troops seen the flat appearance. The jejunal mucosa in in Burma were not affected during World War II these patients has invariably shown a convoluted lends support to this view'." On the other hand appearance. There is no suggestion of a flat mosiac F Klipstein'3 denied the presence of a racial factor pattern. ..' With perhaps a rare exception this rule because tropical sprue is common amongst persons of still holds true. African descent living in Haiti. In 1970, Moshal et al4 After leaving London I spent two years as Donner from Durban reported that in the first 12 months after research fellow at the Royal Victoria Hospital, the establishment of a gastroenterology unit in the on September 25, 2021 by guest. Protected Montreal. This further whetted my appetite for the King Edward VIII hospital, eight cases of an illness study of small bowel disease but in 1967, when I resembling tropical sprue were seen amongst returned to a permanent position in Trinidad I found Africans and he concluded that the establishment of that sprue was rarely recognised in the Caribbean more specialist units in Africa would lead to more islands. cases being found as well as a variety of diseases In 1970, Mike Ashcroft of the MRC Epidemiology associated with secondary malabsorption. Unit in the University of the West Indies recorded Over the past 20 years several physicians with a that E K Cruickshank (professor of medicine) had special interest in gastroenterology have been not seen a single case of tropical sprue in the period appointed to hospitals in the Caribbean. Yet up to 1950-1970.7 Similarly, Banwell et al,x" Foy and this year, 230 years after Hillary's publication, not a Kondi,"' and Cook' were unable to find tropical single case of tropical sprue has been documented in sprue in Africa. A W Woodruff in his textbook, Trinidad and Tobago, neither in expatriates here, Medicine in the tropics, speculated that 'Although nor in those who have returned to their original tropical sprue occurs widely in the tropics this does homes, nor in the indigenous population. The same not apply to Africa and its virtual non-occurrence in applies to the other English speaking Caribbean the people of that continent may indicate a genetic- islands, including Barbados (C Edwards, personal Gut: first published as 10.1136/gut.30.Spec_No.17 on 1 November 1989. Downloaded from

William Hillary and Sprue in the Caribbean: 230years later 19

Fig. 1 Histology ofjejunal mucosa ofthefiat type showing Fig. 2 Higher magnification ofjejunal mucosa showing S stercorales in the crypts. S strongyloides curled in crypts. communication 1989). It is remarkable that we are condition2' we first recognised cases of a sprue-like unable to find any document recording the history of syndrome in patients with chronic diarrhoea, the decline of tropical sprue in Barbados. In contrast, peripheral oedema, marked weight loss, anaemia, studies by Rodriguez-Molina,5 Milanes,'6 and and hypoproteinaemia.22 In one case the mucosa was Sheehy et al'2 have shown evidence that the incidence flat when viewed through the dissecting microscope. of tropical sprue has declined in Puerto Rico and In 1963, we would have thought this to be a case of copyright. Cuba, but it is said to have remained widespread adult coeliac disease. Through the light microscope, among the rural population in Haiti. An explanation however, there was not only subtotal villous atrophy is certainly needed to account for the present as seen in coeliac disease but also numerous ova and restriction of sprue to the Spanish and French adult forms of strongyloides stercoralis lying curled speaking Caribbean islands (Cuba, Puerto Rico, the up in the crypts of Lieberkuhn (Figs 1 and 2). Dominican Republic, and Haiti) and its absence from Parasitic infestation as a cause of diarrhoea and

the English speaking Commonwealth chain of islands malabsorption is well recognised. It may occur in http://gut.bmj.com/ from Jamaica in the north to Trinidad and Tobago heavy infestations with hookworm as reported by farthest south. Sheehy in Puerto Rico23 and with Giardia lamblia as The patchy occurrence of tropical sprue in the reported by Professor O'Donovan of Dublin.24 In Tropics also remains unexplained and indeed after hookworm and giardial infestations tissue invasion of years of extensive research the aetiology of tropical the small intestine has been observed occasionally25 sprue remains elusive. Its restriction to the Tropics but Strongyloides stercoralis has much greater suggests that an infectious agent may be involved but potential in this respect. A sprue-like syndrome despite many efforts none has been identified neither caused by this parasite is not uncommon in the on September 25, 2021 by guest. Protected by culture nor by direct observation through the Caribbean islands, particularly in Jamaica,26 Trinidad electron microscope. A viral aetiology remains a and Tobago,22 and Puerto Rico.27 Under the light possibility." I would remind you that in the West microscope the mucosal surface may appear normal Indies we had a similar problem with the aetiology of but more often there is partial villous atrophy. Our tropical spastic paraparesis.'9 It was not until 1986 observations show that occasionally there is complete that a type C retrovirus (the human T-cell leukemia/ flattening of the mucosa and so strongyloidiasis must lymphoma virus, HTLV-I) was found to be associ- be added to the ever increasing which ated with this tropical syndrome. cause subtotal villous atrophy. The inflammatory The absence of sprue in the English speaking response in the interstitial mucosa is characterised by Caribbean is not restricted to the tropical variety. a local eosinophilia and an increased number of Coeliac sprue is also rarely seen. For example, since plasma cells. Sometimes filariform larvae may be 1967, only one case of adult coeliac disease has been found in the enlarged mesenteric nodes and the recognised in Trinidad and Tobago and that was in a sinuses may be packed with macrophages, poly- Trinidadian with Caucasian ancestry. Similarly morphonuclear neutrophils and a few eosinophils. coeliac sprue is rare in Africa.' On the other hand Radiological studies in strongyloidiasis have lactase deficiency is common and in studying this also shown a sprue-like pattern.28 In the Trinidad Gut: first published as 10.1136/gut.30.Spec_No.17 on 1 November 1989. Downloaded from

20 Bartholomnewt series, three patients with heavy infestation with Nostratibus Seu Belgarum Sprou w. Amsterdam: strongyloides were subjected to laparotomies after a Bernard, 1715. mistaken diagnosis of partial small bowel obstruc- 5 Baker SJ. Idiopathic tropical steatorrhoea. A repo'rt of tion and at operation there were dilated loops of 60 cases. Ind J Med Sci 1957; 11: 687-9. 6 Ciba Foundation Study Group no. 14. Wolstenholme jejunum without evidence of mechanical obstruc- GEW, Cameron MP, eds. Intestinal biopsy. Edinburgh: tion. The mesenteric nodes were enlarged in all these Churchill, Livingstone, 1962. cases. Thus the clinical picture may mimic sprue as 7 Ashcroft MT. Tropical sprue in the Caribbean. Lancet abdominal colic and episodes of pseudo-obstruction 1970; ii: 724-5. may occur in tropical and non-tropical varieties.'9 8 Banwell JG, Hutt MRS, Marsden PD. Blackman V. Fone et al3" reported that in 12 patients with coeliac Malabsorption syndromes among African people in sprue, five had colicky abdominal pains leading to Uganda. East Afr Med J 1967; 41: 188-93. laparotomy in two cases. In both these patients the 9 Banwell JG. Hutt MSR. Leonard PJ. et al. Exocrine small bowel was oedematous and the mesenteric pancreatic disease and the malabsorption syndrome in tropical Africa. Gut 1964; 8: 388-401. lymph nodes were enlarged. Baker and Mathan"' 10 Foy H, Kondi A. Megaloblastic anaemia in East Africa. have also observed that abdominal colic and a In: Tropical sprue and megaloblastic tanaemia. dilated small intestine have resulted in erroneous Wellcome Trust Colaborative Study, Wellcome Trust. laparotomy in cases of tropical sprue. Edinburgh, London: Churchill Livingstone. 1971: Thus 230 years after Hillary's treatise on sprue in 261-8. Barbados, the scene has changed and in West Indian 11 Cook GC. Malabsorption in Africa. Tr-ans R Soc TrIo)p immigrants to the United Kingdom a sprue-like Med Hyg 1974; 68: 419-35. syndrome is more likely to be the result of infestation 12 Woodruff AW. ed. Medicine in the Tropics. Edinburgh with Strongyloides than to tropical sprue. This may and London: Churchill Livingstone, 1974. 13 Klipstein F. Tropical sprue. In: Bockus HL, ed. Gasjro- not be true for immigrants from the Latin Caribbean enterology: Vol 11. Philadelphia, London. and Toronto: islands. WB Saunders, 1976. 14 Moshal MG, Hift W, Kallichurum S. Pillay K. Endemic I wish to thank Dr Graham Neale for inviting me tropical sprue in Africa. J Trop Med Hvg 1975: 78: 2-5. copyright. to contribute to this festschrift in honour of Sir 15 Rodriquez-Molina R. Sprue in Puerto Rico: 10 years Christopher Booth. I also wish to thank Dr Farley later. Puerto Rico J Public Healthi Trop Med 1943: 18: Cleghorn for assisting me in the preparation of this 314-40. manuscript and Dr Henry Fraser for procuring for me 16 Milanes F. Changes in the epidemiology and clinical a copy of William Hillary's book from the Barbados features of sprue in Cuba between 1927 and 1957. Arch Museum. Hosp Univ HABANA 1960; 12: 125-36. 17 Sheehy TW, Cohen WC, Wallace DK, Legters LJ. Tropical sprue in North Americans. JAMA 1965: 194: http://gut.bmj.com/ University ofthe West Indies 1069-76. and the 18 Baker SJ. Idiopathic small intestinal diseases in the General Hospital, tropics. In: Chandra RK, ed. Critical reviews in tropical Port ofSpain, medicine. New York and London: Plenum Press, 1982. Trinidad 19 Rodgers PEB. The clinical features and aetiology of the neuropathic syndrome in Jamaica. W I Med J 1965; 36: 36-47.

References 20 Trowell HC, Jelliffe DB. Diseases ofchlildrlenl in the sub- on September 25, 2021 by guest. Protected tropics and tropics. London: Arnold, 1958. 1 The extant works of Arataeus, the Cappadocchian. 21 Bartholomew C. Young Pong 0. Lactosc intoleciancc in Edited and translated by Francis Adams, LLD. London: East Indians of Trinidad. Trop) Geog Med 1976; 28: Sydenham Society, 1856. 336-38. 2 Hillary W. Observations on the changes of the air and 22 Bartholomew C, Butier AK. Bhaskar AG, Jankey N. the concomitant epidemical diseases in the Island of Pseudo-Obstruction and a sprue-like syndrome from Barbadoes, to which is added a treatise on the putrid strongyloidiasis. Postgrcad Med J 1977; 53: 139-42. biliousfever, commonly called the yellowfever; and such 23 Sheehy TW, Meroney WH, Cox RS, Soler JE. Hook- other diseases as are indigenous or endemical in the West worm disease and malabsorption. Gastroenterology Indian Islands. London: Hawes, Clarke and Collins, 1962; 42: 148-50. 1759. 24 O'Donovan DK, McGrath J, Bolan SJ. Giardial infesta- 3 Manson P. Notes on sprue. In: China, Imperial Maritime tion with steatorrhoea. Lancet 1942; ii: 4-5. Customs, Special Series No. 2, Medical Reports for the 25 Brandborg LL, Tankersley CB, Gottlieb S. Barancik M. Half-Year Ended 31st March, 1880. (19th issue). Sartor BE. Histological demonstration on mucosal Shanghai: Statistical Department of the Inspectorate invasion by Giardia lamblia in man. Gastroenterolog, General, 1880: 33-7. 1967; 52: 143-5. 4 Ketelaer V. Commentarius Medicus de Apthis 26 Bras G, Richards RC, Irvine RA, Miner PFA, Ragbir Gut: first published as 10.1136/gut.30.Spec_No.17 on 1 November 1989. Downloaded from

William Hillary and Sprue in the Caribbean: 230years later 21

MMS. Infection with Strongyloides stercorales in 879-81. Jamaica. Lancet 1964; ii: 1257-8. 30 Fone DJ, Cooke WT, Maynell MJ, et al. Jejunal biopsy 27 Rivera E. Maldonado N, Velez-Garcia E, Grillo AJ, in adult coeliac disease and allied disorders. Lancet Mallaret G. Hyperinfection with Strongyloides 1960; i: 933-5. stercorales. Ann Intern Med 1970; 72: 199-201. 31 Baker SJ. Mathan VI. In: Tropical sprue and megalo- 28 Patterson DE. Strongyloides infestation of jcjunum. blastic anemia. Wellcome Trust Collaborative Study. BrJ Radiol 1958; 31: 102-4. Wellcome Trust. Edinburgh and London: Churchill 29 Badenoch J. Stcatorrhoea in the adult. Br MedJ 1960; ii: Livingstone, 1971. copyright. http://gut.bmj.com/ on September 25, 2021 by guest. Protected