View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by Elsevier - Publisher Connector

Kidney International, Vol. 16 (1979), pp. 15-22

Renal disease due to schistosomiasis of the lower urinary tract

A.B.O.O. OYEDTRAN

Department of Preventive and Social Medicine, University of Ibadan, Ibadan, Nigeria

Vesical schistosomiasis was known to ancient This paper reviews the literature concerning renal Egyptians, and there are numerous references to its impairment and damage due to S. haematobium in- most prominent clinical manifestation, hematuria, fections, with emphasis on radiologic, biochemical, in various medical papyri [1]. The adult causative and renographic studies of renal function in affected worm, Schistosoma haematobiu,n, was first identi- persons. fied in 1851, and it was not until many years later that the clinical features and life-cycles of S.japoni- Radiologic studies cum and S. mansoni were described. Despite this, it Techniques which have been used to study the is ironic that, presently, far more is known about radiographic manifestations of vesical schistoso- infections due to the latter two species than those miasis include plain X-ray of the abdomen and pel- due to S. haematobium. Indeed, there is still some vis, intravenous and retrograde urography, mictu- debate regarding the amount of morbidity and mor- rating with or without , tality attributable to vesical schistosomiasis in en- , and vesiculography. The find- demic areas, whereas it is generally accepted that ings have been reported by many authors [7, 13-24] infections with S. mansoni and S.japonicum are re- and have revealed a very high prevalence (up to sponsible for very significant disease, disability, 50%) of radiographic abnormalities in infected chil- and deaths in affected populations [2]. dren and adults, including those who are asympto- Reports concerning the amount of renal impair- matic except for hematuria. They have further ment and damage due to S. haematobium infections shown that, although the prostate, , seminal have varied not only from country to country but vesicles, and other organs are commonly involved, also from place to place in the same country. This is most of the lesions are in the , ure- partly because various workers have used differing ter, and . criteria for assessing the amount of damage caused Bladder. The most common early manifestations by vesical schistosomiasis. Moreover, some of the in the bladder are nodular filling defects, which may criteria which have been used could not have yield- be single but are usually multiple. They are particu- ed reliable estimates of the size and nature of the larly common in children, respond well to specific problem under investigation. For example, clinical chemotherapy [7, 20, 25-28], and may be spontane- manifestations including blood pressure studies ously reversible [26]. Late lesions include calcifica- have been used, but it is now widely recognized that tion and fibrotic reduction of bladder capacity. these are of limited value in assessing the impact of "Bilharzial bladder outlet obstruction" has been the disease on the renal function of affected per- described [29, 30], as well as carcinoma of the blad- sons. It is not uncommon for patients to present der, but the relationship between the latter and S. very late with chronic disease and clinical manifes- haematobium infection is the subject of con- tations of uremia [3]. The majority of infected per- troversy [31]. sons, however, even those with demonstrable ad- . Radiographic abnormalities of the ureter, vanced disease, show no specific clinical manifesta- tions, and are often apparently in good health [4-7]. Furthermore, reports on a possible association be- Received for publication July 11, 1978 tween vesical schistosomiasis and 0085-2538179/0016-0015 $01.60 have been conflicting [7—121. © 1979 by the International Society of Nephrology

15 16 Oyediran especially its lower third, are very common in vesi- schistosomiasis may have hydronephrosis [37], and cal schistosomiasis and are often associated with these lesions may be seen in up to 10% of infected bladder lesions. The most common finding in the children, even in areas of low to moderate endemic- lower ureter is stasis with or without dilatation in ity [7, 8, 38]. the lowest segment, and it is usually combined with Hydronephrosis causes renal damage due to symmetric fusiform narrowing at the ureterovesical back-pressure effects or secondary bacterial infec- junction. This lesion may be due to fibrosis in the tion. It is now known, however, that, particularly in ureteral wall with resultant atony or dyskinesia [13, children, hydronephrosis may be reversible follow- 17, 32,33].It may also be caused by a nodule at the ing specific chemotherapy [23, 25, 26, 391. Further- ureterovesical junction or by inflammatory reaction more, there have been conflicting reports con- to the presence of schistosome ova in the cerning the relationship between vesical schistoso- without fibrosis. Such cases respond well to chemo- miasis and bacterial infections of the kidneys and therapy [23]. urinary tract [7, 10-12, 39—54]. Standardized studies Ureters, which are irregularly narrowed over a are required to resolve this conflict, and such stud- short distance, show marginal filling defects or a ies should include observations on the possible role beaded appearance; these changes have been attrib- of surgical instrumentation of the urinary tract in uted to fibrosis, ureteritis cystica, ureteritis glandu- affected patients. laris, and other chronic changes. The abnormalities In some cases, a normal ureter may be seen in may also be produced by ureteral nodules or edema association with calicectasis affecting the upper cal- from acute primary involvement of the ureter. It has yces alone or the whole of the collecting system. been reported that trigonal fibrosis may cause a Such lesions are thought to be due to an aberrant characteristic cow-horn" deformity of the ureters vessel or congenital ureteropelvic obstruction, re- [24]. This lesion may be identical with the "snake- spectively [23]. head ureter" described by earlier workers [211. In Radiographically non-functioning" kidney has such cases, ureteral catheterization is difficult, and been described in up to 8% of infected persons and therefore a stricture may be simulated. However, is reported to be associated with a poor prognosis true strictures of the ureter do occur in vesical [55]. There may be radiologic evidence of pyelone- schistosomiasis, although some workers consider phritis and, rarely, stones and calcification of the them rare [241. renal capsule may be seen [21, 56]. Various forms of ureteral calcification, including It has been reported that the frequencies of bilat- stones, have been reported to be common. In ad- eral obstructive uropathy, hydronephrosis, hydro- vanced cases, stasis and dilatation, often with tor- ureter, "non-functioning" kidney, calcified blad- tuousity, are common in the upper ureters, and may der, ureterolithiasis, and bladder retention increase involve the whole length of the ureter. These cases linearly with age, whereas urographic filling defects may result from mechanical obstruction by nodules and egg excretion decrease linearly with increasing and fibrosis. They also may be due to hypotonia and age [50]. atonia of the ureters, leading to functional derange- ment. Biochemical studies Pyelonephritis following obstructive uropathy is It is clear from the foregoing that patients with S. well understood, but it is being increasingly recog- haematobium infections have a high prevalence of nized that pyelonephritis may occur in patients structural abnormalities of the kidney and urinary without demonstrable obstruction. The role that tract demonstrable radiologically. It has been right- vesicoureteral reflux may play in such cases has ly observed, however, that it is not what a kidney been emphasized [34, 35]. Vesicoureteral reflux oc- looks like but how it works that counts" [57]. Re- curs in patients with S. haematobium infection, but cent refinements of urographic examination, includ- reports concerning its incidence in infected patients ing the use of modern contrast media, enable good have been conflicting [10, 21, 23, 36]. contrast density to be visualized even when renal Kidney. The most common radiographic lesion in function has been minimal. Thus, older criteria re- the kidney is hydronephrosis which is usually asso- lating urographic opacity to renal function are no ciated with and secondary to lesions lower down longer valid [58, 59]. There has, therefore, been the urinary tract. In such patients, there may be, in doubt regarding the clinical significance and ulti- addition, delayed calyceal filling. In some endemic mate prognosis of structural lesions observed in areas, up to 17% of unselected patients with vesical pyelograms of patients with vesical schistosomiasis Renal function in schistosomiasis 17

[21. This doubt is further underlined by the fact that has its limitations, such as its inability to indicate an many of the affected patients have been apparently exact anatomic or pathologic diagnosis, and its sus- well, and the observation that some of the lesions, ceptibility to dehydration and other extraneous fac- including hydronephrosis, are reversible following tors. It is, however, safe, sensitive, simple, and specific chemotherapy. quick, and allows repeated examination of individ- Biochemical tests that have been used to assess ual renal function to be carried out without undue renal function in patients with vesical schistoso- trauma or inconvenience to the subject. The tech- miasis include serum urea and creatinine values, nique is considered to reflect largely renal tubular creatinine clearance studies, as well as maximal excretory activity. urine concentration and phenylsuiphonthalin (PSP) 1311-hippuran renography has been used to assess excretion tests. In some endemic areas, including renal function in infected Nigerian children and Tanzania and Nigeria, these tests have not been young adults before and after specific chemother- helpful [7, 8, 38]. For example, serum urea and apy. In a preliminary study, renograms were quali- creatinine values in infected patients have been tatively assessed in 314 children of both sexes aged within normal limits. In a recent study of Nigerian 6 to 15 years, 188 of whom were infected with S. children and young adults aged 9 to 21 years with haematobium [64]. The results confirmed earlier re- moderately high urine egg count, 11 of them with ports concerning the marked effect of urine flow hydronephrosis or pelviureteric obstruction were rate on the renogram, and showed that renographic found to have a mean 24-hour creatinine clearance abnormalities that persist after a water-load were value that was significantly lower than that of 76 more common in infected than they were in unin- others whose urograms were normal or showed le- fected children. Such abnormalities occurred more sions confined to the bladder and ureters. Clearance frequently in infected children who had heavy urine values, however, in 7 of the 11 were still within ac- egg excretion and abnormal urograms than they did cepted normal limits [71. in those with light infections and normal urograms, Workers in some other endemic areas have found but the observed differences were not statistically conventional tests useful in detecting renal func- significant. In some infected children, specific tional impairment in patients with S. haematobium chemotherapy with niridazole (Ambilhar®) seemed infection. For example, in Egypt it has been report- to restore the renogram to normal within 3 weeks ed that the maximal urine concentration and PSP (Fig. 1). excretion tests are impaired in patients (mainly In a definitive study of 114 infected patients of adults) with bilateral obstructive uropathy, particu- both sexes aged 9 to 21 years, semiquantitative as- larly those with bacteriuria [46, 47, 51]. sessment of renograms (Fig. 2) was carried out with The conflicting reports regarding the status of nomographs obtained from a study of uninfected renal function in infected patients may well be due healthy controls [65]. Seventeen patients (15%) had to the varying epidemiologic pattern and clinical renograms that were abnormal or equivocal (Fig. 3). features of schistosomiasis from community to In nine of them, the excretory index was affected, community, and within the same community at dif- whereas the corresponding uptake index was nor- ferent points in time. On the other hand, conven- mal. In one patient, the left kidney tracing showed tional biochemical tests of renal function are known an abnormal uptake index with a normal excretory to be of limited sensitivity, and they assess overall index, and in the remaining seven patients both the renal function, whereas it is known that urologic le- uptake and excretory indices of the renograms were sions seen on pyelograms of patients with urinary affected. Abnormal and equivocal tracings were sig- schistosomiasis are often unilateral. nificantly more common in patients with pyelo- graphic abnormalities, especially ureteral and kid- Reno graphic studies ney lesions, than they were in those whose pyelo- Radioisotope renography is widely accepted as a grams were normal. Furthermore, there was a valuable tool for the investigation, management, highly significant correlation between ureteral and and follow-up of patients with renal disease [57, 60- renal urographic lesions on the one hand and abnor- 63]. Several radioactive preparations have been mal excretory and uptake indices of the ipsilateral used for renography, but 1311-hippuran has become renographic tracing on the other. the most widely used because it is selectively and Some patients whose urograms were normal had efficiently taken up by the kidneys and does not suf- renographic evidence of impaired renal function. fer the disadvantage of hepatic uptake. Renography This finding supports an earlier report that vesical 18 Oyediran

0

a I

Fig. 2. Semiquantitative assessment of renograms from nomo- graphs of uninfected healthy controls. AC equals CD equals half- peak amplitude. Uptake index (tm) equals OA. Excretory index (B) equals AB.

3.0 A 2.5

C No. 0183 J 2.0 Posttreatment(D) 00, -J F 1.5 w 0 -J 1.0

0.5

Fig. 1.L.ffectof niridazole therapy for 3 weeks on renogram of patient infected with S. haematobium. —2.0—1.5 —1.0 -—0.5 0 0:5 1.0 1.5 2.0 2:5 LogeFR Fig. 3. Renographic classification, 15% of the renograms as ab- normal or equivocal. x—x denotes abnormal; 0—0denotes schistosomiasis may cause renal damage by mecha- equivocal; s---•denotesnormal renographic findings. AB is 95% nisms other than obstructive uropathy [661. This upper limit; CD is predicted value; EF is 95% lower limit. E and view is further supported by recent reports that tmaredefined in Fig. 2. some patients with S. haematobium infection have renal lesions associated with immune complexes [511, and that circulating schistosomal antigens and in Figs. 4 to 8. Lower tract abnormalities at intra- antibodies are demonstrable in some infected pa- venous pyelography (IVP) were defined as those tients [671. confined to the bladder, and they include calcifica- Of the 114 patients, 61 were successfully followed tion and nodular filling defects. Middle tract abnor- for up to 21 months after treatment with niridazole. malities were those occurring in the ureters any- Posttreatment findings showed that, although renal where from below the pelviureteric junction up to function had improved in some patients, renal func- and including the ureterovesical junction with or tional impairment responded, on the whole, poorly without bladder lesions. Upper tract lesions were to specific chemotherapy despite parasitologic and those occurring within the kidney up to and includ- pyelographic improvement. ing the pelviureteric junction, with or without ab- Findings before and after treatment are illustrated normalities lower down the urinary tract. Renal function in schistosorniasis 19

3.0

2.5

2.0 2.0 w uJ 00,1.5 1.5 -J -J0

1.0 1.0

0.5 0.5

—2.0 —1.5 —1.0 —0.5 0 0.5 1.0 1.5 2.0 2.5 2.O _: _: _: 1:0 1:5 2.02.5 Loge FR Log, FR Fig.4. Pretreatmentrenogramsof patients with normal IVP Fig. 6. Pretreatment renograms of patients with middle tract le- (log,E vs. log,FR). sions at the time of IVP (log, E vs. log, FR). endemic areas should be clearly defined so as to Discussion guide governments, planners, and funding agencies It has been reported that, in African countries in their choice of priorities. alone, 39 million persons are infected with S. hae- Unlike the situation in S. mansoni and S. japoni- matobium [68], and the disease is spreading to pre- cum infections, patients with vesical schistoso- viously uninfected areas as a result of development- miasis often present with little or no clinical signs of al activities such as man-made lakes, dams, and serious disease until the very late stages of the in- other agroindustrial and energy production pro- fection. It has therefore been difficult to establish a grams [2]. To ensure that maximum benefits accrue clinical gradient with respect to S. haematobium in- from investment in development, it is important fections. Pyelographic studies of infected patients that the public health importance of the disease in added a new dimension to the understanding of the

3.0

2.5

2.0

LU LU 1.5 0 0 -J -J

1.0

0.5

2.0 —1.5 —1.0—0.5 0 0.5 1.0 1.5 2.0 2.5 Log, FR Log, FR Fig.5. Pretreatment renograms of patients with lower tract Ic- Fig.7. Pretreatment renogra,ns of patients with upper tract le- ions at the time of IVP (log,E vs. log,FR). sions at the time of IVP (log,E vs. log,FR). 20 Oyediran

size and scope of the problem, and to control the disease and prevent its spread.

Summary The literature concerning renal impairment and damage due to vesical schistosomiasis has been re- viewed, with emphasis on radiologic, biochemical, w and renographic studies of renal function in affected 0 persons. Presently available evidence suggests that -J infections due to S. haematobium constitute an im- portant public health problem because they are widely prevalent. A high proportion of affected per- sons suffer renal impairment and damage due to ob- structive uropathic lesions in the lower urinary tract and, probably, through direct immunologic in- volvement of the kidney. It is therefore important that efforts should be intensified to better define the Log, FR size and scope of the problem, and to control the Fig.8. Posttreatment renograms of patients with upper tract le- disease. sions at the time of IVP (log,.E vs. log,FR). Reprint requests to Dr. A.B.O.O. Oyediran, Department of Preventive and Social Medicine, University of Ibadan, Ibadan, problem by revealing severe structural abnormal- Nigeria ities of obstructive uropathy in some patients who References were apparently well. In some endemic areas, con- 1. FOSTER WD: A History of Parasitology. Edinburgh and Lon- ventional biochemical tests showed evidence of don, Livingstone, 1965 renal functional impairment in some of the patients 2. World Health Organisation: Schistosomiasis control: Report with structural abnormalities. In other areas, how- of a WHO expert committee. Tech. Rep. Ser. No. 515, 1973 ever, such tests did not reveal impaired renal func- 3. DUKES HM, MYNORS, JM: Obstructive renal failure in bil- tion in affected patients, and therefore doubts exist- harziasis. Br J Surg 57:347—349, 1970 4. RAMSAY GWSC: A study on schistosomiasis and certain oth- ed about the functional significance of the structural er helminthic infections in Northern Nigeria. W Afr Med J lesions observed. Radioisotope renography has 8:2—10, 1934 added a further dimension to the understanding of 5. Editorial: Schistosomiasis in West Africa. W Afr Med J vesical schistosomiasis in such areas by providing 13:131—132, 1964 evidence of renal functional impairment in some of 6. FORSYTH DM: Clinical patterns in urinary schistosomiasis, in Bilharziasis: International Academy of Pathology Special the patients with structural abnormalities at pyelog- Monograph, edited by MOSTOFI FK, Berlin, Heidelberg, raphy. Moreover, renographic findings have sug- New York; Springer-Verlag; 1967, pp. 86-92 gested that some patients with normal pyelograms 7. OYEDIRAN ABOO: Renal function in vesical schistoso- may have impaired renal function. Further longitu- miasis. M.D. Thesis, University of London, 1976 dinal studies of infected patients are desirable and 8. FORSYTH DM, MACDONALD G: Urological complications of endemic schistosomiasis in schoolchildren: Part 1. Usagara should yield useful information particularly in pa- school. Trans R Soc Trop Med Hyg 59:171-178, 1965 tients whose renographic abnormalities persist de- 9. GELFAND, M: Bilharziasis: A serious ailment. Cent Afr J spite good parasitologic response to specific chemo- Med 14:141-144, 1968 therapy. 10. EDINGTON GM, GILLES HM: Pathology in the Tropics. Lon- All the foregoing suggest that, even in areas of don, Edward Arnold, 1969, p. 142 11. SOYANNWO MAO: Studies on the prevalence of renal dis- low to moderate endemicity, a high proportion of ease and hypertension in relation to schistosomiasis: A patients with S. haematobium infection suffer renal cross-sectional survey of Omi-Adio, a community of high impairment and damage due to obstructive uropath- bilharzia endemicity, and Ofa-tedo, one with low endemici- ic lesions in the lower urinary tract and, probably, ty. M.D. Thesis, University of Ibadan, 1973 through direct immunologic involvement of the kid- 12. WILKINS HA: Schistosoma haematobium in a Gambian com- munity. III. The prevalence of bacteriuria and of hyper- ney. The disease therefore constitutes an important tension. Ann Trop Med Parasitol 71:179-186, 1977 public health problem in affected areas. Efforts 13. HONEY RM, GELFAND M: The UrologicalAspects of Bilhar- should be intensified to more accurately define the ziasis in Rhodesia. London, Livingstone, 1960 Rena/function in schistosomiasis 21

14. MIDDLEMISS JH: Radiological pathology and methods of in- 36. WEINBERG RW, GELFAND M: Observations on the in- vestigation in schistosomiasis, in Bilharziasis, edited by cidence of vesico-ureteric reflux in urinary bilharziasis. Br J MOSTOFIFK,New York, Berlin, Springer-Verlag, 1967, pp. Urol40:68—71,1968 197—211 37. BHAGWANDEEN SB: The pathology of ureteric bilharziasis. 15. NABAWYM,GABRM,RAGABMM:Visceral schistosomiasis S Afr Med J 41:950-955, 1967 in childhood: A clinical radiological study. J Trop Med Hyg 38. FORSYTH DM, MACDONALD G: Urological complications of 64:314—318, 1961 endemic schistosomiasis in schoolchildren: Part 2. Donge 16. TARABULCYEZ:The radiographic aspect of urogenital schis- School, Zanzibar. Trans R Soc Trop Med Hyg 60:568-578, tosomiasis (Bilharziasis). J Urol 90:470—475, 1963 1966 17. JAMESWB:Urological manifestations in Schistosoma hae- 39.MACDONALD G, FORSYTHDM:Urological complications of matobium infestation. Br J Radiol 36:40—45, 1963 endemic schistosomiasis in schoolchildren: Part 3. Follow- 18. GILLESHM,LUCASA,ADENIYI-JONES C, LINDNER R, up studies at Donge School, Zanzibar. Trans R Soc Trop ANAND SV, BRABANDH,COCKSHOTTWP,COWPERSG, Med Hyg 62:766—774, 1968 MULLER RL, HIRAPR,WILsONAMM:Schistosoma haema- 40. PI-SUNYER FX,GILLES HM, WILsoNAMM: Schistosoma tobiuni infection in Nigeria: II. Infection at a primary school haematobium infection in Nigeria: I. Bacteriological and im- in Ibadan. Ann Trop Med Parasitol 59:441—450, 1965 munological findings in the presence of schistosomal infec- 19. GILLESHM,LUCASA,LINDNER R, COCKSHOTTWP, tion. Ann Trop Med Parasitol 59:304—311, 1965 ANANDSV, IKEME A,COWPER SG:Schistosoma haemato- 41. FORSYTHDM, BRADLEY Di:The consequences of bilhar- bium infection in Nigeria: III. Infection in boatyard workers ziasis: Medical and public health importance in North-West at Epe. Ann Trop Med Parasitol 59:45 1-456, 1965 Tanzania.BullWHO 34:715-735, 1966 20. CHAPMAN DS: The surgical importance of bilharziasis in 42. WOLFE MS, QUARTEY JMK: Urinary schistosomiasis in South Africa. Br J Surg 53:544-557, 1966 Ghana: a report of 53 cases, with special reference to pye- 21. AL-GHORABMM:Radiological manifestations of genito-uri- lographic and cystoscopic abnormalities. Trans R Soc Trop nary bilharziasis. Clin Radiol 19:101—111,1968 Med Hyg 61:90-99, 1967 22.MAGEDA,SOLIMAN LAM: Bilharzial pseudo-calculus of the 43. CHOPRASA,BRADLEYDi,FORSYTHDM:Bacterial super- ureter. J Urol 99:30—34, 1968 infection of the urine in bilharzial hydronephrosis. EAfr 23. BOHRERSP, LUCASAO, COCKSHOTTWP:Roentgeno- Medi44:241-245, 1967 graphic features of Schistosomiasis in Children. Z Tro- 44. GELFANDM,WEINBERG R: Early inflammatory changes in penmed Parasitol 22:177—188, 1971 the kidney in bilharziasis of the lower urinary tract. J Trop 24. UMERAH BC: The less familiar manifestations of schistoso- Med Hyg 71:285-287, 1968 miasis of the urinary tract. Br J Radio! 50:105-109, 1977 45.CARTER JP, DIABAS,NASIFF,5, SANBORN WR,GRIVETTI 25. LUCAS AO, ADENIYI-JONES CC,COCKSHOTT WP,GILLES LE,DAVIESJA:Bacteriologicaland urinary findings in ado- HM:Radiological changes after medical treatment lescentof vesical Egyptian males withandwithout urinary schistoso- schistosomiasis. Lancet 1:631—633, 1966 miasis, JTrop Med Hyg 73:211—217, 1970 26. LUCAS AO, AKPOM CA, COCKSHOTT WP, BOHRER SP: Re- 46. LEHMANJS, FARm Z, BASSILY 5:Mortalityin urinary schis- versibility of the urological lesions of schistosomiasis in chil- tosomiasis. Lancet 2:822—823,1970 dren after specific therapy. Ann NYAcad Sc! 160:629-644, 47. LEHMANiS,FARIDZ,BASSILY5,KENTDC: Renal function 1969 inurinary schistosomiasis. Am J Trop Med Hyg 19:1001- 27.GELFAND M, DAWSON NG: The effect of antimony on ad- 1006,1970 vanced ureteral lesions in bilharziasis: A case report. J Trop 48.FARIDZ, BASSILY5,KENTDC,SANBORNWR,HASSANA, Med Hyg70:87-89,1967 ABDEL-WAHABMF, LEHMANJS:Chronic urinarysalmonel- 28. MACDONALD G, FORSYTH DM, RA5HID C: Urological com- la carriers with intermittent bacteraemia. J Trop Med Hyg plications of endemic schistosomiasis in school children: 73:153—156, 1970 Part 4. As modified by treatment. Trans R Soc Trop Med 49. EDINGTON GM,VON LICHTENBERG F, NWABUEBOI,TAY- Hyg62:775—781,1968 LOR JR. SMITH JH: Pathologiceffects of schistosomiasis in 29. ATALAA, ZAHERMF,RAGY1:Bilharzial bladder outlet ob- Ibadan, Western State of Nigeria: I. Incidence and intensity struction. J Urol 101:183—185, 1969 of infection: Distribution and severity of lesions. Am J Trop 30. ZAHER MF, EL-DEEB AA: Bilharziasis of the prostate: Its Med Hyg 19:982—995, 1970 relation to bladder neck obstruction and its management. J 50.LEHMANiS,FARID Z, SMITH JH, BASSILYS,EL-MASRY Urol 106:257—261, 1971 NA:Urinary schistosomiasis in Egypt: Clinical, radio- 31. ATTAH EB, NKPOSONG EO: Schistosomiasis and carcinoma logical,bacteriological, and parasitological correlations. of the bladder: A critical appraisal of causal relationship. Trans R Soc Trop Med Hyg 67:384—399, 1973 Trop Geogr Med 28: 268—272, 1976 51. YOUNG SW, FARID Z: Urinary osmolality and acid excretion 32. MAKAR N: The bilharzial ureter: Some observations on the in schistosomal uropathy. Ann Intern Med 79:275—276, 1973 surgical pathology and surgical treatment. Br J Surg 36:148— 52.SMITHJH, KAMELIA,ELWIA,VON LICHTENBERG F: A 155, 1948 quantitative postmortem analysis of urinary schistosomiasis 33. GELFAND M: Some remarks on the clinical and pathological in Egypt: I. Pathology and pathogenesis. AmJ Trop Med aspects of schistosomiasis in Central Africa, in Bilharziasis, Hyg 23:1054—1071,1974 edited by MosToFi FK, New York, Berlin, Springer-Ver- 53.SMITH JH,ELWIA,KAMELIA, VONLICHTENBERGF:A lag, 1967, pp. 104-114 quantitativepostmortem analysisof urinary schistosomiasis 34. HUTCHJA, MILLERER, HINMAN F: Vesico-ureteral refiux: in Egypt. II.Evolution and epidemiology. Am J Trop Med Role in pyelonephritis Am J Med 34:338-349, 1963 Hyg24:806—822, 1975 35. MCGOVERN JH, MARSHALL VF: Refiux and pyelonephritis 54.SADIGURSKY M,CHEEVERAW, ANDRADEZA, KAMEL IA, in 35 adults. J Urol 101:668—672, 1969 DANNER R, ELWIAM:Absence of schistosomal glomerulo- 22 Oyediran

pathy in Schistosoma haematobium infection in man. Trans 62. VITYLB:Quantitative analysisof the thirdsegmentof the RSoc TropMedHyg70:322—323, 1976 renogramand its application for the detection of urinary 55. FORSYTH DM, BRADLEY DJ, MCMAUONJ:Deaths attribut- tract obstruction and renalarterial constriction. J Urol able to in communities withedemic urinary 107:21—22, 1972 schistosomiasis.Lancet 2:472—473,1970 63. FUJITA K,NAKAUCHIK,MATSUMOTOK,NAKANISHIT, KASAMATSU T, OYAMADA H: Correlation between radio- 56.ATALAA,ZAHERMF:Bilharzialcalcification of the renal isotope renographic findings and results alter relief of ure- capsule:acasereport.J Urol 101:125—126, 1969 teral obstruction. J Urol 107:23—25, 1972 57.BRITTON KE,BROWN NJG:Clinical Renography. London, 64.OYEDIRANABOO,ABAYOMI10,AKINKUGBE00,BOHRER Lloyd-Luke, 1971 SP, LUCAS A0: Renographic studies in vesical schistoso- 58.SCHWARTZ WB,HURWITA,ETTINGERA:Intravenous urog- miasis in children. AmJ TropMedHyg24:274—279,1975 raphyin the patient with renal insufficiency. NEngi J Med 65. OYEDIRAN ABOO: The importance of the urine flow rate for 269:277—283, 1963 semi-quantitative assessment of the renogram. J Urol 119: 59.WAX SH, MCDONALD DF: The renogram vs. the : 783—786, 1978 evaluation of the significance of upper urinary tract obstruc- 66.OYEDIRANAB0,AKINKUGBE00: Chronic renal failure in tion. J Urol96:816—827,1966 Nigeria. Trop Geogr Med 21:41-44, 1970 60.WINTERCC:RadioisotopeRenography. Baltimore,Wil- 67. MADWAR MA, VOLLER A: Circulatingsoluble antigens and liams and Wilkins, 1963 antibodyin schistosomiasis. BrMed J 1:435—436, 1975 61.MESCHANI, WATTS FC, MAYNARD CD,WITCOFSKIRL, 68. JORDAN P: Egg-output in bilharziasis in relation to epide- SMITHSN: Quantification of the glomerular filtration of the miology, pathology, treatment and control, in Bilharziasis, individual kidney by the 1'31-renograffin renogram. Radiolo- editedbyMOSTOFI FK,NewYork, Berlin, Springer-Ver- gy 88:984—987, 1967 lag, 1967, pp. 93—103