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Urinary schistosomiasis in children in the United Kingdom
Journal of Pediatric Urology (2012) 8, 438e441
EDUCATIONAL ARTICLE
Urinary schistosomiasis in children in the United Kingdom Abid Qazi a, Jens Stahlschmidt b, Ramnath Subramaniam a,* a
Dept of Paediatric Urology, Leeds Teaching Hospitals NHS Trust, F floor Martin Wing, Great George Street, Leeds LS1 3EX, United Kingdom b Dept of Paediatric Pathology, Leeds Teaching Hospitals NHS Trust, Bexley Wing, Leeds LS97TF, United Kingdom Received 31 July 2011; accepted 28 November 2011 Available online 30 December 2011
Abstract We report on two patients with urinary schistosomiasis, who both presented within a fortnight to our hospital with similar symptoms of persistent painless haematuria. Ultrasound, cystoscopic biopsies and histology were used to confirm diagnosis. Treatment with praziquantel was given. Symptoms of urinary schistosomiasis can easily be missed in non-endemic areas and possibly confused with a more sinister pathology. A thorough history and awareness of disease can avoid interventional investigations. ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
Introduction Haematuria is an uncommon symptom in children. If not accompanied by proteinuria, it should be referred for urological assessment for stones, bladder pathology or rarely Wilms’ tumour. In the developed world, a clinician rarely encounters a pathology like urinary schistosomiasis, which is endemic in Africa and is the commonest cause of haematuria in children [1]. However, due to economic migration from endemic areas and increased foreign travel generally, it is not so unexpected to find this pathology in developed countries [2e5]. In the UK, there were 116 cases of Schistosoma haematobium reported between 2003 and * Corresponding author. Tel.: þ44 113 3926251; fax: þ44 113 2066634. E-mail address: [email protected] (R. Subramaniam).
2005, according to the England and Wales national laboratory database [2]. Over two thirds of patients in this report were from London and the adjacent area. Recognition of acute symptoms frequently does not occur due to the rarity of the disease.
Case summaries Patient 1 A 14-year-old boy presented with gross terminal haematuria for 2 months. The condition was painless but he reported having general symptoms of malaise and fatigue with poor appetite for some time. Previously, he had been fit and well except that he was a known carrier of the thalassaemia trait. Urine examination showed frank haematuria, and microscopy showed numerous red blood cells
1477-5131/$36 ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jpurol.2011.11.008
Urinary schistosomiasis in children in UK but was otherwise unremarkable. An ultrasound scan of the urinary tract revealed localized thickening of the bladder trigone on the left side (Fig. 1a). The left ureteric orifice area was thickened. A good ureteric jet was visible. There was mild hydronephrosis of the left kidney (AP diameter 11 mm) but no ureteric dilatation was seen. His haemoglobin was 11.4 gm/dl. Full blood count was normal except eosinophilia 0.71 109 (normal range 0.04e0.40). The thickened bladder wall and its location raised suspicion of rhabdomyosarcoma of the bladder. Cystoscopy revealed multiple lesions in the area of the trigone, studded with white spots within the lesion (Fig. 1b). There were lesions adjacent to both ureteric orifices, and these were inflamed and friable. Punch biopsy and urine specimen were sent for histology and cytology. The biopsy proved the presence of eggs of S. haematobium. The inflammatory mass constituted eosinophil-rich inflammatory cells surrounding mature eggs of S. haematobium. Some of the cells were degenerating and calcified. Revisiting the patient’s history revealed that he had been to Malawi, a year ago, where his father was working. A diagnosis of schistosomiasis was made and the patient was treated with two doses of praziquantel 20 mg/kg 6 h apart. He stopped having
439 haematuria within 3 weeks of treatment. A follow-up ultrasound after 6 weeks showed improvement in the bladder wall thickening.
Patient 2 A 12-year-old girl migrated from Zimbabwe 8 months prior to presentation with gross haematuria. There were no other associated symptoms. Her general health was satisfactory. Her mother, who was resident in the UK for the past few years, suggested it might be due to Bilharzia (schistosomiasis), as this girl’s cousins in Zimbabwe had been diagnosed and treated for urinary schistosomiasis. An ultrasound scan of the urinary system was normal. Urine microscopy at least on two occasions showed only numerous red cells. At cystoscopy there were multiple lesions of granular appearance mainly to the left and anterior bladder wall. There were also signs of chronic inflammation of the bladder. Punch biopsy of the bladder confirmed the presence of eggs of S. haematobium and eosinophils as the main feature of the inflammatory lesions. She was treated with 20 mg/kg praziquantel followed by a second dose at the same level. She showed symptomatic improvement at 6-week follow-up.
Discussion
Figure 1 a. Ultrasound image showing thick-walled bladder. The trigonal area of the bladder has polypoidal lesions, with thickening of mucosa around both ureteric orifices. b. Cystoscopic image showing polypoidal mucosal lesions, inflamed and friable.
British expatriate children involved in water sports like paddling, fishing and swimming activities in freshwater lakes while visiting endemic areas are exposed to schistosomiasis infection [4]. The severity and mode of infection varies between travelling and migrant children. In travellers, the worm load is typically low but acute symptoms may be more marked. In comparison, the migrant population is chronically and repeatedly infected [5]. Lake Malawi and Zimbabwe, where our two patients contracted the infection, are both endemic areas for schistosomiasis. Urinary schistosomiasis is caused by S. haematobium, a parasite endemic in sub-Saharan Africa and the Arabian peninsula [2]. It is a waterborne disease affecting humans when the larval form penetrates the skin from freshwater reservoirs. During the course of its life cycle, this organism causes various symptoms. The larvae grow into the adult form in human blood and release eggs via the urine. For this to happen, the eggs must leave the circulation and traverse the bladder wall, where they cause an immunopathological response with tissue damage manifesting as painless haematuria, usually several months after the skin penetration. To complete the life cycle, the eggs have to be released into freshwater [3]. Schistosomiasis can present clinically in various different phases. The immediate form is transient, and occurs soon after the penetration of skin by larvae. This leads to ‘swimmer’s itch’, with skin flare and urticarial rash [6]. The acute phase, also known as Katayama fever, may take place over the next few weeks to months. This is an immunological response to migrating schistosomulae in the vascular compartment. It is characterized by fever, fatigue, myalgia, malaise, respiratory symptoms and rash [3]. These symptoms are usually self-limiting. In our first patient, although these symptoms did exist, they were not
440 significant enough to warrant any clinical investigations. In an endemic population these symptoms are less common due to desensitization, as was the case in our second patient. The chronic form may present in months to years with dysuria, proteinuria, and terminal haematuria being the main features, and may accompany chronic anaemia in school-age children [7]. Occasionally, the entire urine specimen can be dark coloured. It can be mistaken as the start of menstruation in girls and in endemic areas even in boys it is known as ‘male menstruation’ [8]. These early signs become less common after adolescence. The eggs of S. haematobium provoke initially urothelial reactive changes with histological hyperplasia and metaplastic changes. A granulomatous reaction with eosinophils ensues (Fig. 2); with time fibrosis of the bladder neck may develop, but the main complication is from obstruction of the ureteric orifices by tissue scarring or pure egg accumulation which may cause obstructive uropathy. Occasionally inflammatory pseudopolyps develop, which on cystoscopy appear as fleshy polypoid patches. The presence of such polypoid lesions in the bladder wall may be apparent as neoplastic growths on ultrasound [9]. One of our patients was referred for possible bladder malignancy following an ultrasound appearance of localized thickening of the bladder. In untreated patients, chronic lesions may lead to fibrosis or calcification of the bladder and lower ureters, resulting in obstructive uropathy and eventual renal failure. In Egypt and other African endemic areas, a high incidence of squamous cell carcinoma of the urinary bladder is associated with chronic schistosomiasis. However, the exact mode of this link is not clear [1,10,11]. A detailed travel history and awareness of the existence of this disease is essential in making a diagnosis. Urinary S. haematobium infection is diagnosed by detecting eggs with terminal spines or live miracidia of the parasite in urine. In heavily contaminated urine the diagnosis is relatively easy. However, in mild infection even a centrifuged sample of urine may fail to reveal eggs. Both of our patients underwent cystoscopic biopsy as urine examination on more than
Figure 2 Diffuse, eosinophil-rich inflammatory cell infiltrate surrounding degenerate eggs. One egg is calcified (arrow) and engulfed by a multinucleated foreign body-type giant cell (H&E, 400 magnification).
A. Qazi et al. one occasion was not diagnostic. A positive history and high index of suspicion are helpful, and may even help to avoid the need for cystoscopy. Eosinophilia in the presence of other relevant symptoms can aid in making the diagnosis. Antibody-based assays are useful diagnostic tests in travellers and migrants but cannot be used in endemic areas due to cost and complexity [4]. Ultrasound imaging in chronic urinary schistosomiasis can be used to visualize thickening of bladder wall, nodules, ureteral obstruction or hydronephrosis [12]. Praziquantel is the treatment of choice, effective against all schistosome species. The recommended standard regimen is 40 mg/kg body weight in a single dose [13]. The recommended dose for children over 4 years is 20 mg/kg followed after 4e6 h by a further dose of 20 mg/kg [14]. It is judged safe for the treatment of young children and pregnant women [15]. Side effects are mild and include nausea, vomiting and abdominal pain. Release of a large antigen load after a dose of praziquantel may cause acute symptoms. Follow-up after treatment should be carried out in 6 weeks with eosinophil count and ultrasound to assess lesions in the bladder as well as to assess any signs of persistent obstructive uropathy. If the eosinophil count is still high, a repeat dose is recommended after 6e12 weeks [3].
Conflict of interest/funding None.
Appendix 1. Urinary schistosomiasis is caused by a. Schistosoma mansoni b. Schistosoma intercalatum c. Schistosoma haematobium d. Schistosoma mekongi 2. During the course of urinary schistosomiasis, inflammation and bleeding from the urinary tract occurs because a. larvae of Schistosoma are excreted in the urine, and embed in the urothelium. b. eggs of Schistosoma are excreted in the urine, and embed in the urothelium. c. inflammation of the urothelium is part of a generalized process of inflammation. d. Schistosoma larvae cause haemolysis which causes discoloration of the urine. 3. Urinary schistosomiasis can be associated with all of the following except a. Katayama fever b. male menstruation c. liver cysts d. swimmer’s itch 4. Treatment of urinary schistosomiasis is a. expectant b. praziquantel c. albendazole d. chloroquine
Urinary schistosomiasis in children in UK 5. Recommended follow-up investigations post treatment for urinary schistosomiasis include a. ultrasound and eosinophil count b. ultrasound and ESR c. cystoscopy and ultrasound d. eosinophil count and cystoscopy
References [1] Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006;368(9541):1106e18. [2] Health Protection Agency. Foreign travel associated illness, England, Wales and Northern Ireland. 2007 report. London: HPA. Available at: http://www.hpa.org.uk/webw/HPAweb&HPA webStandard/HPAweb_C/1204186178825?pZ1158945066450; 2007 [accessed 28.11.2011]. [3] US Centers for Disease control and Prevention. Schistosomiasis. Health information for overseas travel 2008. Atlanta: Elsevier; 2007. 297e300. [4] Samuel M, Misra D, Larcher V, Price E. Schistosoma haematobium infection in children in Britain. BJU Int 2000;85:316e8. [5] Clerinx J, Van Gompel A. Schistosomiasis in travellers and migrants. Travel Med Infect Dis 2011;9:6e24. [6] Meltzer E, Artom G, Marva E, Assous MA, Rahav G, Schwartz E. Schistosomiasis among travelers: new aspects of an old disease. Emerg Infect Dis 2002;12:1696e700.
441 [7] Tatala SR, Kihamia CM, Kyungu LH, Svanberg U. Risk factors for anaemia in schoolchildren in Tanga Region, Tanzania. Tanzan J Health Res 2008;10:189e202. [8] Jordan P. From Katayama to the Dakhla Oasis: the beginning of epidemiology and control of bilharzia. Acta Trop 2000;77:9e40. [9] Merrot T, Retornaz K, Chaumoitre K, Garnier JM, Alessandrini P. Tumorlike form of bladder schistosomiasis in children. Arch Pediatr 2003;10:710e2. [10] Salem S, Mitchell RE, El Alim El-Dorey A, Smith JA, Barocas DA. Successful control of schistosomiasis and the changing epidemiology of bladder cancer in Egypt. BJU Int 2011;107:206e11. [11] Schistosomiasis. World Health Organization, Media centre, Fact sheet No. 115, www.who.int/mediacentre/factsheets/fs115/ en/#; February 2010. Available at:[accessed 28.11.2011]. [12] Ekwunife CA, Okafor FC, Nwaorgu OC. Ultrasonographic screening of urinary schistosomiasis infected patients in Agulu community, Anambra state, southeast Nigeria. Int Arch Med 2009;2:34. [13] WHO Expert Committee. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Technical report series. Geneva: World Health Organization; 2002. [14] Joint Formulary Committee. British National Formulary for children. 2010e2011. London: BMJ Group, Pharmaceutical Press and RCPCH Publications Ltd; 2010. [15] WHO. Report of the WHO informal consultation on the use of praziquantel during pregnancy/lactation and albendazole/mebendazole in children under 24 months (WHO/CDS/CPE/ PVC/2002.4). Geneva: World Health Organization; 2002.
EDUCATIONAL ARTICLE
Urinary schistosomiasis in children in the United Kingdom Abid Qazi a, Jens Stahlschmidt b, Ramnath Subramaniam a,* a
Dept of Paediatric Urology, Leeds Teaching Hospitals NHS Trust, F floor Martin Wing, Great George Street, Leeds LS1 3EX, United Kingdom b Dept of Paediatric Pathology, Leeds Teaching Hospitals NHS Trust, Bexley Wing, Leeds LS97TF, United Kingdom Received 31 July 2011; accepted 28 November 2011 Available online 30 December 2011
Abstract We report on two patients with urinary schistosomiasis, who both presented within a fortnight to our hospital with similar symptoms of persistent painless haematuria. Ultrasound, cystoscopic biopsies and histology were used to confirm diagnosis. Treatment with praziquantel was given. Symptoms of urinary schistosomiasis can easily be missed in non-endemic areas and possibly confused with a more sinister pathology. A thorough history and awareness of disease can avoid interventional investigations. ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
Introduction Haematuria is an uncommon symptom in children. If not accompanied by proteinuria, it should be referred for urological assessment for stones, bladder pathology or rarely Wilms’ tumour. In the developed world, a clinician rarely encounters a pathology like urinary schistosomiasis, which is endemic in Africa and is the commonest cause of haematuria in children [1]. However, due to economic migration from endemic areas and increased foreign travel generally, it is not so unexpected to find this pathology in developed countries [2e5]. In the UK, there were 116 cases of Schistosoma haematobium reported between 2003 and * Corresponding author. Tel.: þ44 113 3926251; fax: þ44 113 2066634. E-mail address: [email protected] (R. Subramaniam).
2005, according to the England and Wales national laboratory database [2]. Over two thirds of patients in this report were from London and the adjacent area. Recognition of acute symptoms frequently does not occur due to the rarity of the disease.
Case summaries Patient 1 A 14-year-old boy presented with gross terminal haematuria for 2 months. The condition was painless but he reported having general symptoms of malaise and fatigue with poor appetite for some time. Previously, he had been fit and well except that he was a known carrier of the thalassaemia trait. Urine examination showed frank haematuria, and microscopy showed numerous red blood cells
1477-5131/$36 ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jpurol.2011.11.008
Urinary schistosomiasis in children in UK but was otherwise unremarkable. An ultrasound scan of the urinary tract revealed localized thickening of the bladder trigone on the left side (Fig. 1a). The left ureteric orifice area was thickened. A good ureteric jet was visible. There was mild hydronephrosis of the left kidney (AP diameter 11 mm) but no ureteric dilatation was seen. His haemoglobin was 11.4 gm/dl. Full blood count was normal except eosinophilia 0.71 109 (normal range 0.04e0.40). The thickened bladder wall and its location raised suspicion of rhabdomyosarcoma of the bladder. Cystoscopy revealed multiple lesions in the area of the trigone, studded with white spots within the lesion (Fig. 1b). There were lesions adjacent to both ureteric orifices, and these were inflamed and friable. Punch biopsy and urine specimen were sent for histology and cytology. The biopsy proved the presence of eggs of S. haematobium. The inflammatory mass constituted eosinophil-rich inflammatory cells surrounding mature eggs of S. haematobium. Some of the cells were degenerating and calcified. Revisiting the patient’s history revealed that he had been to Malawi, a year ago, where his father was working. A diagnosis of schistosomiasis was made and the patient was treated with two doses of praziquantel 20 mg/kg 6 h apart. He stopped having
439 haematuria within 3 weeks of treatment. A follow-up ultrasound after 6 weeks showed improvement in the bladder wall thickening.
Patient 2 A 12-year-old girl migrated from Zimbabwe 8 months prior to presentation with gross haematuria. There were no other associated symptoms. Her general health was satisfactory. Her mother, who was resident in the UK for the past few years, suggested it might be due to Bilharzia (schistosomiasis), as this girl’s cousins in Zimbabwe had been diagnosed and treated for urinary schistosomiasis. An ultrasound scan of the urinary system was normal. Urine microscopy at least on two occasions showed only numerous red cells. At cystoscopy there were multiple lesions of granular appearance mainly to the left and anterior bladder wall. There were also signs of chronic inflammation of the bladder. Punch biopsy of the bladder confirmed the presence of eggs of S. haematobium and eosinophils as the main feature of the inflammatory lesions. She was treated with 20 mg/kg praziquantel followed by a second dose at the same level. She showed symptomatic improvement at 6-week follow-up.
Discussion
Figure 1 a. Ultrasound image showing thick-walled bladder. The trigonal area of the bladder has polypoidal lesions, with thickening of mucosa around both ureteric orifices. b. Cystoscopic image showing polypoidal mucosal lesions, inflamed and friable.
British expatriate children involved in water sports like paddling, fishing and swimming activities in freshwater lakes while visiting endemic areas are exposed to schistosomiasis infection [4]. The severity and mode of infection varies between travelling and migrant children. In travellers, the worm load is typically low but acute symptoms may be more marked. In comparison, the migrant population is chronically and repeatedly infected [5]. Lake Malawi and Zimbabwe, where our two patients contracted the infection, are both endemic areas for schistosomiasis. Urinary schistosomiasis is caused by S. haematobium, a parasite endemic in sub-Saharan Africa and the Arabian peninsula [2]. It is a waterborne disease affecting humans when the larval form penetrates the skin from freshwater reservoirs. During the course of its life cycle, this organism causes various symptoms. The larvae grow into the adult form in human blood and release eggs via the urine. For this to happen, the eggs must leave the circulation and traverse the bladder wall, where they cause an immunopathological response with tissue damage manifesting as painless haematuria, usually several months after the skin penetration. To complete the life cycle, the eggs have to be released into freshwater [3]. Schistosomiasis can present clinically in various different phases. The immediate form is transient, and occurs soon after the penetration of skin by larvae. This leads to ‘swimmer’s itch’, with skin flare and urticarial rash [6]. The acute phase, also known as Katayama fever, may take place over the next few weeks to months. This is an immunological response to migrating schistosomulae in the vascular compartment. It is characterized by fever, fatigue, myalgia, malaise, respiratory symptoms and rash [3]. These symptoms are usually self-limiting. In our first patient, although these symptoms did exist, they were not
440 significant enough to warrant any clinical investigations. In an endemic population these symptoms are less common due to desensitization, as was the case in our second patient. The chronic form may present in months to years with dysuria, proteinuria, and terminal haematuria being the main features, and may accompany chronic anaemia in school-age children [7]. Occasionally, the entire urine specimen can be dark coloured. It can be mistaken as the start of menstruation in girls and in endemic areas even in boys it is known as ‘male menstruation’ [8]. These early signs become less common after adolescence. The eggs of S. haematobium provoke initially urothelial reactive changes with histological hyperplasia and metaplastic changes. A granulomatous reaction with eosinophils ensues (Fig. 2); with time fibrosis of the bladder neck may develop, but the main complication is from obstruction of the ureteric orifices by tissue scarring or pure egg accumulation which may cause obstructive uropathy. Occasionally inflammatory pseudopolyps develop, which on cystoscopy appear as fleshy polypoid patches. The presence of such polypoid lesions in the bladder wall may be apparent as neoplastic growths on ultrasound [9]. One of our patients was referred for possible bladder malignancy following an ultrasound appearance of localized thickening of the bladder. In untreated patients, chronic lesions may lead to fibrosis or calcification of the bladder and lower ureters, resulting in obstructive uropathy and eventual renal failure. In Egypt and other African endemic areas, a high incidence of squamous cell carcinoma of the urinary bladder is associated with chronic schistosomiasis. However, the exact mode of this link is not clear [1,10,11]. A detailed travel history and awareness of the existence of this disease is essential in making a diagnosis. Urinary S. haematobium infection is diagnosed by detecting eggs with terminal spines or live miracidia of the parasite in urine. In heavily contaminated urine the diagnosis is relatively easy. However, in mild infection even a centrifuged sample of urine may fail to reveal eggs. Both of our patients underwent cystoscopic biopsy as urine examination on more than
Figure 2 Diffuse, eosinophil-rich inflammatory cell infiltrate surrounding degenerate eggs. One egg is calcified (arrow) and engulfed by a multinucleated foreign body-type giant cell (H&E, 400 magnification).
A. Qazi et al. one occasion was not diagnostic. A positive history and high index of suspicion are helpful, and may even help to avoid the need for cystoscopy. Eosinophilia in the presence of other relevant symptoms can aid in making the diagnosis. Antibody-based assays are useful diagnostic tests in travellers and migrants but cannot be used in endemic areas due to cost and complexity [4]. Ultrasound imaging in chronic urinary schistosomiasis can be used to visualize thickening of bladder wall, nodules, ureteral obstruction or hydronephrosis [12]. Praziquantel is the treatment of choice, effective against all schistosome species. The recommended standard regimen is 40 mg/kg body weight in a single dose [13]. The recommended dose for children over 4 years is 20 mg/kg followed after 4e6 h by a further dose of 20 mg/kg [14]. It is judged safe for the treatment of young children and pregnant women [15]. Side effects are mild and include nausea, vomiting and abdominal pain. Release of a large antigen load after a dose of praziquantel may cause acute symptoms. Follow-up after treatment should be carried out in 6 weeks with eosinophil count and ultrasound to assess lesions in the bladder as well as to assess any signs of persistent obstructive uropathy. If the eosinophil count is still high, a repeat dose is recommended after 6e12 weeks [3].
Conflict of interest/funding None.
Appendix 1. Urinary schistosomiasis is caused by a. Schistosoma mansoni b. Schistosoma intercalatum c. Schistosoma haematobium d. Schistosoma mekongi 2. During the course of urinary schistosomiasis, inflammation and bleeding from the urinary tract occurs because a. larvae of Schistosoma are excreted in the urine, and embed in the urothelium. b. eggs of Schistosoma are excreted in the urine, and embed in the urothelium. c. inflammation of the urothelium is part of a generalized process of inflammation. d. Schistosoma larvae cause haemolysis which causes discoloration of the urine. 3. Urinary schistosomiasis can be associated with all of the following except a. Katayama fever b. male menstruation c. liver cysts d. swimmer’s itch 4. Treatment of urinary schistosomiasis is a. expectant b. praziquantel c. albendazole d. chloroquine
Urinary schistosomiasis in children in UK 5. Recommended follow-up investigations post treatment for urinary schistosomiasis include a. ultrasound and eosinophil count b. ultrasound and ESR c. cystoscopy and ultrasound d. eosinophil count and cystoscopy
References [1] Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006;368(9541):1106e18. [2] Health Protection Agency. Foreign travel associated illness, England, Wales and Northern Ireland. 2007 report. London: HPA. Available at: http://www.hpa.org.uk/webw/HPAweb&HPA webStandard/HPAweb_C/1204186178825?pZ1158945066450; 2007 [accessed 28.11.2011]. [3] US Centers for Disease control and Prevention. Schistosomiasis. Health information for overseas travel 2008. Atlanta: Elsevier; 2007. 297e300. [4] Samuel M, Misra D, Larcher V, Price E. Schistosoma haematobium infection in children in Britain. BJU Int 2000;85:316e8. [5] Clerinx J, Van Gompel A. Schistosomiasis in travellers and migrants. Travel Med Infect Dis 2011;9:6e24. [6] Meltzer E, Artom G, Marva E, Assous MA, Rahav G, Schwartz E. Schistosomiasis among travelers: new aspects of an old disease. Emerg Infect Dis 2002;12:1696e700.
441 [7] Tatala SR, Kihamia CM, Kyungu LH, Svanberg U. Risk factors for anaemia in schoolchildren in Tanga Region, Tanzania. Tanzan J Health Res 2008;10:189e202. [8] Jordan P. From Katayama to the Dakhla Oasis: the beginning of epidemiology and control of bilharzia. Acta Trop 2000;77:9e40. [9] Merrot T, Retornaz K, Chaumoitre K, Garnier JM, Alessandrini P. Tumorlike form of bladder schistosomiasis in children. Arch Pediatr 2003;10:710e2. [10] Salem S, Mitchell RE, El Alim El-Dorey A, Smith JA, Barocas DA. Successful control of schistosomiasis and the changing epidemiology of bladder cancer in Egypt. BJU Int 2011;107:206e11. [11] Schistosomiasis. World Health Organization, Media centre, Fact sheet No. 115, www.who.int/mediacentre/factsheets/fs115/ en/#; February 2010. Available at:[accessed 28.11.2011]. [12] Ekwunife CA, Okafor FC, Nwaorgu OC. Ultrasonographic screening of urinary schistosomiasis infected patients in Agulu community, Anambra state, southeast Nigeria. Int Arch Med 2009;2:34. [13] WHO Expert Committee. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Technical report series. Geneva: World Health Organization; 2002. [14] Joint Formulary Committee. British National Formulary for children. 2010e2011. London: BMJ Group, Pharmaceutical Press and RCPCH Publications Ltd; 2010. [15] WHO. Report of the WHO informal consultation on the use of praziquantel during pregnancy/lactation and albendazole/mebendazole in children under 24 months (WHO/CDS/CPE/ PVC/2002.4). Geneva: World Health Organization; 2002.