Skip to main content

Advertisement

Log in

The WHO ultrasonography protocol for assessing morbidity due to Schistosoma haematobium. Acceptance and evolution over 14 years. Systematic review

  • Review
  • Published:
Parasitology Research Aims and scope Submit manuscript

An Erratum to this article was published on 27 March 2015

Abstract

In 2000, the World Health Organization (WHO) published an ultrasound field protocol for assessing morbidity due to schistosomiasis. The present study aims to review the acceptance of the WHO protocol for Schistosoma haematobium. A PubMed literature research using the keywords “ultrasound OR ultrasonography (US) AND schistosomiasis,” “US AND S. haematobium,” “US AND urinary schistosomiasis” from 2001 through 2014 was performed. Thirty-eight eligible publications reporting on 17,861 patients from 13 endemic and 2 non-endemic countries were analysed. Of these, 33 referred to field studies on 17,317 patients. The Niamey protocol was applied to 15,367/17,317 (88.74 %) patients in 23/33 (69.70 %) of field studies (all studies: 15,649/17,861 [87.61 %] patients (25/38 [68.42 %] studies). The acceptance of the protocol by single country in field studies varied from 0 to 100 %. It varied over time between 55.56 % (5/9) in the period from 2001 to 2004, to 87.50 % (7/8) from 2005 to 2008, to 62.50 % (5/8) from 2009 to 2011 and 75.00 % (6/8) from 2012 through 2014 (all studies: 50 % [5/10], 88.89 % [8/9], 62.50 % [5/8], 63.64 % [7/11], respectively). The Niamey protocol was applied also in 2/5 hospital studies in 282/544 (51.84 %) patients.

The usefulness of the WHO protocol for S. haematobium infections is confirmed by its worldwide acceptance. Some simplifications might facilitate its use also for focused ultrasound examinations performed by less skilled examiners. Organ abnormalities due to schistosomiasis detectable by ultrasonography not yet covered by the WHO protocol should be added to the additional investigations section.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdelrahim AF, Abdelmaguid A, Abuzeid H, Amin M, Mousa el-S, Abdelrahim FJ (2008) Rigid ureteroscopy for ureteral stones: factors associated with intraoperative adverse events. Endourology 22(2):277–280

    Article  Google Scholar 

  • Abdel-Wahab MF, Abdel-Latif Z, El Kady NM, Arafa NM (1978) The use of ultrasonography in the diagnosis of different schistosomal syndromes. Proceedings of the third International Workshop on Diagnostic Ultrasound Imaging. Al-Ahram Press, Cairo, Egypt 458–463

  • Abou-Elela A, Torky M, Salah E, Morsy A, Elsherbiny M (2010) Inverted ureteral nipple as antireflux technique in surgical management of bilharzial ureteral strictures. Urology 76(4):983–987

    Article  PubMed  Google Scholar 

  • Ahmed FO, Hamdan HZ, Abdelgalil HB, Sharfi AA (2014) A comparison between transabdominal ultrasonographic and cystourethroscopy findings in adult Sudanese patients presenting with haematuria. Int Urol Nephrol 6. [Epub ahead of print]

  • Ajit MK, Groenewald EA, Speakman M (2005) An unusual presentation of genitourinary schistosomiasis in a Caucasian woman in the UK. Ann R Coll Surg Engl 87(6):481

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Amonkar P, Murali G, Krishnamurthy S (2001) Schistosoma induced squamous cell carcinoma of the bladder. Indian J Pathol Microbiol 44:363–364

    CAS  PubMed  Google Scholar 

  • Badmos KB, Popoola AA, Buhari MO, Abdulkadir AY (2009) Ureteric schistosomiasis with obstructive uropathy. J Coll Physicians Surg Pak 19(7):456–458

    PubMed  Google Scholar 

  • Bakari AA, Gadam IA, Aliyu S, Suleiman I, Ahidjo AA, Pindiga UH (2012) Use of Mitrofanoff and Yang-Monti techniques as ureteric substitution for severe schistosomal bilateral ureteric stricture: a case report and review of the literature. Niger J Surg 18(1):30–33

    PubMed Central  PubMed  Google Scholar 

  • Barsoum RS (2003) Schistosomiasis and the kidney. Semin Nephrol 23(1):34–41

    Article  PubMed  Google Scholar 

  • Benchekroun TS, Kriouil A, Belkacem A, Jorio-Benkhraba M, el Fakir Y, Benhammou M, Outarahout O, el Malki-Tazi A (1997) Urogenital tuberculosis in children. Arch Pediatr 4(9):857–861

    Article  CAS  PubMed  Google Scholar 

  • Ben-Chetrit E, Lachish T, Mørch K, Atias D, Maguire C, Schwartz E (2014) Schistosomiasis in pregnant travelers: a case series. J Travel Med 13. doi: 10.1111/jtm.12165. [Epub ahead of print]

  • Bonnard P, Boutouaba S, Diakhate I, Seck M, Dompnier JP, Riveau G (2011) Learning curve of vesico-urinary ultrasonography in Schistosoma haematobium infection with WHO practical guide: a "simple to learn" examination. Am J Trop Med Hyg 85:1071–1074

    Article  PubMed Central  PubMed  Google Scholar 

  • Brouwer KC, Ndhlovu PD, Wagatsuma Y, Munatsi A, Shiff CJ (2003) Urinary tract pathology attributed to Schistosoma haematobium: does parasite genetics play a role? Am J Trop Med Hyg 68(4):456–462

    PubMed  Google Scholar 

  • Burki A, Tanner M, Burnier E, Schweizer W, Meudt R, Degrémont A (1986) Comparison of ultrasonography, intravenous pyelography and cystoscopy in detection of urinary tract lesions due to Schistosoma haematobium. Acta Trop 43(2):139–151

    CAS  PubMed  Google Scholar 

  • Cairo Working Group (1991) Meeting on the use of ultrasound for the assessment of pathology due to schistosomiasis. World Health Organization, Geneva

    Google Scholar 

  • Cairo Working Group Hatz C, Jenkins J (eds) (1992) The use of diagnostic ultrasound in schistosomiasis-attempts at standardization of methodology. Acta Trop 51:45–61

  • Campagne G, Garba A, Barkiré H, Vera C, Sidiki A, Chippaux JP (2001) Continued ultrasonic follow-up of children infected with Schistosoma haematobium after treatment with praziquantel. Trop Med Int Health 6(1):24–30

    Article  CAS  PubMed  Google Scholar 

  • Chippaux JP, Campagne G, Garba A, Véra C (2001) [Significance of rapid evaluation indicators during the monitoring of graduated treatment against Schistosoma haematobium]. [Article in French]. Bull Soc Pathol Exot 94(1):36–41

    CAS  PubMed  Google Scholar 

  • Coulibaly Y, Ouattara Z, Togo A, Konate M, Ouattara M, Ouattara K (2011) [Bilharziasis and urinary lithiasis: a study of 23 cases at the Gabriel Toure Hospital] [Article in French]. Mali Med 26(1):26–28, French

    CAS  PubMed  Google Scholar 

  • Das KM, Indudhara R, Vaidyanathan S (1992) Sonographic features of genitourinary tuberculosis. Am J Roentgenol 158(2):327–329

    Article  CAS  Google Scholar 

  • Degremont A, Burki A, Burnier E, Schweizer W, Meudt R, Tanner M (1985) Value of ultrasonography in investigating morbidity due to Schistosoma haematobium infection. Lancet 23(1):662–665

    Article  Google Scholar 

  • Del Carpio M, Mercapide CH, Salvitti JC, Uchiumi L, Sustercic J, Panomarenko H, Moguilensky J, Herrero E, Talmon G, Volpe M, Araya D, Mujica G, Calabro A, Mancini S, Chiosso C, Labanchi JL, Saad R, Goblirsch S, Brunetti E, Larrieu E (2012) Early diagnosis, treatment and follow-up of cystic echinococcosis in remote rural areas in Patagonia: impact of ultrasound training of non-specialists. PLoS Negl Trop Dis 6:1444

    Article  Google Scholar 

  • Doehring E, Ehrich JH, Reider F, Dittrich M, Schmidt-Ehry G, Brodehl J (1985) Morbidity in urinary schistosomiasis: relation between sonographical lesions and pathological urine findings. Trop Med Parasitol 36(3):145–149

    CAS  PubMed  Google Scholar 

  • Duarte DB, Vanderlei LA, Bispo RK, Pinheiro ME, Silva Junior GB, Daher EF (2014) Acute kidney injury in Schistosomiasis: a retrospective cohort of 60 patients in Brazil. J Parasitol. 2014 Nov 13. [Epub ahead of print]

  • Ekwunife CA, Okafor FC, Nwaorgu OC (2009) Ultrasonographic screening of urinary schistosomiasis infected patients in Agulu community, Anambra state, southeast Nigeria. Int Arch Med 2(1):34. doi:10.1186/1755-7682-2-34

    Article  PubMed Central  PubMed  Google Scholar 

  • El Baz MA, Morsy TA, El Bandary MM, Motawea SM (2003) Clinical and parasitological studies on the efficacy of Mirazid in treatment of schistosomiasis haematobium in Tatoon, Etsa Center, El Fayoum Governorate. J Egypt Soc Parasitol 33(3):761–776

    PubMed  Google Scholar 

  • Elmadani AE, Hamdoun AO, Monis A, Karamino NE, Gasmelseed N (2013) Ultrasound findings in urinary schistosomiasis infection in school children in the Gezira State Central Sudan. Saudi J Kidney Dis Transpl 24(1):162–167

    Article  PubMed  Google Scholar 

  • El-Nahas AR, Shoma AM, El-Baz M (2003) Bilharzial pyelitis: a rare cause of secondary ureteropelvic junction obstruction. J Urol 170(5):1946–1947

    Article  PubMed  Google Scholar 

  • el Scheich, T, Holtfreter MC, Ekamp H, Singh DD, Mota R, Hatz C, Richter J (2014) The WHO ultrasonography protocol for assessing hepatic morbidity due to Schistosoma mansoni. Acceptance and evolution over 12 years. Parasitol Res 113(11):3915–3925

  • Figueiredo J, Richter J, Belo S, Grácio MA (2013) Urogenital schistosomiasis presenting genital and urinary tract lesions and abdominal discomfort in a sterile Angolan woman. J Genit Syst Disord\ 2(3):1–4

    Google Scholar 

  • Figueiredo J, Santos Â, Clemente H, Lourenço A, Costa S, Grácio MA, Belo S (2014a) Schistosomiasis and acute appendicitis. Acta Med Port 27(3):396–399, Portuguese

    PubMed  Google Scholar 

  • Figueiredo JC, Richter J, Borja N, Balaca A, Costa S, Belo S, Grácio MA (2014b). Prostate adenocarcinoma associated with prostatic infection due to Schistosoma haematobium. Case report and systematic review. Parasitol Res Dec 30 Epub ahead of print]

  • Garba A, Campagne G, Tassie JM, Barkire A, Vera C, Sellin B, Chippaux JP (2004) Long-term impact of a mass treatment by praziquantel on morbidity due to Schistosoma haematobium in two hyperendemic villages of Niger. Bull Soc Pathol Exot 97(1):7–11

    CAS  PubMed  Google Scholar 

  • Gasmelseed N, Karamino NE, Abdelwahed MO, Hamdoun AO, Elmadani AE (2014) Genetic diversity of Schistosoma haematobium parasite is not associated with severity of disease in an endemic area in Sudan. BMC Infect Dis 14(469). doi: 10.1186/1471-2334-14-469

  • Gilligan T, Dreicer R (2007) The atypical urothelial cancer patient: management of bladder cancers of non-transitional cell histology and cancers of the ureters and renal pelvis. Semin Oncol 34(2):145–153

    Article  PubMed  Google Scholar 

  • Gouvras AN, Kariuki C, Koukounari A, Norton AJ, Lange CN, Ireri E, Fenwick A, Mkoji GM, Webster JP (2013) The impact of single versus mixed Schistosoma haematobium and S. mansoni infections on morbidity profiles amongst school-children in Taveta, Kenya. Acta Trop 128(2):309–317

    Article  PubMed  Google Scholar 

  • Hasegawa Y, Nishiii M, Masui S, Yoshio Y, Kanda H, Kanai M, Yamada Y, Arima K, Sugimura Y (2014) Urinary schistosomiasis: report of a case. Hinyokika Kiyo 60(2):91–94, Japanese

    PubMed  Google Scholar 

  • Hatz CF (2001) The use of ultrasound in schistosomiasis. Adv Parasitol 48:225–284

    Article  CAS  PubMed  Google Scholar 

  • Hatz CF, Vennervald BJ, Nkulila T, Vounatsou P, Kombe Y, Mayombana C, Mshinda H, Tanner M (1998) Evolution of Schistosoma haematobium-related pathology over 24 months after treatment with praziquantel among school children in southeastern Tanzania. Am J Trop Med Hyg 59(5):775–781

    CAS  PubMed  Google Scholar 

  • Heller T, Wallrauch C, Lessells RJ, Goblirsch S, Brunetti E (2010) Short course for focused assessment with sonography for human immunodeficiency virus/tuberculosis: preliminary results in a rural setting in South Africa with high prevalence of human immunodeficiency virus and tuberculosis. Am J Trop Med Hyg 88:512–515

    Article  Google Scholar 

  • Holman E, Khan AM, Flasko T, Toth C, Salah MA (2004) Endoscopic management of pediatric urolithiasis in a developing country. Urology 63(1):159–162

    Article  PubMed  Google Scholar 

  • Hsieh HC, Lu PL, Chen YH, Chen TC, Tsai JJ, Chang K, Chen TP (2006) Genitourinary tuberculosis in a medical center in southern Taiwan: an eleven-year experience. J Microbiol Immunol Infect 39(5):408–413

    CAS  PubMed  Google Scholar 

  • Hussein A, Rifaat E, Zaki A, Abol-Nasr M (2006) Stenting versus non-stenting after non-complicated ureteroscopic manipulation of stones in bilharzial ureters. Int J Urol 13(7):886–890

    Article  PubMed  Google Scholar 

  • Jang TB, Casey RJ, Dyne P, Kaji A (2010a) The learning curve of resident physicians using emergency ultrasonography for obstructive uropathy. Acad Emerg Med 17:1024–1027

    Article  PubMed  Google Scholar 

  • Jang TB, Ruggeri W, Dyne P, Kaji AH (2010b) Learning curve of emergency physicians using emergency bedside sonography for symptomatic first-trimester pregnancy. J Ultrasound Med 29:1423–1428

    PubMed  Google Scholar 

  • Kardorff R, Döhring E (2001) Ultrasound diagnosis of bilharziasis. Ultraschall Med 22(3):107–115, Review. German

    Article  CAS  PubMed  Google Scholar 

  • Keita AD, Dembélé M, Kané M, Fongoro S, Traoré M, Sacko M, Diallo S, Sidibe S, Traoré HA, Doumbo O, Traoré I (2001) Ultrasonographic aspects of urinary schistosomiasis in children of the Dogon plateau and the Niger office; impact of praziquantel treatment. Bull Soc Pathol Exot 94(4):335–338

    CAS  PubMed  Google Scholar 

  • Keita AD, Sangho H, Sacko M, Diarra Z, Simaga SY, Traore I (2005) Prevalence of schistomasiasis lesions detected by ultrasonography in children in Molodo, Mali. Gastroenterol Clin Biol 29(6–7):652–655

    Article  PubMed  Google Scholar 

  • Khalaf I, Shokeir A, Shalaby M (2012) Urologic complications of genitourinary schistosomiasis. World J Urol 30(1):31–38

    Article  PubMed  Google Scholar 

  • Kimberly HH, Murray A, Mennicke M, Liteplo A, Lew J, Bohan JS, Tyer-Viola L, Ahn R, Burke T, Noble VE (2010) Focused maternal ultrasound by midwives in rural Zambia. Ultrasound Med Biol 36:1267–1272

    Article  PubMed  Google Scholar 

  • King CH (2002) Ultrasound monitoring of structural urinary tract disease in Schistosoma haematobium infection. Mem Inst Oswaldo Cruz 97(suppl I):149–152

    Article  PubMed  Google Scholar 

  • King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, Muchiri E, Ouma JH (2001) Schistosoma haematobium-induced urinary tract morbidity correlates with increased tumor necrosis factor-alpha and diminished interleukin-10 production. J Infect Dis 184(9):1176–1182

    Article  CAS  PubMed  Google Scholar 

  • King CH, Muchiri EM, Mungai P, Ouma JH, Kadzo H, Magak P, Koech DK (2002) Randomized comparison of low-dose versus standard-dose praziquantel therapy in treatment of urinary tract morbidity due to Schistosoma haematobium infection. Am J Trop Med Hyg 66(6):725–730

    CAS  PubMed  Google Scholar 

  • King CH, Blanton RE, Muchiri EM, Ouma JH, Kariuki HC, Mungai P, Magak P, Kadzo H, Ireri E, Koech DK (2004) Low heritable component of risk for infection intensity and infection-associated disease in urinary schistosomiasis among Wadigo village populations in Coast Province, Kenya. Am J Trop Med Hyg 70(1):57–62

    PubMed  Google Scholar 

  • Kirkpatrick AW (2007) Clinician-performed focused sonography for the resuscitation of trauma. Crit Care Med 35:162–172

    Article  Google Scholar 

  • Koukounari A, Sacko M, Keita AD, Gabrielli AF, Landouré A, Dembelé R, Clements AC, Whawell S, Donnelly CA, Fenwick A, Traoré M, Webster JP (2006) Assessment of ultrasound morbidity indicators of schistosomiasis in the context of large-scale programs illustrated with experiences from Malian children. Am J Trop Med Hyg 75(6):1042–1052

    PubMed  Google Scholar 

  • Koukounari A, Webster JP, Donnelly CA, Bray BC, Naples J, Bosompem K, Shiff C (2009) Sensitivities and specificities of diagnostic tests and infection prevalence of Schistosoma haematobium estimated from data on adults in villages northwest of Accra, Ghana. Am J Trop Med Hyg 80(3):435–441

    PubMed Central  PubMed  Google Scholar 

  • Koukounari A, Donnelly CA, Sacko M, Keita AD, Landouré A, Dembelé R, Bosqué-Oliva E, Gabrielli AF, Gouvras A, Traoré M, Fenwick A, Webster JP (2010) The impact of single versus mixed schistosome species infections on liver, spleen and bladder morbidity within Malian children pre- and post-praziquantel treatment. BMC Infect Dis 10:227. doi:10.1186/1471-2334-10-227

    Article  PubMed Central  PubMed  Google Scholar 

  • Lengeler C, Kilima P, Mshinda H, Morona D, Hatz C, Tanner M (1991) Rapid, low.cost, two-step method to screen for urinary schistosomiasis at the district level: the Kilosa experience. Bull WHO 69:179–189

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lougue-Sorgho LC, Cisse R, Kagone M, Bamouni YA, Tapsoba TL, Sanou A (2002) Radiography and ultrasonography in the management of bladder tumors: 71 cases at the National Hospital Center of Yalgado Ouedraogo (Burkina Faso)]. Bull Soc Pathol Exot 95(4):244–247

    CAS  PubMed  Google Scholar 

  • Lyons B, Stothard R, Rollinson D, Khamis S, Simai KA, Hunter PR (2009) A comparison of urinary tract pathology and morbidity in adult populations from endemic and non-endemic zones for urinary schistosomiasis on Unguja Island, Zanzibar. BMC Infect Dis 9:189. doi:10.1186/1471-2334-9-189

    Article  PubMed Central  PubMed  Google Scholar 

  • Malik MO, Ibrahim A (1982) Scrotal swellings in Sudanese patients: a surgical pathology study. Int Surg 67(4 Suppl):513–515

    CAS  PubMed  Google Scholar 

  • Medhat A, Zarzour A, Nafeh M et al (1997) Evaluation of an ultrasonographic score for urinary bladder morbidity in Schistosoma haematobium infection. Am J Trop Med Hyg 57:16–19

    CAS  PubMed  Google Scholar 

  • Meurs L, Mbow M, Vereecken K, Menten J, Mboup S, Polman K (2012) Bladder morbidity and hepatic fibrosis in mixed Schistosoma haematobium and S. mansoni Infections: a population-wide study in Northern Senegal. PLoS Negl Trop Dis 6(9):e1829. doi:10.1371/journal.pntd.0001829

    Article  PubMed Central  PubMed  Google Scholar 

  • Meurs L, Mbow M, Boon N, van den Broeck F, Vereecken K, Dièye TN, Abatih E, Huyse T, Mboup S, Polman K (2013) Micro-geographical heterogeneity in Schistosoma mansoni and S. haematobium infection and morbidity in a co-endemic community in northern Senegal. PLoS Negl Trop Dis 7(12):e2608. doi:10.1371/journal.pntd.0002608

    Article  PubMed Central  PubMed  Google Scholar 

  • Mostafa MH, Sheweita SA, O'Connor PJ (1999) Relationship between schistosomiasis and bladder cancer. Clin Microbiol Rev 12(1):97–111

    PubMed Central  CAS  PubMed  Google Scholar 

  • Naples J, Isharwal S, Shiff CJ, Bosompem KM, Veltri RW (2009) Clinical utility of squamous and transitional nuclear structure alterations induced by Schistosoma haematobium in chronically infected adults with bladder damage verified by ultrasound in Ghana. Anal Quant Cytol Histol 31(3):143–152

    PubMed  Google Scholar 

  • Nayama M, Garba A, Boulama-Jackou ML, Touré A, Idi N, Garba M, Nouhou H, Decanter C (2007) Uro-genital schistosomiasis with S. haematobium and infertility in Niger. Prospective study of 109 cases. Mali Med 22(3):15–21, French

    CAS  PubMed  Google Scholar 

  • Neal PM (2004) Schistosomiasis—an unusual cause of ureteral obstruction: a case history and perspective. Clin Med Res 2(4):216–227

    Article  PubMed Central  PubMed  Google Scholar 

  • Niamey Working Group: Richter J, Hatz C, Campagne G, Jenkins J (2000) Ultrasound in Schistosomiasis. A practical guide to the standardized use of ultrasonography for the assessment of schistosomiasis-related morbidity. World Health Organization, World Health Organization / TDR / STR/ SCH / WHO-document: 1-51. www.who.int/tdr/publications/publications/ultrasound.htm; last accessed January 25, 2015

  • Njaanake KH, Simonsen PE, Vennervald BJ, Mukoko DA, Reimert CM, Gachuhi K, Jaoko WG, Estambale BB (2014) Urinary cytokines in Schistosoma haematobium-infected schoolchildren from Tana Delta District of Kenya. BMC Infect Dis 14(501) doi: 10.1186/1471-2334-14-501

  • Nmorsi OP, Ukwandu NC, Ogoinja S, Blackie HO, Odike MA (2007) Urinary tract pathology in Schistosoma haematobium infected rural Nigerians. Southeast Asian J Trop Med Public Health 38(1):32–37

    CAS  PubMed  Google Scholar 

  • Oranusi CK, Nwofor A, Onyiaorah IV, Ukah CO (2011) Schistosomal stricture of the ureter-diagnostic dilemma. Niger J Clin Pract 14(4):495–498

    Article  CAS  PubMed  Google Scholar 

  • Ouma JH, King CH, Muchiri EM, Mungai P, Koech DK, Ireri E, Magak P, Kadzo H (2005) Late benefits 10-18 years after drug therapy for infection with Schistosoma haematobium in Kwale District, Coast Province, Kenya. Am J Trop Med Hyg 73(2):359–364

    PubMed  Google Scholar 

  • Poda JN, Traoré A, Sondo BK (2004) Schistosomiasis endemic in Burkina Faso. Bull Soc Pathol Exot 97(1):47–52

    CAS  PubMed  Google Scholar 

  • Poggensee G, Sikelu M, Saría M, Richter J, Krantz I, Feldmeier H (1998) Schistosomiasis of the lower reproductive tract without egg excretion in urine. Am J Trop Med Hyg 59(9):782–783

    CAS  PubMed  Google Scholar 

  • Qazi A, Stahlschmidt J, Subramaniam R (2012) Bladder morbidity and hepatic fibrosis in mixed Schistosoma haematobium and S. mansoni Infections: a population-wide study in Northern Senegal. J Pediatr Urol 8(4):438–441. doi:10.1016/j.jpurol.2011.11.008

    Article  PubMed  Google Scholar 

  • Ramarakoto CE, Leutscher PD, van Dam G, Christensen NO (2008) Ultrasonographical findings in the urogenital organs in women and men infected with Schistosoma haematobium in northern Madagascar. Trans R Soc Trop Med Hyg 102(8):767–773

    Article  CAS  PubMed  Google Scholar 

  • Rambau PF, Chandika A, Chalya PL, Jackson K (2011) Scrotal swelling and testicular atrophy due to schistosomiasis in a 9-year-old boy: a case report. Case Rep Infect Dis 2011:787961

    PubMed Central  PubMed  Google Scholar 

  • Red Urine Study Group (1995) Identification of high-risk communities for schistosomiasis in Africa. A multicountry study. WHO TDR document, World Health Organization Geneva, Switzerland, pp 1–83

    Google Scholar 

  • Richter J (2000) Evolution of schistosomiasis-induced pathology after therapy and interruption of exposure to schistosomes: a review of ultrasonographic studies. Acta Trop 77:111–131

    Article  CAS  PubMed  Google Scholar 

  • Richter J (2003) The impact of chemotherapy on the morbidity due to schistosomiasis. Acta Trop 86:161–183

    Article  PubMed  Google Scholar 

  • Richter J, Poggensee G, Helling-Giese G, Kjetland E, Chitsulo L, Koumenda N, Gundersen S, Krantz I, Feldmeier H (1995) Transabdominal ultrasound for the diagnosis of genital schistosomiasis in women with Schistosoma haematobium infection: a preliminary report. Trans R Soc Trop Med Hyg 89:500–501

    Article  CAS  PubMed  Google Scholar 

  • Richter J, Wagatsuma Y, Aryeetey M, Feldmeier H (1996) Sonographic screening for urinary tract abnormalities in patients with Schistosoma haematobium infection: pitfalls in examining pregnant women. Bull World Health Organ 74(2):217–221

    PubMed Central  CAS  PubMed  Google Scholar 

  • Richter J, Stegemann U, Häussinger D (2002) Hydrocele in a young boy with Schistosoma mansoni infection. Br J Urol 89:1–2

    Google Scholar 

  • Richter J, Hatz C, Häussinger D (2003) Ultrasound in tropical and parasitic diseases. Lancet 362:900–902

    Article  PubMed  Google Scholar 

  • Richter J, Lux J, Reinecke P, Müller-Mattheis V (2008) Of flukes and fistulae. Lancet 371:1308

    Article  PubMed  Google Scholar 

  • Salas-Coronas J, Vázquez-Villegas J, Villarejo-Ordóñez A, Sánchez-Sánchez JC, Espada-Chavarría J, Soriano-Pérez MJ, Cabeza-Barrera MI, Cabezas-Fernández MT (2013) Radiological findings in patients with imported schistosomiasis. Enferm Infecc Microbiol Clin 31(4):205–209

    Article  PubMed  Google Scholar 

  • Sayed HA, Hammam O, Sabry H, Akl M, Amin T, El Lithy T, Roshdy M, El Ganzoury H (2007) Epidemiologic approach for early detection and control of renal and urinary tract diseases in rural populations. J Egypt Soc Parasitol 37(1):313–328

    PubMed  Google Scholar 

  • Schanz A, Richter J, Beyer I, Baldus SE, Hess AP, Kruessel JSJ (2010) Genital schistosomiasis as a cause of female sterility and acute abdomen. Fertil Steril 93(6):2075.e7–9

    Google Scholar 

  • Schleenvoigt BT, Gajda M, Baier M, Groten T, Oppel-Heuchel H, Grimm MO, Pfister W, Richter J, Pletz MW (2014) Placental Schistosoma haematobium infection in a German returnee from Malawi. Infection 42(6):1061–1064

    Article  CAS  PubMed  Google Scholar 

  • Shebel HM, Elsayes KM, Abou El Atta HM, Elguindy YM, El-Diasty TA (2012) Genitourinary schistosomiasis: life cycle and radiologic-pathologic findings. Radiographics 32(4):1031–1046

    Article  PubMed  Google Scholar 

  • Shiff C, Veltri R, Naples J, Quartey J, Otchere J, Anyan W, Marlow C, Wiredu E, Adjei A, Brakohiapa E, Bosompem K (2006) Ultrasound verification of bladder damage is associated with known biomarkers of bladder cancer in adults chronically infected with Schistosoma haematobium in Ghana. Trans R Soc Trop Med Hyg 100:847–854

    Article  PubMed  Google Scholar 

  • Silva IM, Thiengo R, Conceição MJ, Rey L, Pereira Filho E, Ribeiro PC (2006) Cystoscopy in the diagnosis and follow-up of urinary schistosomiasis in Brazilian soldiers returning from Mozambique, Africa. Rev Inst Med Trop Sao Paulo 48(1):39–42

    Article  PubMed  Google Scholar 

  • Singh DD, Vogel M, Müller-Stöver I, el Scheich T, Winzer M, Göbels S, Hüttig F, Heinrich S, Mackenzie C, Jensen B, Reuter S, Häussinger D, Richter J (2011) TB or nor TB? Difficulties in the diagnosis of tuberculosis in HIV-negative immigrants to Germany. Eur J Med Res 16(9):381–384

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sousa-Figueiredo JC, Basáñez MG, Khamis IS, Garba A, Rollinson D, Stothard JR (2009) Measuring morbidity associated with urinary schistosomiasis: assessing levels of excreted urine albumin and urinary tract pathologies. PLoS Negl Trop Dis 3(10):e526. doi:10.1371/journal.pntd.0000526

    Article  PubMed Central  PubMed  Google Scholar 

  • Stothard JR, Sousa-Figueiredo JC, Simba Khamis I, Garba A, Rollinson D (2009) Urinary schistosomiasis-associated morbidity in schoolchildren detected with urine albumin-to-creatinine ratio (UACR) reagent strips. J Pediatr Urol 5(4):287–291

    Article  Google Scholar 

  • Strahan R, McAdam D, Schneider ME (2013) Sonographic response in the liver and urinary bladder of children 14 months after treatment for schistosomiasis. Trop Dr 43(2):71–74

    Article  Google Scholar 

  • Tamarozzi F, Nicoletti GJ, Neumayr A, Brunetti E (2014) Acceptance of standardized ultrasound classification, use of albendazole, and long-term follow-up in clinical management of cystic echinococcosis: a systematic review. Curr Opin Infect Dis 27(5):425–431

  • Tikkakoski T, Karstrup S, Lohela P, Hulkko A, Apaja-Sarkkinen M (1993) Tuberculosis of the lower genitourinary tract: ultrasonography as an aid to diagnosis and treatment. J Clin Ultrasound 21(4):269–271

    Article  CAS  PubMed  Google Scholar 

  • Tohon ZB, Mainassara HB, Garba A, Mahamane AE, Bosqué-Oliva E, Ibrahim ML, Duchemin JB, Chanteau S, Boisier P (2008) Controlling schistosomiasis: significant decrease of anaemia prevalence one year after a single dose of praziquantel in Nigerian schoolchildren. PLoS Negl Trop Dis 2(5):e241. doi:10.1371/journal.pntd.0000241

    Article  PubMed Central  PubMed  Google Scholar 

  • Van der Werf MJ, de Vlas SJ (2004) Diagnosis of urinary schistosomiasis: a novel approach to compare bladder pathology measured by ultrasound and three methods for hematuria detection. Am J Trop Med Hyg 71(1):98–106

    PubMed  Google Scholar 

  • Vancauwenberghe T, Oyaert M, Termote JL, Mulkens T, Bellinck P (2013) Ureteral obstruction caused by schistosomiasis. JBR-BTR 96(5):292–294

    PubMed  Google Scholar 

  • Wagatsuma Y, Aryeetey ME, Sack DA, Morrow RH, Hatz C, Kojima S (1999) Resolution and resurgence of Schistosoma haematobium-induced pathology after community-based chemotherapy in Ghana, as detected by ultrasound. J Infect Dis 179(6):1515–1522

    Article  CAS  PubMed  Google Scholar 

  • Wagatsuma Y, Aryeetey ME, Nkrumah FK, Sack DA, Kojima S (2003) Highly symptom-aware children were heavily infected with urinary schistosomiasis in southern Ghana. Cent Afr J Med 49(1–2):16–19

    CAS  PubMed  Google Scholar 

  • Wamachi AN, Mayadev JS, Mungai PL, Magak PL, Ouma JH, Magambo JK, Muchiri EM, Koech DK, King CH, King CL (2004) Increased ratio of tumor necrosis factor-alpha to interleukin-10 production is associated with Schistosoma haematobium-induced urinary-tract morbidity. J Infect Dis 190(11):2020–2030

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Muhoho ND, Mutua WR, Kiliku FM, Awazawa T, Moji K, Aoki Y (2011) Assessment of voiding function in inhabitants infected with Schistosoma haematobium. J Trop Pediatr 57(4):263–268

    Article  PubMed  Google Scholar 

  • Wong-You-Cheong JJ, Woodward PJ, Manning MA, Davis CJ (2006) From the archives of the AFIP: inflammatory and nonneoplastic bladder masses: radiologic-pathologic correlation. Radiographics 26(6):1847–1868

    Article  PubMed  Google Scholar 

  • Zhong X, Isharwal S, Naples JM, Shiff C, Veltri RW, Shao C, Bosompem KM, Sidransky D, Hoque MO (2013) Hypermethylation of genes detected in urine from Ghanaian adults with bladder pathology associated with Schistosoma haematobium infection. PLoS One 8(3):e59089. doi:10.1371/journal.pone.0059089

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joachim Richter.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akpata, R., Neumayr, A., Holtfreter, M.C. et al. The WHO ultrasonography protocol for assessing morbidity due to Schistosoma haematobium. Acceptance and evolution over 14 years. Systematic review. Parasitol Res 114, 1279–1289 (2015). https://doi.org/10.1007/s00436-015-4389-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4389-z

Keywords

Navigation