Improving the management of imported schistosomiasis haematobia in China: lessons from a case with multiple misdiagnoses
© Hua et al.; licensee BioMed Central Ltd. 2013
Received: 25 August 2013
Accepted: 10 September 2013
Published: 11 September 2013
Human Schistosoma haematobium infection that causes urinary schistosomiasis occurs in Africa and the eastern Mediterranean, and China is only endemic for S. japonicum. In this report, we reported an imported case with S. haematobium infection returning from Angola to Shaanxi Province, northwestern China, where S. japonicum is not endemic.
The case was misdiagnosed as ureteral calculus, invasive urothelial carcinoma and eosinophilic cystitis in several hospitals, and was finally diagnosed by means of serological assay followed by microscopic examination of the urine sediment. The patient was then treated with praziquantel, and a satisfactory outcome was obtained.
As S. haematobium is not indigenous to China, most Chinese doctors and medical technicians are unfamiliar with this introduced parasitic disease, therefore, they need to increase the awareness of its existence when they encounter persons who have visited or resided in endemic areas, and the techniques for detection of the parasite, so as to reduce the misdiagnosis. In addition, health education should be given to those who will go to the endemic areas to improve their knowledge and awareness on prevention and control of schistosomiasis haematobia, thereby reducing the risk of exposure to the infested freshwater.
Among the global parasitic diseases, schistosomiasis ranks second behind malaria in terms of socio-economic and public health importance in tropical and subtropical areas of the world . This neglected tropical disease is estimated to be endemic in 76 countries of the developing world, which affects 300 million people, with a further 779 million at risk of infection . Three major schistosome species are known to infect humans, including Schistosoma haematobium that causes urinary schistosomiasis which occurs in Africa and the eastern Mediterranean, S. mansoni that is endemic in Africa, the eastern Mediterranean, the Caribbean, and South America, and S. japonicum that is endemic mainly in China and the Philippines [3, 4]. China is only endemic for S. japonicum. However, the increasing globalization of the world economy and population migration makes the introduction of S. haematobium and S. mansoni infection possible into the non-endemic areas . Currently, an estimated 10 million Chinese people are working in African countries each year, and they usually stay there for several years . These workers usually lack knowledge and awareness on prevention and control of schistosomiasis haematobia, resulting in the possibility of exposure to S. haematobium-infested freshwater in endemic regions. In addition, these migrant workers are often misdiagnosed if they are infected in Africa and have clinical symptoms after returning to their original residence in China, due to scarce knowledge and awareness of schistosomiasis haematobia prevention and control . In this study, we reported a case with S. haematobium infection that was misdiagnosed as ureteral calculus, invasive urothelial carcinoma and eosinophilic cystitis in several hospitals. This study was approved by Jiangsu Institute of Parasitic Diseases and Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health. An informed consent was obtained from the patient, following a detailed description of the potential benefits of the study.
A 36-year-old man from Qianxian County of Shaanxi Province, China worked in Luanda, Angola during the period from July 2007 to March 2011, due to export of labor services. Before moving to Angola, his living and working areas were limited in Shaanxi Province where schistosomiasis japonica is not endemic. The man returned to Shaanxi Province between July and September, 2009. During the stay in Africa, he was frequently in contact with local rivers due to the need of living and production.
S. haematobium, the etiologic agent of urogenital schistosomiasis, is the most prevalent anthropophilic schistosome species globally, which accounts for nearly half of the number of cases with schistosomiasis primarily in sub-Saharan Africa and the Middle East . Although the symptoms are varied, the bulk of the morbidity and mortality of urogenital schistosomiasis can be ultimately attributed to the host immune response against Schistosoma eggs deposited within the walls of the urinary tract. This inflammation leads to compromise of urothelial integrity promoting urinary tract infections, hematuria, and protein-wasting; urothelial changes leading to carcinogenesis; and urinary tract fibrosis causing bladder dysfunction, obstruction, infection, and renal failure . In addition, female genital schistosomiasis has been identified as a co-factor in Africa's AIDS epidemic, especially in Zimbabwe and Tanzania, where it was linked to a 3–4 times increased risk in acquiring HIV infection .
Currently, the gold standard for diagnosis of schistosomiasis haematobia still relies on the microscopic detection of parasite eggs present in urine specimens ; however, parasitological diagnosis in adults is difficult, particularly among persons who have chronic infections and pass only small numbers of eggs. Many immunodiagnostics and DNA-based diagnostics have been developed [15–20], which facilitate the detection of this neglected tropical disease. In the current study, three immunodiagnostic assays for the detection of antibodies against S. japonicum, including DDIA, IHA and COPT, were employed to detect S. haematobium infection, and the detection results coincided with the microscopic examination. It has been shown that DDIA using S. japonicum soluble egg antigen (SEA) can be used for the diagnosis of schistosomiasis mansoni and schistosomiasis mekongi [21, 22]. Taken together, it seems that the currently available immunodiagnostics directed against S. japonicum antibody seem effective for the detection of S. haematobium infection. However, further studies are required to validate the performance of these immunodiagnostic assays in detection of schistosomiasis haematobia. In addition, in the absence of diagnostics for imported African schistosomiasis in China, a search for novel immunodiagnostics or molecular assays is urgently needed and should be given a high priority [23, 24].
S. haematobium infection has been linked to bladder tumors, and the infection is reported to be responsible for the development of carcinoma of the urinary bladder [25–28]. In the current study, the imported case infected with S. haematobium was misdiagnosed as invasive urothelial carcinoma. The patient has not developed bladder tumors to date. Given that S. haematobium infection is identified as a factor in the pathogenesis of carcinoma of the urinary bladder , periodic health examination is suggested to detect bladder tumors at an early stage.
Features of imported cases with schistosomiasis haematobia
Most infections occur in young adults who are exported to African countries for labor services.
Potential underestimation of actual number of cases. Most of the infections are detected at physical examinations, and few patients seek medical care; therefore, the actual number of patients with S. haematobium infections may be underestimated.
High proportion of misdiagnosis. The major clinical manifestations of schistosomiasis haematobia involve hematuresis, bladder irritation, and urinary tract obstruction, which are often misdiagnosed as sexually transmitted diseases, cystitis, tuberculosis and tumors due to the lack of knowledge on diagnosis of the disease in Chinese clinicians.
The cases are widely distributed in China, and have a high mobility .
Problems currently present in the control of imported schistosomiasis haematobia
Lack of sound multi-sector collaborations.
No national criteria for the diagnosis and treatment of imported schistosomiasis haematobia.
Lack of diagnostics for the detection of imported cases with S. haematobium infection.
The exporting laborers have little knowledge on prevention and control of S. haematobium infections, and they lack active pursuit of medical care even if infected.
Medical professionals lack awareness, diagnosis and treatment experiences as well as techniques regarding S. haematobium infection.
Countermeasures to improve the management of imported schistosomiasis haematobia in China
Strengthening multi-sector collaborations and the detection at the entry-exit inspection and quarantine sections, and involvement of schistosomiasis diagnosis in the routine physical examinations for worker returning from Africa.
Development of national criteria for the diagnosis and treatment of imported schistosomiasis haematobia.
Assessing the performance of immunodiagnostics directed against S. japonicum antibodies in detection of S. haematobium infection, and development of novel immunodiagnostics or molecular assays for the detection of S. haematobium infection.
A systematic survey of the labor export to the schistosomiasis haematobia-endemic areas, and an evaluation of the true infections.
Strengthening the training on knowledge about schistosomiasis haematobia among medical professionals, including diagnosis and treatment.
Improving the access to health education pertaining to schistosomiasis status, prevention and control as well as international travel healthcare among those moving to Africa due to work, business or travel, so as to enhance their self-protection awareness and active pursuit of medical care if infected.
As S. haematobium is not indigenous to China, most Chinese doctors and medical technicians are unfamiliar with this introduced parasitic disease, therefore, they need to increase the awareness of its existence when they encounter persons who have visited or resided in endemic areas, and the techniques for detection of the parasite, so as to reduce missing diagnosis and misdiagnosis. In addition, health education should be performed among those who will go to the endemic areas to improve their knowledge and awareness on prevention and control of schistosomiasis haematobia, thereby reducing the risk of exposure to the infested freshwater. It is considered that the management of imported schistosomiasis haematobia should be improved in China based on the lessons from this case undergoing multiple misdiagnoses.
This work was supported by the National Important Sci-Tech Special Projects (2012ZX10004-220), National Science and Technology Pillar Program of China (2009BAI78B06), Jiangsu Department of Health (X200901 and X201103), and the Jiangsu Provincial Government Overseas Scholarship. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
- Gryseels B, Polman K, Clerinx J, Kestens L: Human schistosomiasis. Lancet. 2006, 368: 1106-1118. 10.1016/S0140-6736(06)69440-3.View ArticlePubMedGoogle Scholar
- Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J: Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006, 6: 411-425. 10.1016/S1473-3099(06)70521-7.View ArticlePubMedGoogle Scholar
- Bergquist R, Tanner M: Controlling schistosomiasis in Southeast Asia: a tale of two countries. Adv Parasitol. 2010, 72: 109-144.View ArticlePubMedGoogle Scholar
- Zhou XN, Bergquist R, Leonardo L, Yang GJ, Yang K, Sudomo M, Olveda R: Schistosomiasis japonica control and research needs. Adv Parasitol. 2010, 72: 145-178.View ArticlePubMedGoogle Scholar
- Lim PL: Schistosoma haematobium in China, ex-Africa: new populations at risk?. J Travel Med. 2013, 20: 211-213. 10.1111/jtm.12031.View ArticlePubMedGoogle Scholar
- Yin H: Development of export of labor services in China since reform and opening. Population J. 2009, 11: 27-28. (in Chinese)Google Scholar
- Wang ZQ, Wang Y, Jia LJ, Cui J: Schistosoma haematobium infection in workers returning from Africa to China. J Travel Med. 2013, 20: 256-258. 10.1111/jtm.12032.View ArticlePubMedGoogle Scholar
- Zhu Y, He W, Liang Y, Xu M, Yu C, Hua W, Chao G: Development of a rapid, simple dipstick dye immunoassay for schistosomiasis diagnosis. J Immunol Methods. 2002, 266: 1-5. 10.1016/S0022-1759(02)00086-8.View ArticlePubMedGoogle Scholar
- Yu JM, de Vlas SJ, Jiang QW, Gryseels B: Comparison of the Kato-Katz technique, hatching test and indirect hemagglutination assay (IHA) for the diagnosis of Schistosoma japonicum infection in China. Parasitol Int. 2007, 56: 45-49. 10.1016/j.parint.2006.11.002.View ArticlePubMedGoogle Scholar
- Lewert RM, Yogore MG: A field circumoval precipitin (FCOP) test for schistosomiasis japonica. Trans R Soc Trop Med Hyg. 1969, 63: 343-348. 10.1016/0035-9203(69)90008-X.View ArticlePubMedGoogle Scholar
- Hotez PJ, Kamath A: Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution and disease burden. PLoS Negl Trop Dis. 2009, 3: e412-10.1371/journal.pntd.0000412.PubMed CentralView ArticlePubMedGoogle Scholar
- Brindley PJ, Hotez PJ: Break out: Urogenital schistosomiasis and Schistosoma haematobium infection in the post-genomic era. PLoS Negl Trop Dis. 2013, 7: e1961-10.1371/journal.pntd.0001961.PubMed CentralView ArticlePubMedGoogle Scholar
- Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA: Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis. 2011, 5: e1396-10.1371/journal.pntd.0001396.PubMed CentralView ArticlePubMedGoogle Scholar
- Bergquist NR: Present aspects of immunodiagnosis of schistosomiasis. Mem Inst Oswaldo Cruz. 1992, 87: 29-38.View ArticlePubMedGoogle Scholar
- Sheele JM, Kihara JH, Baddorf S, Byrne J, Ravi B: Evaluation of a novel rapid diagnostic test for Schistosoma haematobium based on the detection of human immunoglobulins bound to filtered Schistosoma haematobium eggs. Trop Med Int Health. 2013, 18: 477-484. 10.1111/tmi.12063.View ArticlePubMedGoogle Scholar
- Coulibaly JT, N'Goran EK, Utzinger J, Doenhoff MJ, Dawson EM: A new rapid diagnostic test for detection of anti-Schistosoma mansoni and anti-Schistosoma haematobium antibodies. Parasit Vectors. 2013, 6: 29-10.1186/1756-3305-6-29.PubMed CentralView ArticlePubMedGoogle Scholar
- Obeng BB, Aryeetey YA, de Dood CJ, Amoah AS, Larbi IA, Deelder AM, Yazdanbakhsh M, Hartgers FC, Boakye DA, Verweij JJ, Van Dam GJ, Van Lieshout L: Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol. 2008, 102: 625-633. 10.1179/136485908X337490.View ArticlePubMedGoogle Scholar
- Kinkel HF, Dittrich S, Bäumer B, Weitzel T: Evaluation of eight serological tests for diagnosis of imported schistosomiasis. Clin Vaccine Immunol. 2012, 19: 948-953. 10.1128/CVI.05680-11.PubMed CentralView ArticlePubMedGoogle Scholar
- Kjetland EF, Hove RJ, Gomo E, Midzi N, Gwanzura L, Mason P, Friis H, Verweij JJ, Gundersen SG, Ndhlovu PD, Mduluza T, Van Lieshout L: Schistosomiasis PCR in vaginal lavage as an indicator of genital Schistosoma haematobium infection in rural Zimbabwean women. Am J Trop Med Hyg. 2009, 81: 1050-1055. 10.4269/ajtmh.2009.09-0081.View ArticlePubMedGoogle Scholar
- Aryeetey YA, Essien-Baidoo S, Larbi IA, Ahmed K, Amoah AS, Obeng BB, van Lieshout L, Yazdanbakhsh M, Boakye DA, Verweij JJ: Molecular diagnosis of Schistosoma infections in urine samples of school children in Ghana. Am J Trop Med Hyg. 2013, 88: 1028-1031. 10.4269/ajtmh.12-0571.PubMed CentralView ArticlePubMedGoogle Scholar
- Zhu YC, Hassen S, He W, Cao GQ: Preliminary study on detection of schistosomiasis mansoni with dipstick dye immunoassay (DDIA) kit. Chin J Schisto Control. 2006, 18: 419-421. (in Chinese)Google Scholar
- Zhu YC, Socheat D, Bounlu K, Liang YS, Sinuon M, Insisiengmay S, He W, Xu M, Shi WZ, Bergquist R: Application of dipstick dye immunoassay (DDIA) kit for the diagnosis of schistosomiasis mekongi. Acta Trop. 2005, 96: 137-141. 10.1016/j.actatropica.2005.07.008.View ArticlePubMedGoogle Scholar
- Bergquist R: Good things are worth waiting for. Am J Trop Med Hyg. 2013, 88: 409-410. 10.4269/ajtmh.12-0741.PubMed CentralView ArticlePubMedGoogle Scholar
- Zheng Q, Vanderslott S, Jiang B, Xu LL, Liu CS, Huo LL, Duan LP, Wu NB, Li SZ, Xia ZG, Wu WP, Hu W, Zhang HB: Research gaps for three main tropical diseases in the People's Republic of China. Infect Dis Poverty. 2013, 2: 15-10.1186/2049-9957-2-15.PubMed CentralView ArticlePubMedGoogle Scholar
- Gelfand M, Weinberg RW, Castle WM: Relation between carcinoma of the bladder and infestation with Schistosoma haematobium. Lancet. 1967, 1: 1249-1251.View ArticlePubMedGoogle Scholar
- Thomas JE, Bassett MT, Sigola LB, Taylor P: Relationship between bladder cancer incidence, Schistosoma haematobium infection, and geographical region in Zimbabwe. Trans R Soc Trop Med Hyg. 1990, 84: 551-553. 10.1016/0035-9203(90)90036-E.View ArticlePubMedGoogle Scholar
- Bedwani R, Renganathan E, El Kwhsky F, Braga C, Abu Seif HH, Abul Azm T, Zaki A, Franceschi S, Boffetta P, La Vecchia C: Schistosomiasis and the risk of bladder cancer in Alexandria, Egypt. Br J Cancer. 1998, 77: 1186-1189. 10.1038/bjc.1998.197.PubMed CentralView ArticlePubMedGoogle Scholar
- Janković S, Radosavljević V: Risk factors for bladder cancer. Tumori. 2007, 93: 4-12.PubMedGoogle Scholar
- Shiff C, Veltri R, Naples J, Quartey J, Otchere J, Anyan W, Marlow C, Wiredu E, Adjei A, Brakohiapa E, Bosompem K: Ultrasound verification of bladder damage is associated with known biomarkers of bladder cancer in adults chronically infected with Schistosoma haematobium in Ghana. Trans Roy Soc Trop Med Hyg. 2006, 100: 847-854. 10.1016/j.trstmh.2005.10.010.View ArticlePubMedGoogle Scholar
- Gao ST, Li XH, Huang SY, Xie X, Mei SJ, Ruan CW, Huang DN: Primary investigation of distribution and ecological environment of Biomphalaria straminea in Dasha and Guanlan Rivers in Shenzhen areas. Chin Trop Med. 2013, 13: 313-317. (in Chinese)Google Scholar
- Mas-Coma S, Valero MA, Bargues MD: Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol. 2009, 163: 264-280. 10.1016/j.vetpar.2009.03.024.View ArticlePubMedGoogle Scholar
- Wang W, Liang YS, Hong QB, Dai JR: African schistosomiasis in mainland China: risk of transmission and countermeasures to tackle the risk. Parasit Vectors. 2013, 6: 249-10.1186/1756-3305-6-249.PubMed CentralView ArticlePubMedGoogle Scholar
- Yi P, Yuan LP, Wang ZH, He YK, Jing QS, Zhou J, Wang HB, Li SM: Retrospective survey of 184 patients infected with Schistosoma haematobium from African countries. Chin J Schisto Control. 2011, 23: 441-442. (in Chinese)Google Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.