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DOI: 10.1055/s-0037-1601452
Ovarian Manson's Schistosomiasis: Rare Diagnosis or Underestimated Prevalence?
Esquistossomose mansônica no ovário: diagnóstico raro ou prevalência subestimada?Address for correspondence
Publication History
19 December 2016
06 February 2017
Publication Date:
31 March 2017 (online)
Abstract
The occurrence of Manson's schistosomiasis in organs of the female reproductive tract is an uncommon event, given that the etiological agent for this disease is a blood parasite that inhabits the mesenteric veins. In this case report, a 45-year-old female patient reported that her first symptoms had been strong pain in the left iliac region around two years earlier. An endovaginal pelvic ultrasonography showed that the left ovary was enlarged, and the report suggested that this finding might be correlated with clinical data and tumor markers. After being examined at several healthcare services, the patient was referred to an oncology service due to suspected neoplasia, where she underwent a left ovariectomy. The result from the histopathological examination showed the presence of granulomatous inflammatory processes surrounding both viable and calcified eggs of Schistosoma mansoni. There was no evidence of any neoplastic tissue. The patient was medicated and followed-up as an outpatient.
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Resumo
A ocorrência da esquistossomose mansônica em órgãos do aparelho reprodutor feminino é um evento pouco comum, tendo em vista que o agente etiológico desta doença é um parasito sanguíneo que habita as veias mesentéricas. Neste relato de caso, uma paciente de 45 anos referiu como primeira sintomatologia fortes dores na região ilíaca esquerda há cerca de 2 anos. Uma ultrassonografia pélvica endovaginal identificou aumento do ovário esquerdo, e o laudo sugeriu correlacionar tal achado com dados clínicos e marcadores tumorais. Após passar por vários serviços de saúde, a paciente foi encaminhada para um serviço de oncologia por suspeita de neoplasia, sendo submetida a uma ovariectomia à esquerda. O resultado do exame histopatológico evidenciou a presença de processos inflamatórios granulomatosos em torno de ovos viáveis e calcificados de Schistosoma mansoni. Não houve qualquer evidência de tecido neoplásico. A paciente foi medicada, e seguiu em acompanhamento ambulatorial.
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Keywords
ectopic schistosomiasis - ovarian schistosomiasis - schistosoma mansoni - granuloma - neoplasiaPalavras-chave
esquistossomose ectópica - esquistossomose de ovário - schistosoma mansoni - granuloma - neoplasiaIntroduction
In Brazil, schistosomiasis continues to be a neglected disease. Despite the healthcare services' efforts to control and reduce its prevalence, it has persisted over the years, and continues to affect thousands of people who live in endemic areas.[1] [2] In these areas, new epidemiological scenarios have emerged to challenge the healthcare services' strategies for diagnosing and controlling this disease.[3] [4] Reports in the literature have drawn attention to the growing number of cases of ectopic forms of schistosomiasis.[5] [6] [7] [8] Prominent among these is one of the severest presentations of this parasitosis: schistosomal myeloradiculopathy, caused by the formation of granulomas in the central nervous system that induce incapacitating lesions in the lower limbs of the individuals affected.[6] [9] [10]
In cases of infection by Schistosoma haematobium, which affects the reproductive and urinary systems of both men and women, findings of granulomas in these tissues are common.[11] [12] [13] [14] However, there are few records regarding Schistosoma mansoni, and the infections caused by this parasite are considered to be ectopic presentations of the disease, given that the habitat of this species is the mesenteric veins that irrigate the digestive tract.[15] [16]
Over the last two decades, there have been several reports from around the world of cases of Manson's schistosomiasis associated with the female reproductive system.[17] [18] Brazil is prominent in this regard, with more than ten scientific papers presenting cases affecting these organs, which include the ovaries, the uterine tubes and the endocervix.[7] [19] [20] Some authors have drawn attention to the underreporting of the ectopic forms of the disease, which would be directly associated with the difficulty in diagnosing them and with the lack of proper investigation for the confirmation of such diagnostic hypotheses.
The aim of this study was to present a case of ovarian schistosomiasis and to raise a discussion on the underreporting of the cases involving the female reproductive system. Written informed consent was obtained from the patient for the publication of this case report and any accompanying images.
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Case Report
A 45-year-old female patient reported that in the middle of 2014 she began to feel a strong pain in her left iliac region. After going to several emergency services, she underwent an endovaginal pelvic ultrasonography (in September 2014), which showed enlargement of the left ovary (image of the cyst: 2.84 cm; total volume of the ovary: 16.82 cm3; normal range: 3.0–9.0 cm3). The report suggested that there might be a correlation between this finding and clinical data and tumor markers. In October 2014, the patient underwent tumor marker tests, which showed that they were within the normal range (cancer antigen [CA] 125: 11.1 IU/mL; CA 19–9: 13.6 IU/mL). However, magnetic resonance imaging showed that the left ovary was enlarged, and that ovarian neoplasia could not be ruled out. The patient underwent new blood tests in the beginning of 2015, to investigate cancer markers (carcinoembryonic antigen: 3.0 ng/mL; CA 125: 8.7 IU/mL), and the results found were also within the normal range.
The patient was then referred to the oncological service of Hospital das Clínicas de Pernambuco, because of suspected neoplasia. A left ovariectomy was performed as surgical treatment to remove the possible tumor tissue. However, the histopathological examination of the material extracted identified ovarian schistosomiasis caused by the presence of granulomatous inflammatory processes surrounding both viable and calcified eggs of S. mansoni. There was no evidence of any neoplastic tissue (in April 2015).
The patient was then referred to the specialized schistosomiasis outpatient service of the same hospital for evaluation, treatment and follow-up, but was only able to get her first consultation with the doctor one year after the surgery (in April 2016). This patient was born in the municipality of Cabo de Santo Agostinho, and was living in the municipality of Jaboatão dos Guararapes, which are both endemic localities for schistosomiasis in Pernambuco. At the time that her history was being taken, she said that she did not have any upper digestive tract hemorrhage or symptoms of pulmonary arterial hypertension. She reported that around ten years earlier, she had habitually been bathing in rivers.
Upon physical examination, the patient was in good general condition. She was eupneic, had normal coloration, and did not present jaundice. Her weight was 52.4 kg, and her height was 1.48 m; therefore, her body mass index (BMI) was normal (23.9). An ultrasound examination of her abdomen did not show any abnormalities of the liver, spleen, portal vein, gallbladder or kidneys. Three parasitological feces examinations were performed using the Kato-Katz method, at the schistosomiasis reference center of Centro de Pesquisas Aggeu Magalhães, Fiocruz, Pernambuco. The examinations revealed a residual S. mansoni infection with the following parasite loads: 60, 192 and 156 eggs per gram of feces respectively.
The results from these examinations and the histopathological material from the left ovary were sent to the clinical pathology service of Hospital das Clínicas. The macroscopic examination showed an irregular elastic yellow-brown tissue formation measuring 5.0 × 4.0 × 2.5 cm. The cut surface was compact and greyish-brown, with a brownish area measuring ∼ 1.5 × 1.2 cm. Under a microscope, the observed surface was coated with simple squamous epithelium. In the cortical region, under the tunica albuginea, there were no ovarian follicles, but a large quantity of corpus albicans. In the medullary region, several foci of chronic granulomatous inflammation in the stroma of loose connective tissue that was richly vascularized and innervated were identified ([Fig. 1]).
![](https://www.thieme-connect.de/media/10.1055-s-00030576/201705/thumbnails/10-1055-s-0037-1601452-i5960-1.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
The granulomas presented degenerated eggs of S. mansoni at their centers, surrounded by lymphoplasmacytic and eosinophilic inflammatory infiltrates, occasional multinucleated giant cells and epithelioid macrophages that were organized into palisades. Slight hyperplasia of the fibroblasts and incipient fibroplasia were observed. ([Fig. 2]).
![](https://www.thieme-connect.de/media/10.1055-s-00030576/201705/thumbnails/10-1055-s-0037-1601452-i5960-2.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Treatment consisting of praziquantel 50 mg/kg (600 mg/tablet; 4.5 tablets) was administered. Because the disease was in one of its ectopic forms, a two additional treatments with the same dose, at two-month intervals, were performed. The patient was followed-up as an outpatient.
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Discussion
The histopathological findings from this case, consisting of the presence of schistosomal granulomas surrounding eggs of S. mansoni, along with the formation of inflammatory infiltrate and the presence of multinucleated giant cells, are expected in cases of chronic S. mansoni infection.[8] [21] [22] These findings have already been described in many other cases of ovarian schistosomiasis.[20] [23] [24] [25] This is an immune-cellular response to the presence of a foreign body in the tissue stroma. Schistosomal granulomas can be characterized as compact and organized collections of migrant cells that, together with cells of the affected organ, become arranged as components of a heterogeneous extracellular matrix that forms a spherical structure surrounding each egg individually.[22] Schistosomal granulomas are the best example in the literature of granulomatous reactions caused by extracellular agents.[26]
According to the data in the literature, the ovaries are the most affected organ in cases of female genital schistosomiasis, followed by the cervix, the fallopian tubes, the uterus and the vulvae.[11] [27] [28] This is due to the migration of the adult parasites through a complex vascular network. Initially, the parasites leave the portal vein and migrate against the venous flow until reaching the anorectal plexus. After overcoming this obstacle, the worms have easy access to the perivesicular and uterovaginal plexuses via the rectovaginal septum or through vascular networks between the bladder and the reproductive organs. In this manner, these parasites can migrate to any genital organ,[11] [29] thus causing the characteristic tissue lesions and a variety of signs and symptoms.
In the present case report, the symptoms presented by the patient were in line with what has been described in the scientific literature. Pain in the pelvic region has, by far, been the symptom most frequently mentioned, followed by bleeding, discharges, changes to the menstrual cycle and pain and bleeding during coitus.[17]
Although ovarian schistosomiasis is not a common clinical finding for infections caused by S. mansoni, several cases have been described in the Brazilian literature.[20] [23] [24] [25] [30] However, it is noteworthy that in most of these cases, neoplasia was not a diagnostic hypothesis at any moment of the clinical investigation.[20] [23] [24] [25] [30] In most cases of ectopic forms of Manson's schistosomiasis, a single parasitological examination may have the capacity to prove the presence of parasitosis and open the way to better directed history-taking and investigation, thus enabling faster diagnoses with less harm to the patients' health.
We should emphasize that the time spent on reaching a precise diagnosis and the therapeutic path followed by the patient until the diagnosis was obtained and the adequate treatment was instituted are unacceptable, given the simplicity of the parasitological diagnosis for this parasitosis. In fact, in most cases, the diagnosis was only made after an exploratory surgical intervention, by means of a histopathological examination of the material extracted.[17] [19] [20] [24] [25] [28] [31] Furthermore, some patients were discharged without the adequate treatment of the parasitosis,[8] and had to seek specialized hospital outpatient services to obtain a simple drug treatment consisting of the administration of praziquantel in a single or fractioned dose.[32] It is important to mention that the use of three doses of praziquantel to treat ectopic forms of the disease is a clinical practice among specialists to ensure parasitological cure. This is done firstly because the cure rate with only one dose is around 75%;[30] and secondly, in the ectopic forms of the disease, the worm eggs are encysted (encapsulated by granulomas), thus hindering drug access.
A certain degree of neglect on the part of healthcare services in Brazil regarding proper treatment and referral for individuals diagnosed with ectopic forms of schistosomiasis has been observed.[8] This goes against the guiding principle of the Brazilian National Health System, which is that healthcare actions should be comprehensive, aiming to meet all of the individuals' needs, going from health promotion to health recovery.[33] Thus, we can presume that many ectopic cases of this disease are underreported. Accidental diagnoses that are reached through investigating other diagnostic hypotheses are less likely to be recorded in the healthcare information systems.
The Brazilian Ministry of Health currently categorizes schistosomiasis as a disease that is “on the way to eradication.” Nevertheless, it persists as a neglected disease because of the lack of knowledge and regard among healthcare professionals and services, which is reflected in maintenance of the prevalence and incidence rates for this disease.
Although uncommon, occurrences of cases of Manson's schistosomiasis associated with the female reproductive system are a reality that needs to be taken into consideration, given the existence of patients coming from endemic areas. According to the data in the literature, between 6 and 27% of women with intestinal schistosomiasis temporarily suffer from pathological conditions induced by the accidental presence of eggs of this parasite in their genital organs.[11] A study in an endemic area for schistosomiasis that used biopsies and cervical smears did not identify any cases, but the authors raised the hypothesis that these results might have been related to the low parasite load of the population of their study.[34]
The data in the literature on occurrences and cases of schistosomiasis associated with the female reproductive tract are divergent. However, a recent bibliographic review on this topic drew attention to the lack of population-based studies in areas that are endemic for Manson's schistosomiasis, taking into account the reports from Brazil regarding the ectopic form of the disease in the female reproductive tract.[18]
Taking into consideration the current estimate of four to six million individuals in Brazil infected by S. mansoni,[2] we hope that healthcare professionals and services will direct their attention to the present study, especially the professionals who act directly in the specialty of obstetrics and gynecology, so that cases like the one described here do not go unnoticed. We should emphasize that reporting these cases is essential in order to gain greater comprehension of the pathophysiology of this ectopic form of the disease.
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Conflicts of Interest
The authors have no conflicts of interest to declare.
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References
- 1 Favre TC, Pieri OS, Barbosa CS, Beck L. Evaluation of control measures implemented from 1977 to 1996 in the endemic area of schistosomiasis in Pernambuco, Brazil. Rev Soc Bras Med Trop 2001; 34 (06) 569-576
- 2 Brazil. Ministry of Health. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a ed. Brasília (DF): Ministério da Saúde; 2014
- 3 de Souza Gomes EC, Leal-Neto OB, Albuquerque J, Pereira da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco--Brazil. Int J Health Geogr 2012; 11: 51
- 4 Barreto MS, Gomes ECS, Barbosa CS. High-risk tourism in areas vulnerable to schistosomiasis mansoni transmission in Brazil. Cad Saude Publica 2016; 32 (03) e00190815
- 5 Raso P, Alves CF, Tafuri A, Tafuri WL. Ectopic cutaneous Schistosomiasis mansoni in the sacral region. Case Rep Dermatol 2010; 2 (01) 1-7
- 6 Araújo KC, Silva CdaR, Santos AGA, Barbosa CS, Ferrari TCA. Clinical-epidemiologic profile of the schistosomal myeloradiculopathy in Pernambuco, Brazil. Mem Inst Oswaldo Cruz 2010; 105 (04) 454-459
- 7 Delmondes LM, Cruz MAF, Guimarães MKH, Santana LG, Gonçalves VPC, Brito HLF. [Endocervical schistosomiasis: case report]. Rev Bras Ginecol Obstet 2014; 36 (06) 276-280
- 8 Gomes ECS, Domingues ALC, Aguiar Junior FCA. , et al. First record of prostatic schistosomiasis in Pernambuco, Brazil: expression of chronicity of an endemic disease. Rev Patol Trop 2016; 45 (01) 132-138
- 9 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Guia de vigilância epidemiológica e controle da mielorradiculopatia esquistossomótica. Brasília (DF): Ministério da Saúde; 2006. Disponível em: http://bvsms.saude.gov.br/ bvs/publicacoes/07_0061_M.pdf
- 10 Ferrari TCA, Drummond S, Reis MG. Neuroesquistossomose. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 807-20
- 11 Feldmeier H, Daccal RC, Martins MJ, Soares V, Martins R. Genital manifestations of schistosomiasis mansoni in women: important but neglected. Mem Inst Oswaldo Cruz 1998; 93 (Suppl. 01) 127-133
- 12 Schwartz E, Pick N, Shazberg G, Potasman I. Hematospermia due to schistosome infection in travelers: diagnostic and treatment challenges. Clin Infect Dis 2002; 35 (11) 1420-1424
- 13 Mazigo HD, Zinga M, Heukelbach J, Rambau P. Case series of adenocarcinoma of the prostate associated with Schistosoma haematobium infection in Tanzania. J Glob Infect Dis 2010; 2 (03) 307-309
- 14 Rambau PF, Chandika A, Chalya PL, Jackson K. Scrotal swelling and testicular atrophy due to schistosomiasis in a 9-year-old boy: a case report. Case Rep Infect Dis 2011; 2011: 787961
- 15 Neves DP. Parasitologia humana. 13a ed. São Paulo: Atheneu; 2016
- 16 Lenzi HL, Jurberg AD, Coelho PMZ, Lenzi JA. Migração e desenvolvimento de schistosoma mansoni no hospedeiro definitivo. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 85-145
- 17 Boers KE, Sastrowijoto PH, Elzakker van EP, Hermans MPM. Schistosomiasis of the uterus in a patient with dysmenorrhoea and menorrhagia. Eur J Obstet Gynecol Reprod Biol 2003; 108 (01) 106-108
- 18 Christinet V, Lazdins-Helds JK, Stothard JR, Reinhard-Rupp J. Female genital schistosomiasis (FGS): from case reports to a call for concerted action against this neglected gynaecological disease. Int J Parasitol 2016; 46 (07) 395-404
- 19 Faria CA, Conceição JCJ, Valadares TF, Rodrigues B, Carneiro L. Schistosoma mansoni: a rare cause of tubal infection. Braz J Infect Dis 2010; 14 (03) 288-290
- 20 Amorim AG, Pagio FAB, Ferreira RN, Chambô Filho A. Genital schistosomiasis: a report on two cases of ovarian carcinomas containing viable egg of schistosoma mansoni. Case Rep Obstet Gynecol 2014; 2014: 508-718
- 21 Andrade ZA. A patologia da esquistossomose humana. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 547-568
- 22 Lenzi HL, Romanha WS, Machado MP, Mota EM, Lenzi JA. Patologia experimental com enfoque no granuloma esquistossomótico. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 569-654
- 23 Poderoso WLS, Santana WB, Costa EF, Cipolotti R, Fakhouri R. Ectopic schistosomiasis: description of five cases involving skin, one ovarian case and one adrenal case. Rev Soc Bras Med Trop 2008; 41 (06) 668-671
- 24 Batista TP, de Andrade JJ, Filho LA. Schistosoma mansoni: an unusual cause of ovarian pseudotumor. Arch Gynecol Obstet 2010; 281 (01) 141-143
- 25 Cavalcanti MG, Gonçalves MMI, Barreto MM. , et al. Genital schistosomiasis mansoni concomitant to genital tumor in areas of low endemicity: challenging diagnosis. Braz J Infect Dis 2011; 15 (02) 174-177
- 26 Lenzi HL, Lenzi JA, Kerr IB, Antunes SLG, Mota EM, Oliveira DN. Extracellular matrix in parasitic and infectious diseases. Mem Inst Oswaldo Cruz 1991; 86 (Suppl. 03) 77-90
- 27 Lambertucci JR, Voieta I, De Brot M. Vulvar schistosomiasis mansoni. Rev Soc Bras Med Trop 2008; 41 (04) 435-436
- 28 Lambertucci JR, Villamil QTMF, Savi D, Dias IC. Genital schistosomiasis mansoni: tubal tumor and parietal peritoneum involvement diagnosed during laparoscopy. Rev Soc Bras Med Trop 2009; 42 (05) 583-586
- 29 Poggensee G, Feldmeier H. Female genital schistosomiasis: facts and hypotheses. Acta Trop 2001; 79 (03) 193-210
- 30 Zwang J, Olliaro PL. Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistosomiasis-a meta-analysis of comparative and non-comparative clinical trials. PLoS Negl Trop Dis 2014; 8 (11) e3286
- 31 Chambô Filho A, Neves RF, Gusmão CB, Saade FTP, Dalvi IR, Leo TR. Genital schistosomiasis: mucinous cystadenocarcinoma of the ovary containing schistosoma mansoni eggs. J Trop Med Parasitol 2010; 33 (01) 36-40
- 32 Rey L. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na África. 3a ed. Rio de Janeiro: Guanabara Koogan; 2001
- 33 Brasil. Lei n. 8.080 de 19 de setembro de 1990 [Internet]. Dispõe sobre as condições para a promoção, proteção e recuperação da saúde, a organização e o funcionamento dos serviços correspondentes e dá outras providências. 1990 [citado 2006 Set 05]. Disponível em: https://www.planalto.gov.br/ccivil_03/LEIS/L8080.htm
- 34 Oliveira FAS, Soares VL, Dacal ARC. , et al. Absence of cervical schistosomiasis among women from two areas of north-eastern Brazil with endemic Schistosoma mansoni. Ann Trop Med Parasitol 2006; 100 (01) 49-54
Address for correspondence
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References
- 1 Favre TC, Pieri OS, Barbosa CS, Beck L. Evaluation of control measures implemented from 1977 to 1996 in the endemic area of schistosomiasis in Pernambuco, Brazil. Rev Soc Bras Med Trop 2001; 34 (06) 569-576
- 2 Brazil. Ministry of Health. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a ed. Brasília (DF): Ministério da Saúde; 2014
- 3 de Souza Gomes EC, Leal-Neto OB, Albuquerque J, Pereira da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco--Brazil. Int J Health Geogr 2012; 11: 51
- 4 Barreto MS, Gomes ECS, Barbosa CS. High-risk tourism in areas vulnerable to schistosomiasis mansoni transmission in Brazil. Cad Saude Publica 2016; 32 (03) e00190815
- 5 Raso P, Alves CF, Tafuri A, Tafuri WL. Ectopic cutaneous Schistosomiasis mansoni in the sacral region. Case Rep Dermatol 2010; 2 (01) 1-7
- 6 Araújo KC, Silva CdaR, Santos AGA, Barbosa CS, Ferrari TCA. Clinical-epidemiologic profile of the schistosomal myeloradiculopathy in Pernambuco, Brazil. Mem Inst Oswaldo Cruz 2010; 105 (04) 454-459
- 7 Delmondes LM, Cruz MAF, Guimarães MKH, Santana LG, Gonçalves VPC, Brito HLF. [Endocervical schistosomiasis: case report]. Rev Bras Ginecol Obstet 2014; 36 (06) 276-280
- 8 Gomes ECS, Domingues ALC, Aguiar Junior FCA. , et al. First record of prostatic schistosomiasis in Pernambuco, Brazil: expression of chronicity of an endemic disease. Rev Patol Trop 2016; 45 (01) 132-138
- 9 Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Guia de vigilância epidemiológica e controle da mielorradiculopatia esquistossomótica. Brasília (DF): Ministério da Saúde; 2006. Disponível em: http://bvsms.saude.gov.br/ bvs/publicacoes/07_0061_M.pdf
- 10 Ferrari TCA, Drummond S, Reis MG. Neuroesquistossomose. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 807-20
- 11 Feldmeier H, Daccal RC, Martins MJ, Soares V, Martins R. Genital manifestations of schistosomiasis mansoni in women: important but neglected. Mem Inst Oswaldo Cruz 1998; 93 (Suppl. 01) 127-133
- 12 Schwartz E, Pick N, Shazberg G, Potasman I. Hematospermia due to schistosome infection in travelers: diagnostic and treatment challenges. Clin Infect Dis 2002; 35 (11) 1420-1424
- 13 Mazigo HD, Zinga M, Heukelbach J, Rambau P. Case series of adenocarcinoma of the prostate associated with Schistosoma haematobium infection in Tanzania. J Glob Infect Dis 2010; 2 (03) 307-309
- 14 Rambau PF, Chandika A, Chalya PL, Jackson K. Scrotal swelling and testicular atrophy due to schistosomiasis in a 9-year-old boy: a case report. Case Rep Infect Dis 2011; 2011: 787961
- 15 Neves DP. Parasitologia humana. 13a ed. São Paulo: Atheneu; 2016
- 16 Lenzi HL, Jurberg AD, Coelho PMZ, Lenzi JA. Migração e desenvolvimento de schistosoma mansoni no hospedeiro definitivo. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 85-145
- 17 Boers KE, Sastrowijoto PH, Elzakker van EP, Hermans MPM. Schistosomiasis of the uterus in a patient with dysmenorrhoea and menorrhagia. Eur J Obstet Gynecol Reprod Biol 2003; 108 (01) 106-108
- 18 Christinet V, Lazdins-Helds JK, Stothard JR, Reinhard-Rupp J. Female genital schistosomiasis (FGS): from case reports to a call for concerted action against this neglected gynaecological disease. Int J Parasitol 2016; 46 (07) 395-404
- 19 Faria CA, Conceição JCJ, Valadares TF, Rodrigues B, Carneiro L. Schistosoma mansoni: a rare cause of tubal infection. Braz J Infect Dis 2010; 14 (03) 288-290
- 20 Amorim AG, Pagio FAB, Ferreira RN, Chambô Filho A. Genital schistosomiasis: a report on two cases of ovarian carcinomas containing viable egg of schistosoma mansoni. Case Rep Obstet Gynecol 2014; 2014: 508-718
- 21 Andrade ZA. A patologia da esquistossomose humana. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 547-568
- 22 Lenzi HL, Romanha WS, Machado MP, Mota EM, Lenzi JA. Patologia experimental com enfoque no granuloma esquistossomótico. Carvalho OS, Coelho PMZ, Lenzi HL. , organizadores. Schistosoma mansoni & esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008: 569-654
- 23 Poderoso WLS, Santana WB, Costa EF, Cipolotti R, Fakhouri R. Ectopic schistosomiasis: description of five cases involving skin, one ovarian case and one adrenal case. Rev Soc Bras Med Trop 2008; 41 (06) 668-671
- 24 Batista TP, de Andrade JJ, Filho LA. Schistosoma mansoni: an unusual cause of ovarian pseudotumor. Arch Gynecol Obstet 2010; 281 (01) 141-143
- 25 Cavalcanti MG, Gonçalves MMI, Barreto MM. , et al. Genital schistosomiasis mansoni concomitant to genital tumor in areas of low endemicity: challenging diagnosis. Braz J Infect Dis 2011; 15 (02) 174-177
- 26 Lenzi HL, Lenzi JA, Kerr IB, Antunes SLG, Mota EM, Oliveira DN. Extracellular matrix in parasitic and infectious diseases. Mem Inst Oswaldo Cruz 1991; 86 (Suppl. 03) 77-90
- 27 Lambertucci JR, Voieta I, De Brot M. Vulvar schistosomiasis mansoni. Rev Soc Bras Med Trop 2008; 41 (04) 435-436
- 28 Lambertucci JR, Villamil QTMF, Savi D, Dias IC. Genital schistosomiasis mansoni: tubal tumor and parietal peritoneum involvement diagnosed during laparoscopy. Rev Soc Bras Med Trop 2009; 42 (05) 583-586
- 29 Poggensee G, Feldmeier H. Female genital schistosomiasis: facts and hypotheses. Acta Trop 2001; 79 (03) 193-210
- 30 Zwang J, Olliaro PL. Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistosomiasis-a meta-analysis of comparative and non-comparative clinical trials. PLoS Negl Trop Dis 2014; 8 (11) e3286
- 31 Chambô Filho A, Neves RF, Gusmão CB, Saade FTP, Dalvi IR, Leo TR. Genital schistosomiasis: mucinous cystadenocarcinoma of the ovary containing schistosoma mansoni eggs. J Trop Med Parasitol 2010; 33 (01) 36-40
- 32 Rey L. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na África. 3a ed. Rio de Janeiro: Guanabara Koogan; 2001
- 33 Brasil. Lei n. 8.080 de 19 de setembro de 1990 [Internet]. Dispõe sobre as condições para a promoção, proteção e recuperação da saúde, a organização e o funcionamento dos serviços correspondentes e dá outras providências. 1990 [citado 2006 Set 05]. Disponível em: https://www.planalto.gov.br/ccivil_03/LEIS/L8080.htm
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