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Schistosomiasis.

Schistosomiasis is a parasitic infection caused by flatworms (trematodes). It is second only to malaria in public health significance, with over 200 million people infected worldwide, leading to severe consequences in 20 million persons and 100,000 deaths, annually. There are four species that cause intestinal schistosomiasis: Schistosoma mansoni; Schistosoma japonicum, Schistosoma mekongi, and Schistosoma intercalatum. Schistosoma haematobium causes urinary schistosomias, and is endemic in Africa and the Middle East, with the greatest prevalence in poor rural areas. Fibrotic changes in the urinary tract can lead to hydroureter, hydronephrosis, bacterial urinary infections, and ultimately, kidney disease or eventually bladder cancer. A rare lesion can also arise in patients infected with Schistosomiasis haematobium, resulting in squamous and adenosquamous prostate cancers. Imported diseases, such as schistosomiasis, are entering the United States through immigration via illegal aliens, refugees, and travelers. Schistosomiasis is a neglected tropical disease, and its global health impact is grossly underestimated.

Key Words: Schistosoma haematobium, schistosomiasis, schistosome, parasitic disease, trematode infections, Bilharziases, Katyama fever.

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Schistosomiasisis is a parasitic disease caused by blood flukes (trematodes) of the genus Schistosoma. Sometimes referred to as Bilharzias, Bilharziasis, or snail fever, schistosomiasis was discovered by Theodore Bilharz, a German surgeon working in Cairo, who first identified the etiological agent Schistosoma hematobium in 1851 (Ahmed & Cunha, 2010). An estimated 700 million people are at risk of infection in 76 countries (considered endemic) because their agricultural work, domestic chores, and recreational activities expose them to infested water. More than 207 million people are infected with schistosomiasis, with 85% living in Africa (Ahmed & Cunha, 2010). After malaria and intestinal helminthiasis, schistosomiasis is the third most devastating tropical disease in the world. An image of a schistosome is seen in Figure 1.

Urinary schistosomiasis has been endemic in Egypt at least since the time of the ancient pharaohs, as indicated by the presence of calcified ova in the Egyptian mummies (Ragheb, 1956). Schistosoma have been found on hieroglyphics dating back to 1900 B.C. in the Kahun Papyrus depicting hematuria related to this infection (see Figure 2).

Objectives:

1. Explain the pathophysiology of urinary schistosomiasis.

2. Discuss the risk of bladder cancer for individuals with urinary schistosomiasis.

3. Describe treatment options for urinary schistosomiasis.

Epidemiology

Schistosomiasis is an important cause of disease in many parts of the world, most commonly in places with poor sanitation. Today, 120 million people are symptomatic with schistosomiasis, with 20 million having severe clinical disease. In chronic schistosomiasis, many of the infected individuals will be asymptomatic, but an estimated 60% have symptoms, and 10% will have advanced organ damage (McPhee, 2012).

According to McPhee (2012), more than 200,000 deaths per year in sub-Saharan Africa are due to schistosomiasis. The intensity and prevalence of infection then rises with age, peaking between 15 to 20 years. In older adults, no significant change is found in the prevalence of the disease; however, the parasite burden or the intensity decreases. Worldwide, 1 in every 30 individuals has Schistosoma infection. Women washing clothes in infested water are at risk. Forty million women of childbearing age are infected. Approximately 10 million women in Africa have schistosomiasis during pregnancy. In endemic areas, the infection is usually acquired as a child. Poor hygiene and playing in mud and water make children vulnerable to infection. Asymptomatic children will suffer from anemia and growth retardation, and will eventually have abdominal pain, anorexia, and weight lOSS.

In Africa, refugee movements and migration to urban areas are introducing the disease to new locations. It has been estimated that 5% to 10% of an endemic community may be heavily infected, and the remainder has mild-to-moderate infections. The risk of infection is highest among those who live near lakes or rivers. School-age children who live in these areas are often most at risk because they tend to spend time swimming or bathing in water containing infectious cercariae (larvae). Anyone who lives in or travels to areas where schistosomiasis is found and is exposed to contaminated freshwater is at risk (Leder & Weller, 2009).

Pathophysiology of Schistosomiasis

The lifecycle of the flatworms (genus Schistosoma, class trematode) that cause human schistosomiasis involves a sexual stage in the human and an asexual stage in the freshwater snail host. The adult worms are small, 12 mm to 26 mm long and 0.3 mm to 0.6 mm wide, and vary with the different species. Adult worms mate and lay eggs; when the ova reach the fresh water, the larvae are released and penetrate the snail. Within 3 to 5 weeks, they asexually multiply into hundreds of fork-tailed cercariae. The cercariae leave the snail and swim to a human or nonhuman animal, where they penetrate the skin. Eggs can end up in the skin, brain, muscle, adrenal glands, and eyes. As the eggs penetrate the urinary system, they can find their way to the female genital region and form granulomas in the uterus, fallopian tube, and ovaries. Central nervous system (CNS) involvement occurs because of embolization of eggs from the portal mesenteric system to the brain and spinal cord via the paravertebral venous plexus (Ahmed & Cunha, 2010).

Human beings become infected when larval forms of the parasite, released by freshwater snails, penetrate their skin during contact with infested water. Skin penetration of cercariae produces an allergic dermatitis (swimmer's itch) at the site of entry, which is typically at hair follicles, and a pruritic papular rash develops. Following loss of their tail, cercariae are transported through blood or lymphatics to the right side of the heart and lungs. In the body, the cercariae develop into adult schistosomes but do not multiply inside the human body. Once inside, cercariae travel to the heart, to the lungs, and through the systemic circulation to reach the portal veins, where they develop into adult worms. The time between cercariae penetration and the first ova production is 4 to 6 weeks. Humans are estimated to excrete approximately 50% of the eggs in the feces. The rest are trapped in various parts of the body (Ahmed & Cunha, 2010). The pathophysiology of infection correlates with the lifecycle of the parasite.

In the venous blood, adult male and female worms mate, and the female lays eggs 4 to 6 weeks after cercarial penetration. Adult worms live in the blood vessels, where the females release eggs. Some eggs are passed out of the body in the feces or urine to continue the parasite lifecycle (see Figure 3). Others become trapped in body tissues, causing an immune reaction and progressive damage to organs.

The female adult worm lives for approximately 3 to 8 years and lays eggs throughout her life span. Heavy infection can cause symptoms, such as cough and fever, and eosinophilia may be observed.

Schistomiasis and the Risk Of Bladder Cancer

There is a large body of evidence linking urinary tract schistosomiasis to bladder cancer (Trabulsi, 2010). Parasitic infection by the blood fluke Schistosoma haematobium is a condition that has a broad spectrum of urologic manifestations secondary to the parasite's lifecycle. Infection begins with penetration through the skin or mucous membranes where there is a hematogenous migration to the perivesical venous plexus and transmural migration into the bladder with shedding into the urine. On cystoscopic examination, patients will typically have polyps or yellow punctate lesions (active infection), or tancolored/sand-like patches (inactive infection). Significant upper urinary tract obstruction (kidneys and ureters) with hydronephrosis and hydroureter is seen in chronic infections. These chronic infections are linked to bladder cancer in individuals 40 to 50 years of age, with 60% to 90% being squamous cell carcinoma and 15% being adenocarcinoma (Trabulsi, 2010). A rare lesion can arise in men infected with Schistosomiasis haematobium that can be confused with more common prostate conditions, such as squamous metaplasia of the prostate.

Women suffer considerably from genital schistosomiasis, which can cause infertility, pre=term labor, anemia, menstrual disorders, and dyspareunia. Treating pregnant and lactating women decreases the disease burden and improves maternal and fetal outcome (Evantash, Hill, & Pernoll, 2003). Schistosomiasis of the cervix is usually secondary to involvement of the pelvic and uterine veins by the blood fluke Schistosoma haematobium. Cervical schistosomiasis may produce a large papillary growth that ulcerates and bleeds on contact, simulating cervical cancer. In other instances, it can be found in endocervical polyps, causing intermenstrual and postcoital bleeding. An ovum can be identified in a biopsy specimen taken from the granulomatus cervical lesion (Evantash et al., 2003).

Figure 4.

Example of Prevalence

From January 1999 through December 2004, the University Teaching
Hospital, Sokota, Nigeria, performed a retrospective epidemiological
study of the characteristics of bladder cancer in the region and to
assess the impact of schistosomiasis on these cases. The study
concluded that bladder cancer was a common malignancy, and the
association with chronic urinary schistomsomiasis was very strong,
with the hospital incidence rising at that time.

Source: Mungadi & Malami, 2007.


Schistosomiasis causes a chronic irritation and inflammation in the urinary bladder (see Figure 4). This constant activity of the schistosomes causes restorative hyperplasia, which promotes propagation of cells in which a DNA-damaging sequence of events occurs. These changes in the DNA subsequently facilitate changes in two stages of the development of the disease. Initiation of premalignant lesions is provoked, and this acts as a promoter to increase the likelihood of converting these lesions to a malignant state (Mostafa, Sheweita, & O'Connor, 1999).

Impact on GU Health

A systematic review of the literature database (via PubMed) was performed in 2010 on the long-standing complications of genitourinary schistosomiasis (Khalaf, Shokeir, & Shalaby, 2012). There are a variety of tissue reactions to schistosome eggs, with subsequent healing or progression and complications in the urinary tract, mainly affecting the urinary bladder and pelvic segments of the ureters. These lesions assume either an atrophic, proliferative, or neoplastic pattern. Although the pathology is usually extensive in the submucosa, all layers--from the mucous membrane through deep to the perivesical or periureteral tissues--may be involved. The resulting urologic conditions may include chronic bladder ulcers, leucoplakia, vesical granuloma, contracted bladder, bladder neck contracture, ureteral strictures, and bladder cancer. The review concluded that urinary schistosomiasis is a preventable disease through nationwide snail control and mass therapy with oral antibilharzial drugs. If not properly treated, long-standing urinary complications may result in these serious sequelae, which may lead to mortality from renal failure or bladder cancer (Khalaf et al., 2012).

Urogenital schistosomiasis is considered to be a risk factor for HIV infection, especially in women. Urogenitial schistosomiasis increases the risk of HIV infection because it causes genital lesions and what is referred to as "sandy patches" that bleed easily in the female genitals (Leder & Weller, 2009). Although schistosomiasis remains a chronic parasitic disease, with the rise of tourism and travel, increasing number of tourists are contracting it. Tourists often present with severe acute infection and unusual problems, including paralysis (Leder & Weller, 2009). The disease, however, is not endemic in United States. The inexperienced practitioner should consult an infectious disease or tropical medicine specialist for definitive diagnosis and treatment.

Treatment

Schistosomiasis control in sub-Saharan Africa has relied on morbidity control solely through preventative chemotherapy with the drug praziquantel. Usually well-tolerated, praziquantel is used both for individual treatment and mass community treatment programs. Praziquantel has been donated by Bayer for community treatment programs (The Carter Center, 2013).

Praziquantel is well-absorbed (approximately 80%) from the gastrointestinal tract, but due to extensive first-pass metabolism, only a relatively small amount enters systemic circulation. Praziquantel has a serum half-life of 1 to 2.5 hours in adults with normal renal and liver function (Bayer, Inc., 2007). Praziquantel is metabolized through the cytochrome P450 pathway via CYP3A4. Agents that induce or inhibit CYP3A4, such as phenytoin, rifampin, and azole antifungals, will affect the metabolism of praziquantel (Bayer, Inc., 2007).

The cure rate is equal to or greater than 85% (Behrman & O'Connor, 2011). In persons not cured, the egg burden is markedly decreased. The average dose of praziquantel is 20 mg/kg orally, three times daily at 4- to 6-hour intervals for one 24-hour period. Response to treatment is evaluated by counting the amount of decrease in egg excretion. In patients with a persistent circulating antigen and the excretion of eggs, residual infection is indicated, and these individuals should be retreated with praziquantel (Behrman & O'Connor, 2011).

Two-Month Follow-Up Assessment

Two months post-treatment, patients should be seen for follow up in the urology clinic to have the urine assessed for any retained egg burden. An egg viability test or microscopic examination is performed to assess for the effectiveness of treatment. The egg burden test requires mixing the stool or urine with room-temperature distilled water and observing for hatching. This would be repeated two months later because the eggs can be excreted for a number of weeks/ months following despite successful treatment. Persons with inactive infections can continue to shed dead eggs into the stool or urine for months; an active infection will produce viable eggs. Active treatment of patients or in those with a history of a prior infection will result in the presence of nonviable eggs and an absence of larvae.

In the event of recurrent bladder malignancy, standard surveillance protocols for bladder cancer are followed. Patients will return for cystoscopic examination of their bladder 90 days following the fulguration of these areas to assess for any cancer recurrence. If the patient continues to remain cancer-free, he should return again in 90 days for a cystoscopic examination, and if still clear, would go to a 6-month schedule and then to an annual cystoscopic surveillance schedule. According to Give Well (2012), there is a low prevalence of follow-up in underserved populations. Agencies, such as the Schistosomiasis Control Initiative (SCI), assist African governments with treatment of neglected tropical diseases. SCI has been a recommended organization because of its demonstrated results, ongoing research, and programs that have been successful in reducing prevalence of this infection. A retrospective review of SCI's studies was performed dating back to 2009, illustrating low patient follow-up rates of 43% to 73%.

According to Kabatereine (2007), in Uganda, out of 4,351 patients, 2,815 (64.7%) were traced and treated at 1-year follow up, and 1,871 (43%) at 2year follow up. In Niger, out of 1,656 patients recruited at baseline, 1,193 were traced (72.4%) and successfully followed up at 1- and 2-year surveys. In Burundi, only 49.6% of the baseline patients surveyed was found to have had 1-year follow up.

Other Diagnostic Tests For Schistosomiasis

Additional laboratory studies that can be performed can include stool or urine analysis, egg viability testing, urine syringe filtration techniques that provide a quantitative estimate of eggs in the urine, and urine analysis and culture. Blood chemistries, including renal and liver function tests, blood cultures, complete blood count (CBC), direct stool examination, and tests for hepatitis B and C, should be considered in suspected liver schistosomiasis. Serologic antibody testing is a useful epidemiological tool but cannot be used to differentiate active and past illness. ELISA and immunoblot assays (sensitivity and specificity of ELISA tests) are currently reported to be greater than both 90% and 95%, respectively (Al-Sherbiny, Osman & Hancock, 1999). Western blot tests are often used to confirm ELISA results.

With acute schistosomiasis, a chest radiograph, plain abdominal radiographs, abdominal/renal ultrasound (including the liver), or CT scan of the abdomen and pelvis should be performed (Vennervald & Dunne, 2005). Esophageal varices occur as a result of massive deposits of collagen in the periportal spaces, leading to fibrosis. This fibrosis will lead to a progressive occlusion of the portal veins and the creation of gastrointestinal and esophageal varices. Bleeding esophageal varices is the most serious and commonly fatal complication of hepatic schistosomiasis. The varices are visualized by barium swallow or endoscopy and can be immediately sclerosed.

CT scan of the lungs may demonstrate early interstitial fibrosis. An echocardiogram can reflect pulmonary hypertension due to egg emboli or pulmonary vasculature. CNS schistosomiasis also occurs with chronic disease, and a CT scan and MRI scan of the brain and spinal cord may show lesions (Gryseels, Polman, Clerinx, & Kestens, 2006).

Schistosomiasis Research

Currently, clinical trials are underway involving human volunteers to develop an effective vaccine against schistosomiasis. Artemether (INN) is an antimalarial used for the treatment of multi-drug-resistant strains of falciparum malaria. It is combined with lumefantrine (antimalarial) and is sold under the brand names Riamet[R] and CoArtem[R]. Clinical studies show that artemether may be used as a prophylactic agent if given once every 2 to 4 weeks (N'Goran, Utzinger, & Gnaka, 2003). This drug is a methyl ether derivative of artemisinin, which is a peroxide lactone isolated from the Chinese antimalarial plant, Artemisia annua. Aretminisins have been found to possess a broad spectrum of activity against a wide range of flatworms (trematodes), including Schistosoma japonicum, S. mansoni, S. Haematobium, Clonorchis sinesis, Fasciola hepatica, and Opisthorcis viverinni. Artememether has received FDA approval as a Class III, B in the United States for use in adults only. The aremether/lumefantrine combination drug is used for both adults and children outside of the U.S., with trade names of Coartem[R] or Riamet[R], and is manufactured by Novartis, U.K. (N' Goran et al., 2003).

Research into the development of new drugs and vaccines, along with improved diagnostics and refined spatial mapping tools, should be funded. A surveillance-response approach could be undertaken with the identification of new cases and endemic areas, combined with a detailed baseline assessment (surveillance) and the tailoring of the intervention strategy mix to these specific endemic settings (response); however, this strategy needs further evaluation. Without continued financial and political support, countries in sub-Saharan Africa will be unable to finance and sustain preventative chemotherapy programs against schistosomiasis (Gray et al., 2011).

Schistosomiasis has been considered a "neglected disease" that disproportionately affects poorer localities, receiving little attention from pharmaceutical companies. Support for current research efforts to develop hookworm vaccines has come from the Schistosomiasis Vaccine Initiative, a program of the Sabin Vaccine Institute, the Oswaldo Cruz Foundation, the Chinese Institute of Parasitic Diseases, the Queensland Institute of Medical Research, and the London School of Hygiene and Tropical Medicine (Sabin Vaccine Institute, 2011).

Conclusions

The association between schistosomiasis and the development of squamous cell carcinoma of the bladder has taken thousands of years to recognize, and this association is now well-established. It is important to consider screening not only patients with hematuria or other symptoms, but also asymptomatic patients who may have been exposed during travel to countries where schistosomiasis is endemic. These individuals may benefit from empiric treatment.

Over the past decade, considerable improvements have been made in methods of testing, with an improved understanding of the pathogenesis of bladder cancer. The ultimate goal should be the translation of these discoveries into therapies, prevention, or strategies to manage patients. With coordinated environmental health efforts, such as public works, ground water projects, public health education, screening, treatment, infrastructure development, and sustainability between governments and multinational organizations, there can be continued success in the battle against schistosomiasis infection, and in turn, bladder cancer.

Case Study.

Mr. H is a 51-year-old Somalian gentleman who immigrated to the United States from an African refugee camp one year ago. He is unemployed with no health care benefits. Mr. H is referred to the urology clinic by his primary care nurse practitioner for hematuria that has been occurring 2 to 3 times per week. He also complains of left lower quadrant and left flank pain, and complains of epigastric symptoms that are worse with eating. Since Mr. H had only rudimentary understanding of the English language, communication is facilitated via a Somalian translator.

A CT scan of the abdomen and pelvis was ordered. The results demonstrated a congenital left hydroureteronephrosis that extended down to and appeared to obstruct the ureterovesical junction. A lasix renogram was then performed, which verified that the ureterovesical junction was obstructed. Based upon these findings, it was determined that Mr. H would need to undergo a cystoscopic examination of his bladder with dilation of the left ureteral orifice and have a stent placed.

Upon initial cystoscopy of the bladder, the anterior urethra was normal in appearance. The prostate was also normal. The bladder was moderately trabeculated and had multiple yellow-colored punctate lesions throughout. These lesions were biopsied, fulgurated, and sent for pathology. The remainder of the procedure and stent placement was completed without complication. Mr. H tolerated these procedures well and left the operating room in good condition.

The pathologists' report on the samples obtained during the cystoscopy was positive for squamous cell carcinoma, schistosomiasis, and the presence of degenerative schistosome ova. Mr. H was referred for gastroenterology and infectious disease consultations. The infectious disease physician treated the schistosomiasis with the standard drug prazinquantel.

Two months following treatment, Mr. H was seen in follow up in the urology clinic to have his urine assessed for any retained egg burden. Mr. H also returned for cystoscopic examination of his bladder 90 days following the fulguration of his bladder to assess for any cancer recurrence. Although there are no prospective studies to identify an optimal surveillance protocol, a commonly used follow-up strategy includes cystoscopy and urine cytology every 3 months for 2 years, then every 6 months for the second 2 years, then yearly thereafter. Patients with a primary, solitary, low-grade Ta tumor may have less frequent cystoscopic examination (3 and 9 months, then annually thereafter). Annual upper tract imaging is recommended for patients with intermediate and high-risk neuromuscular invasive bladder cancer. Any recurrence resets the clock in the follow-up schedule. Random and/or directed biopsies at the first 3-month follow-up visit may be performed for those high-risk patients. Any suspicious or positive cytology requires repeat biopsy. If negative, ureteral washings and radiological upper tract assessment with biopsy of the prostatic urethra should all be performed because 20% of previously aggressive bladder cancer relapses outside the bladder (American Urologic Association, 2012). These recommendations were discussed and implemented in the treatment plan for Mr. H.

Mr. H returned to the clinic for his routine surveillance cystoscopies to assess for any return of his bladder cancer and schistosomiasis. Urine was taken directly from his bladder during the cystoscopy and sent for cytology and microbiology testing. Currently, Mr. H is healthy, feels well, and fully understands the importance of committing to a long-term schedule of cystoscopic surveillance bladder examinations. To date, there has been no recurrence.

Implications for Advanced Practice Nursing

Milwaukee has an influx of Somalian refugees; with the immigration of these refugees come rare and exotic diseases unusual to North America. This emphasizes the need for effective communication between the patient and the health care provider. In Mr. H's situation, a Somalian interpreter would accompany him to all clinic visits and necessary procedures. However, the interaction was still limited; there was often an inability to translate medical terminology. Nurse practitioners can also reinforce the importance of the required 6-month follow-up urinalysis checks to confirm parasite eradication, as well as reinforce the importance of contacting the clinic with any initial signs of hematuria.

Mr. H had social and economic barriers to health care, including unemployment, lack of health insurance, and lack of financial resources necessary to pay for his medical treatment and medication. Praziquantel is dosed at 20 mg/kg of weight. It is taken orally with food every 4 to 6 hours over a 24-hour period only. The typical adult dose is 2,400 mg to 3,500 mg (4 to 6 of the 600 mg tablets). The cost of six 600 mg tablets required by Mr. H was $100.00. Children ages 8 to 12 are dosed at 1200 mg to 1800 mg (2 to 3) tablets, and children ages 4 to 7 are dosed at one 600 mg tablet only. An anonymous individual paid for Mr. H's medication. The social services department was also recruited to assist Mr. H with his needs as an outpatient.

In Mr. H's case, there was an accurate diagnosis with an effective treatment that resulted in a positive outcome. First-hand understanding of this relatively rare disease process in the United States is gaining. Cases of schistosomiasis have been seen in New Mexico, Colorado, and the upper Midwest region (Brant & Loker, 2009). Just two doses of an oral antiparasitic medication eradicated a potentially life-threatening infection; however, without financial assistance, Mr. H's lack of resources could have prevented him from receiving the appropriate diagnostic testing, receiving the proper treatment, and paying for his medications. As urologic specialists, it is often difficult to develop close relationships with many of our patients, and we are therefore typically unaware of many intricate details of their daily lives. Unfortunately, this was the case with Mr. H because he was non-English speaking and always presented with a Somalian interpreter. The sole purpose of his clinic visits was to perform surveillance cystoscopic bladder examinations, which take less than 10 minutes. All discussion between the health care team and the patient must be repeated twice for the purpose of translation. To his benefit, Mr. H has subsequently relocated to Minneapolis-St. Paul, Minnesota, where there is a large Somalian population to better serve him.

As health care providers, it is important to look beyond the obvious when considering cultural factors, considering the patient's country of origin, language barriers, and current living conditions, to determine the possible etiology of symptoms and disease.

Sources: American Urological Association (AUA), 2012; Brant & Loker, 2009; Mungadi & Malami, 2007.

References

Ahmed, S.H., & Cunha, B.A. (2010). Schistosomiasis. Retrieved from http://emedicine.medscape.com/ article/228392-overview

Al-Sherbiny, M.M., Osman, A.M., & Hancock K., (1999). Application of iinmunodiagnostic assays: Detection of antibodies and circulating antigens in human schistosomiasis and correlation with clinical findings. American Journal of Tropical Medicine and Hygiene, 60(6), 960-966.

American Urological Association (AUA). (2012). AUA guidelines. Retrieved from http://www.auanet.org/education/ aua-guidelines.cfm

Bayer, Inc. (2007). Praziquantel drug monograph. Retrieved from http:// www.bayer.ca/files/BILTRICIDE-PM-ENC-30NOV2007-116425-2.pdf

Behrman, A.J., & O'Connor, R.E. (2011). Emergent management of acute schistosomiasis. Retrieved from http:// emedicine.medscape.com/article/ 788867-overview

Brant, S.V., & Loker, E.S. (2009). Schistosomes in the southwest United States and their potential for causing cercarial dermatitis or 'swimmers itch.' Journal of Heminthology, 83(2), 191-198.

Carter Center, The. (2013) Schistosomiasis Control Program. Retrieved June 4, 2013, from http://www.cartercenter. org/health/schistosomiasis/index. html

Centers for Disease Control and Prevention (CDC). (2012a). Parasites: Schistosomiasis. Retrieved from http://www. cdc.gov/parasites/schistosomiasis/ Centers for Disease Control and Prevention (CDC). (2012b). Parasites: Schistosomiasis--Biology. Retrieved from http://www.cdc.gov/parasites/schisto somiasis/epi.html

Evantash, E., Hill, E.C., & Pernoll, M.L. (2003). Benign disorders of the uterine cervix. In A.H. DeCherney & L. Nathan (Eds.), Current obstetric & gynecologic diagnosis & treatment (9th ed). (pp. 677-692). New York, NY: McGraw-Hill.

Give Well. (2012). Schistosomiasis Control Initiative (SCI). Retrieved from http://www.givewell.org/inter national/top-charities/schistosomia sis-control-initiative

Gray, D.J., McManus, D.P., Yuesheng, L., Williams, G.M., Bergquist, R., & Ross, A.G. (2011). Schistosomiasis elimination [Author's reply]. The Lancet,/1(5), 346-347.

Gryseels, B., Polman, K, Clerinx, J., & Kestens, L. (2006). Human schistosomiasis. Lancet, 386(9541), 1106-1118.

Kabatereine, N.B. (2007). Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bulletin of the World Health Organization, 85, 91-99.

Khalaf, I., Shokeir, A., & Shalaby, M. (2012). Urologic complications of genitourinary schistosomiasis. World Journal of Urology, 30(1), 31-38.

Leder, K., & Weller, P. (2009). Epidemiology; pathogenesis and clinical features of schistosomiasis. Retrieved from http://www.uptodate.com/con tents/epidemiology-pathogenesisand-clinical-features-of-schistosomiasis

McPhee, S.J. (2012). Current medical diagnosis & treatment (pp. 1469-1471). New York, NY: McGraw-Hill.

Mostafa, M.H., Sheweita, S.A., & O'Connor, P.J. (1999). Relationship between schistosomiasis and bladder cancer. Clinical Microbiology Reviews, 12(1), 97-111.

Mungadi, I.A.. & Malami, S.A. (2007). Urinary bladder cancer and schistosomiasis in northwestern Nigeria. West African Journal of Medicine, 26(3), 226-229.

N'Goran, E.K., Utzinger, J., & Gnaka, H.N. (2003). Randomized, double-blind, placebo-controlled trial of oral artemether for the prevention of patient Schistosoma haematobium infections. American Journal of Tropical Medical Hygiene, 88(1), 24-32.

Ragheb, M. (1956). Schistosomiasis of the liver: clinical, pathological and laboratory studies in Egyptian cases. Gastroenterology, 30, 631-636.

Sabin Institute (2011). History.. Retrieved from http://www.sabin.org/programs/ schistosomiasis-vaccine/history

Salem, S., Mitchell, R.E., E1-Dorey, A.E., Smith, J.A., & Barocas, D.B. (2010). Successful control of schistosomiasis and the changing epidemiology of bladder cancer in Egypt. British Journal of Urology International, 107, 206-211.

Trabulsi, E.J. (2010). Short topics: A to Z. In L.G. Gomella (Ed.), The 5-minute urology consult (2nd ed.). (pp. 543-680). Philadelphia: Wolters Kluwer.

Vennervald, J., & Dunne, D.W. (2005). Measuring schistosomiasis morbidity. Retrieved from http://www.tropika. net/review/051114-Schistosomiasis Morbidity/article.pdf

Jenkins-Holick, D.S., & Kaul, T.L. (2013). Schistosomiasis. Urologic Nursing, 33(4), 163-170. doi: 10.7257/1053-816X.2013.33.4.163

Darcy S. Jenkins-Holick, DNP, FNP-BC, CUNP, is a Family Nurse Practitioner, Department of Urology, Columbia-St. Mary's Community Physicians, Milwaukee, WI.

Teri L. Kaul, PhD, APRN-BC, ANP, FNP, is Director of Graduate Nursing, Concordia University Wisconsin, Mequon, WI. References

Ahmed, S.H., & Cunha, B.A. (2010). Schistosomiasis. Retrieved from http://emedicine.medscape.com/ article/228392-overview

Al-Sherbiny, M.M., Osman, A.M., & Hancock K., (1999). Application of iinmunodiagnostic assays: Detection of antibodies and circulating antigens in human schistosomiasis and correlation with clinical findings. American Journal of Tropical Medicine and Hygiene, 60(6), 960-966.

American Urological Association (AUA). (2012). AUA guidelines. Retrieved from http://www.auanet.org/education/ aua-guidelines.cfm

Bayer, Inc. (2007). Praziquantel drug monograph. Retrieved from http:// www.bayer.ca/files/BILTRICIDE-PM-ENC-30NOV2007-116425-2.pdf

Behrman, A.J., & O'Connor, R.E. (2011). Emergent management of acute schistosomiasis. Retrieved from http:// emedicine.medscape.com/article/ 788867-overview

Brant, S.V., & Loker, E.S. (2009). Schistosomes in the southwest United States and their potential for causing cercarial dermatitis or 'swimmers itch.' Journal of Heminthology, 83(2), 191-198.

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Jenkins-Holick, D.S., & Kaul, T.L. (2013). Schistosomiasis. Urologic Nursing, 33(4), 163-170. doi: 10.7257/1053-816X.2013.33.4.163

Darcy S. Jenkins-Holick, DNP, FNP-BC, CUNP, is a Family Nurse Practitioner, Department of Urology, Columbia-St. Mary's Community Physicians, Milwaukee, WI.

Teri L. Kaul, PhD, APRN-BC, ANP, FNP, is Director of Graduate Nursing, Concordia University Wisconsin, Mequon, WI.
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Author:Jenkins-Holick, Darcy S.; Kaul, Teri L.
Publication:Urologic Nursing
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Date:Jul 1, 2013
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