• View in gallery

    Fasciola eggs seen in two cases under ×40 objective lens. Size variation makes it hard to diagnose the exact species especially in areas where both Fasciola gigantica and F. heptatica coexist (A and B).

  • View in gallery

    (A) Abdominal computed tomography (CT) image of a 29-year-old female, shows multiple heterogeneous hepatic focal lesions “arrows,” and mild ascites (before treatment). A picture suggestive of hepatic abscess. (B) Abdominal CT scan of the same patient after 3 months from receiving treatment.

  • 1.

    Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41146.

    • Search Google Scholar
    • Export Citation
  • 2.

    Periago MV, Valero MA, El Sayed M, Ashrafi K, El Wakeel A, Mohamed MY, Desquesnes M, Curtale F, Mas-Coma S, 2008. First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infect Genet Evol 8: 5158.

    • Search Google Scholar
    • Export Citation
  • 3.

    Lotfy WM, El-Morshedy HN, Abou El-Hoda M, El-Tawila MM, Omar EA, Farag HF, 2002. Identification of the Egyptian species of Fasciola. Vet Parasitol 103: 323332.

    • Search Google Scholar
    • Export Citation
  • 4.

    Valero MA, Perez-Crespo I, Periago MV, Khoubbane M, Mas-Coma S, 2009. Fluke egg characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and F. gigantica. Acta Trop 111: 150159.

    • Search Google Scholar
    • Export Citation
  • 5.

    Soliman MF, 2008. Epidemiological review of human and animal fascioliasis in Egypt. J Infect Dev Ctries 2: 182189.

  • 6.

    Marcos LA, Terashima A, Gotuzzo E, 2008. Update on hepatobiliary flukes: fascioliasis, opisthorchiasis and clonorchiasis. Curr Opin Infect Dis 21: 523530.

    • Search Google Scholar
    • Export Citation
  • 7.

    Zali MR, Ghaziani T, Shahraz S, Hekmatdoost A, Radmehr A, 2004. Liver, spleen, pancreas and kidney involvement by human fascioliasis: imaging findings. BMC Gastroenterol 4: 15.

    • Search Google Scholar
    • Export Citation
  • 8.

    Vatsal DK, Kapoor S, Venkatesh V, Vatsal P, Husain N, 2006. Ectopic fascioliasis in the dorsal spine: case report. Neurosurgery 59: E706E707; discussion E706–E707.

    • Search Google Scholar
    • Export Citation
  • 9.

    Lim JH, Mairiang E, Ahn GH, 2008. Biliary parasitic diseases including clonorchiasis, opisthorchiasis and fascioliasis. Abdom Imaging 33: 157165.

    • Search Google Scholar
    • Export Citation
  • 10.

    Fang W, Chen F, Liu H-K, Yang Q, Yang L, 2014. Comparison between albendazole and triclabendazole against Fasciola gigantica in human. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 26: 106108.

    • Search Google Scholar
    • Export Citation
  • 11.

    Abdel-Hafeez EH, Ahmad AK, Ali BA, Moslam FA, 2012. Opportunistic parasites among immunosuppressed children in Minia District, Egypt. Korean J Parasitol 50: 5762.

    • Search Google Scholar
    • Export Citation
  • 12.

    Abdel-Aziz NM, 1993. Incidence and Public Health Importance of Fascioliasis in Slaughtered Animals in Assiut Province, M.Sc. Thesis, Faculty of Veterinary Medicine, Assiut University, Egypt.

    • Search Google Scholar
    • Export Citation
  • 13.

    Arafa MI, Fouad IA, 2008. Studies on some internal parasites of goats in assiut governorate especially which affecting liver. Assiut Univ Bull Environ Res 11: 5773.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mas-Coma MS, Esteban JG, Bargues MD, 1999. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ 77: 340346.

    • Search Google Scholar
    • Export Citation
  • 15.

    Esteban JG, Gonzalez C, Curtale F, Muñoz-Antoli C, Valero MA, Bargues MD, El Sayed M, El Wakeel AAEW, Abdel-Wahab Y, Montresor A, Engels D, Savioli L, Mas-Coma S, 2003. Hyperendemic fascioliasis associated with schistosomiasis in villages in the Nile Delta of Egypt. Am J Trop Med Hyg 69: 429437.

    • Search Google Scholar
    • Export Citation
  • 16.

    Youssef AI, Uga S, 2014. Review of parasitic zoonoses in Egypt. Trop Med Health 42: 314.

  • 17.

    El-Khoby T, Galal N, Fenwick A, Barakat R, El-Hawey A, Nooman Z, Habib M, Abdel-Wahab F, Gabr NS, Hammam HM, Hussein MH, Mikhail NNH, Cline BL, Strickland GT, 2000. The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. Am J Trop Med Hyg 62: 8899.

    • Search Google Scholar
    • Export Citation
  • 18.

    Barakat RMR, 2013. Epidemiology of schistosomiasis in Egypt: travel through time review. J Adv Res 4: 425432.

  • 19.

    Trent SC, 1963. Reevaluation of World War II veterans with filariasis acquired in the South Pacific. Am J Trop Med Hyg 12: 877887.

  • 20.

    Marcos LA, Tagle M, Terashima A, Bussalleu A, Ramirez C, Carrasco C, Valdez L, Huerta-Mercado J, Freedman DO, Vinetz JM, Gotuzzo E, 2008. Natural history, clinicoradiologic correlates, and response to triclabendazole in acute massive fascioliasis. Am J Trop Med Hyg 78: 222227.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

Human Fascioliasis: A Re-emerging Disease in Upper Egypt

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  • Department of Gastroenterology and Tropical Medicine, Faculty of Medicine, Assiut, Egypt; Department of Parasitology, Faculty of Medicine, Assiut University, Assiut, Egypt; Department of Internal Medicine, Faculty of Medicine, Assiut, Egypt; Department of Diagnostic Radiology, Faculty of Medicine, Assiut, Egypt

In recent years, the number of humans infected with Fasciola has risen rapidly. Diagnosis is based mainly on detection of eggs in stool analysis. The rate of infection in Egypt is unknown. In this retrospective study, we describe 23 cases of hepatic fascioliasis, and only 2 of these cases showed eggs in stools. The symptoms of infection, such as pyrexia of unknown origin, epigastric pain, and abdominal distension, were suggestive. Imaging techniques, including abdominal ultrasonography and computed tomography, were very helpful in detecting hepatic changes. An indirect hemagglutination assay proved to be of value for diagnosis. Treatment using a 2-day triclabendazole regimen cured the infection and signs of hepatic involvement disappeared. Combining both imaging techniques and laboratory tests is essential for diagnosis of fascioliasis in the early stage.

Introduction

Fascioliasis is a food-borne zoonotic disease caused by digenetic trematode of the genus Fasciola. The number of human cases increased significantly in the last decade, with an estimated number of the infected population ranging from 2,400,000 to 17,000,000 worldwide.1 In Egypt, intermediate hybrid forms exist together with Fasciola hepatica and F. gigantica.2 The wide range of egg-size variability makes it difficult to determine species from eggs found in stool analysis.3,4 Fascioliasis has been endemic in certain villages in the Nile Delta, but overall prevalence in Egypt is unknown because reports show wide variations in infection rates.5

Infection occurs through ingestion of encysted metacercariae that contaminate water or food. The clinical manifestations range from asymptomatic to fever, mild hepatomegaly, or cholangitis, which depend on worm burden. Chronic cases can be discovered accidently.1,6 Unusual clinical manifestations are common as Fasciola can be found to be ectopic in the spine, pancreas, kidney, and spleen.7,8 Diagnosis depends mainly on finding eggs in stool analysis, but other serological and imaging techniques are also of great value. Computed tomography (CT) can detect microabscesses caused by worms tunneling liver tissues, which is important in follow-up.6,9 The drug of choice is triclabendazole at a single dose of 10 mg/kg body weight for for 2 days.10

The clinical presentation of human fascioliasis infection is unusual, ranging from asymptomatic cases to cholangitis, hepatitis, and hepatic focal lesions (HFLs). The real burden of the problem in Egypt is not fully understood. Therefore, herein, we present 23 cases of individuals who were diagnosed with hepatic fascioliasis and were presented at Assiut University Hospital with variable symptoms.

Patients and Methods

During the period from March 2012 to December 2013, we were retrospectively able to recruit 23 cases diagnosed to have hepatic fascioliasis among inpatients of the Assiut University Hospitals. Patients were admitted with varying complaints and all of them were subjected to routine investigations, including complete blood count and peripheral blood film examination, liver and kidney function tests, abdominal ultrasonographic (US) examination, and routine stool examination to exclude parasitic infection.

Further investigations were conducted for cases following the clinical picture, and results of the routine investigations include:

  1. 1. Indirect hemagglutination assay (IHA) using Distomatose Fumouze (Laboratories Fumouze Diagnostic, Levallois Perret, France). A titer of 1/320 or more was considered to be positive according to the manufacturer's instructions.
  2. 2. Abdominal CT scan.
  3. 3. Endoscopic retrograde cholangiopancreatography (ERCP).

All patients were given two doses of triclabendazole at a dose of 10 mg/kg body weight/day. Patients were clinically followed up with for at least 3 months. Stool analysis, abdominal US and/or CT, and serology were used according to each case's needs.

This study was approved by our Institutional Review Board and ethical committee.

Results

Twenty-three patients (14 males; mean age: 21.2 ± 10.6 years) were diagnosed to have hepatic fascioliasis among inpatients of the Assiut University Hospitals. All patients presented with clinical symptoms, except for two who had HFLs on routine abdominal US. The main complaint was pyrexia of unknown origin (PUO) for more than 1 month (N = 10), followed by distended abdomen (N = 4), epigastric pain (N = 4), and jaundice (N = 3). Nineteen patients came from rural areas and had farm animals at their residences (data shown in Table 1).

Table 1

Clinical and demographic data of patients recruited in this study showing the main complaint and percentage of eosinophilia

 SexAgeResidencyCity/GovernorateFarm animalsMain complaintAbsolute eosinophilia (%)
1Female5RuralManfalut/AssiutYesDistended abdomen70
2Male4RuralManfalut/AssiutYesDistended abdomen55
3Male10RuralManfalut/AssiutYesProlonged fever45
4Male6RuralDayr Mawas/MinyaYesProlonged fever70
5Female11RuralMallawi/MinyaYesDistended abdomen30
6Male12RuralDayrout/AssiutYesProlonged fever70
7Male14RuralManfalut/AssiutYesJaundice50
8Male16RuralMallawi/MinyaYesJaundice55
9Male19UrbanSohag/SohagNoNo symptoms40
10Female19UrbanAssiut/AssiutNoEpigastric pain40
11Male20RuralDayrout/AssiutYesEpigastric pain50
12Male22RuralEdfu/AswanYesNo symptoms70
13Female22RuralDayr Mawas/MinyaYesProlonged fever70
14Female23RuralEsna/QenaYesProlonged fever30
15Male24RuralDayrout/AssiutYesProlonged fever50
16Male27RuralEdfu/AswanYesJaundice60
17Female29RuralManfalut/AssiutYesProlonged fever55
18Male30RuralManfalut/AssiutYesEpigastric pain30
19Male31RuralMallawi/MinyaYesDistended abdomen45
20Male33RuralManfalut/AssiutYesEpigastric pain30
21Female34RuralDayr Mawas/MinyaYesProlonged fever70
22Female39UrbanAssiut/AssiutNoProlonged fever55
23Female39UrbanAssiut/AssiutNoProlonged fever35

Routine stool analysis revealed operculated eggs of genus Fasciola in two cases (Figure 1A and B), while the remaining cases were negative when tested for any intestinal parasites. Routine complete blood count showed absolute eosinophilia ranging between 30% and 70% in all patients. Such high eosinophilia was a milestone to suspect parasitic infection. A routine liver function test detected elevated transaminases in all cases and elevated total bilirubin in 15 cases.

Figure 1.
Figure 1.

Fasciola eggs seen in two cases under ×40 objective lens. Size variation makes it hard to diagnose the exact species especially in areas where both Fasciola gigantica and F. heptatica coexist (A and B).

Citation: The American Society of Tropical Medicine and Hygiene 93, 1; 10.4269/ajtmh.15-0030

Abdominal US examination revealed just ascites in 7 cases, HFLs in 10 cases (3 of which also had ascites), dilated common bile duct (CBD) in 3 cases, and gall bladder stones in 2 cases. All cases with HFL underwent an abdominal CT scan and in three cases liver biopsy was taken from the lesion. CT revealed multiple hypodense HFL suggestive of liver abscess (Figure 2A). Histopathological examination of biopsy tissue revealed necrotic tissue in one case and eosinophilic liver abscess in two cases. ERCP was performed in three cases with dilated CBD, and necrotic remains of worms were extracted (data shown in Table 2).

Figure 2.
Figure 2.

(A) Abdominal computed tomography (CT) image of a 29-year-old female, shows multiple heterogeneous hepatic focal lesions “arrows,” and mild ascites (before treatment). A picture suggestive of hepatic abscess. (B) Abdominal CT scan of the same patient after 3 months from receiving treatment.

Citation: The American Society of Tropical Medicine and Hygiene 93, 1; 10.4269/ajtmh.15-0030

Table 2

Imaging findings using abdominal ultrasonographic (US) examination and or abdominal computed tomography (CT) scan

Imaging findings (US and/or CT)Frequency (%)
Normal1 (4.3)
HFLs7 (30.4)
Dilated CBD3 (13)
Ascites7 (30.4)
GB stones3 (13)
HFL with ascites7 (30.4)

CBD = common bile duct; HFL = hepatic focal lesion; GB = gallbladder.

All patients received two doses of triclabendazole at a dose of 10 mg/kg body weight/day. Those who had HFL with ascites were given a low dose of cortisone (15 mg/day) for 2 weeks. Follow-up at 1-month interval was conducted using clinical examination, abdominal US, abdominal CT (for those who had HFL), and serology using IHA to measure antibodies titer. All patients showed signs of disease regression with no ova detectable in stool analysis and healing of HFL as shown in CT (Figure 2B). However, two patients maintained the same antibody titer 3 months after treatment.

It is noteworthy that one female patient developed severe hypotension and cyanosis 1 hour post-CT-guided liver biopsy, a picture similar to anaphylactic shock, and she was admitted to the intensive care unit until she regained normal blood pressure and blood oxygen tension.

Discussion

Cases of human fascioliasis are increasing worldwide, making it an emerging threat to humans. Fasciola has previously existed in Egypt, and human cases are increasing with endemic areas in the Nile Delta.1,5 The overall prevalence is unknown as only limited-size data samples are available. Soliman5 assumes that the prevalence of Fasciola is approximately 3% among humans. This presumption is based on a survey of 3,000 children in an endemic village in the Nile Delta where 3% were found to be infected. Such data are opposed by the fact that overall rates of Fasciola infection in animals slaughtered in slaughterhouses in Egypt were 2.02% for sheep and goats, 3.54% for cattle, and 1.58% for buffaloes, as stated by the same author. Moreover, a recent study in the Minia district, Upper Egypt, showed that Fasciola species eggs were not detected in both immuno-compromised and immune-competent children in that study.11 This outcome is consistent with our findings. Although we report an increasing number of cases admitted to Assiut University Hospitals (23 cases in 21 months: 11 cases in 2012 and 12 cases in 2013) while we used to see one or two isolated cases per year. The number of cases is still low per the total population of Upper Egypt, where Assiut University is located. Although Soliman5 cite higher rates of fascioliasis in animals by the Ministry of Agriculture, we tend not to accept those numbers that depend on veterinary convoys for which only sick animals are presented. In Assiut, a study of slaughterhouses all over the governorate state that the infection rates were 1.2% for sheep, 0.5% for goats, 5.3% for cattle, and 3.5% for buffaloes.12 In a more recent study in 2008, a limited sample number of slaughtered goats in Assiut revealed infection rate of 3.5% for fascioliasis.13

The infection rate was higher among males than females, adults than children, and those who came from rural areas and had farm animals than those from urban areas with no farm animals. The higher prevalence in adults can be explained through the pattern of age distribution among nonendemic areas.14 Higher infection rates among males may be explained by lifestyle factors as men are usually responsible for feeding animals and working in the fields in rural areas in Upper Egypt. The presence of Fasciola as an endemic parasite in the Nile Delta may be due to the fact that the lymnaeid snail lives in slow or shallow water habitats, which are more common in the Nile Delta than in Upper Egypt. The infection rate of fascioliasis ranged from 5.2% to 19% in an endemic area in the Nile Delta, such infection rate was comparable to Schistosoma mansoni.15,16 This result supports the theory of snail habitat compatibility in the Nile Delta, where rice fields and slow canals are common. In addition, the low infection rate of S. mansoni in Upper Egypt supports the comparably low fascioliasis infection rate finding.17,18 As infection is due to ingestion of metacercariae contaminating water or vegetables, the recent increase of the number of cases in Upper Egypt may be due to political instabilities that have occurred since January 2011, which may have affected the snail control programs of the Ministry of Health. The increase could also be due to the use of partially processed sewage water, intended to grow trees used for wood and not meant to plant vegetables for irrigation.

Although finding an egg in stool analysis is the main diagnostic test for fascioliasis,4 eggs were detected in only two cases in this study. This outcome may be due to the fact that diagnosis occurred in the hepatic phase, where an immature worm feeds on liver tissue with no egg production as all cases had eosinophilia and HFL, which are observed in early infection.6 It also can be an indicator that Fasciola is not yet an endemic disease for humans in Upper Egypt as the immune systems react strongly to the parasites giving rise to severe symptoms. While in endemic areas, immune system tends to be exposed to parasite antigens through whole life leading to moderate immune reaction. This phenomenon was seen in U.S. soldiers who were in filariasis endemic areas, they tend to show lymphadenitis and microfilariae were detected in rare cases.19 HFL, found in 10 cases, was detected in both abdominal US and abdominal CT and had a picture suggestive of liver abscess. This outcome is consistent with the previous studies finding that during the early infection phase, immature worms dig through liver parenchyma forming minute cavities, which mainly come from tissue necrosis, unlike a pyogenic abscess where a single large cavity is observed.9,20 Histopathology of biopsies revealed necrosis with eosinophilic infiltrations. Thus, imaging could be quite useful for screening and suspecting cases in nonendemic regions.

Indirect hemagglutination test (IHA) was very helpful in diagnosing cases, and it can be used for follow-up to detect the falling titer of antibodies after treatment. Human fascioliasis should not be ignored, unless IHA or more specific enzyme-linked immunosorbent assay of Fasciola hepatica cystein proteinase antigen 2 (ELISA Fas2) is performed.

In conclusion, human fascioliasis should be suspected in patients who exhibit fever, eosinophilia, and hepatic infiltrates. Physicians also need to become familiar with this presentation, especially, in areas where Fasciola is common. The rising number of cases in Upper Egypt should be alarming and call for more work on studying the snail infection rate and snail control programs to avoid an epidemic of fascioliasis or appearance of new endemic foci in this locality.

  • 1.

    Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41146.

    • Search Google Scholar
    • Export Citation
  • 2.

    Periago MV, Valero MA, El Sayed M, Ashrafi K, El Wakeel A, Mohamed MY, Desquesnes M, Curtale F, Mas-Coma S, 2008. First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infect Genet Evol 8: 5158.

    • Search Google Scholar
    • Export Citation
  • 3.

    Lotfy WM, El-Morshedy HN, Abou El-Hoda M, El-Tawila MM, Omar EA, Farag HF, 2002. Identification of the Egyptian species of Fasciola. Vet Parasitol 103: 323332.

    • Search Google Scholar
    • Export Citation
  • 4.

    Valero MA, Perez-Crespo I, Periago MV, Khoubbane M, Mas-Coma S, 2009. Fluke egg characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and F. gigantica. Acta Trop 111: 150159.

    • Search Google Scholar
    • Export Citation
  • 5.

    Soliman MF, 2008. Epidemiological review of human and animal fascioliasis in Egypt. J Infect Dev Ctries 2: 182189.

  • 6.

    Marcos LA, Terashima A, Gotuzzo E, 2008. Update on hepatobiliary flukes: fascioliasis, opisthorchiasis and clonorchiasis. Curr Opin Infect Dis 21: 523530.

    • Search Google Scholar
    • Export Citation
  • 7.

    Zali MR, Ghaziani T, Shahraz S, Hekmatdoost A, Radmehr A, 2004. Liver, spleen, pancreas and kidney involvement by human fascioliasis: imaging findings. BMC Gastroenterol 4: 15.

    • Search Google Scholar
    • Export Citation
  • 8.

    Vatsal DK, Kapoor S, Venkatesh V, Vatsal P, Husain N, 2006. Ectopic fascioliasis in the dorsal spine: case report. Neurosurgery 59: E706E707; discussion E706–E707.

    • Search Google Scholar
    • Export Citation
  • 9.

    Lim JH, Mairiang E, Ahn GH, 2008. Biliary parasitic diseases including clonorchiasis, opisthorchiasis and fascioliasis. Abdom Imaging 33: 157165.

    • Search Google Scholar
    • Export Citation
  • 10.

    Fang W, Chen F, Liu H-K, Yang Q, Yang L, 2014. Comparison between albendazole and triclabendazole against Fasciola gigantica in human. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 26: 106108.

    • Search Google Scholar
    • Export Citation
  • 11.

    Abdel-Hafeez EH, Ahmad AK, Ali BA, Moslam FA, 2012. Opportunistic parasites among immunosuppressed children in Minia District, Egypt. Korean J Parasitol 50: 5762.

    • Search Google Scholar
    • Export Citation
  • 12.

    Abdel-Aziz NM, 1993. Incidence and Public Health Importance of Fascioliasis in Slaughtered Animals in Assiut Province, M.Sc. Thesis, Faculty of Veterinary Medicine, Assiut University, Egypt.

    • Search Google Scholar
    • Export Citation
  • 13.

    Arafa MI, Fouad IA, 2008. Studies on some internal parasites of goats in assiut governorate especially which affecting liver. Assiut Univ Bull Environ Res 11: 5773.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mas-Coma MS, Esteban JG, Bargues MD, 1999. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ 77: 340346.

    • Search Google Scholar
    • Export Citation
  • 15.

    Esteban JG, Gonzalez C, Curtale F, Muñoz-Antoli C, Valero MA, Bargues MD, El Sayed M, El Wakeel AAEW, Abdel-Wahab Y, Montresor A, Engels D, Savioli L, Mas-Coma S, 2003. Hyperendemic fascioliasis associated with schistosomiasis in villages in the Nile Delta of Egypt. Am J Trop Med Hyg 69: 429437.

    • Search Google Scholar
    • Export Citation
  • 16.

    Youssef AI, Uga S, 2014. Review of parasitic zoonoses in Egypt. Trop Med Health 42: 314.

  • 17.

    El-Khoby T, Galal N, Fenwick A, Barakat R, El-Hawey A, Nooman Z, Habib M, Abdel-Wahab F, Gabr NS, Hammam HM, Hussein MH, Mikhail NNH, Cline BL, Strickland GT, 2000. The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. Am J Trop Med Hyg 62: 8899.

    • Search Google Scholar
    • Export Citation
  • 18.

    Barakat RMR, 2013. Epidemiology of schistosomiasis in Egypt: travel through time review. J Adv Res 4: 425432.

  • 19.

    Trent SC, 1963. Reevaluation of World War II veterans with filariasis acquired in the South Pacific. Am J Trop Med Hyg 12: 877887.

  • 20.

    Marcos LA, Tagle M, Terashima A, Bussalleu A, Ramirez C, Carrasco C, Valdez L, Huerta-Mercado J, Freedman DO, Vinetz JM, Gotuzzo E, 2008. Natural history, clinicoradiologic correlates, and response to triclabendazole in acute massive fascioliasis. Am J Trop Med Hyg 78: 222227.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Mohammed Tolba, Department of Parasitology, Faculty of Medicine, Assiut University, Assiut 71515, Egypt. E-mail: essa3eg@yahoo.com

Authors' addresses: Mohamed A. Mekky and Mohamed O. Abdel-Malek, Department of Gastroenterology and Tropical Medicine, Faculty of Medicine, Assiut University, Assiut, Egypt, E-mails: doc_mekky0000@yahoo.com and momar7619@gmail.com. Mohammed Tolba, Department of Parasitology, Faculty of Medicine, Assiut University, Assiut, Egypt and Sugano Lab, Human Genome Center, Building 2, Institute of Medical Science, The University of Tokyo, Tokyo, Japan, E-mail: essa3eg@yahoo.com. Wael A. Abbas, Department of Internal Medicine, Assiut University, Assiut, Egypt, E-mail: drwaelabbas@yahoo.com. Mohamed Zidan, Department of Diagnostic Radiology, Faculty of Medicine, Assiut University, Assiut, Egypt, E-mail: mzidan74@yahoo.com.

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