Digestive Diseases and Sciences

, Volume 61, Issue 7, pp 2118–2126 | Cite as

Increased Hepatic Arterial Blood Flow Measured by Hepatic Perfusion Index in Hepatosplenic Schistosomiasis: New Concepts for an Old Disease

  • Bernardo Times de Carvalho
  • Ana Lúcia Coutinho Domingues
  • Edmundo Pessoa de Almeida Lopes
  • Simone Cristina Soares Brandão
Original Article



Portal vein obstructive lesions associated with hypertrophy of the hepatic artery territory are observed in Schistosoma mansoni schistosomiasis. Liver perfusion scintigraphy is a method used for evaluation of hepatic perfusion changes in liver diseases. It has been suggested that, like in cirrhosis, where compensatory increase in perfusion through the hepatic artery is documented, perfusion changes occur in hepatosplenic schistosomiasis (HSS).


This study aims to determine changes in liver hemodynamics using hepatic perfusion scintigraphy and correlate them with clinical and laboratory variables and ultrasound findings in HSS.


Nineteen patients with schistosomiasis underwent ultrasound evaluation of degree of liver fibrosis, splenic length, and splenic and portal vein diameter, digestive endoscopy, and quantification of platelets. Subsequently, perfusion scintigraphy with measurement of hepatic perfusion index (HPI) was performed.


It was observed that patients with hepatosplenic schistosomiasis had significantly higher HPI compared with normal individuals (p = 0.0029) and that this increase correlated with splenic length (p = 0.038) and diameter of esophageal varices (p = 0.0060). Angioscintigraphy showed high accuracy for predicting presence of large esophageal varices.


Angioscintigraphy could show that patients with HSS had increased HPI, featuring greater liver “arterialization,” as previously described for cirrhotic patients. Correlations were also observed between HPI and longitudinal splenic length, caliber of esophageal varices, caliber of portal vein, and blood platelet count. Angioscintigraphy is a promising technique for evaluation of hepatosplenic schistosomiasis.


Hepatosplenic schistosomiasis Scintigraphy Angioscintigraphy Hepatic perfusion 



Special thanks go to Socrates Times de Carvalho for mathematical assistance with regression analysis of graphical data.

Author’s contributions

Bernardo Times de Carvalho: study concept and design, data acquisition, statistical analysis, data interpretation, and manuscript writing. Ana Lúcia Coutinho Domingues: study concept and design and critical manuscript review for important intellectual concepts. Edmundo Pessoa de Almeida Lopes: critical manuscript review for important intellectual concepts. Simone Cristina Soares Brandão: study concept and design, and data acquisition.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Pereira GJM, Torres MEG. Epidemiologia. In: Malta J, ed. Esquistossomose Mansônica. Primeira. Recife: Editora Universitária da UFPE; 1994:47–48.Google Scholar
  2. 2.
    WHO. Sustaining the drive to overcome the global impact of neglected tropical diseases. Second WHO Rep Neglected Trop Dis. 2013;3:67–71.Google Scholar
  3. 3.
    Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368:1106–1118.CrossRefPubMedGoogle Scholar
  4. 4.
    Ross AG, Bartley PB, Sleigh AC, et al. Schistosomiasis. N Engl J Med. 2002;346:1212–1220.CrossRefPubMedGoogle Scholar
  5. 5.
    Andrade ZA. Schistosomal hepatopathy. Mem Inst Oswaldo Cruz. 2004;99:51–57.CrossRefPubMedGoogle Scholar
  6. 6.
    Andrade ZA. Schistosomiasis and liver fibrosis. Parasite Immunol. 2009;31:656–663.CrossRefPubMedGoogle Scholar
  7. 7.
    Hidayat M, Wahid H. A study of the vascular changes in bilharzic hepatic fibrosis and their significance. Surg Gynecol Obstet. 1971;132:997–1004.PubMedGoogle Scholar
  8. 8.
    Magalhães-Filho A, Menezes H, de Coelho R. B. Patogênese da fibrose hepática na esquistossomose mansoni (Estudo das alterações vasculares portais mediante modelo plástico). Rev Assoc Med Bras. 1960;6:284–294.PubMedGoogle Scholar
  9. 9.
    Mies S, Larsson E, Mori T, Williams GM. Sistema porta e as artérias hepatica, esplênica e mesentérica superior na esquistossomose hepatoesplênica. Estudo angiográfico. Rev do Hosp das Clínicas Fac Med São Paulo. 1980;35:121–131.Google Scholar
  10. 10.
    Cleva R, Pugliese V, Zilberstein B, Saad WA, Pinotti W, Laudanna AA. Systemic hemodynamic changes in mansonic schistosomiasis with portal hypertension treated by azygoportal disconnection and splenectomy. Am J Gastroenterol. 1999;94:1632–1637.CrossRefPubMedGoogle Scholar
  11. 11.
    Cleva R, Herman P, D’albuquerque LA, Pugliese V, Santarem OL, Saad WA. Pre- and postoperative systemic hemodynamic evaluation in patients subjected to esophagogastric devascularization plus splenectomy and distal splenorenal shunt: a comparative study in schistosomal portal hypertension. World J Gastroenterol. 2007;13:5471–5475.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Warren HW, Gallagher H, Hemingway DM, et al. Prospective assessment of the hepatic perfusion index in patients with colorectal cancer. Br J Surg. 1998;85:1708–1712.CrossRefPubMedGoogle Scholar
  13. 13.
    Koranda P, Myslivecek M, Erban J, Seidlová V, Husák V. Hepatic perfusion changes in patients with cirrhosis indices of hepatic arterial blood flow. Clin Nucl Med. 1999;24:507–510.CrossRefPubMedGoogle Scholar
  14. 14.
    O’Connor MK, Krom RF, Carton EG, et al. Ratio of hepatic arterial-to-portal venous blood flow-validation of radionuclide techniques in an animal model. J Nucl Med. 1992;33:239–245.PubMedGoogle Scholar
  15. 15.
    Pandharipande PV, Krinsky GA, Rusinek H, Lee VS. Perfusion imaging of the liver: current challenges and future goals. Radiology. 2005;234:661–673.CrossRefPubMedGoogle Scholar
  16. 16.
    Dragoteanu M, Balea IA, Dina LA, et al. Staging of portal hypertension and portosystemic shunts using dynamic nuclear medicine investigations. World J Gastroenterol. 2008;14:3841–3848.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Razzak MA. The use of radioactive isotopes to study the hemodynamic pattern, function and morphology of the liver in hepato-splenic bilharziasis (schistosomiasis). J Nucl Med. 1964;5:125–133.PubMedGoogle Scholar
  18. 18.
    Mustafa AG, Razzak MA, Mahfouz M, Guirgis B. Radioisotope photoscanning of the liver in bilharzial hepatic fibrosis. J Nucl Med. 1966;7:909–916.PubMedGoogle Scholar
  19. 19.
    Iio M, Iuchi M, Kitani K, Yamada H, Ishiwa M. Scintigraphic evaluation of the liver with schistosomiasis japonica. J Nucl Med. 1971;12:655–659.PubMedGoogle Scholar
  20. 20.
    Homeida M, Abdel-Gradir AF, Cheever AW, et al. Diagnosis of pathologically confirmed Symmers’ periportal fibrosis by ultrasonography: a prospective blinded study. Am J Trop Med Hyg. 1988;38:86–91.PubMedGoogle Scholar
  21. 21.
    Abdel-Wahab MF, Esmat G, Milad M, Abdel-Razek S, Strickland GT. Characteristic sonographic pattern of schistosomal hepatic fibrosis. Am J Trop Med Hyg. 1989;40:72–76.PubMedGoogle Scholar
  22. 22.
    Richter J, Hatz C, Campagne G, Bergquist NR, Jenkins JM, eds. Ultrasound in Schistosomiasis: A Practical Guide to Standardized Use of Ultrasonography for the Assessment of Schistosomiasis-related Morbidity. Geneva: World Health Organization, TDR/STR/SCH/00.1; 2000.Google Scholar
  23. 23.
    Richter J, Coutinho Domingues AL, Barata CH, Prata AR, Lambertucci JR. Report of the second satellite symposium on ultrasound in schistosomiasis. Mem Inst Oswaldo Cruz. 2001;96:151–156.CrossRefPubMedGoogle Scholar
  24. 24.
    Palmer E, Brick I. Correlation between the severity of esophageal varices in cirrhosis and their propensity toward hemorrhage. Gastroenterology. 1956;30:85–90.PubMedGoogle Scholar
  25. 25.
    Leveson SH, Wiggins PA, Nasiru TA, Giles GR, Robinson PJ, Parkin A. Improving the detection of hepatic metastases by the use of dynamic flow scintigraphy. Br J Cancer. 1983;47:719–721.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Sarin S, Mosca P, Sabba C, Groszmann R. Hyperdynamic circulation in a chronic murine schistosomiasis model of portal hypertension. Hepatology. 1991;13:581–584.CrossRefPubMedGoogle Scholar
  27. 27.
    Denié C, Vachiery F, Elman A, et al. Systemic and splanchnic hemodynamic changes in patients with hepatic schistosomiasis. Liver. 1996;16:309–312.CrossRefPubMedGoogle Scholar
  28. 28.
    Azeredo LM, Queiroz LCD, Marinho CC, et al. Sonographic and hemodynamic findings of schistosomiasis mansoni: Doppler sonography assessment in endemic areas. Radiol Bras. 2010;43:69–76.CrossRefGoogle Scholar
  29. 29.
    De Arruda SMB, Barreto VST, Do Amaral FJ. Duplex sonography study in schistosomiasis portal hypertension: characterization of patients with and without a history of variceal bleeding. Arq Gastroenterol. 2008;45:11–16.CrossRefPubMedGoogle Scholar
  30. 30.
    Zipprich A, Steudel N, Behrmann C, et al. Functional significance of hepatic arterial flow reserve in patients with cirrhosis. Hepatology. 2003;37:385–392.CrossRefPubMedGoogle Scholar
  31. 31.
    Kleber G, Steudel N, Behrmann C, et al. Hepatic arterial flow volume and reserve in patients with cirrhosis: use of intra-arterial Doppler and adenosine infusion. Gastroenterology. 1999;116:906–914.CrossRefPubMedGoogle Scholar
  32. 32.
    Lautt WW. Mechanism and role of intrinsic regulation of hepatic arterial blood flow: hepatic arterial buffer response. Am J Physiol Gastrointest Liver Physiol. 1985;249:G549–G556.Google Scholar
  33. 33.
    Lautt WW. Hepatic circulation physiology and pathophysiology. In: Lautt WW, ed. Colloquium Series on Integrated Systems Physiology: From Molecule to Function. San Rafael: Morgan & Claypool Life Sciences; 2009.Google Scholar
  34. 34.
    Kollmar O, Corsten M, Scheuer C, Vollmar B, Schilling MK, Menger MD. Portal branch ligation induces a hepatic arterial buffer response, microvascular remodeling, normoxygenation, and cell proliferation in portal blood-deprived liver tissue. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1534–G1542.CrossRefPubMedGoogle Scholar
  35. 35.
    Moeller M, Thonig A, Pohl S, Ripoll C, Zipprich A. Hepatic arterial vasodilation is independent of portal hypertension in early stages of cirrhosis. PLoS One. 2015;10:e0121229.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Ezzat WR, Lautt WW. Hepatic arterial pressure-flow autoregulation is adenosine mediated. Am J Physiol. 1987;252:H836–H845.PubMedGoogle Scholar
  37. 37.
    Lautt WW. Mechanism and role of intrinsic regulation of hepatic arterial blood flow: hepatic arterial buffer response. Am J Physiol. 1985;249:549–556.Google Scholar
  38. 38.
    Lautt WW. Control of hepatic arterial blood flow: independence from liver metabolic activity. Am J Physiol. 1980;239:H559–H564.PubMedGoogle Scholar
  39. 39.
    Vollmar B, Menger MD. The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair. Physiol Rev. 2009;89:1269–1339.CrossRefPubMedGoogle Scholar
  40. 40.
    Eipel C, Abshagen K, Vollmar B. Regulation of hepatic blood flow: the hepatic arterial buffer response revisited. World J Gastroenterol. 2010;28:6046–6057.CrossRefGoogle Scholar
  41. 41.
    Strauss E. Hepatosplenic schistosomiasis: a model for the study of portal hypertension. Ann Hepatol. 2002;1:6–11.PubMedGoogle Scholar
  42. 42.
    Warren KS. Hepatosplenic schistosomiasis mansoni: an immunologic disease. Bull N Y Acad Med. 1975;51:545–550.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Da Silva LC. Portal hypertension in schistosomiasis: pathophysiology and treatment. Mem Inst Oswaldo Cruz. 1992;87:183–186.CrossRefPubMedGoogle Scholar
  44. 44.
    Jorge PAR, dos Carvalhal SS. Sobre a rede vascular intra-hepática na esquistossomose mansonica, forma de Symmers: Estudo com modelos plásticos. Rev Assoc Med Bras. 1967;13:435–441.PubMedGoogle Scholar
  45. 45.
    Widman A, Speranzini MB, de Lima JT, Wierman P, de Oliveira MR, Raia A. Arterial and operative portography in patients with portal hypertension caused by hepato-splenic schistosomiasis and those with spleno-renal anastomosis (comparative study). Rev do Hosp das Clínicas Fac Med São Paulo. 1973;28:177–187.Google Scholar
  46. 46.
    Alves C, Alves A, Abreu W, Andrade ZA. Hepatic artery hypertrophy and sinusoidal hypertension in advanced schistosomiasis. Gastroenterology. 1977;72:126–128.PubMedGoogle Scholar
  47. 47.
    Mies S, Braghirolli-Neto O, Beer A, et al. Systemic and hepatic hemodynamics in hepatosplenic manson’s schistosomiasis with and without propranolol. Dig Dis Sci. 1997;42:751–761.CrossRefPubMedGoogle Scholar
  48. 48.
    Baptista AP, Andrade ZA. Angiogenesis and schistosomal granuloma formation. Mem Inst Oswaldo Cruz. 2005;100:183–185.CrossRefPubMedGoogle Scholar
  49. 49.
    Lacerda CM, Ramos H, Raia S, Kelner S. Fisiopatologia da hipertensão portal esquistossomótica e efeitos da esplenectomia com ligadura de varizes de esôfago. Acta Cir Bras. 1993;8:113–117.Google Scholar
  50. 50.
    Pereira FM, Evangelista-Neto J, Brito N, Amaral F, da Fonseca-Neto OC, Lacerda CM. Angiografic and pressoric changes determined by splenectomy with left gastric vein ligature in mansoni schistosomiasis. Arq Bras Cir Dig. 2013;26:302–308.CrossRefPubMedGoogle Scholar
  51. 51.
    Coutinho A. Hemodynamic studies of portal hypertension in schistosomiasis. Am J Med. 1968;44:547–555.CrossRefPubMedGoogle Scholar
  52. 52.
    Morgan J, Groszmann R, Rojkind M, Enriquez R. Hemodynamic mechanism of emerging portal hypertension caused by schistosomiasis in the hamster. Hepatology. 1990;11:98–104.CrossRefPubMedGoogle Scholar
  53. 53.
    Andrade ZA. A double and paradoxical role for angiogenesis. Rev Patol Trop. 2013;42:259–264.Google Scholar
  54. 54.
    Rocheleau B, Ethier C, Houle R, Huet PM, Bilodeau M. Hepatic artery buffer response following left portal vein ligation: its role in liver tissue homeostasis. Am J Physiol. 1999;277:G1000–G1007.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Bernardo Times de Carvalho
    • 1
  • Ana Lúcia Coutinho Domingues
    • 1
  • Edmundo Pessoa de Almeida Lopes
    • 2
  • Simone Cristina Soares Brandão
    • 2
  1. 1.General HospitalFederal University of PernambucoRecifeBrazil
  2. 2.General HospitalFederal University of PernambucoRecifeBrazil

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