Advertisement
Research Article| Volume 97, ISSUE 1, P59-67, April 18, 2002

Impaired autonomic control of heart interval changes to Valsalva manoeuvre in Chagas' disease without overt manifestation

  • Luiz Fernando Junqueira Jr.
    Correspondence
    Corresponding author. Cardiovascular Laboratory, Clinical Medicine Area, Faculty of Medicine, University of Brasilia, Brasilia, DF, 70910-900, Brazil. Tel.: +55-61-307-2274; fax: +55-61-273-3907
    Affiliations
    Cardiovascular Laboratory, Clinical Medicine Area, Faculty of Medicine, University of Brasilia, Brasilia, DF, 70910-900, Brazil

    Division of Cardiology, Brasilia University Hospital, Brasilia, Brazil
    Search for articles by this author
  • Joaquim Domingos Soares
    Affiliations
    Cardiovascular Laboratory, Clinical Medicine Area, Faculty of Medicine, University of Brasilia, Brasilia, DF, 70910-900, Brazil

    Division of Cardiology, Brasilia University Hospital, Brasilia, Brazil
    Search for articles by this author

      Abstract

      Background: In the apparent indeterminate form of Chagas' disease, which lacks any overt clinical, electrocardiographic, and radiological manifestations of organ damage, lesions of the intrinsic autonomic innervation of heart are not striking features and evidences for cardiac autonomic dysfunction are elusive and conflicting. Objective: To evaluate the cardiac autonomic modulation based on Valsalva manoeuvre-associated heart interval variation in Chagas' disease subjects with apparent indeterminate form. Subjects and methods: We examined 36 outpatient volunteers aged 15–51 years old (median: 36.5), in comparison with 52 healthy control individuals aged 17–49 years old (median: 29) (p<0.001). Each subject sequentially performed in the supine position three to four manoeuvres at an intra-oral pressure of 40 mm Hg during 20 s, under continuous DII lead electrocardiographic registration, and rate- and time-dependent indices of Valsalva manoeuvre-associated R–R interval variation were obtained. The t-test or the Mann–Whitney test was employed to compare the data between the groups. Results: No correlation was found between every index and age for the control group (p=0.39–0.71). The chagasic group presented similar basal to phase IV median increment (relative bradycardia) (23.7% vs. 22.7%; p=0.63) and smaller basal to phase III median decrement of R–R interval (relative tachycardia) (−31.7% vs. −35%; p=0.02) in comparison to the control group, respectively. The median Valsalva ratio showed a tendency for reduction in chagasics (1.78 vs. 1.90; p=0.08). Prolonged median time (14.2 vs. 10.3 s; p<0.001) and slowed median velocity (5.1%/s vs. 8.9%/s; p<0.001) of the phases III–IV bradycardia were also observed in chagasic group. The majority (58.3%) of the chagasics presented exclusively at least one depressed, and 8.3% presented at least one enhanced index of rate- and/or time-dependent heart interval responses beyond the 25th or 75th control percentiles, and 27.8% presented at least one depressed and other enhanced index, while 5.6% showed all indices within the control interquartile range. All the indices outside the 25th or 75th control percentiles were noted in 13.9% of chagasics. Conclusion: Chagas' disease subjects without overt manifestations presented variable and subtle depression and less frequent enhancement or normality of the rate- and time-dependent tachycardia and bradycardia reflex responses related to Valsalva manoeuvre, which demonstrates distinct patterns of finely disturbed cardiac sinus parasympathetic and sympathetic modulation, probably due to inflammatory or autoimmunological damage of intrinsic innervation and/or to autoantibodies-induced derangement in neurotransmitter receptors.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Amorim D.S.
        • Manço J.C.
        • Gallo Jr., L.
        • Marin-Neto J.A.
        Chagas' heart disease as an experimental model for studies of cardiac autonomic function in man.
        Mayo Clin. Proc. 1982; 57: 48-60
        • Andrade Z.
        The canine model of Chagas' disease.
        Mem. Inst. Oswaldo Cruz. 1984; 79 (suppl.): 77-83
        • Baldwa V.S.
        • Ewing D.J.
        Heart rate response to Valsalva manoeuvre. Reproducibility in normals, and relation to variation in resting heart rate in diabetics.
        Br. Heart J. 1977; 39: 641-644
        • Baroldi G.
        • Oliveira S.J.
        • Silver M.D.
        Sudden and unexpected death in clinically silent Chagas' disease. A hypothesis.
        Int. J. Cardiol. 1997; 58: 263-268
        • Bennett T.
        • Hosking D.J.
        • Hampton J.R.
        Baroreflex sensitivity and responses to the Valsalva manoeuvre in subjects with diabetes mellitus.
        J. Neurol. Neurosurg. Psychiatry. 1976; 39: 178-183
        • Chapadeiro E.
        • Florêncio R.F.C.
        • Afonso P.C.
        • Beraldo P.S.S.
        • Jesus P.C.
        • Junqueira Jr., L.F.
        Neuronal counting and parasympathetic dysfunction in the hearts of chronically Trypanosoma cruzi-infected rats.
        Rev. Inst. Med. Trop. São Paulo. 1991; 33: 337-341
        • Chapadeiro E.
        • Silva E.L.
        • Silva A.C.M.
        • Fernandes P.
        • Ramirez L.E.
        Despopulação neuronal cardı́aca em hamsters (Mesocricetus auratus) cronicamente infectados com o Trypanosoma cruzi.
        Rev. Soc. Bras. Med. Trop. 1999; 32: 35-39
        • Dávila D.F.
        • Inglessis G.
        • Dávila C.A.M.
        Chagas' heart disease and autonomic nervous system.
        Int. J. Cardiol. 1998; 66: 123-127
        • Dias J.C.P.
        The indeterminate form of human chronic Chagas' disease. A clinical epidemiological review.
        Rev. Soc. Bras. Med. Trop. 1989; 22: 147-156
        • Eckberg D.L.
        Parasympathetic cardiovascular control in human disease: a critical review of methods and results.
        Am. J. Physiol. 1980; 239: H581-H593
        • Espi F.
        • Canteras M.
        • Benages A.
        • Carmena R.
        Evaluación de la maniobra de Valsalva y del ejercicio muscular isometrico en los individuos normales.
        Rev. Esp. Cardiol. 1986; 39: 213-219
        • Ewing D.J.
        Cardiovascular reflexes and autonomic neuropathy.
        Clin. Sci. Mol. Med. 1978; 55: 321-327
        • Ewing D.J.
        • Winney R.
        Autonomic function in patients with chronic renal failure on intermittent hemodialysis.
        Nephron. 1975; 15: 424-429
        • Ewing D.J.
        • Martyn C.N.
        • Young R.J.
        • Clarke B.F.
        The value of cardiovascular autonomic function tests: 10 years experience in diabetes.
        Diabetes Care. 1985; 8: 491-498
        • Gallo Jr., L.
        • Morelo Filho J.
        • Maciel B.C.
        • Marin-Neto J.A.
        • Martins L.E.B.
        • Lima Filho E.C.
        Functional evaluation of sympathetic and parasympathetic system in Chagas' disease using dynamic exercise.
        Cardiovasc. Res. 1987; 21: 922-927
        • Guzzetti S.
        • Iosa D.
        • Pecis M.
        • Bonura L.
        • Prosdocimi M.
        • Malliani A.
        Impaired heart rate variability in patients with chronic Chagas' disease.
        Am. Heart J. 1991; 121: 1727-1734
        • Iosa D.J.
        • Caeiro T.F.
        • Palmero H.A.
        Abnormal hyperventilation test in chronic Chagas' disease.
        J. Auton. Nerv. Syst. 1980; 2: 87-92
        • Junqueira Jr., L.F.
        Ambulatory assessment of cardiac autonomic function in Chagas' heart disease patients based on indexes of R–R interval variation in the Valsalva maneuver.
        Braz. J. Med. Biol. Res. 1990; 23: 1091-1102
        • Junqueira Jr., L.F.
        Sobre o possı́vel papel da disfunção autonômica cardı́aca na morte súbita associada a doença de Chagas.
        Arq. Bras. Cardiol. 1991; 56: 429-434
        • Junqueira Jr., L.F.
        • Gallo Jr., L.
        • Manço J.C.
        • Marin-Neto J.A.
        • Amorim D.S.
        Subtle cardiac autonomic impairment in Chagas' disease detected by baroreflex sensitivity testing.
        Braz. J. Med. Biol. Res. 1985; 18: 171-178
        • Junqueira Jr., L.F.
        • Beraldo P.S.S.
        • Chapadeiro E.
        • Jesus P.C.
        Cardiac autonomic dysfunction and neuroganglionitis in a rat model of chronic Chagas' disease.
        Cardiovasc. Res. 1992; 26: 324-329
        • Kruter R.H.E.
        • Eizirik D.L.
        • Gross J.L.
        Relationship of the Valsalva ratio to autonomic neuropathy and other complications of diabetes mellitus.
        Braz. J. Med. Biol. Res. 1982; 15: 35-41
        • Levin A.B.
        A simple test of cardiac function based upon the heart rate changes induced by the Valsalva maneuver.
        Am. J. Cardiol. 1966; 18: 90-99
        • Levy M.N.
        Sympathetic–parasympathetic interactions in the heart.
        Circ. Res. 1971; 29: 437-445
        • Lopes E.R.
        • Tafuri W.L.
        Involvement of the autonomic nervous system in Chagas' heart disease.
        Rev. Soc. Bras. Med. Trop. 1983; 16: 206-212
        • Low P.A.
        • Walsh J.C.
        • Huang C.Y.
        • McLeod J.G.
        The sympathetic nervous system in diabetic neuropathy. A clinical and pathological study.
        Brain. 1975; 98: 341-356
        • Macêdo V.
        Indeterminate form of Chagas' disease.
        Mem. Inst. Oswaldo Cruz. 1999; 94: 311-316
        • Macêdo V.O.
        • Prata A.R.
        • Silva A.
        Teste da pilocarpina na forma indeterminada da doença de Chagas.
        Rev. Goiana Med. 1974; 20: 191-199
        • Machado C.R.
        • Caliari M.V.
        • de Lana M.
        • Tafuri W.L.
        Heart autonomic innervation during the acute phase of experimental American trypanosomiasis in the dog.
        Am. J. Trop. Med. Hyg. 1998; 59: 492-496
        • Maciel B.C.
        • Almeida Filho O.C.
        • Schmidt A.
        • Marin-Neto J.A.
        Ventricular function in Chagas' heart disease.
        Rev. Paul. Med. 1995; 113: 814-820
        • Manço J.C.
        • Gallo Jr., L.
        • Godoy R.A.
        • Fernandes R.G.
        • Amorim D.S.
        Degeneration of the cardiac nerves in Chagas' disease. Further studies.
        Circulation. 1969; 40: 879-885
        • Marin-Neto J.A.
        Cardiac dysautonomia and pathogenesis of Chagas' heart disease.
        Int. J. Cardiol. 1998; 66: 129-131
        • Marin-Neto J.A.
        • Gallo Jr., L.
        • Manço J.C.
        • Rassi A.
        • Amorim D.S.
        Mechanisms of tachycardia on standing: studies in normal individuals and in chronic Chagas' heart patients.
        Cardiovasc. Res. 1980; 14: 541-550
        • Marin-Neto J.A.
        • Bromberg-Marin G.
        • Pazin-Filho A.
        • Simões M.V.
        • Maciel B.C.
        Cardiac autonomic impairment and early myocardial damage involving the right ventricle are independent phenomena in Chagas' disease.
        Int. J. Cardiol. 1998; 65: 261-269
        • Nishimura R.A.
        • Tajik A.J.
        The Valsalva maneuver and response revisited.
        Mayo Clin. Proc. 1986; 61: 211-217
        • Oliveira J.S.M.
        A natural human model of intrinsic heart nervous system denervation: Chagas' cardiopathy.
        Am. Heart J. 1985; 110: 1092-1098
        • Oliveira Jr., W.
        • Salazar L.F.
        • Malta J.
        • Assi N.
        Análise crı́tica da forma indeterminada da doença de Chagas.
        Arq. Bras. Cardiol. 1986; 47: 283-288
        • Palmero H.A.
        • Caeiro T.F.
        • Iosa D.J.
        Distinctive abnormal response to tilting test in chronic Chagas' disease.
        Klin. Wochenschr. 1980; 58: 1307-1311
        • Ribeiro A.L.P.
        • Rocha M.O.C.
        Forma indeterminada da doença de Chagas: considerações acerca do diagnóstico e do prognóstico.
        Rev. Soc. Bras. Med. Trop. 1998; 31: 301-314
        • Ribeiro A.L.P.
        • Moraes R.S.
        • Ribeiro J.P.
        • Ferlin E.L.
        • Torres R.M.
        • Oliveira E.
        • Rocha M.O.C.
        Parasympathetic dysautonomia precedes left ventricular systolic dysfunction in Chagas' disease.
        Am. Heart J. 2001; 141: 260-265
        • Schofield C.J.
        • Dias J.C.P.
        The Southern Cone Initiative against Chagas' disease.
        Adv. Parasitol. 1998; 42: 1-27
        • Simões M.V.
        • Pintya A.O.
        • Bromberg-Marin G.
        • Sarabanda A.V.
        • Antloga C.M.
        • Pazin-Filho A.
        • Maciel B.C.
        • Marin-Neto J.A.
        Relation of regional sympathetic denervation and myocardial perfusion disturbance to wall motion impairment in Chagas' cardiomyopathy.
        Am. J. Cardiol. 2000; 86: 975-981
        • Souza M.M.
        • Andrade S.G.
        • Barbosa Jr., A.A.
        • Santos R.T.M.
        • Alves V.A.F.
        • Andrade Z.A.
        Trypanosoma cruzi strains and autonomic nervous system pathology in experimental Chagas' disease.
        Mem. Inst. Oswaldo Cruz. 1996; 91: 217-224
        • Sterin-Borda L.
        • Borda E.
        Role of neurotransmitter autoantibodies in the pathogenesis of chagasic peripheral dysautonomia.
        Ann. N. Y. Acad. Sci. 2000; 917: 273-280
        • Tafuri W.L.
        Pathogenesis of lesions of the autonomic nervous system of the mouse in experimental acute Chagas' disease.
        Am. J. Trop. Med. Hyg. 1970; 19: 405-417
        • Trimarco B.
        • Volpe M.
        • Ricciardelli B.
        • Vigorito C.
        • De Luca N.
        • Sacca V.
        • Condorelli M.
        Valsalva maneuver in the assessment of baroreflex responsiveness in borderline hypertensives.
        Cardiology. 1983; 70: 6-14
        • Tristani F.E.
        • Kamper D.G.
        • McDermott D.J.
        • Peters B.J.
        • Smith J.J.
        Alterations of postural and Valsalva responses in coronary heart disease.
        Am. J. Physiol. 1977; 233: H694-H699
        • WHO
        Control of Chagas' disease.
        WHO Technical Report Series. vol. 811. World Health Organization, Geneva1991