O Papel da Ecocardiografia sob Estresse na Detecção Precoce de Disfunção Diastólica em Pacientes com Doença Pulmonar Obstrutiva Crônica Não Grave

Zheyna Cherneva; Radostina Cherneva

doi:10.36660/abc.20190623

. 2021 Feb 19;116(2):259–265. [Article in Portuguese] doi: 10.36660/abc.20190623

View full-text in English

O Papel da Ecocardiografia sob Estresse na Detecção Precoce de Disfunção Diastólica em Pacientes com Doença Pulmonar Obstrutiva Crônica Não Grave

Zheyna Cherneva ¹, Radostina Cherneva ²

PMCID: PMC7909987 PMID: 33656074

Resumo

Fundamento

A dispneia por esforço é uma queixa comum de pacientes com insuficiência cardíaca com fração de ejeção preservada (ICFEP) e doença pulmonar obstrutiva crônica (DPOC). A ICFEP é comum na DPOC e é um fator de risco independente para a progressão e exacerbação da doença. A detecção precoce, portanto, tem grande relevância clínica.

Objetivos

O objetivo deste estudo foi detectar a frequência de ICFEP mascarada em pacientes com DPOC não grave com dispneia aos esforços, sem doença cardiovascular manifesta, e analisar a correlação entre ICFEP mascarada e os parâmetros do teste cardiopulmonar de exercício (TCPE).

Métodos

Aplicamos o TCPE em 104 pacientes com DPOC não grave com dispneia aos esforços, sem doença cardiovascular evidente. A ecocardiografia foi realizada antes e no pico do TCPE. Os valores de corte para disfunção diastólica ventricular esquerda e direita induzida por estresse (DDVE/DDVD) foram E/e’ >15; E/e’ >6, respectivamente. A análise de correlação foi feita entre os parâmetros do TCPE e o estresse E/d’. Valor de p<0,05 foi considerado significativo.

Resultados

64% dos pacientes tinham DDVE induzida por estresse; 78% tinham DDVD induzida por estresse. Ambos os grupos com estresse DDVE e DDVD obtiveram carga menor, V’O₂ e pulso de O₂mais baixos, além de apresentarem redução na eficiência ventilatória (maiores inclinações de VE/VCO₂). Nenhum dos parâmetros do TCPE foram correlacionados com E/e’ DDVE/DDVD induzida por estresse.

Conclusão

Há uma alta prevalência de disfunção diastólica induzida por estresse em pacientes com DPOC não grave com dispneia aos esforços, sem doença cardiovascular evidente. Nenhum dos parâmetros do TCPE se correlaciona com E/e’ induzida por estresse. Isso demanda a realização de Ecocardiografia sob estresse por exercício (EES) e TCPE para detecção precoce e manejo adequado da ICFEP mascarada nesta população. (Arq Bras Cardiol. 2021; 116(2):259-265)

Keywords: Ecocardiografia sob Estresse/métodos, Insuficiência Cardíaca Diastólica, Volume Sistólico, Doença Pulmonar Obstrutiva Crônica, Testes de Função Respiratória

Introdução

As anormalidades cardiovasculares são comuns na doença pulmonar obstrutiva crônica (DPOC).^1,2A rigidez arterial está presente mesmo em pacientes com DPOC leve e sem doenças cardiovasculares. Trata-se de um fator de risco cardiovascular independente que contribui para o desenvolvimento de disfunção diastólica.³ Dispneia e intolerância ao exercício são sintomas comuns da DPOC e disfunção diastólica.⁴ Estudos recentes com grandes coortes de pacientes identificaram um fenótipo cardiovascular em pacientes com DPOC que apresentam curso clínico e prognóstico diferentes.⁵ O diagnóstico e o manejo precoces são, portanto, muito importantes do ponto de vista clínico.

O teste cardiopulmonar de exercício (TCPE) pode distinguir dispneia cardíaca e respiratória ou diminuição da atividade física.^6-9A combinação de ecocardiografia sob estresse por exercício (EES) e TCPE é uma abordagem confiável para identificar pacientes com insuficiência cardíaca mascarada pela fração de ejeção preservada (ICFEP). Além disso, os resultados das medições invasivas são comparáveis aos dados obtidos em estudos não invasivos durante o EES.¹⁰

Os objetivos de nosso estudo foram: 1) detectar a frequência de disfunção diastólica subclínica do ventrículo esquerdo (VE) e do ventrículo direito (VD) em pacientes com DPOC não grave sem doença cardiovascular; 2) estabelecer uma correlação entre exercício cardiopulmonar e os parâmetros ecocardiográficos para disfunção diastólica (E/e’).

Materiais e métodos

Pacientes e protocolo de estudo

Este foi um estudo retrospectivo realizado com 224 pacientes ambulatoriais clinicamente estáveis com diagnóstico de DPOC no Hospital Universitário de Doenças Respiratórias “St. Sophia”, Sofia. Apenas 163 deles atenderam aos critérios de inclusão para DPOC não grave: volume expiratório forçado no primeiro segundo maior que 50% (VEF₁>50%). Todos os indivíduos apresentavam dispneia aos esforços, mas um total de 104 pacientes (64 homens, 40 mulheres; idade média de 62,9±7,5 anos) foram considerados elegíveis, assumindo-se os critérios de exclusão. O período de recrutamento foi entre maio de 2017 e abril de 2018, e foi aprovado pelo Comitê de Ética local (protocolo 5/12.03.2018). Todos os participantes assinaram o termo de consentimento livre e esclarecido antes do início do estudo.

Foram considerados os seguintes critérios de exclusão: 1) fração de ejeção do ventrículo esquerdo (FEVE) <50%; 2) disfunção diastólica do ventrículo esquerdo em repouso superior ao primeiro grau; 3) achados ecocardiográficos sugerindo hipertensão pulmonar (pressão arterial pulmonar sistólica >36 mmHg, regurgitação tricúspide (RT), velocidade máxima do jato >2,8 m/s; 4) cardiopatia valvar; 5) cardiomiopatia documentada; 6) hipertensão grave não controlada (pressão arterial sistólica >180 mmHg e pressão arterial diastólica >90 mmHg); 7) fibrilação atrial ou arritmia ventricular maligna; 8) doença isquêmica do coração; 9) anemia; 10) diabetes mellitus; 11) câncer; 12) doença renal crônica (DRC); 13) cirurgia torácica ou abdominal recente; 14) exacerbação recente (nos últimos três meses); 15) mudança recente (nos últimos três meses) na terapia médica.

Procedimentos

Teste de função pulmonar

Todos os indivíduos foram submetidos a um exame clínico preliminar, incluindo radiografia de tórax, espirometria, eletrocardiografia e ecocardiografia. Os pacientes elegíveis para o estudo realizaram espirometria e teste ergométrico em Vyntus, teste cardiopulmonar de exercício (Carefusion, Alemanha), de acordo com as diretrizes da European Respiratory Society (ERS).¹¹ Apenas pacientes com obstrução leve a moderada das vias aéreas (VEF₁> 50%) foram selecionados.

Protocolo de teste de estresse – teste cardiopulmonar de exercício (TCPE)

Um protocolo em rampa contínua foi aplicado de acordo com diretrizes.⁶ Após dois minutos de pedalada sem carga (fase de repouso 0W), seguiu-se uma fase de aquecimento de três minutos (20W). A fase de teste incluiu incrementos de carga de 20W/2min. Os pacientes foram orientados a pedalar a 60 rotações por minuto.

Os gases expiratórios foram coletados respiração a respiração. O pico de VO₂ foi expresso como o maior valor médio de 30 segundos, obtido na última etapa do teste de esforço. Os valores de pico de VO₂ são expressos como -O₂ ml/kg/min. A eficiência ventilatória (EV/VCO₂) foi medida pelo método V-slope. O pico da razão de troca respiratória (pRTR) foi o maior valor médio de 30 segundos no último estágio do teste. RTR >1,10 ao final do teste EES-TCPE foi considerado como esforço máximo.

Métodos ecocardiográficos

Foram realizados ecocardiografia modo M, bidimensional com Doppler.^12,13 Incidências apicais de quatro câmaras foram usadas para medir os volumes das câmaras com base na regra modificada de Simpson e a fração de ejeção do VE foi considerada preservada se >50%. A análise da ecocardiografia Doppler tecidual foi realizada na dimensão septo-lateral do anel mitral e na dimensão lateral do anel tricúspide para avaliar as ondas sistólica (S) e diastólica miocárdica (E’, A’) do VE e VD. O valor E’ foi usado como média das medições mediais e laterais. O pico da razão E/e’ >15 foi considerado um marcador para disfunção diastólica ventricular esquerda induzida por estresse.

A função sistólica do ventrículo direito foi avaliada por meio da excursão sistólica do plano do anel tricúspide (TAPSE) e da velocidade de pico S do Doppler tecidual. A espessura da parede do ventrículo direito (EPVD) foi medida a partir do corte subcostal no eixo longo na extremidade do folheto tricúspide anterior ao final da diástole. A pressão pulmonar foi calculada diretamente pela amostra da insuficiência tricúspide e indiretamente pelo tempo de aceleração (TA) do fluxo pulmonar. O índice de volume do átrio direito (IVAD) foi medido com o volume sistólico final do ventrículo direito pela regra modificada de Simpson. A disfunção diastólica do VD induzida por estresse foi considerada se a razão E/e’ induzida por estresse fosse >6. Todos os parâmetros foram medidos no final da expiração e três vezes durante diferentes ciclos cardíacos.¹⁴

Análise estatística

Os dados demográficos e clínicos foram apresentados em estatística descritiva. O teste de Kolmogorov-Smirnov foi usado para explorar a normalidade da distribuição. As variáveis contínuas em cada grupo foram expressas como mediana e intervalo interquartil quando os dados não foram normalmente distribuídos, e como média ± desvio-padrão (DP) se a distribuição foi normal. Variáveis categóricas foram apresentadas em proporções. Os dados foram comparados entre pacientes com e sem DDVE, bem como entre pacientes com e sem DDVD. O teste t de Student não pareado foi usado para analisar variáveis contínuas normalmente distribuídas. O teste de Mann-Whitney-U foi usado em outros casos. Variáveis categóricas foram comparadas pelo teste de χ² ou exato de Fisher. A correlação de Spearman foi usada para avaliar a associação entre os parâmetros TCPE e a razão E/e’ induzida por estresse nos ventrículos esquerdo e direito.

Em todos os casos, um valor de p inferior a 0,05 foi considerado significativo, conforme determinado pelas estatísticas do software SPSS® 13.0 (SPSS, Inc, Chicago, Ill).

Resultados

No grupo DPOC, 30% (32/104) dos pacientes apresentaram DDVE grau I em repouso; 14% (15/104) tinham DDVD grau I em repouso e apenas 3% (4/104) tinham tanto DDVE quanto DDVD em repouso. Após o TCPE, a ecocardiografia sob estresse estabeleceu que 64% (67/104) dos indivíduos tinham DDVE induzida por estresse e 78% (82/104) tinham DDVD induzida por estresse. Todos os pacientes com DDVE induzida por estresse também tinham DDVD induzida por estresse. Os dados demográficos e clínicos dos pacientes estão listados na Tabela 1. Os parâmetros ecocardiográficos dos pacientes estão apresentados na Tabela 2. Exceto para IVAD, EPVD, TA e pressão arterial pulmonar sistólica após carga, nenhuma outra diferença significativa foi encontrada entre os pacientes com e sem DDVE (Tabelas 1 e 2). Os resultados para pacientes com e sem DDVD foram semelhantes (Tabelas 1 e 2).

Tabela 1. – Características antropométricas e cardiopulmonares de pacientes com e sem DDVE e DDVD.

	Pacientes sem DDVE por estresse (37)	Pacientes com DDVE por estresse (67)	Pacientes sem DDVD por estresse (22)	Pacientes com DDVD por estresse (82)
Dados demográficos
Idade, ano	60,44 ± 7,72	64,16 ± 6,97*	6,95±7,36	63,74±7,60*
Masculino:feminino, n	21:16	44:23^ǂ	14:8	50:32^ǂ
Pacote, anos	27,21 (23,87-31,76)	33,79 (30,51± 37,87)^†	26,52 (23,46-30,43)	32,11(28,82-36,13)^ǂ
Índice de massa corpórea, kg/m²	27,00 (24,75-31,00)	27,96 (22,75-30,75)^†	28,00 (25,25-30,5)	26,52 (22,72-30,61)^†
Função respiratória
CVF, l/min	2,06 (1,76-3,09)	2,34 (1,77-3,09)^†	2,05 (2,11-3,73)	2,21 (1,71-2,93)^†
FEV₁, l/min	1,31 (0,94-1,53)	1,36 (1,14-1,75)^†	1,60 (1,15-2,42)	1,52 (1,14-1,75)^†
FEV₁/CVF %	60,5 (46,91-67,47)	53,30 (45,76-66,55)^†	65,50 (54,81-68,82)	62,59 (46,57-66,79)^†
Equilíbrio ácido-base
pO₂, mmHg	68,60(63,4-71,8)	71,35 (64,7-74)^†	67,20 (63,56-71,68)	70,6 (63,2-74)^†
pCO₂, mmHg	32,30 (30,1-35,37)	37,65 (32,5-40)^†	34,73 (31,27-39,21)	35,7 (32,5-40)^†
Saturação, %	94,9 (94,4-95,25)	95,00 (94,02-95,67)^†	94,75 (92,67-95,0)	95,00 (93,9-95,5)^†
Parâmetros TCPE
Pico de carga, W	82,75 (69,8-89,1)	▪ 76,05 (68,4-92,1)^†	86,66 (78,65-94,76)	▪▪73,08 (68,93-83,16)^†
Pico de VM, l/min	40 (34-52,5)	38,50 (32-48)^†	41,1 (32,12-48,17)	39,07 (31,89-48,32)^†
Pico de V’O₂, ml/min/kg	14,30(12,6-16,15)	13,90 (12,67-15,7)^†	14,30 (12,6-16,15)	13,40(15,77-12,55)^†
RTR	1,06 (0,98-1,19)	1,09 (1,00-1,28)^†	1,05 (0,98-1,18)	1,08 (1,01-1,19)^†
Pico de pulso de O₂ ml/min/kg	9,80 (9,5-12,2)	▪7,90 (6,15-9,32)^†	9,51 (9,02-13,1)	▪▪7,92(6,27-9,84)^†
Pico de inclinação VM/VCO₂	34,08 (33,98-36,72)	▪36,93 (34,19-38,74)^†	34,11 (33,78-36,89)	▪▪36,98 (34,26-38,91)^†

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*Teste t não pareado; †Teste U de Mann-Whitney; Teste ǂchi-quadrado; DDVE: disfunção diastólica do ventrículo esquerdo; DDVD: disfunção diastólica do ventrículo direito; CVF: capacidade vital forçada; Pulso de O²: pulso de oxigênio; VM: ventilação minuto; RTR: razão de troca respiratória; V’O²: consumo de oxigênio; TCPE: parâmetros do teste cardiopulmonar de exercício. Inclinação VM/VCO²: eficiência ventilatória; ▪p<0,05 entre pacientes com e sem DDVE; ▪▪p<0,05 entre pacientes com e sem DDVD.

Tabela 2. – Parâmetros ecocardiográficos de pacientes com e sem DDVE e DDVD.

	Pacientes sem DDVE por estresse (37)	Pacientes com DDVE por estresse (67)	Pacientes sem DDVD por estresse (22)	Pacientes com DDVD por estresse (82)
Parâmetros estruturais do VE
FEVE, %, Simpson	63,50(60-66)	60,00(57-65)*	65,00(60-66)	61,00 (67-65)*
Septo, mm	12,00(11-13)	12,00(11-13) *	12,00 (11-12,75)	12,00 (11-13)*
PW, mm	12,00(11,75-12)	12,00(11-13) *	12,00 (11,25-12,75)	12,00 (11-13)*
Parâmetros funcionais do VE em repouso
Razão E/A	0,79(0,75-0,85)	0,85 (0,76-1,20)*	0,78 (0,76-0,83)	0,84 (0,75-1,21,)*
Razão média E/e’	6,66 (6,25-8,33)	6,97 (5,76-8,15)*	6,96 (6,27-8,33)	6,66 (5,63-8,1)*
Parâmetros funcionais do VE após o teste de esforço
Razão E/A	1,25(0,8-1,5)	ǂ1,73 (1,55-2,00)*	1,22 (0,88-1,37)	ǂǂ1,71 (1,5-2,00)*
Razão média E/e’	8,07 (6,7-9,6)	ǂ17,33 (15,71-8,46)*	8,12 (7,25-10)	ǂǂ17,14 (14,66-18,39)*
Parâmetros estruturais do VD
IVAD, ml/m²	17,57 (16,07-19,97)	ǂ22,66 (21,31-24,13)*	16,55 (15,81-17,54)	ǂǂ22,27 (20,65-23,85)*
RWT, mm	5,00 (4,5-6,5)	ǂ6,50 (6-7)*	5,00 (4,12-5,00)	ǂǂ6,50 (6,00-7,00)*
TAPSE, mm	23,00 (22,00-26,00)	22,00 (21,00-23,00)*	23,00 (21,25-26,00)	22,00 (21-23,5)*
Parâmetros funcionais do VD em repouso
Razão E/A	0,83 (0,75-0,95)	0,69 (0,62-0,75)*	0,83 (0,76-1,16)	0,71 (0,66-0,83)*
Razão média E/e’	5,47 (4,56-5,69)	4,16(3,33-5,00)*	5,47 (4,56-5,69)	4,54(3,33-5,22)*
TA, msec	170 (163,75-180)	170(160-180)*	170 (165-180)	170(160-180)*
sPAP, mmHg	26,00 (25-28)	28,00 (25-30)*	25,00 (23-27)	28,00 (25-30)*
Parâmetros funcionais do VD após o teste de esforço
Razão E/A	1,26 (1,09-1,48)	1,31(1,18-1,49)*	1,28 (1,14-1,5)	1,37 (1,22-1,52)*
Razão média E/e’	6,21 (5,38-7,89)	10,83 (9,04-13,23)*	6,92 (5,46-8,00)	ǂǂ11,25 (9,00-13,33)*
TA, msec	165(155-175)	ǂ105(95-110)*	162,5(155-170)	ǂǂ110(95-115)*
sPAP, mmHg	32,00(30-33,25)	ǂ38,00 (36-42)*	32,00 (30-33,75)	ǂǂ 38,00 (35-40)*

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DDVE: disfunção diastólica do ventrículo esquerdo; DDVD: disfunção diastólica do ventrículo direito; FEVE: fração de ejeção do ventrículo esquerdo; IVAD: índice de volume do átrio direito; TAPSE: excursão sistólica do plano do anel tricúspide; ǂp <0,05 entre pacientes com e sem DDVE; PW: parede posterior; SPAP: pressão arterial pulmonar sistólica; EPVD: espessura da parede do ventrículo direito; TA: tempo de aceleração. ǂǂp <0,05 entre pacientes com e sem DDVD.

A capacidade de exercício foi reduzida em pacientes com DPOC com disfunção diastólica direita e esquerda induzida por estresse, em comparação com pacientes sem (Tabela 1). Os pacientes DPOC-DDVD/DDVE alcançaram carga mais baixa, VO₂ e pulso de O₂ mais baixos. Tiveram um desempenho com inclinações de VM/VCO₂ significativamente maiores (Tabela 1). Nenhum dos parâmetros TCPE foi associado à razão E/e’ esquerda ou direita induzida por estresse (Tabela 3.)

Tabela 3. – Análise de correlação entre os parâmetros de teste de exercício respiratório e cardiopulmonar com a razão E/e’ induzida por estresse para ventrículo esquerdo/ventrículo direito, respectivamente.

Parâmetros	DDVE		DDVD
Parâmetros	Spearman rho	valor de p	Spearman rho	valor de p
Pico de carga, W	0,02	0,84	0,03	0,78
Pico de VM, l/min	0,02	0,85	0,12	0,28
Pico de VO₂, ml/min/kg	0,12	0,56	0,03	0,73
RTR	0,06	0,74	0,12	0,27
Pico de pulso de O₂ ml/min/kg	0,10	0,60	0,11	0,32
Pico de inclinação VM/VCO₂	0,35	0,07	0,02	0,80
CVF, l/min	0,28	0,11	0,10	0,34
FEV₁, l/min	0,01	0,95	0,04	0,71

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Teste U de Mann-Whitney; † Abreviaturas: DDVE: disfunção diastólica do ventrículo esquerdo; DDVD: disfunção diastólica do ventrículo direito; CVF: capacidade vital forçada; RTR: razão de troca respiratória; ǂp<0,05 entre pacientes com e sem DDVE; VM/VCO_2: eficiência ventilatória; ǂǂp<0,05 entre pacientes com e sem DDVD

Discussão

Nossos principais achados foram: 1) 64% dos pacientes com DPOC não grave e dispneia aos esforços que estão livres de doença cardiovascular clinicamente evidente têm DDVE induzida por estresse; 1) 78% do mesmo grupo de pacientes têm DDVD induzida por estresse; 3) nenhum dos parâmetros TCPE foi correlacionado com a razão E/e’ induzida por estresse no ventrículo esquerdo ou direito. Até onde sabemos, este é o primeiro estudo usando a combinação EES-TCPE em pacientes com DPOC não grave, dispneia aos esforços e livres de doenças cardiovasculares evidentes. Aumento da razão E/e’ induzida por estresse >15 do ventrículo esquerdo foi detectado em 64% deles; elevação induzida por estresse da razão E/e’ >6 no ventrículo direito foi encontrada em 78% dos casos. Não podemos comparar nossos dados com outros estudos de populações de pacientes com DPOC não grave porque a maioria deles relata a incidência de disfunção diastólica em repouso.^15-17

Nedeljkovic et al. realizaram EES em uma população de 87 pacientes hipertensos com dispneia aos esforços e função ventricular esquerda normal. Reportaram, em 9,2% dos pacientes, razão por estresse E/e’ >15.¹⁸ Kaiser et al. também investigaram uma população geral de 87 pacientes com dispneia aos esforços e relataram disfunção diastólica em 9% deles.¹⁹

A maior prevalência de disfunção diastólica de estresse que descrevemos em pacientes com DPOC confirma que a própria DPOC é um fator de risco cardiovascular.^20,21 Rigidez arterial é uma característica da DPOC, independentemente do impacto do tabagismo. O estresse da parede ventricular observado durante a respiração também é relatado como um mecanismo fisiopatológico independente para a remodelação do VE em pacientes com DPOC leve sem patologia cardiovascular evidente.²² Tanto a rigidez arterial quanto o estresse da parede ventricular causam fibrose ventricular difusa em pacientes com DPOC livres de doenças cardiovasculares.^23,24

Em nosso estudo, pacientes com disfunção diastólica induzida por estresse (ambos DDVE e DDVD) atingem carga, VO₂ e pulso de O₂ mais baixos e apresentam desempenho em inclinações de VM/VCO₂ significativamente maiores. Nenhum dos parâmetros TCPE, no entanto, se correlaciona com a razão de estresse E/e’ (nem no VE nem no VD). Esses achados são semelhantes aos relatados na população em geral. Nedeljkovic et al. detectaram menor carga, menor consumo de oxigênio e menor eficiência ventilatória em pacientes hipertensos com dispneia aos esforços e DDVE induzida por estresse.¹⁸ Kaiser et al. descreveram aumento da reserva de frequência cardíaca e redução do pulso de oxigênio em uma população geral de pacientes com dispneia aos esforços.¹⁹ Guazzi et al. também estabeleceram uma associação entre disfunção diastólica (razão E/e’) e consumo ao pico de oxigênio, eficiência ventilatória e recuperação da frequência cardíaca.²⁵ No grupo de pacientes com patologia cardiovascular evidente e ecocardiografia normal em repouso de Guazzi, a eficiência ventilatória se correlacionou melhor com o pico da razão E/e’ >15. A vantagem clínica da relação VM/VCO₂ como melhor preditor da razão por estresse E/e’ também foi confirmada nos pacientes com insuficiência cardíaca diastólica analisados por Nedeljkovic et al.¹⁸ Kaiser et al. não apoiam tais conclusões, enfatizando a importância do aumento da reserva da frequência cardíaca e da diminuição no pulso de oxigênio como preditores da razão por estresse E/e’ na população geral de pacientes com dispneia aos esforços e livres de doença cardiovascular evidente.¹⁹

Parece que os parâmetros TCPE podem ajudar no diagnóstico diferencial de dispneia na população em geral, bem como em pacientes com patologia cardiovascular diagnosticada.^6-9 De acordo com nossos resultados, em pacientes com DPOC, esses não são parâmetros clínicos confiáveis que podem servir como preditores independentes de anormalidade cardiovascular e, portanto, não são aplicáveis no algoritmo de diagnóstico de disfunção diastólica mascarada.

Nossos achados corroboram a presença de comprometimento funcional em pacientes com DPOC não grave com dispneia aos esforços e livres de doença cardiovascular evidente. O Doppler tecidual durante o exercício mostra a complexa interação coração-pulmão e as alterações induzidas pelo esforço, que aumentam os comprometimentos funcionais cardíacos que podem não ser evidentes em repouso. Nossos achados apoiam as recomendações atuais de EES-TCPE como uma ferramenta para detecção precoce de ICFEP.⁶ Como nenhum dos parâmetros do teste de esforço cardiopulmonar provou ser preditivo de DDVE/DDVD induzida por estresse, a ecocardiografia de estresse tem grande relevância clínica para um diagnóstico preciso de patologia cardíaca e respiratória em pacientes com DPOC não graves e dispneia aos esforços.

Limitações do estudo

O estudo teve as seguintes limitações: 1) tamanho de amostra relativamente pequeno; 2) falta de pletismografia corporal e medida da capacidade de difusão, que são informativos para uma avaliação adequada da dispneia; 3) pacientes com DPOC apresentam oscilações de pressão aumentada durante o ciclo respiratório, e a medição foi realizada ao final da expiração, o que pode influenciar os resultados; 4) as medições foram feitas no início do período de recuperação (aproximadamente dois minutos) após o exercício limitado por sintomas. A linha do tempo das mudanças das pressões pulmonar e intratorácica durante o breve intervalo entre o pico do exercício e sua medida no início da recuperação não é bem conhecida e poderia, portanto, ser subestimada.

Conclusão

Há uma alta prevalência de disfunção diastólica induzida por estresse em pacientes com DPOC não grave com dispneia aos esforços, sem doença cardiovascular evidente. Nenhum dos parâmetros do TCPE se correlaciona com a razão E/e’ induzida por estresse. Portanto, a realização do EES-TCPE é necessária para a detecção precoce e o manejo adequado da ICFEP mascarada nesta população.

Vinculação acadêmica

Não há vinculação deste estudo a programas de pós-graduação.

Fontes de financiamento.O presente estudo não teve fontes de financiamento externas.

Referências

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Arq Bras Cardiol. 2021 Feb 19;116(2):259–265. [Article in English]

The Role of Stress Echocardiography in the Early Detection of Diastolic Dysfunction in Non-Severe Chronic Obstructive Pulmonary Disease Patients

Zheyna Cherneva ¹, Radostina Cherneva ²

Abstract

Background

Exertional dyspnea is a common complaint of patients with heart failure with preserved ejection fraction (HFpEF) and chronic obstructive pulmonary disease (COPD). HFpEF is common in COPD and is an independent risk factor for disease progression and exacerbation. Early detection, therefore, has great clinical relevance.

Objectives

The aim of the study is to detect the frequency of masked HFpEF in non-severe COPD patients with exertional dyspnea, free of overt cardiovascular disease, and to analyze the correlation between masked HFpEF and the cardiopulmonary exercise testing (CPET) parameters.

Methods

We applied the CPET in 104 non-severe COPD patients with exertional dyspnea, free of overt cardiovascular disease. Echocardiography was performed before and at peak CPET. Cut-off values for stress-induced left and right ventricular diastolic dysfunction (LVDD/ RVDD) were E/e’>15; E/e’>6, respectively. Correlation analysis was done between CPET parameters and stress E/e’. A p-value <0.05 was considered significant.

Results

64% of the patients had stress-induced LVDD; 78% had stress-induced RVDD. Both groups with stress LVDD and RVDD achieved lower load, lower V’O₂ and O₂-pulse, besides showing reduced ventilatory efficiency (higher VE/VCO₂ slopes). None of the CPET parameters were correlated to stress-induced left or right E/e’.

Conclusion

There is a high prevalence of stress-induced diastolic dysfunction in non-severe COPD patients with exertional dyspnea, free of overt cardiovascular disease. None of the CPET parameters correlates to stress-induced E/e’. This demands the performance of Exercise stress echocardiography (ESE) and CPET for the early detection and proper management of masked HFpEF in this population. (Arq Bras Cardiol. 2021; 116(2):259-265)

Keywords: Echocardiography,Stress/methods; Heart Failure,Diastolic; Stroke Volume; Pulmonary Disease,Chronic Obstructive; Respiratory Funstion Tests

Introduction

Cardiovascular abnormalities are common in chronic obstructive pulmonary disease (COPD).^1,2 Arterial stiffness is present even in mild COPD patients free of cardiovascular diseases. It is an independent cardiovascular risk factor that contributes for the development of diastolic dysfunction.³ Dyspnea and exercise intolerance are common symptoms for both COPD and diastolic dysfunction.⁴ Recent studies with large patient cohorts have identified a cardiovascular phenotype in COPD patients who present with a different clinical course and prognosis.⁵ Early diagnosis and management is, therefore, very important from the clinical point of view.

Cardiopulmonary exercise testing (CPET) may distinguish cardiac and respiratory dyspnea or diminished physical activity.^6-9 The combination of exercise stress-echocardiography (ESE) and CPET is a reliable approach to identify patients with masked heart failure with preserved ejection fraction (HFpEF). Moreover, the results from invasive measurements are comparable to data obtained with non-invasive studies during ESE.¹⁰

The aims of our study were: 1) to detect the frequency of subclinical left ventricular (LV) and right ventricular (RV) diastolic dysfunction in non-severe COPD patients free of cardiovascular disease; 2) to establish a correlation between cardiopulmonary exercise and echocardiographic parameters for diastolic dysfunction (E/e^’).

Materials and Methods

Patients and Study Protocol

This was a retrospective study conducted with 224 clinically stable outpatients diagnosed with COPD at the University Hospital for Respiratory Diseases “St. Sophia”, Sofia. Only 163 of them met the inclusion criteria for non-severe COPD – forced expiratory volume in the first second higher than 50% (FEV₁>50%). All subjects had exertional dyspnea, but a total of 104 patients (64 men, 40 women; mean age of 62.9±7.5 years) were considered eligible, assuming the exclusion criteria. The recruitment period was between May 2017 and April 2018, and was approved by the local Ethics Committee (protocol 5/12.03.2018). All participants signed the informed consent form before the study initiation.

The following exclusion criteria were considered: 1) left ventricular ejection fraction (LVEF) <50%; 2) left ventricular diastolic dysfunction at rest higher than first grade; 3) echocardiographic findings suggesting pulmonary hypertension (systolic pulmonary arterial pressure >36 mmHg, tricuspid regurgitation (TR) jet maximum velocity >2.8 m/s; 4) valvular heart disease; 5) documented cardiomyopathy; 6) severe uncontrolled hypertension (systolic blood pressure >180 mmHg and diastolic blood pressure >90 mmHg); 7) atrial fibrillation or malignant ventricular arrhythmia; 8) ischemic heart disease; 9) anemia; 10) diabetes mellitus; 11) cancer; 12) chronic kidney disease (CKD); 13) recent chest or abdominal surgery; 14) recent exacerbation (over the last three months); 15) recent change (over the last three months) in medical therapy.

Procedures

Pulmonary Function Testing

All subjects underwent preliminary clinical examination including chest X-ray, spirometry, electrocardiography, echocardiography. Patients eligible for the study performed spirometry and an exercise stress test. They were performed on Vyntus, Cardiopulmonary exercise testing (Carefusion, Germany), in accordance with the European Respiratory Society (ERS) guidelines.¹¹Only patients with mild to moderate airway obstruction (FEV1 >50%) were selected.

Stress Test Protocol – Cardiopulmonary exercise testing (CPET)

A continuous ramp protocol was applied according to guidelines.⁶ After two minutes of unloaded pedaling (rest phase 0W), a three-minute warm-up phase (20W) followed. The test phase included 20W/2min load increments. Patients were instructed to pedal with 60 rotations per minute.

Expiratory gases were collected on a breath-by-breath basis. Peak VO₂ was expressed as the highest 30-second average value, obtained during the last stage of the exercise test. The peak values of VO₂ are expressed as -O₂ ml/kg/min. Ventilatory efficiency (VE/VCO₂) was measured by the V-slope method. Peak respiratory exchange ratio (pRER) was the highest 30-second value averaged in the last stage of the test. RER >1.10 at the end of the ESE-CPET test was considered as achievement of maximal effort.

Echocardiographic Methods

M-mode, two-dimensional and Doppler echocardiography were performed.^12,13 Apical four-chamber views were used to measure chamber volumes based on Simpson’s modified rule and LV ejection fraction was considered preserved if >50%. Doppler tissue echocardiography (DTE) analysis was performed in the septal-lateral dimension of mitral annulus, and lateral dimension of tricuspid annulus to assess myocardial systolic (S) and diastolic (E’, A’) waves of LV and RV. The E’ value was used as average of medial and lateral measurements. Peak E/e’ ratio >15 was considered a marker for stress-induced left ventricular diastolic dysfunction.

Right ventricular systolic function was assessed using tricuspid annular plane systolic excursion (TAPSE) and tissue Doppler S peak velocity. Right ventricular wall thickness (RVWT) was measured from the subcostal long-axis view at the tip of the anterior tricuspid leaflet in end-diastole. Pulmonary pressure was calculated directly by sampling the tricuspid insufficiency and indirectly by the acceleration time (AT) on pulmonary flow. Right atrium volume index (RAVI) was measured with the right ventricular end-systolic volume by the Simpson’s modified rule. Stress-induced RV diastolic dysfunction was considered if stress-induced E/e’ ratio >6. All parameters were measured at end-expiration and in triplicate during different heart cycles.¹⁴

Statistical Analysis

Demographic and clinical data were presented with descriptive statistics. The Kolmogorov-Smirnov test was used to explore the normality of distribution. Continuous variables in each group of subjects were expressed as median and interquartile range when data was not normally distributed and as mean ± standard deviation (SD) if normal distribution was observed. Categorical variables were presented as proportions. Data were compared between patients with and without LVDD, as well as between patients with and without RVDD. The unpaired Student’s t test was used to analyze normally distributed continuous variables. The Mann-Whitney-U test was used in other cases. Categorical variables were compared by the χ² test or the Fisher’s exact test. The Spearman’s rank correlation was used to assess the association between CPET parameters and stress-induced E/e’ ratio for the left and right ventricles.

In all cases, a p value of less than 0.05 was considered significant, as determined with SPSS® 13.0 Software (SPSS, Inc, Chicago, Ill) statistics.

Results

In the COPD group, 30% (32/104) of patients had grade I LVDD at rest; 14% (15/104) had grade I RVDD at rest and only 3% (4/104) had both RV and LVDD at rest. After CPET, the stress-echocardiography established that 64% (67/104) of the subjects had stress-induced LVDD, and 78% (82/104) had stress-induced RVDD. All patients with stress-induced LVDD also had stress-induced RVDD. The demographic and clinical data of patients are listed in Table 1. The echocardiographic parameters of patients are shown in Table 2. Except for RAVI, RVWT, acceleration time and systolic pulmonary arterial pressure after load, no other significant differences were found between patients with and without LVDD (Tables 1 and 2). The results for patients with and without RVDD were similar (Tables 1 and 2).

Table 1. – Anthropometric and cardiopulmonary characteristics of patients with and without LVDD and RVDD.

	Patients w/o stress LVDD (37)	Patients with stress LVDD (67)	Patients w/o stress RVDD (22)	Patients with stress RVDD (82)
Demographic data
Age, year	60.44 ± 7.72	64.16 ± 6.97*	6.95±7.36	63.74±7.60*
Male:Female gender, n	21:16	44:23^ǂ	14:8	50:32^ǂ
Packet, years	27.21 (23.87-31.76)	33.79 (30.51± 37.87)^†	26.52 (23.46-30.43)	32.11(28.82-36.13)^ǂ
Body mass index, kg/m²	27.00 (24.75-31.00)	27.96 (22.75-30.75)^†	28.00 (25.25-30.5)	26.52 (22.72-30.61)^†
Respiratory function
FVC, l/min	2.06 (1.76-3.09)	2.34 (1.77-3.09)^†	2.05 (2.11-3.73)	2.21 (1.71-2.93)^†
FEV₁, l/min	1.31 (0.94-1.53)	1.36 (1.14-1.75)^†	1.60 (1.15-2.42)	1.52 (1.14-1.75)^†
FEV₁/FVC %	60.5 (46.91-67.47)	53.30 (45.76-66.55)^†	65.50 (54.81-68.82)	62.59 (46.57-66.79)^†
Acid-base balance
pO₂, mmHg	68.60(63.4-71.8)	71.35 (64.7-74)^†	67.20 (63.56-71.68)	70.6 (63.2-74)^†
pCO₂, mmHg	32.30 (30.1-35.37)	37.65 (32.5-40)^†	34.73 (31.27-39.21)	35.7 (32.5-40)^†
Sat, %	94.9 (94.4-95.25)	95.00 (94.02-95.67)^†	94.75 (92.67-95.0)	95.00 (93.9-95.5)^†
CPET parameters
Peak Load, W	82.75 (69.8-89.1)	76.05 (68.4-92.1)^†	86.66 (78.65-94.76)	▪73.08 (68.93-83.16)^†
Peak VE, l/min	40 (34-52.5)	38.50 (32-48)^†	41.1 (32.12-48.17)	39.07 (31.89-48.32)^†
Peak V’O₂, ml/min/kg	14.30(12.6-16.15)	13.90 (12.67-15.7)^†	14.30 (12.6-16.15)	13.40(15.77-12.55)^†
RER	1.06 (0.98-1.19)	1.09 (1.00-1.28)^†	1.05 (0.98-1.18)	1.08 (1.01-1.19)^†
Peak O₂ pulse ml/min/kg	9.80 (9.5-12.2)	7.90 (6.15-9.32)^†	9.51 (9.02-13.1)	▪7.92(6.27-9.84)^†
Peak VE/VCO₂ slope	34.08 (33.98-36.72)	36.93 (34.19-38.74)^†	34.11 (33.78-36.89)	▪36.98 (34.26-38.91)^†

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*Unpaired t test; †Mann-Whitney U test; ǂchi-square test; §Abbreviations: LVDD: left ventricular diastolic dysfunction; RVDD: right ventricular diastolic dysfunction; O₂ pulse: oxygen pulse; FVC: forced vital capacity; VE: minute ventilation; RER: respiratory exchange ratio; V’O₂: oxygen consumption; VE/VCO₂ slope: ventilatory efficiency; ▪p<0.05 between patients with and without LVDD; ▪▪p<0.05 between patients with and without RVDD.

Table 2. – Echocardiographic parameters of patients with and without LVDD and RVDD.

	Patients w/o stress LVDD (37)	Patients with stress LVDD (67)	Patients w/o stress RVDD (22)	Patients with stress RVDD (82)
LV structural parameters
LVEF, %, Simpson	63.50(60-66)	60.00(57-65)*	65.00(60-66)	61.00 (67-65)*
Septum, mm	12.00(11-13)	12.00(11-13) *	12.00 (11-12.75)	12.00 (11-13)*
PW, mm	12.00(11.75-12)	12.00(11-13) *	12.00 (11.25-12.75)	12.00 (11-13)*
LV functional parameters at rest
E/A ratio	0.79(0.75-0.85)	0.85 (0.76-1.20)*	0.78 (0.76-0.83)	0.84 (0.75-1.21.)*
E/e’ aver ratio	6.66 (6.25-8.33)	6.97 (5.76-8.15)*	6.96 (6.27-8.33)	6.66 (5.63-8.1)*
LV functional parameters after exercise stress test
E/A ratio	1.25(0.8-1.5)	ǂ1.73 (1.55-2.00)*	1.22 (0.88-1.37)	ǂǂ1.71 (1.5-2.00)*
E/e’ aver	8.07 (6.7-9.6)	ǂ17.33 (15.71-8.46)*	8.12 (7.25-10)	ǂǂ17.14 (14.66-18.39)*
RV structural parameters
RAVI, ml/m²	17.57 (16.07-19.97)	ǂ22.66 (21.31-24.13)*	16.55 (15.81-17.54)	ǂǂ22.27 (20.65-23.85)*
RWT, mm	5.00 (4.5-6.5)	ǂ6.50 (6-7)*	5.00 (4.12-5.00)	ǂǂ6.50 (6.00-7.00)*
TAPSE,mm	23.00 (22.00-26.00)	22.00 (21.00-23.00)*	23.00 (21.25-26.00)	22.00 (21-23.5)*
RV functional parameters at rest
E/A ratio	0.83 (0.75-0.95)	0.69 (0.62-0.75)*	0.83 (0.76-1.16)	0.71 (0.66-0.83)*
E/e’ aver	5.47 (4.56-5.69)	4.16(3.33-5.00)*	5.47 (4.56-5.69)	4.54(3.33-5.22)*
AT, msec	170 (163.75-180)	170(160-180)*	170 (165-180)	170(160-180)*
sPAP, mmHg	26.00 (25-28)	28.00 (25-30)*	25.00 (23-27)	28.00 (25-30)*
RV functional parameters after exercise stress test
E/A ratio	1.26 (1.09-1.48)	1.31(1.18-1.49)*	1.28 (1.14-1.5)	1.37 (1.22-1.52)*
E/e’ aver	6.21 (5.38-7.89)	10.83 (9.04-13.23)*	6.92 (5.46-8.00)	ǂǂ11.25 (9.00-13.33)*
AT, msec	165(155-175)	ǂ105(95-110)*	162.5(155-170)	ǂǂ110(95-115)*
sPAP, mmHg	32.00(30-33.25)	ǂ38.00 (36-42)*	32.00 (30-33.75)	ǂǂ 38.00 (35-40)*

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*Mann-Whitney U test; LVDD: left ventricular diastolic dysfunction; RVDD: right ventricular diastolic dysfunction; LVEF: left ventricular ejection fraction; RAVI: Right atrium volume index; TAPSE: tricuspid annular plane systolic excursion; PW: posterior wall; SPAP: systolic pulmonary arterial pressure; RWT: right ventricular wall thickness; AT: accelaration time. ǂp<0.05 between patients with and without LVDD; ǂǂp<0.05 between patients with and without RVDD.

Exercise capacity was reduced in COPD patients with stress-induced right and left diastolic dysfunction, compared to those without it (Table 1). The COPD-RVDD/LVDD patients achieved lower load, lower VO₂ and O₂-pulse. They performed with significantly higher VE/VCO₂ slopes (Table 1). None of the CPET parameters was associated with stress-induced left or right E/e’ ratio (Table 3.)

Table 3. – Correlation analysis between respiratory and cardiopulmonary exercise testing parameters with stress-induced E/e’ ratio for the left ventricle/right ventricle, respectively.

Parameters	LVDD		RVDD
	Spearman rho	p-value	Spearman rho	p-value
Peak Load , W	0.02	0.84	0.03	0.78
Peak VE, l/min	0.02	0.85	0.12	0.28
PeakVO₂, ml/min/kg	0.12	0.56	0.03	0.73
RER	0.06	0.74	0.12	0.27
PeakO₂ pulse ml/min/kg	0.10	0.60	0.11	0.32
Peak VE/VCO₂ slope	0.35	0.07	0.02	0.80
FVC, l/min	0.28	0.11	0.10	0.34
FEV₁, l/min	0.01	0.95	0.04	0.71

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LVDD: left ventricular diastolic dysfunction; RVDD: right ventricular diastolic dysfunction; RER: respiratory exchange ratio; VO_2: oxygen consumption; VE/VCO₂ slope: ventilatory efficiency; FVC: forced vital capacity; VE: minute ventilation.

Discussion

Our main findings were: 1) 64% of the patients with non-severe COPD and exertional dyspnea who are free of clinically evident cardiovascular disease have stress-induced LVDD; 1) 78% of the same group of patients have stress-induced RVDD; 3) none of the CPET parameters was correlated with stress-induced E/e’ ratio either in the left or the right ventricle. To our knowledge, this is the first study using combined ESE-CPET in non-severe COPD patients with exertional dyspnea and free of overt cardiovascular diseases. Stress-induced increase of E/e’ ratio >15 of the left ventricle was detected in 64% of them; stress-induced elevation of E/e’ ratio >6 of the right ventricle was met in 78% of cases. We cannot compare our data to other studies of non-severe COPD patient populations because most of them report on the incidence of diastolic dysfunction at rest+^15-17

Nedeljkovic et al. performed ESE in a population of 87 hypertensive patients with exertional dyspnea and normal left ventricular function. They found in 9.2% of the patients a stress ratio E/e’ >15.¹⁸ Kaiser et al. also investigated a general population of 87 patients with exertional dyspnea and reported diastolic dysfunction in 9% of them.¹⁹

The higher prevalence of stress diastolic dysfunction that we describe in COPD patients confirms that COPD itself is a cardiovascular risk factor.^20,21Arterial stiffness is a feature of COPD, regardless of the smoking burden. The ventricular wall stress seen during respiration is also reported as an independent pathophysiological mechanism for LV remodeling in mild COPD patients without overt cardiovascular pathology.²² Both arterial stiffness and ventricular wall stress cause diffuse LV fibrosis in COPD patients free of cardiovascular diseases.^23,24

In our study, patients with stress-induced diastolic dysfunction (both LVDD and RVDD) achieve lower load, VO₂ and O₂-pulse and perform with significantly higher VE/VCO₂ slopes. None of the CPET parameters, however, correlates with stress E/e’ ratio (neither in LV nor RV). These findings are similar to what have been reported in the general population. Nedeljkovic et al. detected lower load, lower oxygen consumption and lower ventilatory efficiency in hypertensive patients with exertional dyspnea and stress-induced LVDD.¹⁸ Kaiser et al. described increased heart rate reserve and reduced oxygen pulse in a general population of patients with exertional dyspnea.¹⁹ Guazzi et al. also established an association between diastolic dysfunction (E/e’ ratio) and peak oxygen consumption, ventilatory efficiency and heart rate recovery.²⁵ In Guazzi’s group of patients with overt cardiovascular pathology and normal echocardiography at rest, ventilatory efficiency correlated best to peak E/e’ ratio>15. The clinical advantage of VE/VCO₂ ratio as the best predictor of stress E/e’ ratio was also confirmed in the diastolic heart failure patients analyzed by Nedeljkovic et al.¹⁸ Kaiser et al. do not support such conclusions, emphasizing the importance of the increased heart rate reserve and diminished oxygen pulse as predictors of stress E/e’ ratio in the general population of patients with exertional dyspnea and free of overt cardiovascular disease.¹⁹

It seems that the CPET parameters may help in the differential diagnosis of dyspnea in the general population, as well as in patients with diagnosed cardiovascular pathology.^6-9 According to our results, in COPD patients, these are not reliable clinical parameters that may serve as independent predictors for cardiovascular abnormality and, thus, are not applicable in the diagnostic algorithm of masked diastolic dysfunction.

Our findings support the presence of functional impairment in non-severe COPD patients with exertional dyspnea and free of overt cardiovascular disease. The performance of tissue Doppler imaging during exercise demonstrates the complex heart-lung interaction and the effort-induced changes, which increase cardiac functional impairments that may not be evident at rest. Our findings support the current recommendations for ESE-CPET as a tool for early detection of HFpEF.⁶As none of the cardiopulmonary exercise testing parameters proved to be predictive of stress-induced LVDD/RVDD, stress echocardiography has great clinical relevance for an accurate diagnosis of cardiac and respiratory pathology in non-severe COPD patients with exertional dyspnea.

Study limitations

The study had the following limitations: 1) relatively small sample size; 2) lack of body plethysmography and diffusion capacity measurement, which are informative for the proper assessment of dyspnea; 3) COPD patients experience enhanced pressure swings during the respiratory cycle, and the measurement was performed at the end of expiration, which may influence results; 4) measurements were made in early recovery period (approximately 2 min) after symptom-limited exercise. The timeline of changes of pulmonary and intrathoracic pressures during the brief interval between peak exercise and their measurement in early recovery is not well known and it could, therefore, be underestimated.

Conclusion

There is a high prevalence of stress-induced diastolic dysfunction in non-severe COPD patients with exertional dyspnea, free of overt cardiovascular disease. None of the CPET parameters correlates with the stress-induced E/e’ ratio. Therefore, the performance of ESE-CPET is needed for the early detection and proper management of masked HFpEF in this population.

Study Association

This study is not associated with any thesis or dissertation work.

Sources of Funding.There were no external funding sources for this study.

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PERMALINK

O Papel da Ecocardiografia sob Estresse na Detecção Precoce de Disfunção Diastólica em Pacientes com Doença Pulmonar Obstrutiva Crônica Não Grave

Zheyna Cherneva

Radostina Cherneva

Resumo

Fundamento

Objetivos

Métodos

Resultados

Conclusão

Introdução

Materiais e métodos

Pacientes e protocolo de estudo

Procedimentos

Teste de função pulmonar

Protocolo de teste de estresse – teste cardiopulmonar de exercício (TCPE)

Métodos ecocardiográficos

Análise estatística

Resultados

Tabela 1. – Características antropométricas e cardiopulmonares de pacientes com e sem DDVE e DDVD.

Tabela 2. – Parâmetros ecocardiográficos de pacientes com e sem DDVE e DDVD.

Tabela 3. – Análise de correlação entre os parâmetros de teste de exercício respiratório e cardiopulmonar com a razão E/e’ induzida por estresse para ventrículo esquerdo/ventrículo direito, respectivamente.

Discussão

Limitações do estudo

Conclusão

Referências

The Role of Stress Echocardiography in the Early Detection of Diastolic Dysfunction in Non-Severe Chronic Obstructive Pulmonary Disease Patients

Zheyna Cherneva

Radostina Cherneva

Abstract

Background

Objectives

Methods

Results

Conclusion

Introduction

Materials and Methods

Patients and Study Protocol

Procedures

Pulmonary Function Testing

Stress Test Protocol – Cardiopulmonary exercise testing (CPET)

Echocardiographic Methods

Statistical Analysis

Results

Table 1. – Anthropometric and cardiopulmonary characteristics of patients with and without LVDD and RVDD.

Table 2. – Echocardiographic parameters of patients with and without LVDD and RVDD.

Table 3. – Correlation analysis between respiratory and cardiopulmonary exercise testing parameters with stress-induced E/e’ ratio for the left ventricle/right ventricle, respectively.

Discussion

Study limitations

Conclusion

ACTIONS

PERMALINK

RESOURCES

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