Echocardiography in chronic liver disease: systematic review

Abstracts

FUNDAMENTO: O ecoDopplecardiograma (Eco) tem-se firmado como método não invasivo de excelente acurácia no rastreio de hipertensão portopulmonar (HPP) e pesquisa dos shunts intrapulmonares (SIP) na doença hepática crônica (DHC). Nesta última década, concretizou-se o Eco como de fundamental importância no diagnóstico da cardiomiopatia cirrótica (CMC). OBJETIVO: Realizar uma revisão sistemática envolvendo artigos relevantes sobre a temática: o Eco na DHC. MÉTODOS: Em novembro de 2011, realizou-se uma revisão sistemática a partir das bases de dados da Pubmed, LILACS e SciELO, sendo relatadas as características dos estudos selecionados. RESULTADOS: Foram encontrados 204 artigos a partir da busca de descritores e um termo livre, sendo 179 da Pubmed, 21 da LILACS e 01 da SciELO. Destes, foram selecionados 22 artigos para revisão sistemática, não sendo possível, pois, fazer uma meta-análise devido à heterogeneidade dos mesmos. CONCLUSÃO: O Eco deve fazer parte da estratificação da DHC para o rastreio de HPP, SIP e da CMC, já que a maioria das vezes, o diagnóstico dessas complicações ocorre nos pacientes na fila de transplante hepático.

Ecocardiografia Doppler; Hepatopatias; Síndrome Hepatopulmonar; Esquistossomose; Hipertensão Portal

Hospital das Clínicas da Universidade Federal de Pernambuco, Recife, PE - Brasil

Mailing Address

ABSTRACT

BACKGROUND: Doppler echocardiography (Echo) is a non-invasive method of excellent accuracy to screen portopulmonary hypertension (PPH) and to assess intrapulmonary shunts (IPS) in chronic liver disease (CLD). In the past decade, Echo proved to play a fundamental role in the diagnosis of cirrhotic cardiomyopathy (CCM).

OBJECTIVE: To perform a systematic review of relevant articles on the subject 'Echo in CLD'.

METHODS: In November 2011, a systematic review was performed in the PubMed, LILACS and SciELO databases, and the characteristics of the studies selected were reported.

RESULTS: The search based on descriptors and free terms obtained 204 articles (179 in Pubmed, 21 in LILACS, and 1 in SciELO). Of those 204 articles, 22 were selected for systematic review. A meta-analysis could not be performed because of the heterogeneity of the articles.

CONCLUSIONS: Echo should be part of CLD stratification for screening PPH, IPS and CCM, because, most of the time, such complications are diagnosed only when patients are already waiting for a liver transplant.

Keywords: Echocardiography, Doppler; Liver Diseases; Hepatopulmonary Syndrome; Schistosomiasis.

Introduction

Chronic liver disease (CLD) has high incidence and prevalence worldwide¹. Among its major causes, chronic and excessive alcohol consumption and viral hepatites stand out¹. Since 1977, echocardiographic findings in patients with CLD have been studied². However, the association between liver disease and the cardiovascular system has been described for more than 50 years³. The relationship between CLD and the cardiovascular system has been defined as cirrhotic cardiomyopathy (CCM)^3,4. The impairment of the respiratory system by CLD has been called hepatopulmonary syndrome⁵.

Liver function deterioration is marked by the increase in nitric oxide and other inflammatory mediators, which have been implicated in splanchnic vasodilation and reduced arterial compliance, acting in the physiopathogeny of CCM and hepatopulmonary syndrome^3-5. Zardi et al³ and Moller et al⁴ have defined CCM as a chronic cardiac dysfunction in patients with liver cirrhosis and/or portal hypertension, characterized by a sudden decrease in the cardiac contractile response to physical, pathological or pharmacological stress, but with normal cardiac output at rest. The hepatopulmonary syndrome, however, is characterized as a triad consisting of CLD, alveolar-arterial oxygen gradient (A-aO2 gradient) > 15 mm Hg or arterial oxygen partial pressure (PaO2) < 80 mm Hg, and presence of intrapulmonary shunt (IPS)^5-13.

Updating that subject might help health professionals with the early diagnosis and treatment of cardiopulmonary complications in patients with CLD. This systematic review was aimed at assessing articles on the echocardiographic changes in patients with CLD.

Methods

Research strategy

This systematic review of the literature was elaborated in November 2011 from the following databases: Medical Literature Analysis and Retrieval System Online (MedLine); Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS); and Scientific Electronic Library Online (SciELO). The research strategy consisted in crossing descriptors (DeCS), which are keywords for retrieving a subject in the scientific literature, and free terms (FT), which are found among neither the DeCS nor the MeSH headings, but are important to search data on the subject.

In Pubmed, the syntax used in the search was as follows: "echocardiography" (MeSH) AND "cirrhotic cadiomyopathy" (free term); "echocardiography" (MeSH) AND "schistosomiasis" (MeSH); "echocardiography" (MeSH) AND "hepatopulmonary syndrome" (MeSH); "echocardiography" (MeSH) AND "portal hypertension" (MeSH). In LILACS and SciELO, the following keywords were used: "ecocardiografia"; "cardiomiopatia cirrótica"; "esquistossomose"; "síndrome hepatopulmonar"; and "hipertensão portal".

Selecting criteria

The inclusion criteria for the studies obtained from the search in the databases were as follows: to be original articles (editorials and case study were excluded); the study subjects had to have CLD; the study should approach the cardiac function changes in that population by using Doppler echocardiography; the study should be published in Portuguese, English and Spanish. Studies not referring to the echocardiographic changes of CLD in their titles were excluded.

Data analysis

The articles obtained from the search in the different databases were selected in three steps. In the first step, the titles of the studies found were read. Those that did not meet the inclusion criteria of this study were excluded. In the second step, the abstracts of the articles selected in the first step were read. Again, those not meeting the inclusion criteria were excluded. In the third step, the full text of all studies selected in the two previous steps were read to be included in this systematic review.

In the MedLine database, via PubMed, the keywords and free terms were crossed, and 204 articles were obtained, 120 of which were excluded based on their titles, 84 abstracts were read, and 32 articles were selected to be fully read. Of those 32 articles, 22 were chosen for this systematic review (Figure 1).

In the SciELO and LILACS databases, 22 articles were found, and all of them were excluded from this review based on their titles.

One single article was excluded because it was written in German, and seven articles were repeated (Figure 1).

Results

General characteristics of the studies included (Table 1).

It became evident that the 'echocardiography in CLD' research line was divided into the three following study areas: portopulmonary hypertension; hepatopulmonary syndrome; and CCM (in which, diastolic dysfunction assessment stands out). It was also evidenced that the production of manuscripts was intensified in the 1990s and first decade of the 21^st century.

The geographic distribution of the publications was predominantly European (40%), mainly Italian and Spanish studies. The American Continent appears as second (22%), with Brazil standing out as the number one producer of articles on the topic (18%). There was only one multicenter study¹⁴.

Twenty-one articles were observation studies. There was only one cohort study¹⁴. The mean sample size was 50 patients. The article¹⁵ with the smallest sample had 15 participants and that with the largest sample had 130 participants¹⁶. In all studies but one⁷, the male sex predominated. The mean age of the individuals in the studies included was approximately 50 years. Only two studies^13,17 had children in their samples. Only one study¹⁵ had no control group, and only two studies^13,18 had patients with schistosomiasis and no other CLD associated. The samples of the remaining studies comprised cirrhotic patients.

The prevalence of IPS ranged from 15% to 82%^16,19. Contrast-enhanced transthoracic echocardiography (CE-TTE) showed sensitivity of 75% and specificity of 100% for detecting IPS as compared with contrast-enhanced transesophageal echocardiography (CE-TEE)⁶.

It is worth noting that, in all studies^17,18,20-23 assessing concomitantly portopulmonary hypertension and right ventricular (RV) echocardiographic parameters, the catheterization of right cardiac chambers proved to have higher diagnostic accuracy than transthoracic echocardiography. In addition, there was enlargement of the right cardiac chambers and/or RV dysfunction as compared to the control group. The prevalence of portopulmonary hypertension ranged from 4% to 15%^21,23. The transthoracic echocardiography showed sensitivity of 100% and specificity of 80% to detect portopulmonary hypertension as compared with the catheterization of right cardiac chambers²³.

Chronology of the studies

Studies from the 1980s

The first studies on the echocardiographic assessment of CLD were published in the 1980s, although one study of 1977², which did not share the strategy of this review, used echocardiography to assess cardiovascular abnormalities in cirrhotic patients. The first article meeting our research criteria was published in 1984¹⁵, being followed by two other articles in the same decade. A ten-year period followed with no article on that topic being published.

The publications in the 1980s^15,19 focused on the occurrence of IPS in patients with CLD. Sanno et al¹⁵, in 1984, assessed the presence of IPS by use of CE-TTE. In 1988, Mimidis et al¹⁹, comparing the diagnostic accuracy of CE-TTE with that of lung perfusion scan with technetium^99m macro aggregated albumin (Tc^99mMAA), showed the diagnostic superiority of CE-TTE. At the end of that decade, Keller et al²⁴ collected left ventricular (LV) parameters, and findings suggestive of CCM began to be elucidated: the increase in the LV end-diastolic and end-systolic volumes after intrahepatic portosystemic shunt²⁴.

Studies from the 1990s

The studies from the 1990s^9,10 focused on comparing CE-TTE and CE-TEE in the diagnosis of IPS. In 1997, Vedrinne et al⁹ had no significant sample to compare those methods. In 1999, Aller et al¹⁰ showed the better diagnostic accuracy of CE-TEE, and also correlated lower degrees of IPS with lower hypercapnia and diffusion capacity of carbon monoxide.

Studies from the 21st century

In the beginning of the 21st century, the trend toward studying portopulmonary hypertension and RV parameters appears²². In 2000, Auletta et al²², assessing 83 patients, showed the high prevalence of portopulmonary hypertension (20%) and LV diastolic dysfunction, in addition to larger diameters of the right atrium and right ventricle in patients with advanced CLD as compared with a group without portopulmonary hypertension and a control group. As a limitation, that was the only study investigating portopulmonary hypertension that has not compared transthoracic echocardiography with right cardiac chamber catheterization, considered the gold-standard test for diagnosing portopulmonary hypertension. From that study onward, the aim of the articles alternated as follows: assessment of portopulmonary hypertension^{17,20,21,23,25} and the diagnostic comparison of transthoracic echocardiography with right cardiac chamber catheterization^20,21,23; IPS screening^{6,7,11-13,16,26}; comparison of the diagnostic accuracy of CE-TTE and CE-TEE for assessing IPS^6,12; comparison of the diagnostic sensitivity between echocardiography and Tc^99mMAA for assessing IPS^13,19,26; and diastolic function assessment of both the right and left ventricles^{7,11,14,17,25,27,28}. Only one study²⁸ has reported the use of dobutamine stress echocardiography, while another²⁵ has assessed the mean variation of LV strain. It is worth noting that some studies^{11,14,16,20,21,23,25-28} have assessed the correlation between diagnostic methods and the CLD severity criteria, specially the Child-Pugh-Turcotte score and the Model for End-Stage Liver Disease.

Studies assessing IPS were resumed in 2004, after five years with no article on the subject. Kim et al, in a cross-sectional study with 130 patients¹⁶, have reported that 82% had IPS on CE-TTE. The severity of the IPS correlated with the Child-Pugh-Turcotte score. Similarly to the end of the 1990s, two other articles^6,12 published in Brazil confirmed the diagnostic superiority of CE-TEE over CE-TTE, although Pavarino et al, in 2004, reported similar efficacy of CE-TTE and CE-TEE.

In addition, in 2007, in a cross-sectional study with 41 patients with hepatopulmonary syndrome, Zamirian et al⁷ described the increase in left atrial volume as a predictor of that syndrome⁷. In 2008, Lenci et al¹¹ also correlated the most severe shunts with hypoxemia, and associated IPS severity with a higher severity of liver decompensation by use of the Child-Pugh-Turcotte classification. Another important finding of that study was that the increase in IPS severity in the vertical position was not statistically greater than that in the supine position.

In 2010, El-Shabraw et al¹³, investigating the IPS, compared CE-TTE and Tc^99mMAA¹³. Conducted in children and unlike the two previous studies^19,29, it showed a higher prevalence of IPS in patients undergoing Tc^99mMAA as compared with CE-TTE. In that same year, Fischer et al¹², using CE-TEE, reported a greater A-aO2 in patients with IPS.

In 2005, Pozzi et al²⁷ resumed the articles directed to CCM. Their study with 100 patients evidenced the presence of eccentric LV hypertrophy and of diastolic dysfunction more evident in patients with hepatitis C virus cirrhosis classified as Child-Pugh-Turcotte A than in patients with hepatitis B virus and those of the control group.

In 2010, Rabie et al¹⁴, studying 101 patients, the only cohort of this review, reported that mild diastolic dysfunction predicted low ascites clearance and mortality after percutaneous intrahepatic portosystemic stent shunt insertion. In that same year, Kim et al²⁸ re-stated that cirrhotic patients abstaining from alcohol for six months, when undergoing stress echocardiography, showed more diastolic dysfunction, low prevalence of coronary artery disease, decrease in the ejection fraction, and increase in LV diastolic and systolic volumes than the control group. The last article on CCM, published in 2011 by Kazankov et al²⁵, innovated by assessing the reduction in mean strain rate of all cirrhotic patients.

Discussion

This is a systematic review about echocardiography in CLD. A meta-analysis could not be performed, because of the elevated heterogeneity and inconsistency of information of the studies here reviewed. There was neither analysis of the selection of the research subjects, nor report on the calculation of the sample size, nor whether it involved convenience sampling.

Other data not found in most studies reviewed were as follows: CLD severity; patients' clinical, social, and demographic characteristics; and time elapsed between the CLD diagnosis and the time the study was performed. Only age group and sex seemed to be homogeneous properties. The greater prevalence of CLD in the age group of 40 to 70 years might result from the long course of that disease.

Most articles reported liver cirrhosis as the etiology of CLD. In such patients, there was a greater trend towards assessing diastolic function and comparing the diagnostic methods for IPS screening. It is worth noting that the studies with patients with CLD whose etiology was hepatosplenic schistosomiasis (HSS) tended to assess portopulmonary hypertension and the right ventricle. Only Brazil and Egypt have published studies with patients with HSS, probably because that disease is endemic in some regions of those countries^13,18. Some articles reviewed have reported that their patients had concomitant mixed liver disease^20-22,28 (Table 1).

It is worth noting that currently the diagnosis of CCM requires eliminating other causes of underlying heart disease (coronary artery disease, arterial hypertension, and heart valve disease) and of liver cirrhosis (some etiologies, such as iron overload and alcohol consumption), which have an impact on myocardial structure and function^3,4. It was only in 2010 that Kim et al²⁸ clearly considered that in a study. Most articles assessing CCM in this review have not excluded alcoholic patients.

Through our research and also out of our search strategy, we observed that echocardiography is the gold-standard test to diagnose SI³⁰ and CCM^3,4, and to screen portopulmonary hypertension³¹. Although it is a systematized, standardized, reliable, reproducible method of easy use to research those pathologies, there is still certain heterogeneity in the gradation and investigation methodology of IPS^{6,7,9-13,15,16,19,29}. However, from the practical viewpoint, those discrepancies do not change the presence of IPS. Nevertheless, the universal standardization of the IPS screening technique is required so that future meta-analyses can be performed on the subject. Such results indicate the need for more detailed studies in that population, considering the heterogeneity found. Thus, further investments in systematic methods and standardized tests are required.

Conclusion

From this review, we concluded that CCM is underdiagnosed in patients with CLD, because, most of the time, the diagnosis of CCM is only established in the terminal phases of CLD. The following diagnostic criteria for CCM have been established: diastolic dysfunction, mainly when assessed on tissue and pulsed Doppler echocardiography; and left atrial volume. When assessing systolic function, stress echocardiography and cardiac strain imaging have been poorly studied.

In the context of diagnosing IPS, contrast-enhanced echocardiography is currently considered gold standard. It is worth noting that, when CE-TTE is dubious or the acoustic window is unsatisfactory, CE-TEE is recommended.

Echocardiography should be part of the screening of patients with CLD, because patients with systolic and/or diastolic dysfunction and portopulmonary hypertension have higher morbidity and mortality. A better understanding of the echocardiographic findings, mainly cardiac strain imaging and 3D echocardiography, in patients with CLD will improve their management.

Acknowledgements

We thank Prof. Dr. Hilton Justino da Silva for his collaboration and valuable guidance in elaborating this article.

Co-researchers

Liana Gonçalves Macedo (PhD candidate in Tropical Medicine - UFPE), Mônica Moraes de Chaves Becker (head of the Echocardiography sector - UFPE), Edmundo Pessoa de Almeida Lopes (Adjunct professor - UFPE), Ana Lúcia Coutinho Domingues (Adjunct professor - UFPE).

Potential Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Sources of Funding

There were no external funding sources for this study.

Study Association

This article is part of the thesis of master submitted by Vítor Gomes Mota, from Centro de Ciências da Saúde - UFPE.

References

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Echocardiography in chronic liver disease: systematic review

Vitor Gomes Mota; Brivaldo Markman Filho

Publication Dates

• Publication in this collection
  22 Mar 2013
• Date of issue
  Apr 2013

History

• Received
  18 May 2012
• Accepted
  09 Oct 2012
• Reviewed
  03 Aug 2012