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ORIGINAL ARTICLE
Year : 2020  |  Volume : 23  |  Issue : 2  |  Page : 198-204

Pulmonary hypertension in patients with end stage renal disease undergoing hemodialysis


1 Department VII, Internal Medicine II, University of Medicine and Pharmacy Victor Babes; County Clinical Emergency Hospital Pius Brinzeu, Timisoara, Romania
2 County Clinical Emergency Hospital Pius Brinzeu, Timisoara, Romania
3 Department VII, Internal Medicine II, University of Medicine and Pharmacy Victor Babes, Timisoara, Romania

Date of Submission23-May-2019
Date of Acceptance15-Oct-2019
Date of Web Publication7-Feb-2020

Correspondence Address:
Dr. C Tudoran
Department VII, Internal Medicine II, University of Medicine and Pharmacy Victor Babes, Timisoara, Romania. County Clinical Emergency Hospital Pius Brinzeu, Timisoara
Romania
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_278_19

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   Abstract 


Background: Pulmonary hypertension (PH) is a serious cardiovascular complication in patients with end stage renal disease (ESRD) undergoing hemodialysis (HD) via arterio-venous fistulas (AVF). Aim: The aim of this study was to assess pulmonary vascular resistance (PVR), AVF flow volume (AVF-FV) and cardiac output (CO) and to highlight the impact of their augmentation, as well as of the duration of HD, on the occurrence of PH in patients with ESRD. Methods: Our study group consisted of 51 dialyzed patients, with ESRD, without history of PH. We determined by ultrasonography the systolic pulmonary arterial pressure (PAPs), the left ventricular ejection fraction (EF), the cardiac output (CO), PVR and AVF-FV. Results: We documented PH in 27 (52.94%) patients. All had elevated PVR, higher AVF-FV and CO comparing to patients without PH. They were undergoing HD for a longer period and had lower EF than those without PH. For all patients, we documented strong correlations between PAPs and PVR (r = 0.933, P < 0.001) and the duration of HD (r = 0.702, P < 0.001), but moderate ones with AVF-FV (r = 0.583, P < 0.001) and CO (r = 0.519, P < 0.001).Conclusion: In patients with ESRD undergoing HD, PH was a common finding being associated with increased PVR, a longer duration of HD and chronic glomerulonephritis as etiology for ESRD. The majority of patients with PH had altered left ventricular systolic function, predisposing them to an increased risk to develop heart failure.

Keywords: Arterio-venous fistula, end stage renal disease, hemodialysis, pulmonary hypertension, pulmonary vascular resistance


How to cite this article:
Tudoran M, Ciocarlie T, Mates A, Pescariu S A, AbuAwwad A, Tudoran C. Pulmonary hypertension in patients with end stage renal disease undergoing hemodialysis. Niger J Clin Pract 2020;23:198-204

How to cite this URL:
Tudoran M, Ciocarlie T, Mates A, Pescariu S A, AbuAwwad A, Tudoran C. Pulmonary hypertension in patients with end stage renal disease undergoing hemodialysis. Niger J Clin Pract [serial online] 2020 [cited 2020 Feb 20];23:198-204. Available from: http://www.njcponline.com/text.asp?2020/23/2/198/277857




   Introduction Top


< One of the most serious cardiovascular complication in patients with end stage renal disease (ESRD) undergoing hemodialysis (HD) is pulmonary hypertension (PH).[1] Using the World Health Organization (WHO) criteria, PH is defined by elevated pressures in the pulmonary artery (PAP) with mean values over 25 mmHg at rest (normal under 20 mmHg). This type of PH is assigned to group 5, with unclear and/or multifactorial mechanisms.[2],[3],[4] Its severity ranges from mild forms to clinically significant ones, that persist or even worsen over time, leading to right heart failure. Current data regarding the prevalence of PH in HD patients are conflicting presenting values ranging from 23%[5] to 56%[6] or even 58.9%.[7]

The pathophysiology of this type of PH is a debated topic in the medical literature.[8],[9] The first assumption was that it develops as a consequence of the chronically increased blood flow, related to the presence of arterio-venous fistulas (AVF), used as an access for HD. The increased venous return to the right ventricle (RV) determines an augmentation of the cardiac output (CO), inducing a “high output state”. In physiological conditions, pulmonary circulation is highly compliant and can accommodate this increased blood flow. Thereby, the occurrence of PH in patients with ESRD undergoing HD, assumes alterations of the pulmonary microvasculature induced by uremic conditions. Most important mechanisms are: a) chronic hypoxia due to anemia and abnormalities in the transport/diffusion of respiratory gases, b) vascular calcifications with thickening of pulmonary arteries, induced by alterations in calcium and phosphate metabolism, c) increased vascular tone of the pulmonary arterioles due to the impaired production of nitric oxide and the imbalance between vasodilator/vasoconstrictor mediators,[10] and d) dysfunctions of the respiratory muscles. All these factors are responsible for the occurrence of vasoconstriction and vasoproliferative processes, leading to an increased precapillary pulmonary vascular resistance (PVR), followed by the development of PH.[11]

Taking into account that the occurrence of PH in patients with ESRD undergoing HD may precipitate their evolution to irreversible heart failure and death, it is important to consider this complication and to evaluate them by means of echocardiography. This method offers the possibility to estimate left and RV function, pulmonary artery pressure (PAPs) and PVR accurately, without the risks of invasive procedures, like right heart catheterization.[12],[13]

The aim of this study is to document, by means of echocardiography, the factors which are mainly responsible for the development of PH in patients with ESRD: the elevated PVR or the increased blood flow through the AVF for a longer time period, as well as their relationship with PAPs values. A second aim is to document if PH is associated with the decline of the left ventricular (LV) systolic function.


   Methods Top


Study population

In our study, 51 patients with ESRD were included – 27 men and 24 women – aged between 39 and 65 years (mean age = 57.62 ± 6.61 years), undergoing HD in the Hemodialysis Department of our hospital and in an ambulatory Hemodialysis Center, over a period of 4 years (1 July 2014-30 June 2018).

The inclusion criteria were as follows: patients with ESRD due to a primary renal disease (chronic glomerulonephritis, polycystic kidney, nephrolithiasis, chronic pyelonephritis) undergoing HD for more than 6 months, with limits between 7-168 months, median 40 (15 to 57) according to patients' files.

Exclusion criteria: all patients with history of idiopathic PH or of other etiology, such as those with PH of group 1, patients with significant cardiovascular pathology leading to PH of group 2, the ones with respiratory diseases, causing PH of group 3 and those with history of pulmonary thromboembolism which could have PH group 4. To prevent the influence of other factors on the occurrence of group 5 PH, we excluded from our study all patients with hematological, systemic, metabolic or other diseases (excepting renal failure) that could induce this form of PH, those treated with vasodilators used to treat PH (prostacyclin analogues or endothelin receptor antagonists, phosphodiesterase type 5 inhibitors and guanylate cyclase stimulators) as well as, patients with ESRD representing a complication of primary hypertension or of diabetes mellitus, taking into account that this disease is associated with an increased cardiovascular morbidity.

The study was approved by the Ethics Committee of our hospital and all patients signed a written informed consent.

Methods

All patients with ESRD included in our study underwent regular HD on maintenance basis, via permanent AVF. This therapy was started for more than 6 months before the inclusion in the study. High-flux HD was performed with highly tissue-compatible membranes using a standard dialysis fluid, three times a week, in sessions of about 4-hour. All patients were carefully evaluated to identify signs of over-hydration and fluid retention, in order to preserve their optimal dry weight. Although 37 patients presented secondary hypertension, blood pressure values were controlled with drugs.

Cardiologic evaluation

All echocardiographic examinations were performed post dialysis, as soon as possible, when patients were at optimal dry weight, taking into account that several echocardiographic parameters are influenced by patients' hydration status.[14] Transthoracic echocardiography was performed with a Siemens ultrasound machine, by the same skilled echocardiographist, in order to avoid inter-observer differences. Three to five separate heartbeats were used to determine mean values. All echocardiographic data were determined based on the American Society of Echocardiography Guidelines.[15] Assessment of LV mass index (LVMI), ejection fraction (EF) determined by Simpson method, tricuspid annular plane systolic excursion (TAPSE), right atrial (RA), right ventricle (RV) size were determined in M-mode and 2-D echocardiography. Conventional Doppler echocardiography was used to assess CO (calculated by using stroke volume and heart rate), the velocity of the tricuspid regurgitation (TRV), to estimate PAPs (based on the peak TRV, taking into account the estimated RA pressure) and pulmonary vascular resistance (PVR) by dividing peak TRV to the tricuspid velocity integral.[12],[13],[16] We considered that PAPs values ≥ 35 mmHg at rest, measured by Doppler echocardiography, indicate PH[12],[13] with severity ranging from mild (35-45 mmHg), moderate (45-60 mmHg) to severe (over 60 mmHg).[16],[17] Echocardiographicaly estimated PVR has been shown to provide a reliable non-invasive estimation of PVR.[12],[13] A normal PVR is under 1.5 Wood Units (WU). In this study, we considered PVR of over 2 WU as elevated and over 3 WU as significant for the diagnosis of PH.[12],[13],[15]

Assessment of AVF flow volume (FV) in mL/min, was performed with the same equipment, with a 7 MHz linear probe, on a single longitudinal scan of the vessel, by using the cross-sectional area of the vessel (cm2) and the mean velocity (cm/s) measured in pulsed Doppler at the site used to determine the area.[18]

Data analysis

Data analysis was performed using SPSS v. 25.0 (Statistical Package for the Social Sciences, Chicago, IL, USA). Continuous variables were presented as mean and standard deviation (SD) or median and interquartile range (IQR), and categorical variables were presented as frequency and percentages. We performed descriptive and inferential statistics analysis to summarize the characteristics of the study population. The results of the normality test (Shapiro-Wilk) showed a non-Gaussian distribution, reason why we continued to use nonparametric tests. In order to highlight the prevailing etiopathogeny of PH, we analyzed the strength of a linear relationship between levels of PAPs and PVR, CO, AVF-FV and the duration of hemodialysis, by using the Spearman's rank-order correlation. To compare patients with/without PH, we used Mann–Whitney U test. To evaluate the distribution of PH in patients we applied the Chi-squared test (χ2). A multivariate linear regression model was built using the stepwise method and Akaike information criteria (AIC) were used to appreciate the best model, in order to evaluate the independent associates of PAPs quantity. Changes in PVR and the duration of HD, according to PAPs threshold, were examined by using the analysis of variance.

A P value of less than 0.05 was considered to indicate a statistically significant difference.


   Results Top


Referring to the etiology of ESRD in our study group, 29 patients (56.86%) had chronic glomerulonephritis, 9 (17.64%) chronic pyelonephritis, 7 (13.72%) polycystic kidney and 6 (9.83%) nephrolithiasis. 37 participants had secondary hypertension controlled with medication (angiotensin converting enzyme inhibitors in 16 patients; angiotensin receptor blockers in 6; beta-blockers in 18; calcium antagonists in 11 and diuretics in 9 patients) and 39 were treated with erythropoietin.

Our patients received HD via permanent AVF for 7 to 168 months, median 40 (15 to 57). The AVF flow volume (AVF-FV) varied between 800 to 1500 mL/min with a median of 1000 (950 – 1300) mL/min. As a general finding, the presence of AVF did not result in elevated CO, only 5 patients (9.8%) having values at the upper normal limit (8L). LV hypertrophy, expressed by LVMI levels, was a common finding among our patients, being determined in 90.19% of cases (46 subjects). Most of the patients had normal LV systolic function: EF was over 50% in 35 participants (68.62%), but 16 (31.37%) had values between 43% and 49%. This finding was more frequent in patients with increased PAPs, 13 of them (48.14%) having moderately reduced EF (P = 0.03). RV function, assessed by TAPSE, was within normal limits, although patients with increased PAPs had values closer to the lower normal limit. 27 patients (52.94%) had PAPs values of over 35 mmHg defining PH. 12 of them had pathological PVR levels of over 3 WU. The clinical characteristics and echocardiography data are presented in [Table 1] and the distribution of PAPs, AVF-FV, PVR and CO in [Figure 1].
Table 1: Clinical characteristics and results of echocardiography in study group

Click here to view
Figure 1: Distribution of PAPs, PVR, flow volume of AVF and duration of HD in patients with and without PH. PAPs = Estimated systolic pressure in the pulmonary artery, PVR = Pulmonary vascular resistance, WU = Wood units, AVF = Arterio-venous fistula, HD = Hemodyalisis; Mann-Whithney U Test between groups

Click here to view


The statistical analyze by using Spearman's test evidenced a strong correlation between PAPs levels and PVR values (r = 0.933, 95% CI = 0.860;0.967, P < 0.001) and with the duration of HD (r = 0.702, 95% CI = 0.420;0.93, P < 0.001), a moderate one with AVF-FV and CO values (r = 0.583, 95% CI = 0.314;0.781, respectively r = 0.519, 95% CI = 0.182;0.795, P < 0.001), [Figure 2]. No significant correlation between AVF flow and CO levels were documented.
Figure 2: Correlation between PAPs and PVR, flow volume of AVF, duration of HD and CO in study group. PAPs = Estimated systolic pressure in the pulmonary artery, PVR = Pulmonary vascular resistance, WU = Wood units, AVF = Arterio-venous fistula, HD = Hemodyalisis, CO = Cardiac output; Spearman?s rank-order correlation test

Click here to view


From the 27 participants (52.94%) diagnosed with PH, 16 were men and 11 women, aged between 43 and 65 years. The prevailing etiology for ESRD was chronic glomerulonephritis (21 patients - 77.77%). Median values of PAPs were 46 (42 to 55) mmHg. 8 patients (29.62%) had mild PH, 13 (48.14%) moderate forms and 6 (22.22%) presented severe PH. 24 patients (88.88%) had abnormal levels of PVR (over 2 WU) and 12 of them (44.44%) had pathological PVR (over 3 WU), defining PH. In these patients AVF-FV was higher, with a median of 1150 (1000-1410) mL/min, 3 patients having even a flow rate of 1500 mL/min and CO at the upper normal limit. The statistical analyze revealed strong correlations between PAPs values and PVR levels (r = 0.888, CI = 0.804-0.932, P < 0.001) and the duration of HD (r = 0.915, CI = 0.749-0.989, P < 0.001), but moderate ones with AVF-FV levels (r = 0.546, CI = 0.203-0.838, P = 0.003) and with CO (CO r = 0.404, CI = 0.089-0.874, P = 0.37). There was a moderate correlation between AVF-FV and CO (r = 0.481, CI = 0.081-0.794, P = 0.011).

The remaining 24 participants (47.05%) had PAPs values under 35 mmHg, being considered without PH. Most of them had lower AVF-FV levels, median 980 (892.5 to 1150) mL/min. The statistical analyze evidenced in these patients, moderate correlations between PAPs values and PVR (r = 0.527, CI = 0.160-0.806, P < 0.008) and CO levels (r = 0.404, CI = 0.056-0.804, P = 0.37), but not with AVF-FV values or with the duration of HD.

In multivariate linear regression analysis, after the addition of variables like the etiology of ESRD, hemodynamic parameters (systolic and diastolic pressures) and echocardiographic measurements (PVR, CO, LVMI, EF, AVF-FV), the significant predictors of PAPs amplitude were: PVR (β = 12.410, P < 0.001), the duration of HD (β = 0.069, P = 0.008) and chronic glomerulonephritis as the etiology of ESRD (β = 1.174, P = 0.01843) [Table 2]. These three predictors explain 95.6% of the variance (R2 = 0.956, F (3,47) = 169.798, P < 0.001).
Table 2: Multivariate linear regression analysis of factors influencing PAPs

Click here to view



   Discussion Top


In our study conducted on patients with ESRD undergoing HD via an AVF, we documented the presence of PH in 52.94% of participants, especially in those with chronic glomerulonephritis, probably due to chronic inflammation and immune mechanisms.[8] The incidence was higher in patients receiving HD over a longer time period. PH has been frequently reported in HD patients, but its prevalence varied largely in the medical literature. The highest prevalence was reported by Fabbian (58.6%)[7] followed by Mukhtar[1] who documented PH in 56% of his patients with HD. On the other side, in a recent metaanalysis of 16 studies, comprising 7,112 patients,[5] Thang found an overall PH prevalence of 23%, but the analyzed studies were heterogeneous with differences regarding patients' inclusion criteria, monitored parameters and statistical methods.

There were quite large differences between our patients regarding the time since they were receiving HD and the AVF-FV values. In our study, we assessed higher values of PAPs in patients undergoing HD for a longer period of time and with fistulas with a larger FV. Thus, in the subset of participants with PH, we determined a strong correlation between PAPs values and the duration of HD and moderate ones with the AVF-FV. No such correlation was documented in patients without PH.

The hemodynamic impact of AVF in hemodialysed patients is a much debated topic in the medical literature. If most authors agree that there are connections between the duration of HD via AVF and the development of PH,[7],[19],[20],[21] the opinions regarding the role of AVF-FV on the occurrence of PH are shared. Since 2008, Yigla et al.[6] evidenced the role of the increased CO after the formation of an AVF on the elevation of PAPs in a small prospective study, by following up 12 patients. In a recent article,[18] Afzal discussed that among the factors contributing to the development of PH, AVF may be one of the causes for the occurrence of unexplained increased PAPs. On the other hand, other authors found no correlation between AVF-FV and PH. Acarturk et al.,[9] in a cross-sectional study, found no significant difference in AVF flow between patients with PH and those without. Most data suggest that in patients with ESRD the formation of AVF is not the primary determinant for the development of PH.[8],[22],[23]

We detected in most of our patients with PH (88.88%), increased values of PVR, by means of echocardiography. We documented a strong correlation between PAPs and PVR values, sustaining the hypothesis that there are other mechanisms affecting the pulmonary microvasculature resulting in increased PVR that could explain the occurrence of PH in patients with ESRD. The role of the increased PVR in the pathogenesis of PH is discussed in the medical literature. Increased precapillary PVR due to vasoconstriction and vasoproliferative processes, inducing the obliteration of small vessels, may represent the main pathophysiological mechanism for the development of PH. In their study Suresh et al.,[24] debate the role of the endothelial dysfunction and of the impaired PVR, as well as of the systemic inflammation.

Although we excluded from our study all participants with cardiovascular pathology (excepting secondary hypertension due to ESRD) and those with diabetes mellitus – associated with increased cardiovascular morbi-mortality, we detected in 31.37% of our patients impaired EF, especially in those with PH (48.14%). There was a significant difference between patients with and without PH regarding this finding, sustaining the hypothesis that PH may represent a negative prognostic factor for the development of heart failure.

The association between heart failure and ESRD was debated in many studies. There are numerous causes responsible for the occurrence of heart failure in this category of patients such as: salt and water overload, secondary hypertension and anemia, effects of uremic toxins, endothelial dysfunction, myocardial ischemia. In his study, conducted on 127 patients with ESRD, 37 of them with PAPs>45 mmHg, Kawar documented a significantly higher prevalence of LV dilatation and systolic dysfunction, but no difference in the prevalence of LV diastolic dysfunction between patients with and without PH.[8] Similar data were debated also in other studies.[25],[26]

The diagnosis of PH in patients with ESRD is frequently overlooked and ignored until it ultimately results in irreversible heart failure and death. That is why it is important to detect this pathology timely, all the more as echocardiography offers the possibility of an accurate diagnosis at low costs and reduced risks for the patient. Those detected with PH should be monitored by regular echocardiography and could be offered alternative methods of dialysis, reversal of the AV fistula or they may be proposed earlier for renal transplant in order to reduce or even reverse PH.

Study limitations

In this study, we have relied only on echocardiography for the determination of hemodynamic parameters and have not used invasive methods to verify our results. Another limit was the small size of our study group, but it was very difficult to find patients meeting the inclusion/exclusion criteria. The third aspect was that we had no previous echocardiographic assessment of PAPs in these patients, before starting HD, in order to certify that values were normal at that time.


   Conclusion Top


In our patients with ESRD undergoing HD, PH determined by means of echocardiography was a common finding. PVR, followed by the duration of HD and chronic glomerulonephritis as etiology for ESRD were stronger predictors for the occurrence of PH than AVF-FV. We proved that the patients with PH had a higher prevalence of altered left ventricular systolic function, predisposing them to an increased risk to develop heart failure.

Acknowledgments

The authors want to thank Dr Camelia Totolici from Hemodialysis Center Nefromed for their help in referring patients.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2]



 

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