|Year : 2021 | Volume
| Issue : 1 | Page : 14-21
Association of total lymphocyte count and echocardiographic parameters in human immunodeficiency virus-positive patients
Abaram Chesa Mankwe1, Jonah Sydney Aprioku2
1 Cardiology Unit, Department of Internal Medicine, Federal Medical Centre, Yenagoa, Bayelsa State, Nigeria
2 Department of Experimental Pharmacology and Toxicology, Faculty of Pharmaceutical Sciences, University of Port Harcourt, Port Harcourt, Nigeria
|Date of Submission||14-Oct-2021|
|Date of Acceptance||01-Nov-2021|
|Date of Web Publication||11-Aug-2022|
Dr. Abaram Chesa Mankwe
Cardiology Unit, Department of Internal Medicine, Federal Medical Centre, Yenagoa, Bayelsa State
Source of Support: None, Conflict of Interest: None
Background: The pathophysiology of cardiovascular diseases in HIV infection has been linked to chronic inflammation that precipitates atherosclerosis and low lymphocyte count is a common finding during the systemic inflammatory response.
Aim: The aim of this study is to evaluate the relationship between total lymphocyte count (TLC) and echocardiographic parameters in HIV positive subjects.
Method: TLC of 100 HAART naïve newly diagnosed HIV/AIDS subjects, recruited from a Nigerian Tertiary Health Institution were analyzed, and their left ventricular (LV) function and geometry were evaluated using transthoracic echocardiography.
Results: Abnormalities in LV function and geometry were observed in the HIV seropositive subjects and their TLCs were lower in those with severe forms of abnormalities.
Conclusion: Concluding, TLC is inversely associated with LV dysfunction or abnormal geometry.
Keywords: Echocardiograghy, left ventricular function, left ventricular geometry, total lymphocyte count, HIV
|How to cite this article:|
Mankwe AC, Aprioku JS. Association of total lymphocyte count and echocardiographic parameters in human immunodeficiency virus-positive patients. Nig J Cardiol 2021;18:14-21
|How to cite this URL:|
Mankwe AC, Aprioku JS. Association of total lymphocyte count and echocardiographic parameters in human immunodeficiency virus-positive patients. Nig J Cardiol [serial online] 2021 [cited 2022 Dec 5];18:14-21. Available from: https://www.nigjcardiol.org/text.asp?2021/18/1/14/353685
| Introduction|| |
The burden of human immunodeficiency virus (HIV) in many developing countries such as Nigeria is high, and majority of HIV-positive patients depend on health centers in rural areas to access healthcare services. Unfortunately, these centers do not have the capacity or capability to measure CD4 cell count which is used to routinely check the immune status of people infected with the virus. World Health Organization guidelines promote total lymphocyte count (TLC) as a surrogate marker for CD4 cell count. In addition, a number of previous studies have indicated that TLC may be useful as a surrogate marker of immune status in certain settings.
Studies have reported that HIV infection is capable of causing cardiovascular diseases. This may be as a result of various factors, including direct effect (s) of the virus, opportunistic infections, or cancers on the cardiovascular system. Cardiovascular complications of HIV infection may result in increased risk of acute coronary syndrome and cardiomyopathy, which are in turn associated with increased left ventricular mass (LVM)., Increased LVM is associated with increased risk of fatal and nonfatal myocardial infarction, sudden cardiac death, severe heart failure, and cerebrovascular diseases, including transient ischemic attacks and stroke.,, The pathophysiology of these cardiovascular diseases in HIV infection has been linked to chronic inflammation that precipitates atherosclerosis. It has been reported that low lymphocyte count is a common finding during the systemic inflammatory response and is thought to promote the progression of atherosclerosis.
Some studies had shown that lymphocyte counts correlated inversely to outcomes in patients with heart failure, chronic ischemic heart disease, and acute coronary syndrome, but there is a paucity of similar data, particularly in the Black population, including Nigeria. Furthermore, some studies have shown the association between CD4 cell count and LV dysfunction in HIV-infected individuals, but TLC has received less attention in this regard. The objective of this study is to investigate the relationship between TLC and LV function and geometry among HIV-positive patients visiting University of Port Harcourt Teaching Hospital, Nigeria.
| Materials and Methods|| |
The study is a descriptive cross-sectional study and was conducted in a HIV clinic and medical wards of a teaching hospital in southern part of Nigeria. This is a tertiary hospital which provides care for patients referred from a wide range of primary and secondary healthcare facilities in the region. Using systematic random sampling technique, the study subjects were selected.
The study population consisted of 100 newly diagnosed HIV/AIDS patients aged 18–69 years who had not commenced highly active antiretroviral therapy (i.e., HAART naïve). The minimum sample size (nf) was obtained using the Kish formula below:
(when sample population size <10,000)
Where: N, desired sample size when population is >10,000; N, actual population size
z = Standard deviation, usually set at 1.96, which corresponds to 95% confidence level
p = The proportion in the target population estimated to have HIV infection, 4.1% (Ministry of Health, Federal Republic of Nigeria, 2010)
q = 1 − p = 1 − 0.041 = 0.959
d = Degree of desired accuracy, set at 0.05
N = Population size (average number of new HIV/AIDS-positive HAART-naïve patients attending University of Port Harcourt Teaching Hospital annually) = 638.
The minimum sample size obtained was 55, but 100 was used for better statistical power.
Study exclusion criteria and clinical evaluation of participants
Study exclusion criteria include individuals on antiretroviral therapy and those with dyslipidemia, abnormal estimated glomerular filtration rate (eGFR) ≤60 ml/min, hypertension, diabetes, obesity, and infective processes that could affect white blood cells (WBC). Individuals who met the study criteria were asked for informed consent and when granted recruited into the study. Participants were asked to return on the day of the study for further evaluation after an overnight fast.
Participants received clinical assessments by the investigators using a structured questionnaire to obtain demographic information and disease-related variables, including age, gender, and previous history of cardiovascular events. Physical examination was equally conducted to determine weight, height, body mass index (BMI), body surface area (BSA), and blood pressure. Bodyweight was measured with a mechanical weighing scale in kilograms with the subject wearing only light clothing (jackets and coats were removed) and with the subject's shoes removed. Height was measured in meters using a stadiometer with the subject standing feet together without shoes or headgear, back and heel together against a vertical ruled bar to which a movable attached horizontal bar was brought to the vertex of the head and reading taken to the nearest 0.5 cm.
BMI was calculated as body weight in kilograms divided by the square of the height in meters. BMI status was classified according to the WHO criteria as normal weight (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), Class I obesity (30.0–34.9 kg/m2), Class II obesity (35.0–39.9 kg/m2), and morbid obesity (≥40 kg/m2). Those who were obese were excluded from the study. BSA was calculated using the formula of Du Bois: BSA (in m2) = 0.0001 × (71.84) × (weight in kg0.4250) × (height in m0.725). Blood pressure was measured with a standard (Accosson) mercury sphygmomanometer (cuff size 12.5 cm × 40 cm) on the patients' right arm in the seated position with feet on the floor after at least 5 min rest. Those found to be hypertensive (blood pressure ≥140/90 mmHg) were excluded from the study.
Measurement of biochemical indices
Venipuncture was also carried out using a peripheral vein, and 7 mL of blood was collected from each subject, 5 mL of which was put into lithium heparin tube for the assessment of fasting lipid profile and serum creatinine. The remaining 2 mL was transferred into fluoride oxalate tubes for fasting plasma glucose test. Creatinine assay was done by alkaline picrate method, while plasma glucose estimation was done using the microglucose oxidase technology. Serum creatinine result was used to calculate the eGFR using the Cockcroft–Gault formula. Patients with eGFR levels ≤60 ml/min or fasting plasma glucose levels ≥7.0 mmol/L were excluded from the study., Fasting cholesterol and triglyceride levels were measured using the enzymatic method, with a reagent from Atlas More Details Medical Laboratories. Patients with abnormal lipid profile were excluded from the study.
Measurement of hematological parameters
WBC count and WBC differential count were determined using an automated blood analyzer (CELL-DYN 1800, Abbott Laboratories Diagnostics Division, USA). TLC was easily obtained from the routine complete blood count with differential through the multiplication of lymphocyte percentage by WBC count. CD4 T-lymphocytes count was determined using the Becton Dickinson (BD) FASCount system (BD Biosciences, USA). The BD FASCount system used flow cytometry for the quantification of the CD4 T-lymphocytes. Both biochemical and hematological parameters were analyzed, respectively, in the laboratories of the Departments of Chemical Pathology and Hematology, University of Port Harcourt, Nigeria.
Echocardiographic examination of the participants was performed by two experienced cardiologists using ALOKA 2-dimensional/Doppler and color flow ultrasound machine (Aloka Co., Ltd. Tokyo, Japan), equipped with a 3.2 MHz transducer according to the guidelines of the American Society of Echocardiography. Echocardiographic examination was performed with participants in the left lateral decubitus position breathing slowly. The cardiologists were blinded to the patient's other data. The LV dimensions, such as the LV end-diastolic diameter (LVEDD), LV posterior wall thickness in diastole (LVPWT), and the interventricular septal wall thickness in diastole (IVST), were measured directly by the leading-edge to leading-edge method. Relative wall thickness (RWT) was derived by the appropriate formula defined as 2 times LVPWT divided by the LVEDD.
The parameter for LV systolic function was based on the LV ejection fraction (LVEF). The derived LVEF was calculated using the Teichholz et al.'s formula. Systolic dysfunction was classified as (a) Stage I (or mild dysfunction), defined as LVEF of 41%–45%; (b) Stage II (or moderate dysfunction), defined as LVEF of 36%–40%; and (c) Stage III (or severe dysfunction), defined as LVEF of ≤35%. Presence of diastolic dysfunction was determined according to the guidelines from the American Society of Echocardiography.,, The parameters for LV diastolic function was based on mitral E/A pulse wave, deceleration time (DT), and isovolumetric relaxation time (IVRT) diastolic flow patterns on Doppler echocardiography. The diastolic mitral flow, assessed by early diastolic peak flow velocity (E), atrial contraction (A), and the ratio of E to A (E/A), and the deceleration time (DECT) of the early mitral velocity were recorded with the sample volume at the mitral leaflet tips. Deceleration time was measured as the time from peak E velocity to the time when the E wave descent intercepts the zero line. IVRT was measured with a continuous wave Doppler beam intersecting LV outflow and inflow tract. Valsalva maneuver was performed when applicable. Three consecutive cardiac cycles were assessed and averaged for Doppler measurements. Filling patterns in evaluated subjects were classified as (1) normal filling pattern, i.e., normal myocardial relaxation and (2) diastolic dysfunction. Diastolic dysfunction was classified as (a) Stage I (or mild dysfunction), defined as impaired relaxation with normal filling pressure; (b) Stage II (or moderate dysfunction), defined as pseudonormal filling pattern; (c) Stage III (or severe reversible dysfunction), defined as a restrictive filling pattern and evidence of reversibility with Valsalva maneuver; and (d) Stage IV (or severe irreversible dysfunction), defined as a restrictive filling pattern without reversibility with Valsalva.
LVM was calculated using the ASE-recommended formula: LVM (g) = 0.8 × 1.04 [(IVST + LVEDD + LVPWT)3 − (LVEDD)3]. LVM was divided by BSA to obtain the left ventricular mass index (LVMI). LV hypertrophy (LVH) was considered to be present when LVMI exceeds 110 g/m2 for female and 134 g/m2 for male. LV geometry was classified based on the evaluations of LVMI and RWT as follows: normal geometry (normal LVMI and RWT), concentric remodeling (normal LVMI and increased RWT), eccentric hypertrophy (increased LVMI and normal RWT), and concentric hypertrophy (increased LVMI and increased RWT).
Data were analyzed using statistical package of the social sciences (SPSS) version 20 software (Inc., Chicago, Illinois, United States of America). Descriptive statistics involved frequencies and proportions for categorical variables, while mean and standard deviation were used to summarize numerical variables. Inferential statistics was performed at significant level of P < 0.05. One-way analysis of variance was used to compare mean TLC values across systolic function, diastolic function, and LV geometry. Pearson's correlation and simple linear regression were performed to explore the association between TLC and echocardiographic parameters. Values were considered significant at P < 0.05.
| Results|| |
A total of 100 HAART-naive HIV-infected subjects were included in this study, among whom 70 (70%) were females and 30 (30%) were males. Subjects within the age group of 30–39 years had the highest frequency (43%), and those with secondary level of education had the highest frequency (57%). The sociodemographic characteristics of the recruited subjects are shown in [Table 1].
The mean systolic and diastolic blood pressures obtained were 107.20 ± 11.55 and 67.20 ± 7.67 mmHg, respectively. BMI was 22.33 ± 3.52 kg/m2, while TLC was 2094.35 ± 1037.44 cells/μL [Table 2]. Comparing TLC across the various classes of LV systolic function, the mean TLC was highest in those with normal LV systolic function and lowest in those with severe (Grade III) LV systolic dysfunction. However, the values in subjects with abnormal forms of LV dysfunction (mild, moderate, or severe) were not significantly different when compared with count obtained in those with normal LV systolic function, P = 0.390 [Table 3]. In our study, LV diastolic dysfunction was assessed using IVRT, deceleration time, and E/A ratio. Prolongation of the IVRT was found in 24 (24%) of the studied population. The mean deceleration time obtained was 169.16 ± 39.85 ms (range = 78–252 ms), and the mean E/A ratio was 1.55 ± 0.66. Among the studied group, 60 (60.0%), 2 (2.0%), 22 (22.0%), and 16 (16.0%) had normal diastolic function, mild, moderate, and severe diastolic dysfunction, respectively. In addition, comparing TLC across the various forms of LV diastolic function, the mean TLC was highest in those with normal LV diastolic function and lowest in those with severe (Grade III) LV diastolic dysfunction. However, there was no statistically significant difference in the level of TLC in subjects with normal LV diastolic function and those with mild, moderate, or severe LV diastolic dysfunction, P = 0.106 [Table 4]. The mean LVM was 153.87 ± 50.613 g, with a range of 72–380 g. The mean LVMI was 92.63 ± 28.719 g/m2. The mean RWT was 0.4892 ± 0.22537 in the studied population. Furthermore, the TLCs that were obtained in subjects with abnormal LV geometry (concentric remodeling, eccentric hypertrophy, or concentric hypertrophy) were lower, but not significant (P = 0.149) compared with those with normal LV geometry. The mean TLC was lowest in those with LV concentric hypertrophy [Table 5].
|Table 3: Total lymphocyte counts in control participants having normal systolic function and participants with human immunodeficiency virus/acquired immunodeficiency syndrome having systolic dysfunction|
Click here to view
|Table 4: Total lymphocyte counts in control participants having normal left ventricular diastolic function and participants with human immunodeficiency virus/acquired immunodeficiency syndrome having diastolic dysfunction|
Click here to view
|Table 5: Total lymphocyte counts in control participants having normal left ventricular geometry and participants with human immunodeficiency virus/acquired immunodeficiency syndrome having abnormal left ventricular geometry|
Click here to view
There was a negative correlation between E/A ratio and TLC (r = −0.098, P = 0.333), while a positive correlation was observed between deceleration time (DECT) and TLC (r = 0.041, P = 0.684) as indicated in [Figure 1] and [Figure 2]. There were negative correlations between IVRT and TLC (r = −0.091, P = 0.368); RWT and TLC (r = −0.183, P = 0.069); and LVMI and TLC (r = −0.096, P = 0.344) as shown in [Figure 3], [Figure 4], [Figure 5]. Furthermore, there was a positive correlation between CD4 count and TLC (r = 0.118, P = 0.241) as presented.
|Figure 1: Correlation between total lymphocyte count and early diastolic peak flow velocity (E) and atrial contraction, A (E/A) ratio in participants with human immunodeficiency virus/AIDS|
Click here to view
|Figure 2: Correlation between total lymphocyte count and deceleration time of early mitral velocity in participants with human immunodeficiency virus/AIDS|
Click here to view
|Figure 3: Correlation between total lymphocyte count and isovolumic relaxation time in participants with human immunodeficiency virus/AIDS|
Click here to view
|Figure 4: Correlation between total lymphocyte count and relative wall thickness in participants with human immunodeficiency virus/AIDS|
Click here to view
|Figure 5: Correlation between total lymphocyte count and left ventricular mass index in participants with human immunodeficiency virus/AIDS|
Click here to view
| Discussion|| |
This study determined the relationship between TLC and LV dysfunction and abnormal LV geometry among newly diagnosed HAART-naïve HIV/AIDS individuals. Previous studies centered on the association between CD4 count and LV function in HIV-positive individuals. However, health providers in resource-constrained settings may not have the capacity to measure CD4 lymphocyte count, making the use of TLC as an alternative surrogate marker justifiable.
The study cohort consisted mostly of female participants which may be explained by the higher percentage of females living with HIV/AIDS. Women are more predisposed to HIV infection than men as a result of biologic, economic, social, and cultural factors. Furthermore, most of the patients were in the age group 30–39 years with a mean age of 35.70 ± 10.13 years. This is similar to the mean age of 35.00 ± 10.40 years that was obtained by Danbauchi et al., who studied on cardiac manifestations in individuals with HIV/AIDS at Stages III and IV. This could be explained by the fact that HIV risk behaviors, such as sexual experimentation and drug abuse are common within this age group, which are often influenced by strong peer-group relationships. Compounding this vulnerability is “generational forgetting” as it appears that the present-day youths perceive the dangers associated with HIV less than older populations who witnessed a higher AIDS mortality rate associated with the rapid progression from HIV to AIDS in the early years of the epidemic.
Low lymphocyte count is a common feature that occurs during systemic inflammatory response, and clinical and animal studies suggest that it plays an important role in accelerated atherosclerosis. In the present study, the mean TLC was highest in subjects with normal LV systolic function and lowest in those with severe (Grade III) LV systolic dysfunction. This is consistent with the findings of Nunez et al., who reported that low lymphocyte count is associated with unfavorable outcomes in patients with heart failure, chronic ischemic heart disease, and acute coronary syndromes. Charach et al. had also reported that patients with low lymphocyte counts (<1600 cells/μL) after 8 years had lower survival rates than those with lymphocyte counts ≥1600 cells/μL (58% vs. 72%, P = 0.012), which is in agreement with the present findings. The pathophysiologic role of reduced lymphocyte levels can also be explained from the observation that increased incidence of cardiovascular events occurs in conditions where lymphopenia is common, such as HIV infection. Depressed ejection fraction observed in the HIV-positive subjects in the present study is a serious cardiovascular incidence that can cause depression of the myocardium.
Diastolic function in this study was assessed by peak early LV filling velocity/peak atrial filling velocity (E/A) ratio, deceleration time (DT), and IVRT. Clinical and echocardiographic findings in previous studies suggest that diastolic dysfunction is relatively common in long-term survivors of HIV infection and LV diastolic dysfunction may precede systolic dysfunction., In this study, there was a negative correlation between E/A ratio and TLC and also between IVRT and TLC. This corroborates the results of an earlier large multicenter echocardiographic study in which asymptomatic HIV-infected patients had 34.6% lower E/A ratio and 19.7% longer IVRT than healthy adults. In another similar study, LV diastolic function in HIV patients was shown to have elevation in IVRT and reduction in the E-wave velocity when compared with healthy control. Longo-Mbenza et al. also reported diastolic dysfunction in 80.0% of its study population and attributed it to systemic amyloidosis and concentric LVH developed by the HIV patients in the study.
Furthermore, the mean TLC was highest in those with normal LV geometry and lowest in those with LV concentric hypertrophy. LV geometry was assessed using the LVMI and RWT, and the the results indicated that there were negative correlations between LVMI and TLC and between RWT and TLC. Prior studies had evaluated LVM among HIV-infected patients and the results have been conflicting., Barbaro et al. reported increased LVM in asymptomatic HIV patients compared to healthy individuals; Mansoor et al. reported that HIV infection is associated with greater LVM but not with a higher prevalence of LVH and concluded that RWT but not LVM was associated with the degree of immunosuppression among HIV-infected women. Multiple factors have been linked to affect LVM in patients with HIV infection. Several autopsies and animal studies have shown that HIV virions directly affect myocardial cells and are associated with the local release of cytokines and other factors, leading to inflammation, myocarditis, and dilated cardiomyopathy., Alternatively, increases or decreases in LVM have been suggested to be associated with opportunistic infections and malnutrition.
| Conclusion|| |
LV dysfunction and abnormal geometry were shown in this study to be present in seropositive carriers at the early stage of HIV infection, including those who are asymptomatic. LV systolic dysfunction and abnormal geometry were more common in participants with lower TLCs (≤1200 cells/μL). However, the limitations of this study include its cross-sectional design as a longitudinal follow-up would have provided further data on incidence and progression of abnormal LV function and geometry. In addition, because of stigmatization, the cohorts of patients who present to the University of Port Harcourt Teaching Hospital for the treatment of this condition are mostly traders and artisans who are unlikely to afford treatment in private hospitals. The results, therefore, may not represent the affluent population that is of higher risk for cardiovascular events.
We are grateful to the laboratory technicians of the Echocardiography laboratory of the University of Port Harcourt Teaching Hospital, Nigeria, for providing logistics assistance in evaluation of echocardiographic profile of the participants.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Obirikorang C, Quaye L, Acheampong I. Total lymphocyte count as a surrogate marker for CD4 count in resource-limited settings. BMC Infect Dis 2012;12:128.
Levy WS, Simon GL, Rios JC, Ross AM. Prevalence of cardiac abnormalities in human immunodeficiency virus infection. Am J Cardiol 1989;63:86-9.
Anthony SF, Cliffort HL. Human Immunodeficiency virus disease; AIDS and related disorders. In: Fauci AS, Braunwald E, Kasper DL, Hauser SL, Longo DL, Jameson JL, editors. Harrison's Principles of Internal medicine. 17th
ed. New York: McGraw-Hill; 2008. p. 1137-204.
Cole JW, Pinto AN, Hebel JR, Buchholz DW, Earley CJ, Johnson CJ, et al.
Acquired immunodeficiency syndrome and the risk of stroke. Stroke 2004;35:51-6.
Barbaro G, Di Lorenzo G, Grisorio B, Barbarini G. Incidence of dilated cardiomyopathy and detection of HIV positive patients. N Engl J Med 1998;339:1093-9.
Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP. Prognostic implications of echocardiographically determined left ventricular mass in the F
ramingham heart study. N Engl J Med 1990;322:1561-6.
Verdecchia P, Porcellati C, Reboldi G, Gattobigio R, Borgioni C, Pearson TA, et al.
Left ventricular hypertrophy as an independent predictor of acute cerebrovascular events in essential hypertension. Circulation 2001;104:2039-44.
Haider AW, Larson MG, Benjamin EJ, Levy D. Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death. J Am Coll Cardiol 1998;32:1454-9.
Nou E, Lo J, Hadigan C, Grinspoon SK. Pathophysiology and management of cardiovascular disease in HIV-infected patients. Lancet Diabetes Endocrinol 2016;4:598-610.
Nunez J, Minana G, Bodi V, Munez E, Sanchiz J, Husser O, et al
. Low lymphocyte count and cardiovascular disease. Curr Med Chem 2011;18:3226-33.
Charach G, Grosskopf I, Roth A, Afek A, Wexler D, Sheps D, et al.
Usefulness of total lymphocyte count as predictor of outcome in patients with chronic heart failure. Am J Cardiol 2011;107:1353-6.
Mankwe AC, Odia OJ. Association between CD4+count and left ventricular diastolic function and geometry in newly diagnosed highly active antiretroviral therapy (HAART) naïve HIV/AIDS patients seen at university of Port Harcourt teaching hospital, Port Harcourt, Rivers State, Nigeria. J Cardiovasc Dis Diagn 2017;5:295.
Kish L. Survey Sampling. New York: John Wiley and Sons, Inc; 1965.
Report of 2010 National HIV sero-prevalence sentinel survey among antenatal and not anta-natal clinic attendees. Presented by C. O. Onyebuchi Chukwu, Hon. Minister of Health, Federal Republic of Nigeria. Digiprove @ 2011 P.M News.
Du Bois D, Du Bois EF. A formula to estimate the approximate surface area if height and weight be known. 1916. Nutrition 1989;5:303-11.
Tietz NW, Pruden EL, Siggard-Anderson O. Electrolytes, Blood Gases and Acid base Balance in Textbook of Clinical Chemistry. 5th
ed. Philadelphia: Saunders; 1986. p. 1188-96.
Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron 1976;16:31-4.
National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am J Kidney Dis 2002;39 Suppl 1:S1-266.
Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 1997;20:1183-97.
Barbour HM. Enzymatic determination ofcholesterol and triglycerides with the Abbott Bichromtic analyzer. Ann Clin Biochem 1977;14:22-8.
Sahn DJ, DeMaria A. Kissio J, Weyman A. Recommendations regarding quantification in M-Mode echocardiography: Results of a survey of echocardiographic measurements. Circulation 1978;58:1072-83.
Koren MJ, Mensah GA, Blake J, Laragh JH, Devereux RB. Comparison of left ventricular mass and geometry in black and white patients with essential hypertension. Am J Hypertens 1993;6:815-23.
Teichholz LE, Kreulen T, Herman MV, Gorlin R. Problems in echocardiographic volume determinations: Echocardiographic-angiographic correlations in the presence of absence of asynergy. Am J Cardiol 1976;37:7-11.
Gibson DG, Francis DP. Clinical assessment of left ventricular diastolic function. Heart 2003;89:231-8.
Zile MR, Brutsaert DL. New concepts in diastolic dysfunction and diastolic heart failure: Part 1: Diagnosis, prognosis and measurements of diastolic function. Circulation 2002;105:1387-93.
Rakowski H, Appleton C, Chan KL, Dumesnil JG, Honos G, Jue J, et al.
Canadian consensus recommendations for the measurement and reporting of diastolic dysfunction by echocardiography: From the Investigators of Consensus on Diastolic Dysfunction by Echocardiography. J Am Soc Echocardiogr 1996;9:736-60.
Nishimura RA, Abel MD, Hatle LK, Tajik AJ. Assessment of diastolic function of the heart: Background and current applications of Doppler echocardiography. Part II. Clinical studies. Mayo Clin Proc 1989;64:181-204.
Parrinello G, Colomba D, Bologna P, Licata A, Pinto A, Paterna S, et al.
Early carotid atherosclerosis and cardiac diastolic abnormalities in hypertensive subjects. J Hum Hypertens 2004;18:201-5.
Heidi M, Connolly K, Joe K. Echocardiography. In: Braunwald's Heart Disease. A Textbook of Cardiovascular Medicine. 8th
ed., Ch. 14. New York: Elsevier Sci; 2007. p. 249.
Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure: Abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 2004;350:1953-9.
Gaasch WH, Little WC. Assessment of left ventricular diastolic function and recognition of diastolic heart failure. Circulation 2007;116:591-3.
Devereux RB, Lutas EM, Casale PN, Kligfield P, Eisenberg RR, Hammond IW, et al
. Standardization of M-mode echocardiographic left ventricular anatomical measurements. J Am Coll Cardiol 1984;4:1222-30.
Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, et al
. Echocardiographic assessment of LVH: comparison to necropsy findings. Am J Cardiol 1986;57:450-8.
United Nations AIDS UNAIDS Report on the Global AIDS Epidemic; 2010. p. 364. Available from: http://www.unaids.org/en/
. [Last accessed on 2011 Oct 25].
Danbauchi S, Sani B, Alhassan A. Echocardiographic Features of HIV/AIDS Subjects on 1-2 Years of ARV Drugs in Nigeria. Available from: hhtp://www. 2umdnj.edu/schinler/hivecho.html. [Last accessed on 2011 Nov 06].
Fisher SD, Bowles NE, Towbin JA, Lipshultz SE. Mediators in HIV-associated cardiovascular disease: A focus on cytokines and genes. AIDS 2003;17:S29.
Starc TJ, Lipshultz SE, Easley KA, Kaplan S, Bricker JT, Colan SD, et al.
Incidence of cardiac abnormalities in children with human immunodeficiency virus infection: The prospective P2C2 HIV study. J Pediatr 2002;141:327-34.
Morse CG, Kovacs JA. Metabolic and skeletal complications of HIV infection: The price of success. JAMA 2006;296:844.
Nzuobontane D, Ngu BK, Christopher K. Cardiovascular autonomic dysfunction in Africans infected with human immunodeficiency virus. J R Soc Med 2002;95:445-7.
Coudray N, De Zuttere D, Force G, Champetier de Ribes D, Pourny JC, Antony I, et al
. Left ventricular diastolic dysfunction in asymptomatic and symptomatic human immunodeficiency virus carriers: An echocardiographic study. Eur Heart J 1995;16:61-7.
Longo-Mbenza B, Seghers KV, Phuati M, Bikangi FN, Mubagwa K. Heart involvement and HIV infection in African patients: Determinants of survival. Int J Cardiol 1998;64:63-73.
Barbaro G, Barbarini G, Di Lorenzo G. Early impairment of systolic and diastolic function in asymptomatic HIV-positive patients: A multicenter echocardiographic and echo-Doppler study. AIDS Res Hum Retroviruses 1996;12:1559-63.
Mansoor A, Golub ET, Dehovitz J, Anastos K, Kaplan RC, Lazar JM. The association of HIV infection with left ventricular mass/hypertrophy. AIDS Res Hum Retroviruses 2009;25:475-81.
Altieri PI, Climent C, Lazala G, Velez R, Torres JV. Opportunistic invasion of the heart in Hispanic patients with acquired immunodeficiency syndrome. Am J Trop Med Hyg 1994;51:56-9.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]