Impaired Hematologic Status in Relation to Clinical Outcomes among HIV-Infected Adults from Uganda: A Prospective Cohort Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population and Design
2.2. Measurements
2.2.1. Primary Determinants: Baseline Serum Ferritin, Baseline Anemia and Anemia Persistence
2.2.2. Anemia Persistence
- (i)
- Persistently anemia free: no anemia in any observation period.
- (ii)
- Completely Resolved Anemia: mild or moderate/severe anemia at enrollment only without evidence of anemia in any follow-up interval.
- (iii)
- Incompletely Resolved Anemia: baseline moderate/severe anemia that was down-modulated to mild in ≥1 follow-up interval.
- (iv)
- Incident moderate/severe or sustained mild anemia: baseline anemia that became moderate/severe in one of three follow-up intervals or mild baseline anemia that was sustained in ≥2 follow-up intervals.
- (v)
- Mild Anemia: one episode of mild anemia at baseline or developed mild anemia in one of the follow-up intervals.
- (vi)
- Progressive or Persistent moderate/severe Anemia: baseline moderate/severe anemia that was sustained in ≥2 assessment intervals or mild baseline anemia that progressed to moderate/severe in ≥1 follow-up intervals.
2.2.3. Outcomes
- (i)
- Immune function: cluster of differentiation 4 (CD4) T-helper cell count: absolute T-cell lymphocyte count in cells/micro liter was measured using a FACS Calibur flow cytometer (Becton-Dickinson, San Jose, CA, USA).
- (ii)
- Body mass index (BMI): was calculated as the ratio of weight (in kilograms) to squared height (in meters).
- (iii)
- QOL: assessed with the Medical Outcomes Study HIV Health Survey translated and culturally adapted for the study area [24]. As described previously [25], overall QOL score was the sum of scores for activities of daily living, cognitive function, emotional and physical health subscales. Overall score was linearly transformed so that the highest score would be 100.
- (iv)
- Death/hospitalization: Occurrence of hospitalization or death event was, for each participant, a composite endpoint to enhance statistical efficiency and provide a more complete picture of serious adverse clinical outcomes among PLWHA, which should become rarer in the HAART era. Censoring was at date of first hospitalization or death. Participants that experienced both events were censored at hospitalization.
2.3. Potential Confounders: Clinical, Socio-Demographic and Behavioral Characteristics
2.4. Statistical Analysis
2.5. Consent Process/Ethical Approval
3. Results
3.1. Baseline Characteristics
3.2. Association between Baseline Ferritin Status and Immune Recovery, BMI and QOL Outcomes
3.3. Baseline Anemia/Anemia Severity and Change in Immune Recovery, Weight Gain, QOL
3.4. Association between Anemia Persistence, Immunologic Status and QOL
3.5. Time to Hospitalization/Death
4. Discussion
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Characteristics | Overall | Low Ferritin n = 68 | Normal Ferritin n = 169 | High Ferritin n = 161 | p-Value |
---|---|---|---|---|---|
n (%) | n (%) | n (%) | n (%) | ||
Age (years) | <0.01 | ||||
18–29 | 98 (24.6) | 26 (38.2%) | 50 (29.6%) | 22 (13.7%) | |
30–35 | 104 (26.1) | 20 (29.4%) | 41 (24.3%) | 43 (26.7%) | |
36–41 | 102 (25.6) | 15 (22.1%) | 39 (23.1%) | 48 (29.8%) | |
42+ | 94 (23.6) | 7 (10.3%) | 39 (23.1%) | 48 (29.8%) | |
Female | 275 (69.1) | 68 (100.0%) | 134 (79.3%) | 73 (45.3%) | <0.01 |
Clinical Measures | |||||
High C-reactive protein (CRP) | 55 (13.9) | 4 (5.97%) | 15 (8.88%) | 36 (22.50%) | <0.01 |
HAART naïve | 199 (50) | 36 (52.94%) | 95 (56.21%) | 68 (42.24%) | 0.03 |
Anemia Severity | 0.03 | ||||
None | 204 (51.3) | 44 (64.7) | 88 (52.1) | 72 (44.7) | |
Mild | 113 (28.4) | 10 (14.7) | 48 (28.4) | 55 (34.2) | |
Moderate/Severe | 81 (20.3) | 14 (20.6) | 33(19.5) | 34 (21.1) | |
Behavioral Factors | |||||
Ever smoked cigarette | 69 (17.3) | 0 (0.0%) | 26 (15.4%) | 43 (26.7%) | <0.01 |
Current Alcohol use | 0.61 | ||||
Never Used | 84 (21.1) | 16 (23.5%) | 40 (23.7%) | 28 (17.4%) | |
Former User | 230 (57.8) | 37 (54.4%) | 97 (57.4%) | 96 (59.6%) | |
Current User | 84 (21.1) | 15 (22.1%) | 32 (18.9%) | 37 (23.0%) | |
Baseline Multivitamin Use | 90 (22.6) | 17 (25.0%) | 34 (20.1%) | 39 (24.2%) | 0.59 |
BMI (kg/m2) | 0.07 | ||||
Underweight (BMI < 18.5) | 22 (5.5) | 2 (2.9%) | 8 (4.7%) | 12 (7.5%) | |
Normal (18.5 ≤ BMI < 25) | 262 (65.8) | 42 (61.8%) | 103 (61.0%) | 117 (72.7%) | |
Overweight (25 ≤ BMI < 30) | 72 (18.1) | 15 (22.1%) | 36 (21.3%) | 21 (13.0%) | |
Obese (BMI ≥ 30) | 42 (10.6) | 9 (13.2%) | 22 (13.0%) | 11 (6.8%) | |
Vitamin D Deficiency | 0.57 | ||||
Deficient | 67 (16.9) | 12 (17.9%) | 25 (14.8%) | 30 (18.8%) | |
Insufficient | 239 (60.4) | 42 (62.7%) | 99 (58.6%) | 98 (61.3%) | |
Sufficient | 90 (22.7) | 13 (19.4%) | 45 (26.6%) | 32 (20.0%) | |
Self-rated Health | 0.03 | ||||
Good, Very good or Excellent | 180 (45.2) | 21 (30.9%) | 83 (49.1%) | 76 (47.2%) | |
Education | 0.88 | ||||
<Primary | 165 (41.6) | 26 (38.2%) | 73 (18.4%) | 66 (41.0%) | |
Primary completed | 54 (13.6) | 13 (19.1%) | 21 (12.5%) | 20 (12.4%) | |
Some O’level | 78 (19.7) | 12 (17.7%) | 32 (19.1%) | 34 (21.1%) | |
O’level or higher | 100 (25.2) | 17 (25.0%) | 42 (25.0%) | 41 (25.5%) | |
Unemployed/No Income | 52 (13.1) | 11 (16.18%) | 21 (12.43%) | 20 (12.4%) | 0.77 |
Continuous Measures | Mean (standard deviation (SD)) | Mean (SD) | Mean (SD) | Mean (SD) | |
Age (in years) | 35.8 (9.0) | 31.5 (7.1) | 35.1 (8.4) | 38.1 (9.5) | <0.01 |
BMI (in kg/m2) | 23.8 (4.4) | 24.5 (4.2) | 24.4 (4.8) | 22.8 (3.8) | <0.01 |
QOL Score | 91.2 (9.9) | 90.4 (10.2) | 91.3 (9.9) | 91.5 (10) | 0.77 |
CD4 cell count (cells/µL) | 149 (96) | 161 (103) | 152.1 (94) | 140.7 (95) | 0.25 |
Hemoglobin (mg/dL) | 12.3 (1.9) | 12.3 (1.76) | 12.3 (1.8) | 12.2 (1.9) | 0.68 |
Vitamin D (ng/mL) | 26.7 (7.0) | 26.0 (7.5) | 26.4 (6.8) | 27.3 (7.1) | 0.37 |
Outcome Hematologic Status Indicator | Month 0 Mean ± SE Diff (95% CI) | Month 6 Mean ± SE Diff (95% CI) | Month 12 Mean ± SE Diff (95% CI) | Month 18 Mean ± SE Diff (95% CI) | p-Value Group × Time | |
---|---|---|---|---|---|---|
Absolute CD4 | Baseline Serum Ferritin | |||||
Normal † | 152.7 ± 6.8 | 231 ± 8.0 | 251 ± 9.4 | 287 ± 10.9 | 0.78 | |
High | −7.3 (−29.0, 14.4) | 0.3 (−16.4, 17.0) | 15.3 (−4.9, 35.4) | 16.3 (−12.8, 45.5) | ||
Low | −7.0 (−34.7, 20.6) | −6.6 (−30.1, 16.9) | 8.1 (−19.1, 35.2) | −4.0 (−37.4, 29.5) | ||
Baseline Anemia Severity | ||||||
No Anemia | 148 ± 6.8 | 227 ± 8.0 | 261 ± 9.4 | 293 ± 10.9 | 0.11 | |
Mild | 15 (−8.6, 38.4) | 20 (−8, 39) | −1 (−31, 30) | −8 (−44, 27) | ||
Moderate/Severe | −14 (−36.4, 9.0) | −9 (−37, 9) | −7 (−41, 28) | 9 (−34, 52) | ||
BMI | Baseline Serum Ferritin | |||||
Normal † | 23.7 ± 0.3 | 24.3 ± 0.2 | 24.3 ± 0.2 | 24.8 ± 0.2 | 0.04 | |
High vs. Normal | 0.0 (−0.4, 0.4) | −0.1 (−0.4, 0.2) | 0.5 (0.2, 0.8) | 0.3 (−0.1, 0.7) | ||
Low vs. Normal | −0.1 (−0.6, 0.4) | −0.1(−0.4, 0.3) | 0.2 (−0.2, 0.6) | 0.4 (−0.2, 0.9) | ||
Baseline Anemia Severity | ||||||
No Anemia | 24.3 ± 0.3 | 24.5 ± 0.3 | 24.± 0.3 | 25.0 ± 0.3 | ||
Mild | − 0.9 (−1.9, 0.1) | −0.5 (−1.5, 0.5) | −0.3 (−1.3, 0.7) | −0.3 (−1.3, 0.8) | <0.01 | |
Moderate/Severe | −1.3 (−2.4, −0.3) | −0.8 (−1.8, 0.2) | −0.4 (−1.4, 0.6) | 0.1 (−1.0, 1.2) | ||
QOL | Baseline Serum Ferritin | |||||
Normal † | 91.4 ± 0.7 | 98.0 ± 0.6 | 97.6 ± 0.6 | 98.9 ± 0.6 | 0.01 | |
High vs. normal | −0.2 (−2.2, 1.8) | −1.6 (−3.6, 0.1) | 1.0 (−0.60, 2.64) | −0.5 (−2.1, 1.2) | ||
Low vs. normal | −0.3 (−2.96, 2.28) | −0.1 (−2.1, 1.9) | 1.6 (−0.46, 3.50) | −3.3 (−6.1, −0.6) | ||
Baseline Anemia Severity | ||||||
No Anemia | 91.4 ± 0.7 | 98.0 ± 0.6 | 97.6 ± 0.6 | 98.9 ± 0.6 | <0.01 | |
Mild | −1.1 (−3.3, 1.2) | −0.6 (−2.8, 1.6) | 0.9 (−0.8, 2.6) | −1.9 (−4.2, 0.4) | ||
Moderate/Severe | −4.5 (−3.5, −0.9) | 1.0 (−1.3, 3.3) | −0.9 (−3.9, 2.1) | 1.3 (−0.9, 3.5) |
Change in Anemia from Enrolment | Absolute CD4 Cell Count | Body Mass Index * | Quality of Life |
---|---|---|---|
Anemia Persistence | Adjusted Mean ± SE | Adjusted Mean ± SE | Adjusted Mean ± SE |
Mean Difference (95% CI) | Mean Difference (95% CI) | Mean Difference (95% CI) | |
Group 1 (n = 166) † | 309 ± 11.6 | 24.7 ± 0.17 | 98.0 ± 0.67 |
Group 2 (n = 58) | 27.4 (−16.8, 71.5) | 1.14 (0.49, 1.80) | −0.26 (−2.8, 2.3) |
Group 3 (n = 35) | −34.6 (−80.0, 20.9) | 1.42 (0.61, 0.60) | 2.4 (−0.8, 5.7) |
Group 4 (n = 55) | −46.2 (−91.2, −1.26) | −0.37 (−1.02, 0.28) | −0.47 (−0.31, 2.1) |
Group 5 (n = 19) | −48.9 (−118.6, 20.9) | −0.40 (−1.40, 0.60) | 2.1 (−1.93, 6.2) |
Group 6 (n = 39) | −72.8 (−125.7, −19.8) | 0.23 (−0.54, 1.01) | −2.1 (−5.2, 1.04) |
p-value (Log Rank test) | 0.01 | <0.0001 | 0.24 |
Hematologic Status Indicator | Number of Events/Person-Months at Risk | Unadjusted Association Hazard Ratio (95% CI) | Adjusted Association ** Hazard Ratio (95% CI) |
---|---|---|---|
Serum Ferritin | |||
High | 32/2477 | 1.83 (1.04, 3.27) | 1.75 (0.92, 3.3) |
Low | 11/1073 | 1.56 (0.73, 3.30) | 1.86 (0.85, 4.1) |
Normal Ferritin | 18/2608 | Ref | Ref |
Baseline Anemia | |||
Present | 40/2906 | 2.09 (1.23, 3.55) | 2.03 (1.18, 3.56) |
Absent | 21/3388 | Ref | Ref |
Baseline Anemia Severity | |||
No Anemia | 21/3388 | Ref | Ref |
Mild Anemia | 22/1840 | 3.4 (1.89, 6.23) | 3.9 (2.1, 7.2) |
Moderate/Severe | 18/1146 | 6.3 (3.34, 11.7) | 6.7 (3.6, 12.7) |
Anemia Persistence *** | |||
Group 1 | 15/2767 | Ref | Ref |
Group 2 | 6/882 | 1.2 (0.5, 3.2) | 1.11 (0.4, 2.9) |
Group 3 | 6/538 | 2.2 (0.8, 5.6) | 2.1 (0.8, 5.5) |
Group 4 | 11/862 | 2.27 (1.04, 4.96) | 2.27 (1.01, 5.1) |
Group 5 | 10/393 | 4.74 (2.1,10.6) | 4.70 (2.0,10.9) |
Group 6 | 13/753 | 3.0 (1.4, 6.4) | 3.1 (1.4, 6.5) |
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Ezeamama, A.E.; Guwatudde, D.; Sikorskii, A.; Kabagambe, E.K.; Spelts, R.; Vahey, G.; Fenton, J.I.; Fawzi, W.W. Impaired Hematologic Status in Relation to Clinical Outcomes among HIV-Infected Adults from Uganda: A Prospective Cohort Study. Nutrients 2018, 10, 475. https://doi.org/10.3390/nu10040475
Ezeamama AE, Guwatudde D, Sikorskii A, Kabagambe EK, Spelts R, Vahey G, Fenton JI, Fawzi WW. Impaired Hematologic Status in Relation to Clinical Outcomes among HIV-Infected Adults from Uganda: A Prospective Cohort Study. Nutrients. 2018; 10(4):475. https://doi.org/10.3390/nu10040475
Chicago/Turabian StyleEzeamama, Amara E., David Guwatudde, Alla Sikorskii, Edmond K. Kabagambe, Raybun Spelts, Grace Vahey, Jenifer I. Fenton, and Wafaie W. Fawzi. 2018. "Impaired Hematologic Status in Relation to Clinical Outcomes among HIV-Infected Adults from Uganda: A Prospective Cohort Study" Nutrients 10, no. 4: 475. https://doi.org/10.3390/nu10040475