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Fungal and Parasitic Infections

In Vitro Growth-Inhibitory Activity and Malaria Risk in a Cohort Study in Mali

Peter D. Crompton, Kazutoyo Miura, Boubacar Traore, Kassoum Kayentao, Aissata Ongoiba, Greta Weiss, Safiatou Doumbo, Didier Doumtabe, Younoussou Kone, Chiung-Yu Huang, Ogobara K. Doumbo, Louis H. Miller, Carole A. Long, Susan K. Pierce
Peter D. Crompton
1Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12441 Parklawn Drive, Twinbrook 2, Rockville, Maryland 20852
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  • For correspondence: pcrompton@niaid.nih.gov
Kazutoyo Miura
2Malaria Vaccine Development Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland
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Boubacar Traore
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Kassoum Kayentao
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Aissata Ongoiba
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Greta Weiss
1Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12441 Parklawn Drive, Twinbrook 2, Rockville, Maryland 20852
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Safiatou Doumbo
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Didier Doumtabe
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Younoussou Kone
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Chiung-Yu Huang
4Biostatistics Research Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
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Ogobara K. Doumbo
3Malaria Research and Training Center, Faculty of Medicine, Pharmacy and Dentistry, University of Bamako, Bamako, Mali
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Louis H. Miller
2Malaria Vaccine Development Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland
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Carole A. Long
5Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland
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Susan K. Pierce
1Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12441 Parklawn Drive, Twinbrook 2, Rockville, Maryland 20852
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DOI: 10.1128/IAI.00960-09
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  • FIG. 1.
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    FIG. 1.

    Distribution of growth-inhibitory activities in the study cohort. The histogram shows the growth-inhibitory activities for the 220 study participants measured just prior to the malaria season. Inhibitory activities ranged from −7% to 97.6%, with a median of 26.0%. Only one individual had a negative value for % growth inhibition (−7% [data not shown]).

  • FIG. 2.
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    FIG. 2.

    Growth-inhibitory activity by age group and whether individuals were parasitemic with P. falciparum just prior to the malaria season. Box-and-whisker plots represent the smallest and largest (whiskers), the lower and upper quartiles of (top and bottom of box), and the median (horizontal line across box) growth-inhibitory activity. Growth-inhibitory activity in nonparasitemic individuals increased with age (P < 0.001). Within each age group, the median growth-inhibitory activity was higher in parasitemic than in nonparasitemic individuals, but this difference reached statistical significance only in the 2- to 4-year-old (P < 0.01) and 8- to 10-year-old (P = 0.02) age groups, as indicated by an asterisk above the bar. Sample sizes for nonparasitemic individuals were as follows: 2- to 4-year-olds, n = 68; 5- to 7-year-olds, n = 45; 8- to 10-year-olds, n = 45; and 18- to 25-year-olds, n = 46. Those for parasitemic individuals were as follows: 2- to 4-year-olds, n = 4; 5- to 7-year-olds, n = 4; 8- to 10-year-olds, n = 5; and 18- to 25-year-olds, n = 3. The nonparametric Kruskal-Wallis test was used for statistical analysis.

  • FIG. 3.
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    FIG. 3.

    Kaplan-Meier estimates of the cumulative probability of malaria in children aged 2 to 10 years during the 6-month malaria season, by whether growth-inhibitory activity was greater or less than 40%. Malaria was defined as an axillary temperature of ≥37.5°C, P. falciparum asexual parasitemia of ≥5,000 parasites/μl, and a nonfocal physical examination by the study physician. The number of individuals at risk for the first malaria episode in the two groups over the course of the study period is shown below the plot. The P value was obtained using the log rank test.

  • FIG. 4.
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    FIG. 4.

    Distribution of growth-inhibitory activities in malaria-immune (no malaria episodes) and susceptible (≥1 malaria episode) children aged 2 to 10 years. Malaria was defined as an axillary temperature of ≥37.5°C, P. falciparum asexual parasitemia of ≥5,000 parasites/μl, and a nonfocal physical examination by the study physician.

Tables

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  • TABLE 1.

    Baseline characteristics of the study cohort

    CharacteristicValue for age groupValue for all participants (n = 225)
    2-4 yr (n = 73)5-7 yr (n = 52)8-10 yr (n = 51)18-25 yr (n = 49)
    Gender (no. [%] of females)42 (57.5)25 (48.1)19 (37.3)30 (61.2)116 (51.6)
    Ethnicity (no. [%])
        Bambara48 (65.8)26 (50.0)27 (53.0)33 (67.4)134 (59.6)
        Sarakole21 (28.8)23 (44.2)20 (39.2)13 (26.5)77 (34.2)
        Fulani3 (4.1)3 (5.8)3 (5.9)2 (4.1)11 (4.9)
        Malinke1 (1.4)0 (0.0)1 (2.0)1 (2.0)3 (1.3)
    No. (%) of individuals with P. falciparum-positive smear at enrollment4 (5.5)4 (7.7)5 (9.8)3 (6.1)16 (7.1)
    Level of parasitemia if smear was positive at enrollment (no. of parasites/μl) (geometric mean [95% CI])1,438 (159-12,973)3,616 (1,500-8,715)415 (134-1,287)953 (39-23,382)1,137 (579-2,232)
    No. (%) of individuals positive for gastrointestinal helminths at enrollmenta9 (13.0)4 (8.3)4 (9.3)0 (0.0)17 (9.0)
    No. (%) of individuals positive for urine schistosomiasis at enrollmentb0 (0.0)0 (0.0)2 (4.3)9 (28.1)11 (6.0)
    Hemoglobin level at enrollment (g/l) (mean ± SD)11.2 ± 1.211.8 ± 1.012.3 ± 1.113.6 ± 1.412.1 ± 1.5
    Distance lived from clinic (km) (mean ± SD)0.39 ± 0.110.40 ± 0.140.37 ± 0.100.36 ± 0.090.38 ± 0.11
    No. (%) of individuals who used bed netsc21 (28.8)16 (30.8)9 (17.6)15 (30.6)61 (27.1)
    No. (%) of individuals with hemoglobin typed
        AA50 (72.5)43 (86.0)35 (68.6)32 (76.2)160 (75.5)
        AS8 (11.6)4 (8.0)5 (9.8)5 (11.9)22 (10.4)
        AC10 (14.5)3 (6.0)11 (21.6)5 (11.9)29 (13.7)
        CC1 (1.5)0 (0.0)0 (0.0)0 (0.0)1 (0.5)
    • ↵ a Data available for 190 subjects.

    • ↵ b Data available for 184 subjects.

    • ↵ c Nightly bed-net use was self-reported at the end of the malaria season.

    • ↵ d Data available for 212 subjects.

  • TABLE 2.

    Malaria-related clinical outcomes during the 9-month study period, by age group

    OutcomeValue for age groupValue for all individuals (n = 225)P valuea
    2-4 yr (n = 73)5-7 yr (n = 52)8-10 yr (n = 51)18-25 yr (n = 49)
    Malaria incidence (mean ± SD)b1.99 ± 1.251.94 ± 1.210.98 ± 1.050.08 ± 0.281.33 ± 1.30<0.001
    No. of cases of severe malariac41005
    Time to first malaria episode for those who experienced malaria (days [median])d1011141301531150.02
    No. (%) of individuals with at least one malaria episode63 (86.3)45 (86.5)31 (60.8)4 (8.2)143 (63.6)<0.001
    Level of parasitemia at first malaria episode (no. of parasites/μl) (geometric mean [95% CI])34,374 (24,955-47,348)15,687 (9,623-25,574)10,433 (5,079-21,427)8,816 (4,082-19,037)19,625 (15,004-25,668)0.04
    • ↵ a P values were derived by using Fisher's exact test for categorical variables and the Kruskal-Wallis test for continuous variables.

    • ↵ b A malaria episode was defined as a temperature of >37.5°C, asexual parasitemia of >5,000 parasites/microliter, and nonfocal physical examination.

    • ↵ c According to WHO definition of severe malaria.

    • ↵ d Days since study enrollment.

  • TABLE 3.

    Results of multivariate regression analysis for children aged 2 to 10 years

    Explanatory variableResult of regression analysis for malaria outcome
    Whether malaria was experiencedTime to first malaria episodeMalaria incidence
    OR (95% CI)PHR (95% CI)PIRR (95% CI)P
    Age (yr)0.78 (0.63-0.95)0.020.86 (0.80-0.94)<0.0010.91 (0.86-0.96)0.001
    Gender2.04 (0.76-5.46)0.161.38 (0.94-2.03)0.101.03 (0.82-1.30)0.80
    Ethnicity, Bambara0.23 (0.03-2.08)0.190.68 (0.34-1.34)0.261.12 (0.79-1.58)0.52
    Ethnicity, Sarakole0.84 (0.08-8.96)0.891.00 (0.49-2.06)0.991.53 (1.07-2.18)0.02
    Distance lived from clinic (km)0.30 (0.004-24.02)0.590.48 (0.07-3.23)0.450.77 (0.23-2.59)0.67
    Bed-net usea0.70 (0.25-1.97)0.500.89 (0.59-1.35)0.590.96 (0.75-1.23)0.77
    HbAS type0.23 (0.06-0.87)0.030.41 (0.21-0.79)0.010.43 (0.27-0.68)<0.001
    HbAC type0.56 (0.16-1.95)0.360.81 (0.47-1.40)0.441.14 (0.80-1.63)0.47
    Growth-inhibitory activityb0.50 (0.30-0.85)0.010.80 (0.63-1.02)0.070.93 (0.75-1.16)0.53
    • ↵ a Nightly bed-net use was self-reported at the end of the malaria season.

    • ↵ b For this analysis, growth-inhibitory activity was divided into deciles, and thus the regression coefficient for this variable represents the change in malaria risk with each 10% increase in growth-inhibitory activity, holding all other independent variables constant.

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In Vitro Growth-Inhibitory Activity and Malaria Risk in a Cohort Study in Mali
Peter D. Crompton, Kazutoyo Miura, Boubacar Traore, Kassoum Kayentao, Aissata Ongoiba, Greta Weiss, Safiatou Doumbo, Didier Doumtabe, Younoussou Kone, Chiung-Yu Huang, Ogobara K. Doumbo, Louis H. Miller, Carole A. Long, Susan K. Pierce
Infection and Immunity Jan 2010, 78 (2) 737-745; DOI: 10.1128/IAI.00960-09

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In Vitro Growth-Inhibitory Activity and Malaria Risk in a Cohort Study in Mali
Peter D. Crompton, Kazutoyo Miura, Boubacar Traore, Kassoum Kayentao, Aissata Ongoiba, Greta Weiss, Safiatou Doumbo, Didier Doumtabe, Younoussou Kone, Chiung-Yu Huang, Ogobara K. Doumbo, Louis H. Miller, Carole A. Long, Susan K. Pierce
Infection and Immunity Jan 2010, 78 (2) 737-745; DOI: 10.1128/IAI.00960-09
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KEYWORDS

Antibodies, Protozoan
malaria

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