Conceived and designed the experiments: ALB JJF IMP PLM EMM FM UK CHK. Performed the experiments: ALB PLM EMM FM UK CHK. Analyzed the data: ALB CLT FM UK CHK. Contributed reagents/materials/analysis tools: ALB CLT FM EMM PLM UK CHK. Wrote the paper: ALB CLT EMM UK CHK. Head supervisor of laboratory technicians: EMM. Household mapping: UK FM.
The authors have declared that no competing interests exist.
To date, there has been no standardized approach to the assessment of aerobic fitness among children who harbor parasites. In quantifying the disability associated with individual or multiple chronic infections, accurate measures of physical fitness are important metrics. This is because exercise intolerance, as seen with anemia and many other chronic disorders, reflects the body's inability to maintain adequate oxygen supply (
Four villages in coastal Kenya were surveyed during 2009–2010. Children 5–18 years were tested for infection with
The 20 mSRT, which has excellent correlation with
Reduced physical fitness, which is a manifestation of the body's inability to maintain adequate oxygen supply to the tissues, can have many causes. In developing countries, a person's low physical fitness is often the result of anemia and undernutrition, which have multifactorial etiologies including poor diet and chronic infections such as malaria, hookworm and schistosomiasis. In past surveys, exercise tolerance has been measured using non-standardized tests that were poorly-suited to young children. In this study, we implemented a well-validated and reliable 20-meter shuttle run test in a low-resource area of Kenya. Results for 1950 children, aged 5–18 years, showed that impaired fitness was common and associated with anemia and poor growth with boys being more affected than girls. The 20 mSRT is a feasible and low-cost tool that can be easily delivered in low-resource settings to identify children who manifest the disabling but often sub-clinical manifestations of their disease. We propose its implementation as a standard fitness test in less developed areas to allow comparisons across morbidity studies assessing the impact of different interventions.
In the context of chronic disease, exercise intolerance due to decreased physical fitness is a measurable outcome strongly related to decreased quality of life in many spheres of human performance. Among children, loss of physical fitness is associated with anemia, chronic inflammatory conditions, and inadequate nutrition leading to impaired growth
Exercise intolerance due to anemia and chronic parasitic diseases such as schistosomiasis can lead to chronic disability in children and to decreased adult productivity. These important morbidities have been routinely underestimated in past disease burden assessments
In this paper we present the results from cross-sectional surveys in four parasite-endemic villages in coastal Kenya, during which participating children were uniformly tested using the well validated, low-technology multistage 20-meter shuttle run test (20 mSRT). Our working hypothesis, as shown in
Ethical clearance was obtained by the Institutional Review Board at the University Hospital Case Medical Center of Cleveland and the Ethical Review Committee of the Kenya Medical Research Institute (KEMRI). Children were eligible if they were residents of the area for at least two years, were between 5–18 years old, and they had provided child assent and written parental consent.
This cross-sectional study was conducted in four
Subjects were enrolled at the time of the village demography survey in February, August and November of 2009 for Nganja, Milalani and Vuga respectively and March of 2010 for Jego. After an initial interview with the head of the household, in which general information about living conditions was obtained, children were screened for the presence of
Egg burden for
The night prior to the parasitology survey, eligible subjects were given a stool container by local community health workers to provide a single stool sample. The following morning, the stool samples were taken to a central facility and examined in duplicate by Kato-Katz method for microscopic detection of parasite eggs.
Finger prick blood was used to obtain a hemoglobin measurement (Hemocue, Ångelholm, Sweden), and a rapid antigen test for
Because growth is considered the best indicator of nutritional status in children, standardized measurements of height and weight were taken. Prior to working in the surveys, all technical staff who performed anthropometric measurements received standardization training followed by independent reliability assessment. Supervised by a trained anthropometrist, candidates performed duplicate measurements of height (agreement within 0.5 cm), weight (agreement within 1.0 kg), for ten healthy volunteer children on the same day. The results were then compared for inter and intra-observer reliability. The trainees' intra- and inter-examiner technical errors of measurement fell within the reference values
Eligible children were measured according to procedures described by Jeliffe
HAZ is considered an indicator of long-term linear growth whereas BAZ variations better reflect acute changes in nutritional status. According to WHO standards
The 20 meter shuttle run test (20 mSRT), initially validated in Canadian schoolchildren, was used to determine the maximal aerobic capacity of children enrolled in this study
Demographic data collected in the field were double entered in hand-held devices (Dell Axim, Round Rock, Texas) using Visual CE 10 (Cambridge, MA) and a paper form. Data were then transferred in duplicate into ACCESS 2007 (Microsoft, Seattle, WA) and the databases compared for errors. Parasitology and anthropometric data were similarly entered to complete the database.
Exploratory analysis started with univariate distributions followed by bivariate analyses to explore the pairwise relationships of individual outcomes (
The model outcome of interest was fitness level (as scored on the 20 m SRT) and the final GEE-linear regression models presented here were fit to establish its multiply-adjusted association with age, anemia, wasting, and stunting (using WHO age-and sex-based definitions). Additional alternative variables that were explored during model development included continuous variables for weight, height, other observed anthropometrics, hemoglobin, and/or hookworm and schistosomiasis burden (using log-transformed egg counts).We also explored the use of dichotomous/polyotomous variables for malaria or filaria infection, and infection intensity categories (light/moderate/heavy) for hookworm and schistosomiasis. All analyses were performed using SAS 9.2 (Cary, NC) and SPSS 17 (Chicago, IL).
Of the 2034 children 5–18 years old who participated in the surveys, 1950 children (95.9%) with complete parasitological data completed the 20 m SRT, and were included in the final analysis. Seven children refused to run, and 23 (1.1%) were unable to participate due to limiting physical conditions that included asthma, seizures, pregnancy, club-foot, leg wounds and feeling unwell. Thirty-six (1.8%) did not wait for fitness testing and left after providing their biological samples.
After a brief explanation and demonstration of the test, study participants were batched in groups of 5–15 individuals for testing. The running surface was dirt and most of the children ran barefoot, with which they typically felt most comfortable. There was a very good overall understanding of the test, with occasional need for repetition of instructions and a few false starts. When this happened, a rest period was instituted that lasted between 15–20 minutes. In performing the test, several situations were taken into consideration: i) If a child was lagging behind the recorded marked pace he/she was asked to stop and the level obtained was recorded accordingly, ii) If a false start happened, all children were asked to re-start, iii) If tripping occurred, the child was asked to stop and after a recovery period he/she restarted the test.
No significant differences were observed among the four villages in terms of sex or age distribution, however significant inter-village differences were observed in the prevalence of anemia, mean hemoglobin and malnutrition parameters as shown in
VILLAGES(Number studied) | TOTAL(N = 2034) | NGANJA(N = 240) | MILALANI(N = 416) | VUGA(N = 726) | JEGO(N = 652) | |
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MEAN AGE (RANGE) | 11.0 yr (0.2–19) | 11.2 yr (5–19.5) | 11.1 yr (5–19) | 11.6 yr (2–19) | 10.4 yr (0.2–18.2) | 0.0715 |
% FEMALE | 48% | 44% | 51% | 51% | 46% | 0.0852 |
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% ANEMIC |
51% | 48% | 51% | 45% | 58% | 0.0567 |
MEAN HEMOGLOBIN (RANGE) | 11.7 g/dL (3.4–18.9) | 11.7 g/dL (4.8–17) | 11.6 g/dL (6.3–15.4) | 11.8 g/dL (5.2–16.4) | 11.9 g/dL (3.4–18.9) | 0.0217 |
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% WASTED |
19% | 19% | 13% | 31% | 10% | <0.001 |
% STUNTED |
36% | 45% | 35% | 43% | 25% | <0.001 |
% SEVERELY WASTED |
6.4% | 3.3% | 2.9% | 13.5% | 2% | <0.001 |
*
Anemia based on WHO age-specific hemoglobin (Hb) criteria (19): for ages<12 yr, Hb<11.5 g/dL; for ages≥12 yr, Hb<12 g/dL; but for males≥15 yr, Hb<13 g/dL.
Wasting: < = −2 in BMI-for-age Z score (BAZ).
̂Stunting: < = −2 in height-for-age Z score (HAZ).
**Severely Wasted: < = −3 in BAZ, based on WHO 2006 growth standards (25).
Both acute and chronic undernutrition were present in each of the four communities, as measured by wasting and stunting prevalence, respectively (see
As was expected, based on growth physiology, there were marked gender differences in 20 m SRT performance scores, so the final analysis of fitness outcomes is stratified here by sex. (Mean scores per age group for boys and girls are shown in
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−0.253 | (−0.51, 0.01) |
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−0.199 | (−0.51, 0.11) |
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0.026 | (−0.08, 0.13) |
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0.083 | (−0.01, 0.17) |
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−0.073 | (−0.22, 0.07) |
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0.194 | (−0.22, 0.60) |
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0.130 | (−0.21, 0.47) |
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−0.006 | (−0.50, 0.49) |
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−0.114 | (−0.47, 0.24) |
Anemia based on WHO age-specific hemoglobin (Hb) criteria (19): for ages<12 yr, Hb<11.5 g/dL; for ages≥12 yr, Hb<12 g/dL; but for males≥15 yr, Hb<13 g/dL.
Wasting:< = −2 in BMI-for-age Z score (BAZ);
Stunting: < = −2 in height-for-age Z score (HAZ); based on WHO 2006 growth standards (25).
Hookworm intensity as log transformation of individual egg count in 1 gm of stool.
Malaria/Filaria infection scored as present or absent by rapid antigen detection card.
Estimates in
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−0.302 | (−0.67,0.07) |
Anemia based on WHO age-specific hemoglobin (Hb) criteria (19): for ages<12 yr, Hb<11.5 g/dL; for ages≥12 yr, Hb<12 g/dL; but for males≥15 yr, Hb<13 g/dL.
Stunting: < = −2 in height-for-age Z score (HAZ); based on WHO 2006 growth standards (25).
Wasting: < = −2 in BMI-for-age Z score (BAZ); Estimates in
For
For
There is a need for a standardized aerobic fitness test in epidemiological surveys. In the past, fitness has been measured among children harboring parasitic infections in several different ways, but none have proven to be both sufficiently easy to perform and reliable so as to become a standard test for field studies
Accelerometers have also been used to measure spontaneous activity
Our choice of the 20 mSRT was based on its simplicity as a field test and its validity vis a vis laboratory-based physiological testing
With slight variations in protocol, the 20 mSRT may be the most widely used aerobic fitness field test among children and adolescents in industrialized countries
Although we were not able to compare 20 m SRT results to formal laboratory or ergometer testing, our results conform to those obtained in Canada in correlating fitness with increasing age, increasing height, and gender differences. This strongly supports the validity and applicability of the 20 m SRT as a useful tool in gauging fitness in less-developed areas. Consistent with international testing results (summarized in a meta-analysis of 109 studies from 37 countries
In our field-based studies of parasitic disease burden, we approached local validation of the 20 m SRT by examining whether sex-specific and age-adjusted fitness scores were significantly modified by physical conditions such as anemia that are known to limit physical fitness in other populations. As expected, anemic girls and boys scored significantly lower on the 20 mSRT than their non-anemic local counterparts, reflecting a measurable relative disability. Girls with hookworm infection had more exercise intolerance than boys, however this effect was not seen in the multivariable-adjusted model suggesting that the hookworm effect was mediated through anemia or nutritional variables in the model. Malaria or filarial infection were not significantly associated with aerobic capacity in either gender, but because these two infections were relatively rare, we might not have had sufficient power in the study to see an independent effect for each infection. The bivariate association seen in boys between schistosomiasis and increased fitness may reflect a selective increase in exposure to infected water in more active children, as previously described among South African boys
Malnutrition parameters, in particular, stunting and wasting, emerged as strong predictors of decreased fitness, predominantly in boys. This is consistent with findings of previous studies about stunting
There were limitations to our study. First, this cross-sectional study can only indicate significant associations with reduced fitness, but cannot indicate causality. We did not approach the comprehensive measurement of fitness testing in terms of aerobic capacity, strength, flexibility, or body composition. However, we were able to establish that the 20 m SRT is feasible, and appears to be reliable in a rural, resource-limited setting, with minimal requirements for observer and participant training. As a limitation of our analysis, misclassification of infection prevalence by underdiagnosis of active infections may have limited our ability to establish a direct association between infection status and fitness. Given that our diagnoses were based on screening parasitology of a single day's blood, urine or stool specimens using methods known to have incomplete sensitivity
In summary, this study was able to link fitness, as measured by a low-technology field test, with prevalent anemia and growth stunting, which are known morbidity outcomes affecting children with chronic parasitic infections. We believe the results presented in this paper can serve as a point of reference for other projects aiming to measure fitness in low-resource settings. Prior international standardization of the 20 mSRT makes it an especially valuable tool for refining estimates of disease burden in less-developed countries. Beyond its use in epidemiological research, it could be easily implemented in rural schools as a screening fitness test to detect underlying health conditions, as is commonly done in industrialized countries. Through simplified detection of sub-clinical morbidity at the community level, children at risk for anemia and/or associated parasite infections could then be brought to earlier medical attention, thereby enhancing the impact of national control programs.
Pearson correlation between exercise level obtained and covariates of interest.
(DOCX)
Exercise level, resulting speed, and VO2 max. Summary means and standard deviations by age and gender.
(DOC)
The authors want to specially acknowledge our energetic field workers, Joyce Bongo, Phyllis Mutemi and Nancy Halloway, for their dedication and meticulous anthropometric measurements and exercise test recording. We also thank the many DVBND laboratory technicians who provided parasitology results. We warmly thank the many children of Nganja, Milalani, Vuga, and Jego who willingly participated in the study. This work is dedicated to the memory of the late Dr. Michael C. Latham (1928–2011), a pioneer in the study of NTD-related nutritional diseases.