Skip to content

Advertisement

Parasites & Vectors

Research
Open Access

Intestinal parasites, growth and physical fitness of schoolchildren in poor neighbourhoods of Port Elizabeth, South Africa: a cross-sectional survey

  • Ivan Müller1, 2, 3,
  • Peiling Yap1, 2, 4,
  • Peter Steinmann1, 2,
  • Bruce P. Damons5, 6,
  • Christian Schindler1, 2,
  • Harald Seelig2, 3,
  • Nan S. N. Htun1, 2,
  • Nicole Probst-Hensch1, 2,
  • Markus Gerber2, 3,
  • Rosa du Randt6,
  • Uwe Pühse2, 3,
  • Cheryl Walter6 and
  • Jürg Utzinger1, 2Email author
Parasites & Vectors20169:488

https://doi.org/10.1186/s13071-016-1761-5

©  The Author(s). 2016

Received: 23 April 2016

Accepted: 16 August 2016

Published: 5 September 2016

Abstract

Background

As traditional lifestyle and diets change with social and economic development, disadvantaged communities in low- and middle-income countries increasingly face a double burden of communicable and non-communicable diseases. We studied the relationship between physical fitness and infections with soil-transmitted helminths (STHs), intestinal protozoa and Helicobacter pylori among schoolchildren in Port Elizabeth, South Africa.

Methods

We conducted a cross-sectional survey among 1009 children, aged 9 to 12 years, from eight primary schools in socioeconomically disadvantaged neighbourhoods of Port Elizabeth. Physical fitness was determined using field-deployable tests of the Eurofit fitness test battery. Stool samples were analysed with the Kato-Katz thick smear technique to diagnose STHs and with rapid diagnostic tests (RDTs) to detect intestinal protozoa and H. pylori infections. Haemoglobin (Hb) levels were assessed and anthropometric indicators determined.

Results

Complete data were available for 934 children (92 %). In two schools, high STH prevalences were found (Ascaris lumbricoides 60 and 72 %; Trichuris trichiura 65 % each). For boys and girls co-infected with A. lumbricoides and T. trichiura (n = 155) the maximal oxygen uptake (VO2 max) was estimated to be 50.1 and 47.2 ml kg-1 min-1, compared to 51.5 and 47.4 ml kg-1 min-1 for their non-infected peers (n = 278), respectively. On average, children without helminth infections had greater body mass (P = 0.011), height (P = 0.009) and a higher body mass index (P = 0.024) and were less often stunted (P = 0.006), but not significantly less wasted compared to their peers with a single or dual species infection. Among 9-year-old boys, a negative correlation between helminth infections and VO2 max, grip strength and standing broad jump distance was observed (P = 0.038). The overall mean Hb level was 122.2 g l-1. In the two schools with the highest prevalence of STHs the Hb means were 119.7 and 120.5 g l-1, respectively.

Conclusions

Intestinal parasite infections appear to have a small but significant negative effect on the physical fitness of infected children, as expressed by their maximal oxygen uptake. We observed a clear impact on anthropometric indicators.

Keywords

Anthropometric indicatorsHaemoglobinIntestinal polyparasitismIntestinal protozoaPhysical fitnessSoil-transmitted helminthsSouth Africa

Background

Globally, more than 1 billion people are infected with soil-transmitted helminths (STHs; Ascaris lumbricoides, hookworms and Trichuris trichiura) and Schistosoma spp. [1–3]. The symptoms most frequently associated with these parasitic worm infections include abdominal pain, diarrhoea, anaemia, growth retardation and cognitive impairment [4], ultimately resulting in reduced physical fitness and work productivity [5]. Important risk factors for STH and Schistosoma spp. infections are a lack of clean water, sanitation and hygiene (WASH) [6, 7]. Permissive conditions are commonly found in socioeconomically deprived neighbourhoods in low- and middle-income countries, including in South Africa [8]. Intestinal protozoa such as Cryptosporidium parvum, Entamoeba spp. and Giardia intestinalis are associated with poor living conditions [9]. Their transmission mostly occurs through faecal contamination of food and water [10]. They may lead to symptoms such as abdominal pain, diarrhoea and nausea. Many low- and middle-income countries struggle to control such infectious diseases stemming from traditional challenges [11]. In South Africa, a country that shows considerable health inequity in global terms (e.g. Gini index of 0.63 in 2011 [12]), socioeconomically deprived communities with a high burden of infectious diseases live in close proximity to affluent ones with a disease burden profile typical of western societies. Among both populations, non-communicable diseases (e.g. diabetes, cardiovascular- and obesity-related conditions and cancers) are rapidly increasing, fuelled by unhealthy lifestyles including poor nutritional habits and sedentary lifestyles [13]. South Africa’s 2014 Report Card on Physical Activity for Children and Youth [14] highlights the current concerns for the health and well-being of children and youth in relation to declining physical activity levels and increasing rates of consumption of soft-drinks and fast food.

Low levels of in-school physical activity have been documented for children in Port Elizabeth in the frame of a study by Walter et al. [15] who focused on primary schoolchildren in disadvantaged schools. Low quality and often inaccessible sport and recreation facilities, a lack of qualified teachers and an irregular physical education schedule complicate the promotion of age-appropriate physical activity among schoolchildren at disadvantaged schools. The resulting dual burden of diseases (i.e. non-communicable chronic conditions and infectious diseases) puts children at an increased risk of compromised health that may hamper their development, wellbeing and future prospects [13, 16, 17]. Moreover, this dual burden is a challenge for the health system.

The “Disease, Activity and Schoolchildren’s Health” (DASH) study in Port Elizabeth, South Africa, aims to investigate this dual disease burden (i.e. non-communicable chronic conditions and infectious diseases) among children in selected primary schools located in disadvantaged neighbourhoods [18]. Here, we report the findings pertaining to parasite infections and physical activity from a cross-sectional survey among 9- to 12-year-old children. The objectives of this cross-sectional survey were (i) to determine the prevalences of intestinal parasite infections and Helicobacter pylori; (ii) to assess the haemoglobin (Hb) levels and anthropometric indicators; (iii) to comprehensively measure the physical fitness levels; and (iv) to investigate possible associations between infection status and other measured variables.

Methods

Study site and school selection

The study was carried out at eight primary schools in socioeconomically disadvantaged neighbourhoods of Port Elizabeth, in the Western region of the Eastern Cape province of South Africa (geographical coordinates: 34°07′54″S to 33°57′29″S latitude and 25°36′00″E to 25°55′49″E longitude, altitude: extends from 0 m to approximately 100 m above sea level) in February 2015. The study population consisted of coloured children (of mixed race ancestry, and generally Afrikaans speaking) and black African children (largely Xhosa speaking), residing in areas previously demarcated for these specific race groups, in accordance with past Apartheid legislation. Colloquially, these respective areas are referred to as the northern areas (for coloured people) and townships (for black African people). The people living in these areas are still detrimentally affected by the legacy of Apartheid [19, 20]. A total of 103 quintile three primary schools (where quintile one denotes the poorest and quintile five the “least poor” schools, with the degree of poverty referring to the neighbourhood around school locations) were contacted to explore interest in study participation. Positive responses were received from 25 schools. Eight schools were finally included in the study, with selection based on (i) size in terms of the number of students; (ii) geographical location; (iii) representation of the different target communities; and (iv) commitment to support the project activities.

Study design

The DASH study is a cohort study with a physical intervention component to determine whether WASH and an education and nutrition programme can reduce the prevalence of parasitic infections and improve physical fitness levels among 9- to 12-year-old children [18]. A single stool and a single urine sample were collected for parasitological work-up to diagnose helminth and intestinal protozoa infections using light microscopy. Anthropometric indicators (i.e. height and weight) and Hb concentrations were assessed by trained examiners or nurses. Physical fitness was determined by measuring the participants’ performance in a grip strength test for upper body strength, standing broad jump test for lower body strength and 20 m shuttle run test for cardiorespiratory endurance.

Study procedures

Stool containers with unique identifiers were handed out to schoolchildren together with the instruction to return them with a small portion (at least 15 g) of their own morning stool. Containers were collected between 9 and 10 a.m. and transferred to a laboratory of the Nelson Mandela Metropolitan University (NMMU) in Port Elizabeth for diagnostic work-up on the same day. Stool samples were first visually examined for the presence of Taenia spp. proglottids, signs of blood, mucus and diarrhoea. Duplicate 41.7 mg Kato-Katz thick smears were prepared from each stool sample [21]. Slides were read under a microscope by experienced laboratory technicians who counted the number of eggs of each helminth species. The two slides were read by different technicians, the results compared for quality control and, in case of inconsistencies (i.e. positive versus negative or egg counts differing by more than 20 %), the slides were re-read. Helminth egg counts were multiplied by a factor of 24 to obtain a proxy for infection intensity, as expressed by the number of eggs per gram of stool (EPG) [22].

At the time of stool collection, children were given an empty urine collection container and asked to return it with a urine sample within the next 30 min. Filled containers were transferred to the laboratory and analysed on the same day. Samples were first inspected visually for macrohaematuria and then tested with Hemastix® strips (Siemens Healthcare Diagnostics GmbH; Eschborn, Germany) to detect blood in urine as a proxy for Schistosoma haematobium infections. A point-of-care circulating cathodic antigen (POC-CCA) urine cassette test (Rapid Medical Diagnostics; Cape Town, South Africa) was used for the diagnosis of S. mansoni infections [23].

For the detection of C. parvum and G. intestinalis, a Crypto-Giardia Duo-Strip® rapid diagnostic test (RDT) was performed on the stool sample, while for the discovery of H. pylori, a Pylori-Strip® RDT was employed (both tests from CORIS, BioConcept; Gembloux, Belgium).

The Hb concentration was measured once, to the nearest 0.1 g l-1, with the HemoCue® Hb 301 system (HemoCue®AB; Ängelholm, Sweden). In brief, after swabbing the child’s fingertip with alcohol, a field worker pricked the fingertip with a safety lancet and squeezed gently to obtain two drops of blood. The first drop was wiped away with the alcohol swab and the second drop was taken up with the microcuvette.

For the anthropometric measurements, each child was asked to remove the shoes and sweater before standing on a digital weighting scale (Micro T7E electronic platform scale, Optima Electronics; Georg, South Africa). Body weight was measured once to the nearest 0.1 kg. The height of each child was assessed with a Seca stadiometer (Surgical SA; Johannesburg, South Africa) whereby the child was standing with the back erect and shoulders relaxed. Body height was taken to the nearest 0.1 cm.

Specific standardised tests from the Eurofit fitness test battery [24] were conducted as follows. Upper body strength was determined through the grip strength test, with both right and left hands. Measurements were taken with the Saehan hydraulic hand dynamometer (MSD Europe BVBA; Tisselt, Belgium) set at handle position two. The examiner demonstrated how to grip the dynamometer with both arms at a 90° angle, while sitting straight and being relaxed. Each participant had three attempts, with about a 30 s rest in between, to grip the dynamometer with alternating hands as hard as possible. The maximum reading, measured to the nearest 1 kg, was recorded. The grip strength of both hands was measured. Additionally, the dominant hand was noted.

Lower body strength was estimated with the standing broad jump test. Before the start, the examiner demonstrated the test. Each child stood behind a straight line and jumped as far as possible with both legs forward. Participants had two attempts, with about a 30 s rest in between. The longer jump measured from the starting line to the heel of the foot closest to the starting line and rounded to the nearest 1 cm, was recorded.

The children’s endurance was measured with the 20 m shuttle run test [25], using the test protocol from Léger et al. [26] for which a great number of scientific international benchmarks exist [27, 28]. The 20 m flat grass running course was measured with a measuring tape and marked with different coloured cones. Five running lanes were created. The majority of the schoolchildren wore school or street shoes, whereas a minority ran barefoot. Shortly before the start of the test, the children were asked if anyone was sick or did not feel well. These children were excluded from the test. Next, the pre-recorded sound signals were played and the children did a trial run of two intervals (40 m). Once they were familiar with the test procedures, they were asked to run in groups, back and forth on the 20 m flat course, following the pace of the sound signals. Starting with a running speed of 8.5 km h-1, the frequency of the signal increased gradually such that every min, the pace increased by 0.5 km h-1. When a child failed to follow the pace in two consecutive intervals, she or he was asked to stop. The number of 20 m laps run to the last fully completed lap was noted as the final score.

Statistical analysis

Data were double-entered, validated using EpiData version 3.1 (EpiData Association; Odense, Denmark) and merged into a single database. For children who had complete parasitological and anthropological data but missed one of the three physical fitness tests, we imputed data, using age- and sex-adjusted mean values. Statistical analysis was performed using STATA version 13.0 (STATA Corp.; College Station, TX, USA). Maps were created with ArcGIS version 10.2.1 (ESRI; Redlands, CA, USA).

Statistical significance was defined as P < 0.05. The parasitological status was described in terms of prevalence and infection intensity (mean EPG) of individual parasite species and the extent of multiparasitism (concurrent infections with more than one helminth or protozoan species). Anthropometric indicators, Hb concentrations and fitness performance scores were expressed as means and standard deviations (SD). Differences between groups were assessed using mixed linear models. The likelihood-ratio test was used to compare models. To describe the anthropometry of the children, body weight and height values were used to calculate the body mass index (BMI), defined as weight (in kg)/height2 (in m2), the sex-adjusted BMI-for-age Z-score (BMIZ) as an indicator for wasting and sex-adjusted height-for-age Z-score (HAZ) as an indicator for stunting [29].

The age of the participating child and the speed at which the child stopped running in the 20 m shuttle run test were converted into a third variable, the maximal oxygen uptake or VO2 max [25]. All statuses and indicators were compared between non-infected and infected children, the latter also further stratified by degrees of multiparasitism. Comparisons between schools were done using the χ 2 test or the one-way ANOVA, as appropriate. Mixed linear and mixed logistic regression models with random intercepts for schools were used to analyse quantitative and binary data, respectively. These analyses included group comparisons with and without adjustment for covariates. For a simple interpolation of georeferenced data of children’s homes, the inverse distance weighting (IDW) method was used to obtain smoothed values of infection intensity, which is based on the assumption that two geographically close sites are more similar than two locations far apart.

Results

Demographic baseline characteristics

All 1009 Grade 4 primary children of the eight selected schools from the northern part of Port Elizabeth were invited to participate. As illustrated in Fig. 1, complete data were available from 934 children (92 %). Reasons for exclusion were age outside the target range of 9–12 years, no stool or urine sample submitted for diagnostic work-up, lack of clinical examination, reported health problems precluding participation in the physical fitness tests (e.g. chronic asthma), or incomplete physical test battery. Children infected with either C. parvum or G. intestinalis and those who reported abdominal pain, blood in the stool or diarrhoea, those with special lung sounds (e.g. chest wheezing or creeping), ringworm infection or signs of tachycardia, were referred to the local clinic. All subsequent analyses refer to the final cohort of 934 children, which included 462 girls (49.5 %) and had a mean age of 10.0 years. No statistically significant difference was observed between the eight schools with regard to the mean age and sex ratio (both P > 0.05).
Figure 1
Fig. 1

Study cohort and compliance of Grade 4 primary schoolchildren from eight schools in disadvantaged neighbourhoods of Port Elizabeth, South Africa in early 2015

Infections with helminths, intestinal protozoa and H. pylori

Overall, 248 children (26 %) were infected with A. lumbricoides and 207 (22 %) with T. trichiura. One child had a S. haematobium infection, while Taenia spp., hookworm and S. mansoni were not observed. A total of 144 children (15 %) were infected with at least one intestinal protozoan species: the G. intestinalis prevalence was 13 % and C. parvum prevalence was 3 %. H. pylori was found at all schools, ranging from 25 % up to 65 % (Fig. 2). Multiparasitism was common: 158 of the 384 infected children (41 %) harboured at least two parasite species, mostly A. lumbricoides and T. trichiura. Thirty triple-species infections were also detected (8 %).
Figure 2
Fig. 2

Prevalence of helminth, intestinal protozoan and Helicobacter pylori infection in eight primary schools in Port Elizabeth, South Africa, in early 2015

Stratification by sex revealed that boys had higher prevalences and mean EPG values compared to girls for both A. lumbricoides and T. trichiura (Table 1). T. trichiura infections were of highest mean intensity in children aged 11 years (mean 940 EPG), while A. lumbricoides infections were of highest intensity in 12-year-old children (mean 18,630 EPG). Infections were spatially clustered: the prevalence of T. trichiura and A. lumbricoides at school B in Hillcrest was 65 and 60 %, respectively, and at school A in Helenvale 65 and 72 %, which was significantly higher than in the other schools (T. trichiura: χ 2 = 592.53, df = 7, P < 0.0001 ; A. lumbricoides: χ 2 = 475.34, df = 7, P < 0.0001) (Fig. 2). Similarly, infection intensities were highest in schools A and B (Fig. 3). At school B in Hillcrest and at school A in Helenvale, the prevalence of G. intestinalis was 16 and 14 %, respectively, and the respective prevalence of H. pylori was 65 and 57 %.
Table 1

Ascaris lumbricoides and Trichuris trichiura prevalence and infection intensity (as mean of duplicate Kato-Katz thick smears) among 934 primary schoolchildren from Port Elizabeth, South Africa, in early 2015, stratified by sex and age

  

Sex

 

Age (years)

  

Male (n = 472)

Female (n = 462)

 

9 (n = 282)

10 (n = 375)

11 (n = 216)

12 (n = 61)

 

n (%)

n (%)

P a

n (%)

n (%)

n (%)

n (%)

P a

A. lumbricoides

Prevalenceb

134 (28)

114 (25)

0.305

43 (15)

108 (29)

74 (34)

23 (38)

0.691

Infection intensityc

        

Mean EPGd (95 % CI)

10,866 (7907–14,934)

9256 (6633–12,915)

0.333

8411 (4357–16,238)

9038 (6309–12,948)

10,899 (7306–16,258)

18,630 (11,725–29,602)

0.252

Light (1–4999)

36 (8)

36 (8)

 

10 (4)

41 (11)

18 (8)

3 (5)

 

Moderate (5000–49,999)

67 (14)

58 (13)

 

26 (9)

43 (11)

39 (18)

17 (28)

 

Heavy (≥50,000)

31 (7)

20 (4)

 

7 (2)

24 (6)

17 (8)

3 (5)

 

T. trichiura

Prevalencee

114 (24)

93 (20)

0.065

31 (11)

88 (23)

68 (32)

20 (33)

0.208

Infection intensityc

        

Mean EPGd (95 % CI)

757 (572–1002)

747 (557–1002)

0.950

737 (471–1155)

640 (467–877)

940 (661–1336)

744 (322–1723)

0.446

Light (1–999)

65 (14)

55 (12)

 

16 (6)

55 (15)

36 (17)

13 (21)

 

Moderate (1000–9999)

44 (9)

35 (8)

 

15 (5)

32 (9)

27 (13)

5 (8)

 

Heavy (≥10,000)

5 (1)

3 (1)

 

0 (0)

1 (0.3)

5 (2)

2 (3)

 

aAll P-values are calculated using either mixed linear or mixed logistic regression, as appropriate, adjusted for clustering of schools

b A. lumbricoides prevalence irrespective of co-infections

c Stratified according to WHO guidelines

d Geometric mean among the infected (95 % confidence interval)

e T. trichiura prevalence irrespective of co-infections

Figure 3
Fig. 3

Trichuris trichiura infection intensities (stratified according to WHO guidelines) in the northern part of Port Elizabeth, South Africa, in February 2015, smoothed and based on 648 geographical coordinates of schoolchildren’s homes

Anthropometric indicators and Hb concentration

The mean height, weight and BMI of the study cohort were 133.2 cm, 30.5 kg and 17.0 kg m-2, respectively. Stunting was observed in 10 % of the children, while wasting was recorded in 4 % of the children. We found statistically significant differences in anthropometric indicators when comparing children without a helminth infection with those with a single species infection of either A. lumbricoides, T. trichiura or a co-infection (Table 2). Non-infected children had greater body mass (χ 2 = 11.09, df = 3, P = 0.011), height (χ 2 = 11.60, df = 3, P = 0.009) and a higher BMI (χ 2 = 9.49, df = 3, P = 0.024) and were less likely to be stunted (χ 2 = 12.29, df = 3, P = 0.006) but not less wasted (χ 2 = 2.83, df = 3, P = 0.418) compared to their peers with a single or dual species infection. Children concurrently infected with A. lumbricoides and T. trichiura had similar anthropometric and haemotologic measures compared to children with a single T. trichiura infection.
Table 2

Anthropometric indicators and haemoglobin concentrations among 934 primary schoolchildren, stratified by Ascaris lumbricoides and/or Trichuris trichiura infection status, from Port Elizabeth, South Africa, in February 2015

 

Non-infected children

A. lumbricoides single infection

T. trichiura single infection

A. lumbricoides-T. trichiura co-infection

 

n = 635

n = 248

n = 207

n =156

P a

Anthropometric

 Meanb weight [kg] (95 % CIc)

31.6 (31.0–32.2)

28.4 (27.7–29.1)

27.8 (27.0–28.5)

27.8 (26.9–28.6)

0.011

 Meanb height [cm] (95 % CIc)

133.9 (133.3–134.5)

131.8 (130.9–132.6)

131.1 (130.1–132.1)

131.1 (130.0–132.2)

0.009

 Meanb BMI [kg m-2] (95 % CIc)

17.5 (17.2–17.7)

16.2 (16.0–16.5)

16.0 (15.7–16.3)

16.1 (15.7–16.4)

0.024

  n (%) wastedd

15 (2.4)

17 (6.9)

16 (7.7)

12 (7.7)

0.418

  n (%) stuntede

37 (5.8)

47 (19.0)

47 (22.7)

36 (23.1)

0.006

Haemotologic

 Meanb haemoglobin [g l-1] (95 % CIc)

123.1 (122.3–123.8)

120.4 (119.2–121.6)

119.5 (118.3–120.6)

119.5 (118.2–120.8)

0.009

aAll P-values are calculated using either mixed linear or mixed logistic regression, as appropriate, adjusted for clustering of schools

bArithmetic mean

c95 % confidence interval

dWasting is defined as ≤ -2 in BMIZ score

eStunting is defined as ≤ -2 HAZ score

The overall mean Hb level was 122.2 g l-1. Hb levels were significantly lower in children harbouring a single or dual species helminth infection (χ 2 = 11.70, df = 3, P = 0.009). In school B in Hillcrest, the mean Hb level was 119.7 g l-1, and at school A in Helenvale, 120.5 g l-1, respectively. These values were significantly lower compared to the overall mean Hb level of the eight schools enrolled in our study.

Physical fitness levels and parasitological status

Non-infected boys achieved statistically significantly higher mean grip strength test results than non-infected girls (13.2 kg versus 11.7 kg; χ 2 = 31.71, df = 1, P < 0.0001) (Fig. 4; Additional file 1: Table S1). Older children (11–12 years) had significantly higher mean grip strength test results compared to their younger counterparts (9–10 years) (χ 2 = 150.25, df = 1, P < 0.0001). Irrespective of age and sex, children with multiple parasite infections had slightly, but not statistically significantly, lower mean grip strength compared to non-infected children.
Figure 4
Fig. 4

Physical fitness test results, namely (a) grip strength, (b) standing broad jump and (c) 20 m shuttle run test, among 934 Grade 4 schoolchildren, stratified by sex, age and infection status, in Port Elizabeth, South Africa, in early 2015. Note: The darker the boxplot is, the more parasite species are hosted by a child; bright boxplots represent infection-free, black boxplots represent quadruple infections; the dashed red line represents the mean

Infection status was not associated with lower achievement in the standing broad jump test, irrespective of age and sex. The VO2 max estimated from the 20 m shuttle run test was higher in non-infected boys than girls (51.5 and 47.4 ml kg-1 min-1; χ 2 = 167.43, df = 1, P < 0.0001), but unrelated to age.

With regard to infection with A. lumbricoides and T. trichiura, irrespective of the co-infection state (Table 3), the estimated mean VO2 max for 9-year-old children infected with T. trichiura was statistically significantly lower than the VO2 max of their non-infected peers (48.1 ml kg-1 min-1 versus 49.6 ml kg-1 min-1; χ 2 = 4.29, df = 1, P = 0.038). Estimates for infected children of higher age were lower compared to non-infected children of the same age, but the difference did not reach statistical significance.
Table 3

Mean maximal oxygen uptake (VO2 max) estimatesa (ml kg-1 min-1) among 934 primary schoolchildren from Port Elizabeth, South Africa, in February 2015, stratified by sex, age and Ascaris lumbricoides and Trichuris trichiura infection status

 

A. lumbricoides

 

T. trichiura

 

Non-infected (n = 686)

Infected (n = 248)

P b

Non-infected (n = 727)

Infected (n = 207)

P b

Sex

 Male (n = 472) (95 % CI)

51.1 (50.7–51.5)

50.0 (49.3–50.6)

0.113

51.1 (50.7–51.5)

49.8 (49.1–50.6)

0.204

 Female (n = 462) (95 % CI)

47.5 (47.2–47.8)

47.4 (46.7–48.0)

0.946

47.5 (47.1–47.8)

47.4 (46.7–48.1)

0.911

Age (years)

 9 (n = 282) (95 % CI)

49.6 (49.1–50.0)

48.6 (47.5–49.6)

0.104

49.6 (49.1–50.0)

48.1 (47.0–49.3)

0.038

 10 (n = 375) (95 % CI)

48.9 (48.4–49.4)

48.8 (48.2–49.5)

0.955

48.9 (48.4–49.4)

48.9 (48.2–49.6)

0.778

 11 (n = 216) (95 % CI)

49.2 (48.4–49.9)

48.8 (47.7–49.8)

0.489

49.3 (48.6–50.0)

48.4 (47.3–49.5)

0.151

 12 (n = 61) (95 % CI)

49.9 (48.7–51.0)

49.0 (47.0–51.1)

0.424

49.2 (48.0–50.5)

50.2 (48.2–52.1)

0.548

aAll mean VO2 estimates are expressed in ml kg−1 min−1 and are adjusted for age, with 95 % confidence intervals in parentheses when appropriate

bAll P-values are calculated using either mixed linear or mixed logistic regression, as appropriate, adjusted for clustering of schools

In the multiple linear regression model presented in Table 4, sex and age were statistically significantly and negatively associated with mean VO2 max estimates. The mean VO2 max estimate of girls overall was 3.48 ml kg-1 min-1 lower than the VO2 max estimate of boys (P < 0.001). The mean VO2 max estimate also decreased by 0.40 ml kg-1 min-1 per year (P = 0.004). Non-significantly higher mean VO2 max estimates were found in H. pylori-infected children compared to their non-infected peers.
Table 4

Associations between mean maximal oxygen uptake (VO2 max) estimates (ml kg-1 min-1) and age, sex and infection status as predictor variables across eight schools. Data are derived from 934 primary schoolchildren from Port Elizabeth, South Africa, in early 2015

 

Multiple linear regression

Explanatory variables

Coefficient

95 % confidence interval

P

A. lumbricoides (reference: not infected)

-0.37

-1.23 to 0.50

0.403

Age (in years)

-0.40

-0.68 to -0.13

0.004

Dual infected (reference: not infected)

-0.42

-1.27 to 0.43

0.332

T. trichiura (reference: not infected)

-0.46

-1.61 to 0.70

0.442

Sex (reference: male)

-3.48

-3.95 to -3.01

< 0.001

P-value of mixed-effects linear regression model P < 0.001, adjusted for clustering within schools

Discussion

We found notable levels of helminth and intestinal protozoa infections in 9- to 12-year-old children in eight schools of poor neighbourhoods in Port Elizabeth, South Africa. Children infected with T. trichiura had significantly lower body weight, were less tall and had a lower BMI compared to their non-infected peers (all P < 0.05). The same trend was observed for A. lumbricoides-infected children.

Helicobacter pylori infections were classified by World Health Organization (WHO) as a carcinogen of class 1 (definite carcinogen) in 1994 [30]. Non-significant associations between an infection with this bacterium and the growth of children were noted, confirming findings by Abdelrazak and Richter et al. [31, 32]. Boys, but not girls, with a T. trichiura or A. lumbricoides infection had significantly lower mean VO2 max estimates than non-infected peers (Fig. 5). Grip strength and standing broad jump test results were also statistically significantly lower in 9- to 10-year-old boys, whereas in girls no difference was seen.
Figure 5
Fig. 5

Physical fitness levels as estimated by maximal oxygen uptake (VO2 max) of children infected with either A. lumbricoides (n = 248) (a) or T. trichiura (n = 207) (b), compared to physical fitness levels of infection-free peers among Grade 4 schoolchildren in Port Elizabeth, South Africa, in early 2015. Note: Curves were generated using a polynomial smooth. Infection-free is here defined as no A. lumbricoides, T. trichiura, Cryptosporidium spp. and Giardia spp. infection (n = 278)

The mean number of completed levels/stages of the 20 m shuttle run test corresponds closely to the mean results reported from other studies in different settings, e.g. the KISS- or the Sportcheck-study with Swiss primary schoolchildren of similar age [33–35]. Yap et al. reported slightly lower VO2 max results, 45.6 ml kg-1 min-1 for boys and 44.7 ml kg-1 min-1 for girls, from 194 children aged 9-12 years and living in south-west Yunnan province in the People’s Republic of China [3]. With regard to T. trichiura infections, Yap et al. [5] found more pronounced impacts on weight, height and BMI than the present study.

The 20 m shuttle run test was the selected measurement method for the assessment of cardio-respiratory fitness in a resource-constrained setting due to its ease of application [25]. An alternative test, though with smaller samples, is the Harvard step test (HST) [36, 37]. However, using different and technically more elaborated methods such as the cycle ergometer test used by Aandstad et al. [38], the estimated maximal oxygen uptake in 9- and 10-year-old children in Tanzania and Norway is significantly higher compared to the VO2 max of the 20 m shuttle run test (P < 0.001), namely for boys 58.6 ml kg-1 min-1 (95 % CI: 57.3–60.0 ml kg-1 min-1) and for girls 54.7 ml kg-1 min-1 (95 % CI: 52.9–56.5 ml kg-1 min-1) [38]. The estimated VO2 max values generated from the 20 m shuttle run test tend to be high in relation to other direct VO2 max measurement methods, such as maximal watt cycle ergometer test, treadmill or spirometry in laboratory settings. This shift in absolute level of VO2 max is not expected to influence the association signals with infection status, though.

Comparing calculated standing broad jump result means of 118 cm for girls and 132 cm for boys of the present survey with results of the Armstrong et al. study [39], also conducted in South Africa with 2819 girls and 3573 boys of the same age, Armstrong and colleagues measured noticeably longer standing broad jump distances, namely 152 cm for girls and 164 cm for boys.

The highest prevalence of stunting was observed in schools in the region of Hillcrest (22 %) and Helenvale (19 %), where also the highest prevalences of A. lumbricoides and T. trichiura were detected. However, these observations need to be interpreted with caution since current infection status is correlated with long-term growth indicators. Potentially, systematic differences in socioeconomic status and malnutrition levels exist between the study schools.

Only few studies have investigated the distribution of STHs in South Africa. Higher prevalences of hookworm and schistosome infections have been reported from warmer KwaZulu-Natal, located further north than Port Elizabeth [40, 41] compared to the results from our study. In our cohort of primary schoolchildren, heavy T. trichiura and A. lumbricoides intensities were observed in areas built in the 1950s to accommodate 6000 predominantly coloured people but where a recent survey estimated that more than 30,000 people are living in the area [39]. The area is characterised by unhygienic living conditions (poor sanitation and litter), high unemployment and gangsterism. Based on our results, biannual mass deworming should be implemented in the Hillcrest and Helenvale region in order to reduce STH prevalences and thus lower the risk of morbidity, complemented by interventions focusing on WASH [7].

Our study has several limitations. First, results reported here stemmed from a cross-sectional survey and as such we only identified associations rather than causality. Also, current infection status and current effects of past, long-term effects such as stunting are not directly linked. Secondly, it is still debated whether cardiorespiratory performance of children, measured here as maximal oxygen uptake (VO2 max), is receptive enough for change [42] due to varying personal living conditions. Thirdly, only single stool samples were collected from each participant. Hence, some infections, particularly those of light intensity, were possibly missed, as seen in other studies where multiple biological samples and a combination of diagnostic methods were employed [22, 43, 44]. Despite these limitations, the study confirms the practicability of the methods employed as suggested by previous experiences in different African and Asian settings, where school-aged children liked to perform physical fitness tests [45–47].

In the 2004 Global Burden of Disease (GBD) study, heavy A. lumbricoides and T. trichiura infections have both been assigned a zero disability weight (DW) as each of the two infections for itself alone is very rarely fatal, whereas the cognitive impairment resulting from both infections clearly differ, namely 0.463 for A. lumbricoides and 0.024 for T. trichiura on a scale from 0 (no disability) to 1 (death) [48]. In the GBD update 2013, a disease burden of 14.2 disability-adjusted life years (DALYs) per 100,000 person-years is estimated for children below the age of 15 years in South Africa who are infected with A. lumbricoides, while the respective estimate for children infected with T. trichiura is almost 10-fold higher (140 DALYs per 100,000 person-years) [49]. As we observed similar prevalences for A. lumbricoides and T. trichiura [41, 50], it appears that the disease burden of the latter helminth infection in under 15-year-old South African children is higher.

Conclusions

This cross-sectional survey of the DASH study provides new insight into helminth and intestinal protozoa infections, physical fitness and growth of Grade 4 children in quintile three primary schools from disadvantaged communities in Port Elizabeth. Our results indicate that boys who are infected with multiple intestinal parasite species have lower physical fitness levels than their non-infected counterparts, as expressed by the maximal oxygen uptake (VO2 max). A significantly higher T. trichiura prevalence was noted in stunted children and those with a significantly lower Hb level, compared to children not infected with this species. Biannual mass deworming in order to control the morbidity due to STH infections is recommended in school B in Hillcrest and school A in Helenvale.

Abbreviations

BMI: 

Body mass index

BMIZ: 

BMI-for-age Z-score

CI: 

Confidence interval

DALY: 

Disability-adjusted life year

DASH: 

Disease, Activity and Schoolchildren’s Health

DW: 

Disability weight

EKNZ: 

Ethics committee of Northwest and Central Switzerland

EPG: 

Eggs per gram (of stool)

GBD: 

Global Burden of Disease (study)

HAZ: 

Height-for-age Z-score

Hb: 

Haemoglobin

HST: 

Harvard step test

IDW: 

Inverse distance weighting

ISRCTN: 

International standard randomised controlled trial number

NMMU: 

Nelson Mandela Metropolitan University

NRF: 

National Research Foundation

POC-CCA: 

Point-of-care circulating cathodic antigen

RDT: 

Rapid diagnostic test

SD: 

Standard deviation

SNSF: 

Swiss National Science Foundation

SSAJRP: 

Swiss-South African joint research programme

STH: 

Soil-transmitted helminth

VO2 max: 

Maximal oxygen uptake

WASH: 

Water, sanitation and hygiene

WHO: 

World Health Organization

Declarations

Acknowledgements

We are grateful to Mrs. Leyli Zondie, Head of the Department of Medical Laboratory Sciences at the Nelson Mandela Metropolitan University, and her team, Mrs. Lindsey Beyleveld, Deverdene Finnis, Cindy Ackers, Anja Montgomery and Jessica Theron for providing diagnostic support in the laboratory. We thank Danielle Smith, Dominique Bänninger, Stefanie Gall and Thomas Hager for their contribution to data collection. Many thanks go to Mr. Chantel Lamon at ICT International, for the donation of the point-of-care circulation cathodic antigen (POC-CCA) urine cassette tests. In addition, in the name of all the study children, we would like to thank Mr. Joel Huber on behalf of CURAPROX for the donation of the toothbrushes and toothpaste (for an ancillary oral health programme).

Funding

This study is conducted within the scope of the Swiss-South African joint research programme (SSAJRP), financially supported by the Swiss National Science Foundation (SNSF, project no. IZLSZ3 149015) and the National Research Foundation (NRF, project no. 87397) in South Africa. The funders had no role in the study design, data collection and analysis, preparation of the manuscript or decision to publish.

Availability of data and material

The datasets are available from the corresponding author on request.

Authors’ contributions

IM, PY, PS, NP-H, MG, RdR, UP, CW and JU designed the study, established the methods and questionnaires and wrote the original study protocol. All other authors contributed to the development of the study protocol. IM, PY, BPD, NSNH, MG, RdR, UP and CW conducted the study. CW was responsible for community sensitisation. IM managed data entry, cleaning and preparation of the database for statistical analysis, supported by CS and HS. IM wrote the first draft of the manuscript. All authors read and provided comments on the drafts and approved the final version of the paper prior to submission.

Competing interests

The authors declare that they have no competing interest.

Consent for publication

Not applicable.

Ethics approval and consent to participate

This study was cleared by the ethics committees of Northwest and Central Switzerland (EKNZ; reference no. 2014-179, approval date: 17 June 2014), the Nelson Mandela Metropolitan University (NMMU; study number H14-HEA-HMS-002, approval date: 4 July 2014), the Eastern Cape Department of Education (approval date: 3 August 2014) and the Eastern Cape Department of Health (approval date: 7 November 2014). The study is registered at ISRCTN registry under controlled-trials.com (unique identifier: ISRCTN68411960, registration date: 1 October 2014).

The school principals, teaching staff and potential participants were briefed on the purpose, procedures, potential risks and benefits of the study. Meetings with parents or guardians were held to explain the project. Children who were absent from school on the clinical examination day or suffering from any chronic illness were excluded from the physical fitness testing prior to the 20 m shuttle run test. Oral assent from each participating child was sought and individual written informed consent was obtained from parents/guardians. For illiterate parents/guardians, the information sheet available in English, Xhosa and Afrikaans was read aloud in the appropriate language or, if needed, an oral translation of the information sheet into another local language was provided. Participation was voluntary, and hence, children could withdraw from the study at any time without further obligations. To ensure confidentiality, each study participant was given a unique identification number. Children with serious health problems were referred to the local clinic. STH infections were managed free of charge according to WHO and national treatment guidelines.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Swiss Tropical and Public Health Institute, Basel, Switzerland
(2)
University of Basel, Basel, Switzerland
(3)
Department of Sport, Exercise and Health, University of Basel, Basel, Switzerland
(4)
Institute of Infectious Disease and Epidemiology, Tan Tock Seng Hospital, Singapore, Singapore
(5)
Faculty of Education, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa
(6)
Department of Human Movement Science, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa

References

  1. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383:2253–64.View ArticlePubMedPubMed CentralGoogle Scholar
  2. Hotez PJ, Alvarado M, Basáñez MG, Bolliger I, Bourne R, Boussinesq M, et al. The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014;8:e2865.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Yap P, Wu FW, Du ZW, Hattendorf J, Chen R, Jiang JY, et al. Effect of deworming on physical fitness of school-aged children in Yunnan, China: a double-blind, randomized, placebo-controlled trial. PLoS Negl Trop Dis. 2014;8:e2983.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, et al. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly. 2012;142:w13727.PubMedGoogle Scholar
  5. Yap P, Du ZW, Chen R, Zhang LP, Wu FW, Wang J, et al. Soil-transmitted helminth infections and physical fitness in school-aged Bulang children in southwest China: results from a cross-sectional survey. Parasit Vectors. 2012;5:50.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Grimes JET, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR. The relationship between water, sanitation and schistosomiasis: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2014;8:e3296.View ArticlePubMedPubMed CentralGoogle Scholar
  7. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11:e1001620.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Pillay P, Taylor M, Zulu SG, Gundersen SG, Verweij JJ, Hoekstra P, et al. Real-time polymerase chain reaction for detection of Schistosoma DNA in small-volume urine samples reflects focal distribution of urogenital schistosomiasis in primary school girls in KwaZulu Natal, South Africa. Am J Trop Med Hyg. 2014;90:546–52.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Steinmann P, Utzinger J, Du ZW, Zhou XN. Multiparasitism: a neglected reality on global, regional and local scale. Adv Parasitol. 2010;73:21–50.View ArticlePubMedGoogle Scholar
  10. Shirley DA, Moonah SN, Kotloff KL. Burden of disease from cryptosporidiosis. Curr Opin Infect Dis. 2012;25:555–63.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2197–223.View ArticlePubMedGoogle Scholar
  12. World Bank Data. GINI index (World Bank estimate). World Bank. Washington, USA. 2016. http://data.worldbank.org/indicator/SI.POV.GINI/countries. Accessed 21 June 2016.
  13. Marshall SJ. Developing countries face double burden of disease. Bull World Health Organ. 2004;82:556.PubMedPubMed CentralGoogle Scholar
  14. Draper C, Basset S, de Villiers A, Lambert EV, et al. Results from South Africa’s 2014 Report Card on Physical Activity for Children and Youth. J Phys Act Health. 2014;11 Suppl 1:S98–104.Google Scholar
  15. Walter CM. In-school physical activity patterns of primary school learners from disadvantaged schools in South Africa. Afr J Phys Health Educ. 2011;17:780–9.Google Scholar
  16. Boutayeb A. The double burden of communicable and non-communicable diseases in developing countries. Trans R Soc Trop Med Hyg. 2006;100:191–9.View ArticlePubMedGoogle Scholar
  17. Santosa A, Wall S, Fottrell E, Hogberg U, Byass P. The development and experience of epidemiological transition theory over four decades: a systematic review. Glob Health Action. 2014;7:23574.PubMedGoogle Scholar
  18. Yap P, Müller I, Walter C, Seelig H, Gerber M, Steinmann P, et al. Disease, activity and schoolchildren’s health (DASH) in Port Elizabeth, South Africa: a study protocol. BMC Public Health. 2015;15:1285.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Agherdien Y, George AC, Hendricks S. South End as we knew it. Port Elizabeth: Western Research Group; 1997.Google Scholar
  20. Southern Africa Development Research and Training Institute (RaTI). One community many communities: a Nelson Mandela Bay Heritage and History Project (NMBHHP): forced removals in South End, North End, Salisbury Park, Fairview, Willowdene and Korsten. 2013.Google Scholar
  21. Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo. 1972;14:397–400.Google Scholar
  22. Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, et al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008;2:e331.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Coulibaly JT, Knopp S, N’Guessan NA, Silué KD, Fürst T, Lohourignon LK, et al. Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d’Ivoire. PLoS Negl Trop Dis. 2011;5:e1384.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Council of Europe. Testing physical fitness: Eurofit experimental battery. Strasbourg, 1983.Google Scholar
  25. Léger LA, Mercier D, Gadoury C, Lambert J. The multistage 20 meter shuttle run test for aerobic fitness. J Sports Sci. 1988;6:93–101.View ArticlePubMedGoogle Scholar
  26. Léger L, Lambert J, Goulet A, Rowan C, Dinelle Y. Capacité aérobie des Québécois de 6 à 17 ans - test navette de 20 mètres avec paliers de 1 minute. Can J Appl Sport Sci. 1984;9:64–9.PubMedGoogle Scholar
  27. Tomkinson GR, Léger LA, Olds TS, Cazorla G. Secular trends in the performance of children and adolescents (1980–2000): an analysis of 55 studies of the 20 m shuttle run test in 11 countries. Sports Med. 2003;33:285–300.View ArticlePubMedGoogle Scholar
  28. Olds T, Tomkinson G, Léger L, Cazorla G. Worldwide variation in the performance of children and adolescents: an analysis of 109 studies of the 20-m shuttle run test in 37 countries. J Sports Sci. 2006;24:1025–38.View ArticlePubMedGoogle Scholar
  29. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum. 1994;61:1–241.Google Scholar
  31. Abdelrazak MA, Walid FE. Potential complications of Helicobacter pylori infection in children of a non-urban community. Arch Pediatr Infect Dis. 2015;3:e23510.Google Scholar
  32. Richter T, Richter T, List S, Müller DM, Deutscher J, Uhlig HH, et al. Five- to 7-year-old children with Helicobacter pylori infection are smaller than Helicobacter-negative children: a cross-sectional population-based study of 3,315 children. J Pediatr Gastroenterol Nutr. 2001;33:472–5.View ArticlePubMedGoogle Scholar
  33. Kriemler S, Zahner L, Schindler C, Meyer U, Hartmann T, Hebestreit H, et al. Effect of school based physical activity programme (KISS) on fitness and adiposity in primary schoolchildren: cluster randomised controlled trial. BMJ. 2010;340:c785.View ArticlePubMedPubMed CentralGoogle Scholar
  34. Meyer U, Schindler C, Zahner L, Ernst D, Hebestreit H, van Mechelen W, et al. Long-term effect of a school-based physical activity program (KISS) on fitness and adiposity in children: a cluster-randomized controlled trial. PLoS One. 2014;9:e87929.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Imhof K, Faude O, Donath L, Bean-Eisenhut S, Hanssen H, Zahner L. The association of socio-economic factors with physical fitness and activity behaviours, spinal posture and retinal vessel parameters in first graders in urban Switzerland. J Sports Sci. 2016;34:1271–80.Google Scholar
  36. Gallagher JR, Brouha L. A simple method of testing the physical fitness of boys. Am Assn Health Phys Ed Rec Res Q. 1943;14:23–31.Google Scholar
  37. Stephenson LS, Latham MC, Kinoti SN, Kurz KM, Brigham H. Improvements in physical fitness of Kenyan schoolboys infected with hookworm, Trichuris trichiura and Ascaris lumbricoides following a single dose of albendazole. Trans R Soc Trop Med Hyg. 1990;84:277–82.View ArticlePubMedGoogle Scholar
  38. Aandstad A, Berntsen S, Hageberg R, Klasson-Heggebo L, Anderssen SA. A comparison of estimated maximal oxygen uptake in 9 and 10 year old schoolchildren in Tanzania and Norway. Br J Sports Med. 2006;40:287–92.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Armstrong ME, Lambert EV, Lambert MI. Physical fitness of South African primary school children, 6 to 13 years of age: discovery vitality health of the nation study. Percept Mot Skills. 2011;113:999–1016.View ArticlePubMedGoogle Scholar
  40. Global Atlas of Helminth Infections (GAHI). Distribution of soil transmitted helminth survey data in South Africa. London School of Hygiene and Tropical Medicine. London, UK. 2015. http://www.thiswormyworld.org/maps/2013/distribution-of-soil-transmitted-helminth-survey-data-in-south-africa. Accessed 30 June 2016.
  41. Karagiannis-Voules DA, Biedermann P, Ekpo UF, Garba A, Langer E, Mathieu E, et al. Spatial and temporal distribution of soil-transmitted helminth infection in sub-Saharan Africa: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2015;15:74–84.View ArticlePubMedGoogle Scholar
  42. Rowland TW. Aerobic response to endurance training in prepubescent children: a critical analysis. Med Sci Sports Exerc. 1985;17:493–7.View ArticlePubMedGoogle Scholar
  43. Steinmann P, Du ZW, Wang LB, Wang XZ, Jiang JY, Li LH, et al. Extensive multiparasitism in a village of Yunnan province, People’s Republic of China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg. 2008;78:760–9.PubMedGoogle Scholar
  44. Booth M, Vounatsou P, N’Goran EK, Tanner M, Utzinger J. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d’Ivoire. Parasitology. 2003;127:525–31.View ArticlePubMedGoogle Scholar
  45. Ziegelbauer K, Steinmann P, Zhou H, Du ZW, Jiang JY, Fürst T, et al. Self-rated quality of life and school performance in relation to helminth infections: case study from Yunnan, People’s Republic of China. Parasit Vectors. 2010;3:61.View ArticlePubMedPubMed CentralGoogle Scholar
  46. Bustinduy AL, Thomas CL, Fiutem JJ, Parraga IM, Mungai PL, Muchiri EM, et al. Measuring fitness of Kenyan children with polyparasitic infections using the 20-meter shuttle run test as a morbidity metric. PLoS Negl Top Dis. 2011;5:e1213.View ArticleGoogle Scholar
  47. Müller I, Coulibaly JT, Fürst T, Knopp S, Hattendorf J, Krauth SJ, et al. Effect of schistosomiasis and soil-transmitted helminth infections on physical fitness of school children in Côte d’Ivoire. PLoS Negl Trop Dis. 2011;5:e1239.View ArticlePubMedPubMed CentralGoogle Scholar
  48. WHO. Global Burden of Disease 2004 update: disability weights for diseases and conditions. Geneva: World Health Organization; 2004.Google Scholar
  49. Global Burden of Disease (GBD). IHME. Seattle, USA. 2016. http://www.healthdata.org/gbd. Accessed 15 Jan 2016.
  50. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil-transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s). 2016

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate. Please note that comments may be removed without notice if they are flagged by another user or do not comply with our community guidelines.

Advertisement

Parasites & Vectors

ISSN: 1756-3305

Contact us