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Social Science & Medicine 70 (2010) 1131–1140

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Social Science & Medicine

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The numbers, educational status and health of enrolled and non-enrolledschool-age children in the Allai Valley, Northwest Frontier Province, Pakistanq

Andrew Hall a,*, Helen Kirby b

a University of Westminster, Centre for Public Health Nutrition, 115 New Cavendish Street, London W1W 6UW, United Kingdomb Save the Children USA, P.O. Box 1952, Islamabad, Pakistan

a r t i c l e i n f o

Article history:Available online 4 February 2010

Keywords:PakistanSchool-age childrenCensusNon-enrolmentNutritional statusIodine deficiencyGender

q We would like to thank the participants inNetherlands Embassy for funding the Partnership foment of the Allai Valley (PRDA) and this survey.

* Corresponding author. Tel./fax: þ44 207 381 5438E-mail address: ah2108@gmail.com (A. Hall).

0277-9536/$ – see front matter � 2010 Elsevier Ltd.doi:10.1016/j.socscimed.2009.12.021

a b s t r a c t

A cluster survey of the age, sex and enrolment status of all school-age children 5–14 years old wasundertaken in 2006 in a remote rural sub-district of the Northwest Frontier Province, Pakistan abouta year after a devastating earthquake. Information was collected on the characteristics of children, theirhouseholds and parents, and on reasons for non-enrolment. The health and nutritional status ofa randomly selected child in each household was assessed and enrolled and non-enrolled children werecompared by sex. A total of 2032 children were recorded in 925 households, 845 girls and 1187 boys,a sex ratio of 71 girls/100 boys. Half of all girls were not enrolled in school compared with a fifth of allboys. There was no common reason for non-enrolment and they differed between the sexes. Therandomly selected children (n ¼ 897) were moderately malnourished: 43% were stunted, 12% were thinand 46% were anaemic. 66% of a sub-sample of children (n ¼ 269) had a low urinary iodine concen-tration, which could contribute to a low IQ and impaired hearing. There were no statistically significantdifferences in the nutritional status or health of non-enrolled and enrolled girls. These data contributetowards an understanding of how to improve the education and health of school-age children ina conservative, rural province of Pakistan.

� 2010 Elsevier Ltd. All rights reserved.

Introduction

The Northwest Frontier Province (NWFP) of Pakistan is a largeand remote area at the western end of the Himalayas, with a borderwith China to the north and with Afghanistan to the north-west.About 75% of the population are Pashtun, an ethno-linguistic groupthat can also be transliterated as Pushtun, Pakhtun and Pukhtun.The majority of Pashtuns are Sunni Muslims of the Hanafi schooland may also practice an unwritten, pre-Islamic code of livingcalled Pashtunwali that promotes honour, self-respect, indepen-dence, justice and revenge (Economist, 2006). This may contributeto the considerable sectarianism reported in the province that canpit tribe against tribe and village against village (International CrisisGroup, 2005, p. 38). Pashtun religious beliefs and conservativecultural practices typically require the strict segregation of thesexes and may prohibit the education of girls. This representsa conflict with the second Millennium Development Goal (MDG) of

the survey and the Royalr the Recovery and Develop-

.

All rights reserved.

universal primary education by 2015, a goal that has been endorsedby the Government of Pakistan (United Nations MDG Indicators,2008).

In Pakistan all children aged 5–14 years are supposed to beenrolled in basic education: first, in a pre-primary class at the age of5 years, then in primary school for 5 years, followed by a middle orhigh school for 3 years. In 2006 Pakistan had a net primary enrol-ment rate of 66% (United Nations MDG Indicators, 2008) anda gender parity index of 0.76, which ranked it 164 out of 170countries in the world (UNDP, 2007). Enrolment by girls is evenlower in rural areas: only 41% of girls aged 5–9 years were enrolledin school in rural areas of the NWFP in 2007–2008 compared with56% of boys (Pakistan Economic Survey, 2008). Pakistan has a longway to go to achieve the second MDG and information aboutreasons for non-enrolment in schools could help to reach thattarget.

The survey reported here was undertaken in Battagram District,one of 24 districts in the NWFP. The survey occurred a year after anearthquake of magnitude of 7.6 Mw that occurred on Saturday 8October 2005, its epicentre about 19 km north east of Muzzafirabadin Pakistan-administered Kashmir (United States Geological Survey,2005). About 73,000 people were killed of whom 18,000 werechildren attending school at the time (ERRA, 2006). Although 78%

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–11401132

of the 525 schools in Battagram District were described as ‘‘fullydamaged’’, relatively few schoolchildren were killed (ERRA, 2007).

Battagram district includes Allai tehsil, a sub-district occupying anisolated valley. The main town, Banna, is reached by a steep, 37 kmunpaved single-track road from Thakot on the Karakoram Highway.Allai tehsil consists mainly of a valley about 40 km long and 20 kmwide with no paved roads and an area of 804 km2 at an altitude of1500 m above sea level or higher. The livelihoods of the estimated135,000 inhabitants depend mainly on growing barley, wheat, riceand maize, and on remittances (WFP/UNICEF, 2005).

An important consequence of the earthquake was to open thevalley to emergency relief efforts which have since expandedinto long-term development programmes with the aim of‘building back better’, a phrase adopted by the Government ofPakistan’s Earthquake Reconstruction and RehabilitationAuthority to reflect the opportunity presented by the aftermathof the earthquake. To help achieve this aim Save the Children (SC)is working to rehabilitate schools and develop educationservices.

The aims of the survey reported here were: to describe theenrolment status of school-age children, particularly girls, ina representative sample of households in the Allai valley; toexamine reported reasons for non-enrolment, by sex; to examinehousehold factors associated with non-enrolment, by sex; and tocompare the health of enrolled and non-enrolled children, by sex.Data on the enrolment of school-age children may help tounderstand reasons for non-enrolment by both sexes and helppromote the enrolment in school of girls, while data on theirhealth status will help to develop school health services and healtheducation that could increase the perceived value of education toparents.

Subject and methods

The present survey had two parts: a census of the age, enrol-ment status and reasons for non-enrolment of all school-agedchildren in every sampled household; and an assessment of thehealth and nutritional status of one randomly selected index childin each household, plus a questionnaire about socio-economiccircumstances. The survey was approved by the NFWP Ministry ofHealth and by the Executive Officers of Health and Education inBattagram District.

Selection of households and subjects

Thirty villages that had been randomly selected for a needsassessment survey after the earthquake in all eight Union Councilsof Allai tehsil were revisited. The villages had been chosen usinga method in which the probability of selection was in proportion tothe population recorded in 2002 in each of the 134 villages in theAllai valley by a local NGO. Thirty new households were randomlyselected in each village by going to the centre and spinning a pencilon a flat surface. Interviewers then visited every house in bothdirections of the pencil moving towards the edge of the village until15 had been visited by each team; if there were more than 200households in a village then every other household was selected.This method is widely used to undertake 30/30 cluster surveyswhere there is no accurate register of households to randomlyselect (Bennett, Woods, Liyanage, & Smith, 1991). A school-age childwas defined as any child aged between 5 and 14y, the ages at whichchildren in Pakistan should be enrolled in basic education. Thedefinition of belonging to a household was any child of school-ageof a male head of household, alive or dead, living under the sameroof and eating from the same kitchen.

The Interviewer read a statement in Pashto or Gujari to an adultclose relation of the child to explain the survey, and signed,informed consent was obtained. An index child was randomlyselected by asking the respondent to draw a numbered card froman opaque bag containing one card for each child in the householdidentified on the census form. This ensured that there could be noclaim of any bias in selecting a child for study.

A replacement was randomly chosen if the selected child wasacutely ill, if a child had a physical or mental disability, or if thechild was not either at home or school. If the selected child wassubsequently not allowed to take part then a new household wasselected. This was done to avoid any bias against selecting girls forstudy.

Data on all children in households

The sex, age and enrolment status of every school-aged childwas recorded as enrolled, non-enrolled, or dropped out of school.The current school and grade of all enrolled children was recorded,and the last grade of any child who had dropped out. If a child wasnot enrolled the respondent was asked the reason why; up to threereasons were recorded for each child.

Data on a randomly selected child in each household

The following information was recorded: the date of birth or, ifunknown, it was estimated using a local calendar of events; thewhereabouts of the child’s parents, so a child who had lost one orboth parents was classified as an orphan (UNAIDS/UNICEF, 2002);the highest level of education of the child’s mother and father, ifalive, and their occupations; the language spoken in the household;the estimated time in minutes to walk to the nearest primaryschool; the damage caused by the earthquake to the respondent’shouse; the receipt of food aid after the earthquake and currently;the presence of a latrine; and the ownership of a radio, a sewingmachine, a car and livestock as indicators of assets. A sample oftable salt was tested for iodate (Iodine test kit, National Institute ofHealth, Islamabad).

Each child was weighed wearing as few clothes as possible toa precision of 0.1 kg on an electronic scale (Tanita, Japan) checkedeach day using a standard weight. The height of each child wasmeasured to a precision of 0.1 cm using a Leicester stadiometer(Child Growth Foundation, UK). Z-scores of anthropometricmeasurements were calculated using a macro for STATA thatapplies the new WHO reference data (de Onis et al., 2007). Anychild with a z-score of height-for-age, weight-for-age (for childrenaged 5–10 years only) or BMI-for-age less than �2 was classified asstunted, underweight or thin, respectively.

The concentration of haemoglobin in a finger-prick bloodsample was estimated using a portable haemoglobinometer(Hemocue, Sweden) to a precision of 1.0 g/L. The machines werechecked before the survey using low, normal and high controls(Hemotrol, Hemocue, Sweden). The thresholds used to classifychildren as anaemic were<115 g/L for children aged 5–11 years and<120 g/L for children 12–14 years (WHO, 2001). As altitude leads toa haemoglobin concentration in a healthy population that is typi-cally 5 g/L higher at 1500 m than at sea level (WHO, 2001), thisamount was added to these thresholds and children were againclassified as anaemic or not.

A faecal sample was collected from most children in 21 of the 30villages and a direct smear was examined in saline under a micro-scope by a laboratory technician at the hospital in Banna for theeggs and cysts of intestinal parasites. Data on the faecal samplesfrom children in nine villages were unfortunately lost.

Table 1The expected and observed numbers of households that reported having between one and four children (n¼ 903) based on the probability of each combination, and assumingthat the ratio of girls to boys at birth should be 94 girls/100 boys. Also shown are the difference and percentage difference between the observed and expected numbers, thevalue of Chi-squared for the difference between the observed and expected numbers and its statistical significance.

Children in households Combinations Probability Expected no. Observed no. Difference % difference Chi-squared P

1 (n ¼ 283) 1 girl 0.485 137 106 �31 �22.6 13.7 <0.0011 boy 0.515 146 177 31 21.3

2 (n ¼ 313) 2 girls 0.235 74 71 �3 �4.0 16.7 <0.0011 girl, 1 boy 0.500 156 128 �28 �17.92 boys 0.266 83 114 31 37.3

3 (n ¼ 225) 3 girls 0.114 26 25 �1 �3.8 22.0 <0.0012 girls, 1 boy 0.363 82 60 �22 �26.82 boys, 1 girl 0.386 87 87 0 0.03 boys 0.137 31 53 22 72.0

4 (n ¼ 82) 4 girls 0.055 5 3 �2 �44.2 8.7 <0.013 girls, 1 boy 0.235 19 13 �6 �31.22 boys, 2 girls 0.374 31 28 �3 �9.83 boys, 1 girl 0.265 22 27 5 23.04 boys 0.071 6 11 5 86.4

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–1140 1133

A urine specimen was collected from one in every three childrenonly, in order to minimise costs, provide a simple sampling method,yet give an adequate sample size. The concentration of iodine wasmeasured at the National Institute of Health in Islamabad usinga standard colorimetric method after digestion in chloric acid(WHO, 2001). Values <100 mg/L were classified as low (WHO,2001).

Each child was given a physical examination by a person of thesame sex who had been trained by a physician. The two rear molarswere examined on both sides of both jaws (8 M) and the number ofdecayed, missing or filled (DMF) teeth was counted, to give a DMFindex. The hair on of each child’s neck was examined for nits, theegg cases of head lice (Pediculus species). The skin on the whole armwas examined for signs of scabies (Sarcoptes scabei). The upperarms were examined for a BCG vaccination scar, an indicator ofaccess to health services and of caring practices.

All people in the household were offered treatment for intes-tinal worms. Any child with a haemoglobin concentration less than110 g/L was given 30 iron tablets. Every household received six barsof soap and every index child was given a packet of notebooks andcoloured pencils as a small reward for taking part.

Analysis of data

Data were entered into a computer using Microsoft Access. Anage-for-grade index was calculated to reflect late enrolment orretention by giving a score of zero to a child in the right grade at theright age, a score of �1 to a child who was a year late, and so on(Partnership for Child Development, 1999). The data were analysedusing the survey module of STATA version 9 (STATA, 2005) in whichthe village was specified as the cluster. Logistic regression was usedto examine associations between enrolment status and explanatoryvariables. Percentages, risk ratios (RR) and odds ratios (OR) areshown with 95% confidence intervals (95% CI). The statisticalsignificance of differences between proportions or means wereestimated using the Chi-squared test, Mann–Whitney U-test or thelincom post-estimation command in STATA. A value of P of <0.05was taken to be statistically significant.

Results

The survey was done in November 2006, a year after theearthquake. The census recorded 2032 children aged 5–14 years in925 households: 845 were girls (41.6%) and 1187 were boys (58.4%).

Sex ratio

The sex ratio was 71 girls/100 boys, which was significantlydifferent from an expected ratio at birth of 94/100 (P < 0.001), theusual ratio in developed countries (Coale, 1991). If this sex ratio wasapplied to the total sample, there should have been 985 girls and1047 boys, an apparent deficit of 140 girls.

To test if the deficit of girls might have occurred in householdsthat had refused to participate, the sex ratio of children in the 23villages in which 3 or fewer households refused to participate in thecensus (18 out of 702 households asked, or 3%) was compared withthe sex ratio in 7 villages in which 4 or more households refused (63out of 224 households asked, or 28%). There were significantly moreboys than girls in the villages in which �4 households refused toparticipate (Chi-squared ¼ 8.16, P ¼ 0.004). Although the recordedsex ratio was 56 girls/100 boys in the villages in which �4 house-holds refused to participate, in the 13 villages in which all house-holds agreed to participate the sex ratio was still only 77 girls/100boys.

Of the 903 households that reported 4 or fewer children, 39.3%contained only boys while 26.8% contained only girls. Table 1 showsthe observed numbers of households containing between 1 and 4children in all possible permutations of the sexes, with the expec-ted numbers based on a sex ratio of 94/girls/100 boys. Table 1shows that there was a statistically significant excess of all-malehouseholds whether there was only one child in the household orfour.

As no questions were asked about children who may have died,which might help explain the apparent deficit of girls, an analysiswas done of the mean age gap in families of four children. The meanage gap per child in 44 households of four boys was 1.7 yearscompared with 1.3 years in the 12 households of four girls(t¼�2.96, P¼ 0.006). This suggests that there may have been otherchildren in all-boy households but does not take into account thedeath or absence of a youngest or eldest child, so the average agegaps are likely to be underestimates.

Age distribution

There was no significant difference in the mean age of girls andboys recorded in the census (girls 8.44 years vs boys 8.72 years, t ¼�1.75, P ¼ 0.091). Fig. 1 shows the distribution of subjects in 925households expressed as a percentage of the total number of chil-dren in each year of age. The proportion of girls did not differ

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Age group (years)

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Fig. 1. The distribution of children by sex and age expressed as a percentage of thenumber of children in each year of age with 95% CI.

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Percentage girls enrolled

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Fig. 3. A scatter plot of the percentage of girls enrolled in school in each of 30 villagesagainst the percentage of boys enrolled, with the line of equivalence. Two data pointsare identical.

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–11401134

significantly with age but there were statistically significantdifferences in the proportions of boys and girls for all age groupsaged 8 years or older, except for age 10 years.

Fig. 2 shows the distribution of school-age children in 925households as a percentage of the total sample (n ¼ 2032). Thesmaller proportions of children aged 9 or 11 years than 8 or 10 yearssuggests some number bias in reporting age. The smallerpercentage of both boys and girls aged 13 and 14 years comparedwith younger children suggests that there may have been under-reporting of children of both sexes in older age groups, perhapsbecause older children had left home to marry or work, althoughthe trend could reflect general population growth.

Enrolment in school

Of the 2032 children recorded in the census, 66.8% wereenrolled, 28.9% were non-enrolled and 4.3% had dropped out ofschool. For further analysis ‘‘dropped out’’ was combined with non-enrolled. A half of all school-age girls were not enrolled in school(49.9%, n ¼ 845) compared with a fifth of all boys (21.3%, n ¼ 1187)and girls were twice as likely as boys to be non-enrolled (RR ¼ 2.0295% CI 1.82, 2.12, P < 0.001). The gender parity index was 0.71.

Fig. 3 shows a plot of the percentage enrolment of girls in eachvillage against the enrolment of boys, with the line of equivalence.The enrolment of girls was largely independent of the enrolment ofboys. For example there were four villages in which >50% of boyswere enrolled but <15% of girls were in school and there were fourvillages in which >80% of both boys and girls were enrolled.

Fig. 4 shows the distribution of the age-for-grade index sepa-rately for boys and girls. About 30% of boys and 20% of girls wereenrolled at the right age, assuming that their date or birth of age

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Year of age

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Fig. 2. The distribution of children in the census by sex and year of age expressed asa percentage of the total sample (n ¼ 2032).

was known or reported correctly. On average children enrolled inschool were 2.4 years older (95% CI 2.58, 2.24) than they should befor their grade in school, indicating that late enrolment and repe-tition were common. Girls were enrolled on average slightly earlierthan boys, but the difference was not significant (girls�2.20 vs boys�2.50, t ¼ 1.88, P ¼ 0.07).

The most common primary reasons given for non-enrolment inschool were: no single sex school (21.2% of all answers and 32.9% ofall answers concerning girls compared with 1.6% of boys); no school(14.5% of all answers and 17.6% of all answers concerning boys);child too small to go to school (14.4% of all answers and 26.1% of allanswers concerning boys); girls must stay at home or educatinggirls is not useful (20.2% of answers concerning girls); and thedistance to school (8.9% of all answers and similar for both sexes ofchild). These five reasons accounted for 62% of all reasons given.Cost was given as a primary reason for not enrolling 18.0% of boysbut for only 4.1% of girls.

Index children

Table 2 shows data on the socio-economic characteristics of therandomly selected index children for whom the data werecomplete in 897 households. Two thirds of fathers and 97% ofmothers were uneducated while 81% of boys and 54% of girls wereenrolled in school.

Five variables were found by logistic regression to be separatelyand significantly associated with non-enrolment: being female (P<0.001); the time taken to walk to the nearest school (P¼ 0.001); thefather’s educational level (P ¼ 0.001); the father’s occupation

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Fig. 4. The distribution of the percentage of all boys and girls enrolled in schoolseparately by the age for grade index.

Table 2The socio-economic characteristics by sex and enrolment status of randomlyselected index children aged 5–14y in 897 households in 30 randomly selectedvillages in the Allai valley, NWFP, Pakistan. The denominator for each percentage isthe N for each row.

Characteristic Classifications N Non-enrolled

Enrolled

Girls Boys Girls Boys

Sex 897 18.1 11.4 21.5 49.1

Language spoken Pashto 832 18.6 11.5 21.9 48.0Gujari 63 11.1 9.5 17.5 61.9Other 2 0.0 0.0 0.0 100.0

Orphan type Father dead 32 15.6 9.4 18.8 56.3Mother dead 17 29.4 0.0 29.4 41.2Both parents dead 2 0.0 0.0 50.0 50.0Total orphan 51 19.6 5.9 23.5 51.0

Father’s education No education 562 19.6 13.0 18.7 48.8Primary (1–5 years) 101 19.8 11.9 22.8 45.5Middle (6–8 years) 60 13.3 13.3 21.7 53.3High (9–10 years) 117 15.4 8.5 26.5 49.6Higher (11–16 years) 57 10.5 0.0 36.8 52.6

Mother’s education Any education 15 20.0 6.7 26.7 46.7

Father’s occupation Farmer 235 19.6 18.3 12.8 49.4Labourer 227 16.3 15.4 21.1 47.1Shopkeeper 44 20.5 4.5 31.8 43.2Teacher 45 8.9 2.2 35.6 53.3No job 63 20.6 9.5 20.6 49.2Other 249 19.3 4.8 26.1 49.8

Earthquake House destroyed 822 17.8 11.4 21.7 49.1Food aid 836 18.3 11.8 21.1 48.8

Capital items Radio 479 19.0 8.8 22.1 50.1Sewing machine 234 15.4 9.8 28.6 46.2Car 32 28.1 9.4 9.4 53.1

Latrine In household 376 14.6 6.6 29.8 48.9

Animals owned Cattle 497 18.9 14.1 16.3 50.7Sheep or goats 361 18.6 12.7 20.5 48.2Poultry 595 17.0 11.4 21.5 50.1

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(11-16 y)

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Fig. 5. The percentage of girls and boys who were non-enrolled in school with 95% CIaccording to the level of education achieved by the child’s father.

y = -1.435x + 74.943

R2 = 0.1983

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Fig. 6. The average reported time to walk to school in 29 villages (excluding one villagein which enrolment was <5%) against the enrolment of (a) girls and (b) boys with theequation for the line and the value of R2, the proportion of enrolment statisticallyexplained by the time taken to walk to school.

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–1140 1135

(P¼ 0.032); and the absence of a latrine (P¼ 0.016). When all thesevariables were entered into a logistic regression model the sex ofthe child (P < 0.001), the time taken to walk to school (P < 0.001),the father’s education (P ¼ 0.045) and the absence of a latrine(P ¼ 0.018) remained statistically significant.

When these data were analysed separately for each sex,different variables were significantly associated with non-enrol-ment. For boys: the time taken to walk to school (P < 0.001); thefather’s education (P ¼ 0.001); the father’s occupation (P ¼ 0.005);the child’s age (P ¼ 0.007); and the child’s height (P ¼ 0.015). Forgirls: the time taken to walk to the nearest school (P ¼ 0.004); thefather’s education (P ¼ 0.004); and the absence of a latrine (P ¼0.003). The father’s occupation and the age and height of girls werenot significantly associated with non-enrolment.

Fig. 5 shows the percentage of non-enrolled girls and boys bythe father’s level of education. If the father was uneducated, 51% ofdaughters and 21% of sons were not enrolled in school (OR ¼ 3.9, P< 0.001). However, even if the father had received 11 or more yearsof education, 22% of the 29 daughters of such men were notenrolled in school whereas all 30 boys were in school. There wasa weak positive correlation between the percentage of fathers ineach village who had been educated and the percentage of childrenenrolled (r ¼ 0.438, P < 0.02).

As only 2.7% of the mothers of children had received any formaleducation, the sample size was too small for a similar analysis.

Fig. 6 shows that the correlation between the mean time to walkto school and the percentage enrolment in each village was lowerand less statistically significant for girls (r ¼ 0.445, P ¼ 0.02) than

for boys (r¼ 0.635, P< 0.001). Fig. 6 indicates that the time taken towalk to school may explain about 40% of the variance in enrolmentamong boys, but only 20% of the variance among girls.

Nutritional status and infections

Table 3 shows that although boys were on average taller andheavier than girls, there was no difference between the sexes intheir anthropometric indices, haemoglobin concentration orurinary iodine concentration. Fig. 7 shows that BMI-for-age appearsto decline with age, which is indicated by the fact that only 4% ofchildren aged 5–7 years were classified as thin compared with 23%of children aged 12–14 years (P < 0.001).

Table 3The mean and 95% CI of anthropometric and nutritional variables and indices with the statistical significance of the differences. Values have been adjusted for clustering andcorrected for the age distribution of the sample.

Means (units) Girls Boys t or z P

N Mean 95% C.I. N Mean 95% CI

Lower Upper Lower Upper

Weight (kg) 348 21.9 21.4 22.3 520 23.1 22.6 23.6 �4.27 <0.001Height (cm) 355 119.2 118.1 120.1 542 122.3 121.3 123.2 �5.07 <0.001BMI (kg/m2) 348 15.0 14.9 15.2 520 15.1 14.9 15.2 �0.58 0.569Z-score height-for-age 346 �1.836 �1.999 �1.672 534 �1.689 �1.848 �1.531 �1.47 0.152Z-score weight-for-agea 243 �1.359 �1.558 �1.160 340 �1.555 �1.714 �1.396 1.84 0.076Z-score BMI-for-age 339 �0.740 �0.827 �0.652 512 �0.863 �0.979 �0.747 1.96 0.060Haemoglobin (g/L) 354 119.0 117.0 121.0 542 119.6 117.2 122.0 �0.53 0.602Urine iodine (mg/L) 116 73.8 46.8 100.7 153 89.3 64.6 114.0 1.46b 0.144

a Only calculated for children 5–10 years (de Onis et al., 2007).b Mann–Whitney U-test z, as values were not normally distributed.

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–11401136

Iodate was detected in the salt of 30.3% of the 888 householdswho had salt tested (95% CI 24.3, 36.3). Households currentlyreceiving food aid were slightly but significantly more likely to haveiodate detected in their salt than houses not receiving food aid(37.9% vs 26.6%, RR ¼ 1.42, 95% CI 1.16, 1.74, Chi-squared 11.3, P <

0.001). The mean concentration of urinary iodine was 82.6 mg/L (n¼ 269, 95% CI 58.5, 106.7) and the median was 50 mg/L. There wasno significant difference between the sexes (Table 3).

Fig. 8 shows the distribution of the concentration of iodine inurine using a WHO classification: 65.8% (95% CI 52.8, 77.8) of chil-dren had insufficient values while 15.2% (95% CI 5.7, 24.8) hadvalues more than adequate (WHO, 2001, p. 107). There was nodifference in the urinary iodine concentration of children inhouseholds with or without iodated salt (88.7 vs 78.7 mg/L, P ¼0.26).

Table 4 shows that 43% of all children were stunted, 34% wereunderweight, 12% were thin, 46% were anaemic using a thresholdadjusted for altitude, 66% had a low urinary iodine concentration,77% had intestinal worms, 79% were infested with nits and only 25%had a BCG scar. There were no statistically significant differencesbetween the sexes except that girls had a higher prevalence of nitsthan boys (87.6% vs 73.1%, P < 0.001).

The intestinal worms identified in the 550 faecal samplesexamined were Ascaris lumbricoides (67.9%), Trichuris trichiura(26.9%), Hymenolepis diminuta (6.3%), Hymenolepis nana (3.8%) andStrongyloides stercoralis (0.4%). Infections with Giardia duodenalis(13.1%) and Entamoeba spp (21.1%) were also identified.

-3.5

-3.0

-2.5

-2.0

-1.5

-1.0

-0.5

0.0

0.50 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

Age (years)

Mea

n z-

scor

e

Girls Boys

Fig. 7. The mean z-scores of body mass index-for-age for school-age boys and girls inthe Allai Valley, Pakistan. Values are offset either side of the middle of the year of ageso that the 95% CI do not overlap. Data for children aged 13 and 14 years have beencombined. The low value for girls aged 11 years was due to outliers in a relatively smallsample size.

Comparison of non-enrolled and enrolled children

The mean age of non-enrolled girls was not significantlydifferent from enrolled girls (102.9 vs 101.4 months, t ¼ 0.39; P ¼0.70). However non-enrolled boys were about 9 months youngerthan enrolled boys (99.2 vs 108.6 months, t ¼ �3.06, P ¼ 0.005) soall percentages have been weighted for age.

Table 5 shows that there were no statistically significantdifferences between the nutritional status and health of non-enrolled and enrolled children for each sex separately. There werealso no statistically significant differences between non-enrolledboys and girls and between enrolled boys and girls (P values notshown).

Discussion

This census of school-age children in 925 households in a remoterural sub-district of the Northwest Frontier Province of Pakistanfound a sex ratio of 71 girls/100 boys and that only a half of all girlswere enrolled in school. The reasons given for non-enrolment werevaried and differed between the sexes. Although the health andnutritional status of 897 index children was generally not good, girlsdo not appear to be disadvantaged compared with boys in terms oftheir growth, nutritional status and health, as there were nosignificant differences between the sexes whether enrolled or not,or between enrolled and non-enrolled girls.

The low sex ratio cannot be explained by differences in birthrates even though it is usual to find that more boys are born thangirls (Coale, 1991). Data from Sri Lanka, for example, show a sexratio at birth which is similar to the ratio observed in Europe ofaround 95 girls/100 boys (Abeykoon, 1995). The observed sex ratioin the Allai valley is substantially smaller than the ratio reported forPakistan as a whole in the 2006–2007 Demographic and HealthSurvey of 92 girls/100 boys aged 5–9 years and 93 girls/100 boysaged 10–14 years (National Institute of Population Studies, 2008, p.379).

There are two main likely explanations for this apparent deficitof girls. First, households containing girls may have refused to takepart or, if they did agree, girls were deliberately not reported tofieldworkers because of social conservatism. But the lack of girlscannot be explained fully by the refusal to participate by 8% ofhouseholds. This is a relatively small proportion of all householdsand the 81 households that refused would have had to contain anaverage of 1.7 girls each to have produced a sex ratio of 94 girls/100boys. The data shown in Figs. 1 and 2 do not indicate that adoles-cent girls in particular were not being reported: the proportion ofgirls to boys in Fig. 1 was relatively constant across all ages and

05

101520253035404550

<20(insufficient:

severe)

20 to <50(insufficient:moderate)

≥50 to <100(insufficient:

mild)

≥100 to <200(optimal)

≥200 to <300(more thanadequate)

Concentration of iodine (μg/L)

Perc

enta

ge

Girls Boys

Fig. 8. The distribution of the concentration of iodine in urine using a WHO classifi-cation (WHO, 2001, p. 107) among a sample of school-age boys (n ¼ 153) and girls(n ¼ 116) in the Allai Valley, Pakistan.

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–1140 1137

Fig. 2 suggests that there was a smaller proportion of both sexesaged 12–14 years than younger children, so there seemed to be notendency to hide adolescent girls.

The second possible explanation is that girls may have a higherdeath rate than boys. Although more boys tend to be born thangirls, when given similar care during infancy and childhood girls areknown to be more robust than boys and to survive better at all ages(Sen, 1992). The mechanism by which the imbalance in the sex ratiohas occurred and which households might contain unreported girlscannot be told from these data. Data on deaths and birth order,which could shed light on age gaps perhaps due to ‘missing’ girls,were not collected. Table 1 shows evidence of a preference for boyswhether there is one or four children in the household as theprobability of an all-male household increased roughly linearlywith household size: the excess of households with one boy is 21%,two boys 37%, three boys 72% and four boys 86%. Admittedly thenumber of households with four children is relatively small, but thetrend is striking. The wider mean age gap for all-boy householdscompared with all-girl households suggests that there are missingchildren, so accurate information on the number of children born isneeded to take any deaths into account. Future surveys in the NWFPmight ask neighbours how many children there are in nearbyhouseholds, to try to verify the number reported.

The most common cause of an imbalanced sex ratio is a prefer-ence for sons (Hesketh & Xing, 2006). This preference manifests ina number of ways including relative neglect, so that more girls than

Table 4The prevalence of health indicators by sex and in total with 95% CI and the statistical signratios (OR).

Health indicator Girls Boys

n % 95% CI n % 95

Lower Upper Lo

Stunted 355 45.6 39.6 51.7 542 41.1 35Underweight 243 32.9 27.0 38.8 340 35.0 29Thin 355 9.0 4.5 13.5 542 14.8 9

Anaemic (sea level) 354 37.3 30.9 43.6 542 33.2 26Anaemic (1,500 m) 354 47.4 40.1 54.8 542 45.2 37Low urinary iodine 116 72.4 56.7 88.1 153 60.8 47

Any DMF teeth 355 56.6 49.2 64.1 542 55.9 51BCG scar 355 23.4 15.8 30.9 542 26.8 19

Intestinal worms 218 77.1 69.3 84.8 337 76.6 69Nits 355 87.6 81.9 93.3 542 73.1 65Scabies 355 3.9 1.5 6.4 542 1.8 0

boys die during childhood of infectious diseases, perhaps exacer-bated by malnutrition or by relative neglect during illness. Boyshave been shown to be better fed than girls during breastfeeding(Rao & Kanade, 1992) while boys may be more likely to be taken fortreatment when sick with acute diarrhoea (Mitra, Rahman, & Fuchs,2000). A study among poor, urban squatters in Karachi found thatgirls aged 6–18 months were nearly three times more likely to bestunted than boys (Baig-Ansari, Rahbar, Bhutta, & Badruddin,2006). An analysis of (admittedly old) data from surveys in Pakistanin the late 1970s indicated that although boys are more likely thangirls to die in the first month of life, thereafter the probability thatboys survive to 5 years of age was greater than girls (Sathar, 1987).Although there were no significant differences in the health ornutritional status of the girls and boys studied in this survey, if onlythe best nourished and healthiest girls have survived the first fiveyears of life, this is perhaps to be expected. Older girls may alsohave an opportunity to eat if involved with food preparation andmay be less likely than boys to get exercise and lose body weightthan if they are kept at home.

Many reasons were given for non-enrolment and the mostcommon, the lack of a single sex school, was given for only 16.1% ofall answers, so there is no single solution to increasing enrolment.Girls were twice as likely as boys to be non-enrolled and thereasons given were different between the sexes, as were thehousehold socio-economic circumstances associated with non-enrolment. The lack of a single sex school, no school and distance tothe school were given as reasons by just over a half of respondentsconcerning non-enrolled girls, but only 11% said that girls shouldstay at home or not be educated. It is possible that respondentsmight not give this answer knowing that such a response may notbe acceptable to the staff an agency working to improve educationin the Allai Valley. The level of education of the father was related toenrolment of both sexes (Fig. 5), but even the daughters of somerelatively highly educated fathers were not enrolled, so having aneducated father does not guarantee enrolment by girls. As only 3%of mothers had any education it was not possible to do the sameanalysis for women, but the fact that 50% of the next generation ofgirls is enrolled is a promising improvement which suggests thata reluctance to educate girls can be overcome with time. Thisreluctance may be related to the fact that educating a girl will notbenefit the family when she gets married and leaves the household.The lack of a linear relationship between the enrolment of girls andboys in the 30 villages (Fig. 3) suggests that factors vary from villageto village. But it was not possible during this relatively quick surveyto study in more depth the social and cultural reasons for the non-

ificance of differences between the sexes estimated by logistic regression with odds

Logistic regression Total

% CI OR t P % 95% CI

wer Upper Lower Upper

.8 46.5 1.20 1.19 0.245 42.9 38.6 47.2

.2 40.7 0.91 �0.52 0.604 34.1 29.9 38.3

.7 20.0 0.57 �1.81 0.080 12.5 8.7 16.3

.3 40.1 1.19 1.26 0.218 34.8 28.9 40.7

.5 52.9 1.09 0.61 0.549 46.1 39.5 52.6

.4 74.1 1.69 1.64 0.112 65.8 52.8 78.8

.0 60.8 1.03 0.22 0.827 56.2 51.1 61.3

.2 34.3 0.84 �1.46 0.156 25.4 18.3 32.6

.6 83.5 1.03 0.14 0.887 76.8 70.4 83.1

.0 81.1 2.60 5.62 <0.001 78.8 72.2 85.5

.8 2.8 2.18 2.40 0.023 2.7 1.3 4.0

Table 5The prevalence of major health conditions among non-enrolled and enrolled children by sex with the sample size (N), 95% CI and odds ratios (OR) calculated by logisticregression, accounting for clustering in villages, and with the statistical significance of the differences.

Variable Sex Non-enrolled Enrolled Logistic regression

N % 95% CI N % 95% CI OR 95% CI t P

Lower Upper Lower Upper Lower Upper

Stunted Girls 162 42.6 33.2 51.9 193 48.2 41.2 55.1 0.80 0.50 1.26 �1.00 0.325Boys 102 49.0 37.4 60.7 440 39.3 32.2 46.4 1.48 0.82 2.69 1.36 0.185

Underweight Girls 107 32.7 24.1 41.3 136 33.1 25.6 40.6 0.98 0.60 1.61 �0.07 0.944Boys 69 44.9 30.0 59.8 271 32.5 26.3 38.6 1.70 0.88 3.27 1.65 0.111

Thin Girls 162 4.3 1.6 7.0 193 9.3 3.3 15.4 0.44 0.16 1.17 �1.72 0.096Boys 102 7.8 2.7 13.0 440 11.8 7.7 15.9 0.64 0.34 1.17 �1.51 0.141

Anaemic (1,500 m) Girls 161 48.4 38.8 58.0 193 46.6 37.1 56.2 1.08 0.66 1.76 0.30 0.766Boys 102 47.0 37.3 56.8 440 44.7 36.2 53.4 1.10 0.70 1.71 0.42 0.675

Low urinary iodine Girls 52 73.1 55.6 90.5 64 71.9 50.4 93.4 1.06 0.32 3.57 0.10 0.920Boys 32 50.0 27.4 72.6 121 63.6 49.3 77.9 0.57 0.21 1.52 �1.17 0.252

DMF teeth Girls 162 59.9 49.4 70.3 193 53.9 44.5 63.3 1.28 0.74 2.20 0.92 0.366Boys 102 51.0 42.0 60.0 440 57.0 52.0 62.0 0.78 0.56 1.09 �1.50 0.145

Worms Girls 105 77.1 64.7 89.5 113 77.0 67.4 86.6 1.01 0.41 2.46 0.02 0.984Boys 73 76.7 61.3 92.1 264 76.5 69.4 83.6 1.01 0.42 2.44 0.03 0.980

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–11401138

enrolment of girls, something that needs to be addressed by deeperanthropological methods of research, so only superficial associa-tions can be analysed here.

Few respondents mentioned the lack of a female teacher in thelocal school but this may have been conflated with the absence ofa single sex school, so that the sex of the teacher may be asimportant as the sex of the children in the school. Finding qualifiedfemale teachers who are married and wiling to work in sucha remote area is very difficult. As only 3% of mothers had receivedany education it may be a generation before women from the Allaivalley will be qualified enough to return to teach.

Although the reported time taken to walk to school may beinaccurate, it is probably a better indicator of access to schools thanthe linear distance between households and schools because of themountainous terrain in the Allai valley. The average time to walk toschool in each village was only weakly associated with thepercentage of girls enrolled, but was more strongly associated withenrolment of boys (Fig. 6). What may be a short direct distance maytake a considerable time to cover on foot, especially for a smallchild, which may explain why height was associated with theenrolment of boys, who are also more likely than girls to be allowedout of the home. Short stature has been associated with lateenrolment in education in Ghana and Tanzania where short chil-dren are not considered to be ‘grown’ enough to walk a longdistance to school each day (Partnership for Child Development,1999). The lower association with the enrolment of girls could bebecause other factors, such as a lack of girls’ schools, are moreimportant than stature, and distance to walk is a secondaryconsideration for girls’ parents.

Curiously the absence of a latrine in the household was signif-icantly associated with non-enrolment of girls (P ¼ 0.003) but notof boys (P ¼ 0.052). This is most probably indicates confounding:the lack of a latrine may simply be related to independent factorsnot described, perhaps related to poverty or parents’ education.

Girls were enrolled in school slightly earlier than boys accordingto the age-for-grade score, but both sexes were late: on average girlswere 2.2 years older for their grade in school compared with 2.5years for boys, a difference that was not quite statistically significant(P¼0.07). This index obviously depends on the accurate reporting ofage and it is possible that if the date of birth was not recorded,a child’s age was estimated based on stature. For example, a nationalsurvey of schoolchildren in Ethiopia found evidence that children

were enrolled in school when they were tall enough, so they werethen assumed to be 7 years old, the age at which children startschool (Hall, Kassa, Demissie, Tegefie, & Lee, 2008). In rural societiesit is important to enrol children as young as possible because there isan increasing tendency to drop out of school with age, perhapsbecause the opportunity cost of keeping adolescent children inschool becomes too high for a poor family to bear or because theseparation or isolation of girls from boys becomes more importantat puberty. The data from the survey did not indicate this to bea problem as only 87 children were reported to have dropped out ofschool, although a half of them were aged 11–14 years. However thissmall number does not agree with data collected in schools by SC ondrop-outs: 17.1% of 1646 boys and 11.2% of 652 girls who wereenrolled in classes 1–4 in the academic year 2006–2007 were notenrolled in classes 2–5 in the next academic year (SC, unpublisheddata). This suggests that the notion of ‘drop-out’ was either not clearto respondents in the survey or it is flexible, and perhaps parentsintend to re-enrol children in school later on. We have no data onenrolment in school before the earthquake, which may have hadsome effect if children were fearful of returning to where they werewhen the earthquake struck.

This is believed to be the first published general survey of thehealth and nutritional status of rural Pakistani school-age children,both enrolled and non-enrolled, and the first survey in a remoterural sub-district of the Northwest Frontier Province. The surveyfound no major differences between the health, nutrition oranthropometric status of girls and boys or between non-enrolledand enrolled children, but overall both sexes were moderatelymalnourished. Some 43% of all children were stunted and 34% ofchildren aged 5–10 years were underweight compared with 17%stunted and about 31% underweight reported by the NationalHealth Survey of Pakistan for urban schoolchildren. In southernPakistan the prevalence of stunting among rural schoolchildrenaged 6–12 years was also lower, at 16.5% (Khuwaja, Selwyn, & Shah,2005). The overall prevalence of thinness of 12% obscured a trendwith age such that nearly 25% of children in the oldest ages werethin compared with <5% of young children. Nearly a half of allchildren were anaemic and two thirds of the children who provideda urine sample had a urinary iodine concentration classified asdeficient. The mean concentration of iodine in urine was less thana half of the value reported in a survey of schoolchildren in SwatDistrict, also in the NWFP (Ahkhtar, Zahoor, Paracha, & Lutfullah,

A. Hall, H. Kirby / Social Science & Medicine 70 (2010) 1131–1140 1139

2004). No data on goitre were reported because the field team wasnot able to classify palpable goitre reliably enough.

The urinary iodine concentrations were recorded after 93% ofhouseholds had received food aid that provided iodised salt. Thismay explain why some urinary iodine concentrations were morethan adequate, but the lack of an association between the urinaryiodine concentration and the presence of iodated salt in thehousehold suggests that the salt is not always being used. The largeproportion of insufficient urinary iodine concentrations ina mountainous area where people are typically at high risk of goitrerequires concerted efforts to make sure that iodised table salt iseasily available and that it is used. A low iodine intake is associatedwith impaired mental and psychomotor development (Pineda-Lucatero, Avila-Jimenez, Ramos-Hernandez, Magos, & Martinez,2008; Santiago-Fernandez et al., 2004; Tang et al., 2007) and poorhearing (Soriguer et al., 2000; van den Briel, West, Hautvast, &Ategbo, 2001) both of which may have consequences for children’seducation.

The prevalence of anaemia of 46% (accounting for altitude)constitutes a severe public health problem according to the WHOand suggests that most children are iron deficient (WHO/UNICEF/UNU, 2001). It would be sensible to provide children with multiplemicronutrients as there are likely to be deficiencies of vitamin Aand other micronutrients, as well as of iron and iodine.

The prevalence of intestinal nematode worms of 77% warrantsmass treatment at least twice a year according to WHO recom-mendations (WHO, 2006). This prevalence is substantially highereven than among children living in urban slums in Pakistan(Mehraj, Hatcher, Akhtar, Rafique, & Beg, 2008). The high preva-lence of head lice, which is rarely recorded during surveys and hasbeen called an ‘underestimated realm’ (Heukelbach & Feldmeier,2004), may be related to crowded sleeping places and the freezingconditions in winter which discourage washing. There is evidencethat this is a common and widespread problem in Pakistan (Sad-dozai & Kakarsulemankhel, 2008).

There were no existing school-based health services in the Allaivalley before this survey. The data provide good evidence of a needfor services such as periodic deworming followed by multiplemicronutrient supplements (Hall, 2007), perhaps most beneficialduring the winter months when fresh fruit and vegetables are inshort supply. There is considerable international experience thatteachers can give simple, mass treatments to all pupils when theprevalence of deficiencies and infections are moderate to high (Hallet al., 2002; Roschnik, Parawan, Baylon, Chua, & Hall, 2004; Siddiqui,Rahman, & Jaleel, 2004; WHO, 2006). Since the earthquake the WHOin Pakistan have constructed six prefabricated health units in theAllai Valley and are training ‘Lady’ Health Workers and male HealthPromoters to deliver basic health services and provide healtheducation (WHO Pakistan, 2006a, 2006b).

School feeding may also have role in improving enrolment in theNWFP: the Tawana Project reported that enrolment in participatingschools increased by an average of 40% and attracted previouslynon-enrolled girls (Badruddin et al., 2008). The project also isreported to have led to a 45% drop in the prevalence of wastingfrom 14.5% initially (Pappas et al., 2008), but there were noconcurrent, untreated controls to account for secular changes andseason. Health education to promote teeth brushing and personalhygiene would also be useful.

Although only schoolchildren will benefit from school-basedhealth services we estimate that around two thirds of all school-agechildren are enrolled in basic education in the Allai Valley. Effortsare now being made to promote the enrolment of the other third, ofwhom almost two thirds are girls, so that there is progress in theAllai Valley towards the second Millennium Development Goal ofuniversal primary education.

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