Background: Representative surveys collecting weight, height and MUAC are used to estimate the prevalence of acute malnutrition. The results are then used to assess the scale of malnutrition in a population and type of nutritional intervention required. There have been changes in methodology over recent decades; the objective of this study was to determine if these have resulted in higher quality surveys. Methods: In order to examine the change in reliability of such surveys we have analysed the statistical distributions of the derived anthropometric parameters from 1843 surveys conducted by 19 agencies between 1986 and 2015. Results: With the introduction of standardised guidelines and software by 2003 and their more general application from 2007 the mean standard deviation, kurtosis and skewness of the parameters used to assess nutritional status have each moved to now approximate the distribution of the WHO standards when the exclusion of outliers from analysis is based upon SMART flagging procedure. Where WHO flags, that only exclude data incompatible with life, are used the quality of anthropometric surveys has improved and the results now approach those seen with SMART flags and the WHO standards distribution. Agencies vary in their uptake and adherence to standard guidelines. Those agen- cies that fully implement the guidelines achieve the most consistently reliable results. Conclusions: Standard methods should be universally used to produce reliable data and tests of data quality and SMART type flagging procedures should be applied and reported to ensure that the data are credible and therefore inform appropriate intervention. Use of SMART guidelines has coincided with reliable anthropometric data since 2007. Keywords: Survey, Anthropometry, Nutrition, Child, Weight-for-height, Weight-for-age, Height-for-age, Mid-upper arm circumference, MUAC , Data quality, Standard deviation, Kurtosis Background appropriate interventions. The surveys estimate the Over the past 30 years, it has become increasingly com- scale and type of nutritional intervention required so mon to use a single round of anthropometric measure- that personnel with relevant skills, logistics and funds ments from a representative sample of children, aged can be requested and mobilised. Where there are many 6–59 months, to assess a population’s nutritional state, malnourished children programs are implemented to particularly in areas thought to be under nutritional identify and treat the affected children; the planning stress. These cross-sectional, population-based surveys is mainly based upon data collected by Governments are used to estimate the prevalence of acute malnutri- and non-government organisations (NGO). At about 5 tion, poor growth attainment, and mortality rates as fun- yearly intervals either UNICEF’s multiple indicator clus- damental health indicators. They can then be interpreted ter surveys (MICS) or USA’s Demographic and Health with contextual information to plan and implement Surveys (DHS) collect information on a large range of health, socio-economic, demographic and environmen- tal variables as well as anthropometric status to give a *Correspondence: Emmanuel.Grellety.Bosviel@ulb.ac.be general overview of a country’s health status [1, 2]. Pro- Research Centre Health Policy and Systems - International Health, viding accurate estimates of the prevalence of stunting, School of Public Health, Université Libre de Bruxelles, Brussels, Belgium wasting and underweight of children is also important Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/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://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 2 of 13 for monitoring individual, country and global progress children per cluster, and non-use of a weight-for-height toward the goals of eradicating hunger, reducing health index. Prudhon and Spiegel  analysed reports only inequalities and assessing the ensuing progress of short- and found them to be inadequate. They were sufficiently and long-term nutrition and health interventions. Mal- inadequate for Spiegel to call for surveys to be conducted nutrition prevalence and mortality rate are the primary by professionals only , largely because they found that statistics; when high, the contextual data can be used to 65% of surveys prior to 2004 were of insufficient quality interpret the potential causes and indicate which strate- to be relied upon . gic interventions are most appropriate to add to the pri- In response to this situation the Standardized Monitor- mary aim of identifying and treating the malnourished. ing and Assessment of Relief and Transitions (SMART) u Th s, in humanitarian emergencies, timely and accu - initiative aimed to simplify and standardize all aspects of rate data are essential to guide decision making by public conducting a survey, including planning, training, sam- health care professionals. The survey’s results together pling, data collection, analysis, data quality estimation with an estimate of the population size show the mag- and reporting . Since the introduction of SMART and nitude and urgency of an affected population’s immedi - Emergency Nutrition Assessment (ENA) software  ate needs and give a baseline to initiate monitoring the in late 2002 many agencies started to adopt these stand- evolution of the emergency and evaluation of the inter- ard methods and most non-governmental organisations vention with follow-up surveys. The data also enable gov - (NGOs) and many governments had adopted SMART by ernments and United Nations (UN) agencies to properly 2007. In particular they have used the automatic analy- coordinate the overall response and allows donors to sis of the data and the inbuilt facility to statistically check allocate funds appropriately and effectively. the data quality (“plausibility check”) to provide feedback These activities all depend critically upon the accuracy to the supervisors concerning the performance of the and credibility of the survey data. enumerators and an estimate of the credibility of the data There have been guidelines for assessing nutritional for presentation to those relying upon survey results . status of individuals since the generation of reference Several steps are involved in assessing the quality of values from a healthy population; these have been suc- anthropometric data such as estimating bias in sampling cessively refined from the Baldwin-Wood , Harvard procedures, age and anthropometric errors, and how , NCHS , CDC  and more recently to the missing and improbable values are handled. The shape of WHO references . However, the first guideline to the distribution (skewness and kurtosis) and the observed propose estimating the prevalence of acute malnutrition standard deviation (SD) of the Z-scores are important of populations from cross-sectional surveys specifically statistics that indicate the quality of the data. With accu- using weight-for-height (WHZ) in Z-scores (standard rate age estimates and anthropometric measurements, deviations of a reference population), instead of percent- the SD of the observed distributions should approximate of-median, was published in 1983 by the World Health to symmetry when the population is undernourished and Organisation (WHO)  to guide the Word Food Pro- have an SD close to the expected value of 1.0 with respect gram on criteria for admission to supplementary feed- to the reference distribution. ing programs. Following further recommendations from Based on the WHO Technical Report , the SD for WHO in 1989 , Epicentre published guidelines for Weight-for-Height (WFH) should be between 0.8 and 1.2 conducting small-scale population based surveys in 1992 Z-score units in all well-conducted surveys [18, 28, 29]. [10, 11]. At this same time, survey sampling schemes for This has been confirmed empirically with well conducted use in complex humanitarian emergencies were explored surveys in both the developed world where large national [12–14]. These initiatives were incorporated in an inter - surveys of heterogeneous populations have been con- national guideline [15, 16] and used to develop the first ducted, for example the National Health and Nutrition software (Epinut)  dedicated to analysis of small- Examination Survey (NHANES) from USA’s National scale cross-sectional nutritional surveys. These initiatives Centre for Health Statistics (NCHS)  and the devel- were followed in 1995 by WHO’s seminal publication on oping world . The SD increases substantially as the anthropometry which incorporated and expanded upon proportion of random measurement errors in the dataset all of the earlier works . increases ; this has a greater effect upon the preva - The application of these survey methods and the accu - lence of wasting (WHZ and/or MUAC), underweight racy of the data produced by various humanitarian agen- (WAZ) and stunting (HAZ) than is usually appreciated. cies have been criticised [19–24]. Spiegel et al.  found The size of the SD and the number of missing, implau - gross deficiencies on the basis of failure to use popula - sible or flagged subjects give an overall measure of the tion proportional to size sampling, small sample size, care with which the enumerators collected and recorded inadequate number of clusters, insufficient number of their data, and hence a survey’s credibility. With a single Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 3 of 13 enumeration team a systematic error does not have an particular parameter on the basis that a measurement effect upon the shape or SD of the distribution; how - was most likely to be incorrectly measured or recorded, ever, with more than one enumeration team, the SD also or that they did not properly represent the population increases if the various teams have different systematic being surveyed. Similarly, for absolute MUAC (MUAC- measurement biases (unpublished: present authors). abs), where the MUAC-for-age Z-scores (corrected for The objective of this paper was to examine the change any height deficit) were more than 3.100 Z-scores above of survey quality over time using the change in the distri- or below the survey’s mean the absolute MUAC values bution of the anthropometric variables as a criterion of were flagged and excluded for the analyses using SMART survey reliability, and in particular to determine the qual- flagging. As WHO recommends retaining all values that ity of surveys since Prudhon’s analysis in April 2004 . are not biologically implausible, the analysis was repeated excluding only those children whose HAZ, WAZ, WHZ Methods or MUAC lay outside the limits considered to be compat- We performed a secondary analysis of 1843 surveys. The ible with life specified by WHO . surveys had been conducted in 55 different countries in For each survey the mean, standard deviation and West Africa (315), Middle Africa (312), East Africa (337), moments of kurtosis and skewness were calculated with Sahel (657), Northern Asia (60), South Asia (106), Cen- their 95% CIs . We compared the mean of the SDs of tral America (7), Europe (3), Middle East (1) and the Car- WHZ obtained from each of the 19 different organisa - ibbean (45) between 1986 and 2015 (Table 1). Detailed tions and the combined “other” organisations. descriptions of the study populations and methods have Agency “s” contains the grouped surveys from the 11 been published previously . In brief, un-cleaned raw “other” organisations. The SD of organisation “t” differs datasets of anthropometric surveys were obtained from significantly from the others (Student’s t test < 0.0001), 19 agencies working in the field of international nutrition with 69% (53/77) of their surveys for WHZ having an (NGOs, United Nations Agencies and Governments). SD of more than 1.2 Z. This organisation was impaired Data from 11 further agencies that contributed fewer by gross insecurity; consequently all aspects of their sur- than 5 surveys were also obtained (designated as “other”). veys were managed remotely from a separate country. The individual survey datasets were initially cleaned by Relatively inexperienced persons were recruited locally, deleting the records of individual children with any of there was no performance testing of enumerators and the following criteria: 1) Age < 6 months (n = 26,951), there was inadequate supervision. It became clear that 2) Age > 59 months (n = 11) and 3) Age, sex, weight, or some of data from some of the surveys had been fabri- height not recorded (10,610, = 0.74% of data). Children cated as blocks of data were replicated from one survey with oedema were also excluded as their anthropometry to another. We therefore omitted this organisation’s data is affected by the oedema fluid (6748 = 0.47% of data). from the main analyses. It became clear from inspection Weight-for-height/length (WHZ), height-for-age of the individual files that agency “u” had censored their (HAZ), weight-for-age (WAZ), mid-upper arm circum- data before we obtained the files. This was shown by quite ference (MUAC) for age (MUAC-AgeZ) and height severe truncation of the tails of the distributions so that (MUAC-HtZ) indices were calculated in Z-scores using each of this agencies’ surveys were unlike any of the other ENA software for SMART . The WHO growth surveys in our database. However, we have included these standards were used for all calculations. The MUAC-for- 8 surveys for completeness (0.5% of surveys). age standards and the height-for-age standards were used We then compared the mean SDs and moments of to derive the MUAC-for-height values. First the “height- excess kurtosis (kurtosis—3) and skewness of all indices age” of each child was calculated (that is the age the child over time using both SMART and WHO flagging pro - would be if the child was 0.00 Z-score height-for-age); cedures. The time periods were chosen to correspond to second the MUAC-for-height was calculated using the major advances in survey methodology. MUAC-for-age procedure, except that the height-age was All analyses were performed in R software version 2.9.2 substituted for the chronological age. Such a procedure . effectively compares the MUAC of the child to that of a child of the same height as the child. The algorithms are Ethics statement incorporated in the ENA software. This is a secondary analysis of anonymous data where In each survey, outliers were excluded using either no individual, cluster or village location could be iden- WHO or SMART flags (Table 1). For SMART flags, tified so that formal ethical clearance was not required. children with a HAZ, WAZ, WHZ and MUAC-AgeZ Permission to use and analyse the datasets was obtained which were more than 3.100 Z-scores above or below from the organisations providing the raw datasets. the survey’s mean were excluded from the analysis of that Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 4 of 13 Table 1 The numbers of surveys, children, oedematous children and percent of subjects flagged using either WHO or SMART flags (excluding oedema), by country Region Country Surveys # Subjects # Oedema % Weight-for-age Height-for-age Weight-for-height MUAC-for-age MUAC-for- Height WHO SMART WHO SMART WHO SMART WHO SMART WHO SMART Northern Asia Afghanistan 55 47,079 0.17 0.10 1.22 0.84 4.15 0.09 1.56 0.03 0.63 0.01 0.41 Europe Albania 1 906 0.00 0.00 1.32 0.33 5.96 0.00 1.43 0.00 0.22 0.00 0.11 Middle Africa Angola 45 38,377 0.77 0.03 1.30 0.86 4.95 0.06 1.39 0.03 0.98 0.01 0.89 South Asia Bangladesh 30 18,407 0.10 0.02 0.39 0.33 1.79 0.01 0.48 0.01 0.11 0.01 0.10 West Africa Benin 7 7897 0.06 0.00 0.72 0.18 2.15 0.00 0.76 0.00 0.56 0.00 0.29 West Africa Burkina Faso 67 41,544 0.11 0.02 0.57 0.11 1.44 0.02 0.60 0.01 0.36 0.01 0.24 East Africa Burundi 32 21,095 1.37 0.09 1.27 1.12 4.04 0.08 1.20 0.02 0.94 0.00 0.68 Middle Africa Cameroon 9 6034 0.17 0.03 1.18 0.46 3.88 0.08 1.36 0.00 0.60 0.00 0.38 Middle Africa CAR 49 37,031 0.59 0.01 1.06 0.32 3.52 0.03 0.97 0.01 0.74 0.01 0.57 Middle Africa Congo-B 1 878 0.46 0.00 0.80 0.00 2.96 0.00 0.91 0.00 0.23 0.00 0.11 Middle Africa DRC 208 183,478 1.11 0.05 0.79 0.59 2.40 0.04 0.87 0.01 0.79 0.01 0.70 East Africa Eritrea 2 1628 0.31 0.00 1.29 0.61 3.93 0.25 1.84 0.00 0.12 0.00 0.06 East Africa Ethiopia 73 64,459 0.23 0.02 0.61 0.23 2.74 0.02 0.67 0.01 0.42 0.00 0.36 West Africa Gambia 8 6792 0.04 0.01 0.66 0.13 1.62 0.06 0.81 0.00 0.28 0.01 0.16 Latin America Guatemala 2 1430 0.14 0.21 2.03 1.33 3.99 0.42 1.96 0.00 1.47 0.00 0.98 West Africa Guinea 17 12,922 0.20 0.02 1.19 0.46 3.10 0.06 1.52 0.02 0.75 0.02 0.58 West Africa Guinea Bissau 4 2440 0.08 0.04 1.39 0.61 3.16 0.08 0.78 0.00 0.49 0.00 0.33 Caribbean Haiti 45 36,100 0.41 0.02 1.30 0.39 3.63 0.04 0.89 0.02 0.76 0.01 0.51 South Asia India 9 5712 0.16 0.23 1.09 1.17 4.11 0.02 0.88 0.00 0.47 0.00 0.26 South Asia Indonesia 1 394 0.00 0.00 1.02 0.51 5.33 0.00 4.57 0.00 1.52 0.25 1.52 West Africa Ivory Coast 6 7711 0.74 0.06 1.19 0.43 3.64 0.08 1.23 0.00 0.93 0.00 0.74 East Africa Kenya 49 33,690 0.30 0.00 0.35 0.19 2.27 0.02 0.51 0.01 0.29 0.00 0.25 Europe Kosovar 1 921 0.00 0.00 1.41 0.22 2.61 0.11 0.76 0.00 0.33 0.00 0.22 West Africa Liberia 76 51,361 0.58 0.06 1.51 0.56 4.71 0.08 1.44 0.02 0.83 0.01 0.68 Europe Macedonia 1 863 0.00 0.00 1.51 0.70 5.91 0.23 1.85 0.12 0.70 0.12 0.60 East Africa Madagascar 6 4145 0.43 0.02 1.18 0.63 3.93 0.10 0.92 0.02 0.84 0.00 0.51 East Africa Malawi 34 20,551 1.12 0.07 1.92 1.22 4.82 0.08 1.95 0.02 1.11 0.01 1.00 Sahel Mali 15 20,060 0.26 0.02 0.86 0.52 4.52 0.16 1.50 0.02 0.47 0.02 0.38 Sahel Mauritania 51 40,772 0.09 0.03 0.47 0.21 1.85 0.05 0.58 0.00 0.36 0.00 0.29 East Africa Mozambique 14 3922 2.32 0.05 2.27 0.82 8.36 0.26 1.56 0.05 1.27 0.00 0.98 South Asia Myanmar 15 11,233 0.17 0.06 0.76 0.66 2.73 0.05 0.56 0.04 0.48 0.00 0.38 South Asia Nepal 7 4351 0.44 0.09 0.41 0.97 2.39 0.05 0.69 0.02 0.23 0.00 0.21 Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 5 of 13 Table 1 (continued) Region Country Surveys # Subjects # Oedema % Weight-for-age Height-for-age Weight-for-height MUAC-for-age MUAC-for- Height WHO SMART WHO SMART WHO SMART WHO SMART WHO SMART Latin America Nicaragua 2 969 0.83 0.00 1.55 0.41 2.27 0.00 0.62 0.00 0.83 0.00 0.42 Sahel Niger 38 47,284 0.09 0.06 0.82 0.51 3.37 0.06 0.87 0.01 0.45 0.01 0.34 West Africa Nigeria 45 30,325 0.11 0.04 1.13 0.41 3.43 0.07 1.54 0.02 0.71 0.00 0.57 South Asia Pakistan 27 24,807 0.13 0.07 0.94 0.50 2.73 0.06 0.97 0.01 0.64 0.00 0.50 South Asia Philippians 7 3937 0.00 0.03 0.86 0.25 2.90 0.08 0.71 0.00 0.30 0.00 0.20 East Africa Rwanda 22 12,204 1.26 0.02 1.23 0.57 4.13 0.09 1.52 0.06 0.79 0.04 0.65 Sahel Senegal 39 30,531 0.09 0.01 0.60 0.18 2.60 0.02 0.51 0.01 0.32 0.01 0.22 West Africa Sierra Leone 71 57,717 0.41 0.04 1.49 0.45 4.32 0.08 1.52 0.07 1.20 0.02 0.99 Sahel Somalia 102 78,271 0.78 0.03 1.14 0.46 4.63 0.07 2.56 0.03 0.99 0.02 0.87 Sahel South Sudan 198 142,796 0.39 0.03 1.23 0.44 5.04 0.14 1.54 0.03 0.70 0.02 0.56 South Asia Sri Lanka 5 4599 0.02 0.00 0.33 0.07 1.28 0.00 0.37 0.02 0.28 0.00 0.20 Sahel Sudan 86 72,672 0.15 0.04 0.84 0.29 3.67 0.08 1.01 0.00 0.39 0.00 0.32 Middle East Syria 1 534 0.19 0.00 0.94 0.75 4.32 0.38 1.69 0.00 0.75 0.00 0.38 Northern Asia Tajikistan 5 4643 2.30 0.11 2.39 0.80 6.14 0.30 3.79 0.04 1.31 0.00 1.08 East Africa Tanzania 13 6890 1.38 0.06 1.12 0.70 4.12 0.17 1.65 0.06 1.00 0.06 0.96 Sahel Chad 128 91,539 0.29 0.03 0.71 0.18 2.87 0.03 0.85 0.02 0.39 0.00 0.30 South Asia Thailand 2 1813 0.00 0.06 0.77 0.66 2.70 0.06 0.77 0.00 0.11 0.00 0.06 South Asia Timor 3 1690 0.00 0.06 0.59 0.65 3.96 0.18 0.83 0.00 0.53 0.00 0.30 West Africa Togo 14 6550 0.56 0.02 0.61 0.15 2.15 0.05 0.52 0.00 0.43 0.00 0.23 East Africa Uganda 83 52,255 0.33 0.03 1.10 0.35 3.41 0.05 1.11 0.01 0.64 0.00 0.52 Latin America Venezuela 3 1776 0.17 0.06 0.56 0.06 1.24 0.06 0.23 0.00 0.11 0.00 0.00 East Africa Zambia 6 3496 0.00 0.00 1.20 0.51 4.66 0.00 1.23 0.00 0.74 0.00 0.49 East Africa Zimbabwe 3 1361 0.00 0.00 1.18 0.51 5.00 0.00 1.91 0.00 0.73 0.00 0.74 Total Total 1843 1412,842 0.48 0.04 0.98 0.45 3.49 0.07 1.16 0.02 0.66 0.01 0.53 The number of subjects column is the number of subjects remaining after exclusion of oedema and missing data. WHO flags = all biologically possible data. SMART flags = data that is more than 3.100 SD from the mean of the survey. DRC = Democratic Republic of Congo; CAR = Central African Republic; Congo-B = Congo Brazzaville Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 6 of 13 Fig. 1 The mean standard deviation in Z-score units of nutritional surveys contributed by different agencies. Agency “a” to “r” and “t” are from single agencies and “agency s” in from 11 different agencies combined that contributed fewer than 5 surveys. The error bars are SDs. The agencies are mainly emergency international non-governmental organisations with 2 governmental and 2 UN agencies Results The mean of WHZ SDs of the surveys from each of the agencies is shown in Fig. 1. The numerical data, by agency, are given in Additional file S1. The agencies’ means varied from about 1.00 Z to over 1.15 Z. The two Fig. 2 The mean standard deviation in Z-score units of nutritional agencies with mean values of over 1.10 were group “s”, surveys by time. The surveys that were contributed by the agencies which is composed of the 11 agencies contributing fewer shown in Fig. 1, divided by the date of the surveys: from 1986 to 2002, 2003 to 2006 and 2007 to 2015. The dates mark changes in survey than 5 surveys that did not apply or use the SMART methodology guidance guidelines, and agency “t” which had inadequate supervi- sion and has been excluded from the main analysis. Although each agency had a different mean SD for and 2015 by the 18 single organisations and the 11 other WHZ, some contributed surveys before standardisation agencies. The data are shown using WHO and SMART was introduced and others started to use SMART meth- flags separately. The SDs have steadily decreased with ods at different intervals (several years) after the guidance both flags from around 1.1Z to 1.0Z using SMART flags, was first introduced. The agency data are thus divided as the quality of surveys has improved and the plausibil- by range of years in Fig. 2. Prior to 2003 only 3 of the 12 ity tests have become more widely used. The mean kurto - (25%) contributing agencies had a mean SD of less than sis of the distributions are very small and negative using 1.05Z and none were at or below 1.00Z. Between 2003 SMART flags; in contrast they are larger and positive and 2006 when agencies were introducing the standard when the WHO flags are used to include all biologically guidelines 8 of the 16 (50% excluding groups “s” and “t”) plausible data. The mean kurtosis of the data cleaned agencies had mean values of less than 1.05Z. From 2007, with SMART flags has been almost zero since 2007. The 10 of the 13 (77%) agencies had values less than 1.05 Z data, on average, have a slight negative skew, which was of which most were close to 1.00Z. Other agencies that initially significantly less with the SMART than with the are relatively new to conducting surveys (“j”, “k”, “m”) had WHO flags. With time, the skewness has reduced. slightly higher mean SDs. Two of the agencies had mean With time the discrepancy between the SD, the skew- values below 0.95 Z. Each of the agencies contributing ness and, since 1997, kurtosis using the WHO flags and surveys undertaken in more than one period had a reduc- the SMART flags has become steadily smaller. Inclu - tion in mean SD except agency “j” and “k”. As the differ - sion of all biologically possible data (WHO procedure), ent agencies trained, implemented and became familiar that would be excluded using SMART flags, results in with SMART there was a reduction in the mean SD of a higher SD, a greater moment of skewness and much their surveys to be close to the expected SD of 1.0Z of the larger kurtosis than with the SMART procedure. With WHO standards. a well conducted survey there should be few, if any, data Figure 3 shows the WHZ distribution from 1766 sur- points flagged for removal from a survey. If no data are veys (excluding agency “t”) conducted between 1986 Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 7 of 13 that with both flagging procedures they are relatively small. Deviations of these moments within plus or minus one unit are generally considered to indicate that the data come from a normally distributed population; this is [36– 38] the case with the surveys using SMART flagging, but not for kurtosis using WHO flags as shown by the magni - tude of the SD-error bars. For each time period the distri- bution of the SDs, moments of kurtosis and moments of skewness are much greater when WHO flagging proce - dures are used than when SMART flags are applied. And with improvements in data quality the results obtained with the two flagging procedures approach one another. Figure 4 shows the corresponding mean SDs for all the anthropometric variables using SMART flags in the upper panel and WHO flags in the lower panel. The abso - lute MUAC is shown in the lower panel (units are mm). These data confirm the observations reported for WHZ with each of the other variables. The SDs of each varia - ble have reduced over the time-span that these data have been collected. With each of the variables the results of using the SMART flagging procedure results in a lower SD than with WHO flag excluded data. The highest SDs are for height-for-age, and the reduction in their SDs with time is most marked when WHO flags are applied (from 1.5 Z to 1.3 Z). The mean MUAC-ageZ and MUAC-htZ SDs are now less than the WHO standards. There has also been a marked reduction in the absolute MUAC’s SDs from 13.5 to 12.2 mm (11%). The corresponding change in kurtosis is shown in Fig. 5. In terms of data quality the moment of kurtosis is a measure of the amount of data that is in the tails of the distribution relative to a Gaussian distribution; the shape of the central portion of the distribution has a neg- Fig. 3 The mean standard deviations, moments of kurtosis and of skewness by date of survey for weight-for-height/length ( WHZ). ligible effect upon the moment of kurtosis . A posi - All survey data except for that contributed by agency “t”. The tive kurtosis indicates that the tails are long and contain blue columns are for the surveys when applying World Health outliers, a negative kurtosis indicates that the tails are Organisation criteria for excluding presumably erroneous data points shorter than expected compared to a Gaussian distribu- and the red columns using SMART criteria for data exclusion. The tion. Using WHO flags there is a much larger and posi - error bars above the columns are the standard errors of the mean and below the columns the standard deviations tive kurtosis for all the anthropometric variables (except absolute MUAC) indicating longer tails and excess outli- ers. There has been a reduction in WHZ, WAZ and HAZ kurtosis between 1997 and post-2007 using both flagging flagged then the two analyses’ flagging procedures would procedures indicating a general increase in the quality of give identical results. The data shown in Table 2 dem- data. Using SMART flags there was initially a small nega - onstrates that between 1986 and 2015 the discrepancy tive kurtosis with a reduction in the kurtosis of WHZ, between the results obtained with the two flagging pro - WAZ to almost zero after 2007; the kurtosis for each of cedures has diminished, indicating that with time there the MUAC variables is close to zero when SMART flag - are far fewer erroneous data points being recorded in ging is applied. a survey’s dataset that require either form of flagging. The mean moments of skewness are shown in Fig. 6. u Th s, the reduction in the discrepancy is an indication Positive skewness indicates that the right tail of the distri- of the improvement of data quality with time. Although bution is longer or fatter than expected with a Gaussian there are differences in the mean moments of kurtosis distribution whereas a negative skewness indicates that and skewness of the surveys, it is important to consider the left tail is similarly asymmetric. However moments Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 8 of 13 Table 2 Change in number of surveys with WHZ SD above 1.2Z over 30 years Date Survey SD > 1.2 WHO SD > 1.2 SMART SD > 1.2 WHO SD > 1.2 SMART Difference # # # % % WHO-SMART 1986–1996 212 90 39 42.5 18.4 24.1 1997–2003 325 80 17 24.6 5.2 19.4 2003–2007 364 57 17 15.7 4.7 11.0 2007–2015 865 55 16 6.4 1.8 4.5 All survey data except for that contributed by agency “t”. The dates are selected to mark changes in survey methodology. The difference between WHO and SMART flags give the difference in the WHZ SD when all biologically possible values (WHO) and only values statistically likely to be true values (SMART ) are included in the dataset. The differences in the data represent the care with which the enumerators measured height and weight and with an error-free survey should tend to zero data has resulted in a large positive skew (relatively more high weights) in the WAZ data. The plots of the individual survey’s SD by the actual date the survey was performed for each of the anthro- pometric variables and flagging procedures are shown in Supplementary File 2. They confirm the summary data presented and show that since 2007 there has not been a further reduction in shape or spread of the distribution the anthropometric variables of interest. The supplemen - tary material also shows that there has been no change in the mean age or height of the subjects included in the surveys over the time-span of the data reported. This indicates that the children, during the time span of the surveys, have not changed and would not account for any change in the distribution of the variables (n.b. a random error of measurement does not alter the mean value of a variable, only its statistical distribution). There has been a slight reduction in the mean absolute weight of the chil- Fig. 4 The standard deviations for anthropometric variables by dren surveyed. time. All survey data except for that contributed by agency “t”. The standard deviations of height-for-age (HAZ), weight-for-age ( WAZ), weight-for-height/length ( WHZ), MUAC-for-age (MUACageZ), Discussion MUAC-for-height (MUAC HtZ) each in Z-score units and absolute Our results show that there has been an improve- MUAC in mm, by date of conducting the survey. The upper panel ment in the distributions of anthropometric variables shows the data applying SMART flags and the lower panel with WHO flags. The error bars above the columns are the standard errors of the used to assess the prevalence of malnutrition over the mean and below the columns the standard deviations past 30 years. Since 2007 the surveys have a mean SD for WHZ, WAZ, MUAC-ageZ and MUAC-HtZ vari- ables which are close to the theoretical of 1.00Z with a of skewness can be difficult to interpret because a long small standard deviation of about 0.05Z as well as tiny tail on one side can be balanced by a fat, but shorter, tail moments of kurtosis and skewness. This is in contrast to on the other side. Nevertheless, it is an indication of the the analysis of surveys prior to 2004 which were heavily symmetry of the data. With SMART flags there is a slight criticised by Prudhon and Spiegel . negative skewness with a marginal reduction with time HAZ always has a higher SD in such surveys because for most of the variables; there is a larger negative skew of the errors inherent in age estimation; even an error of with HAZ. This indicates that using SMART flags there 2 months can increase the SD from 0.0Z to 1.45Z and a is slightly more of a tail on the malnourished end of the random error of 3 months to about 2.0Z . Nearly all distribution; this indicates that the flagging procedure surveys show age “heaping” at 6 month intervals. has not stripped excess negative (i.e. malnourished chil- As survey protocols, training, cluster sampling dren) values from the dataset relative to positive values. schemes, cleaning criteria and feedback using the plausi- The skewness using WHO flags has generally lessened bility check, have been progressively taken up by agencies with time; however, including all biologically possible there has been a marked improvement in data quality. Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 9 of 13 In the past survey managers had no method of assess- ing the data quality until after the survey was completed and analysed, and there was no standard report format with space indicated for essential narrative informa- tion to be incorporated. As the software analyses and “writes” the basic report, analytical and clerical errors are reduced and essential information is prompted . Also the automatic data quality procedures, built into the ENA software, has enabled survey managers to check on both the overall quality and the performance of each of the enumeration teams separately as the survey is in progress. They can identify any under-performance, need for re-training, changing or additional supervision to correct defects and errors . Prior to the introduc- tion of SMART in 2002 many surveys had a higher than acceptable SD. As agencies began to adopt and become familiar with these standardised methods to conduct a nutritional survey between 2003 and 2007 there was an Fig. 5 The moments of kurtosis for anthropometric variables by time. improvement in data quality. Since 2007, most agencies All survey data except for that contributed by agency “t”. The kurtosis of height-for-age (HAZ), weight-for-age ( WAZ), weight-for-height/ that used the guidance provided by SMART produce length ( WHZ), MUAC-for-age (MUACageZ), MUAC-for-height (MUAC surveys whose data quality has stabilised with a mean HtZ) and absolute MUAC (MUAC Abs), by date of conducting the SD of close to 1.00 Z scores. The agencies that have not survey. The upper panel shows the data applying SMART flags and followed this guidance (e.g. group “s”) or have not been the lower panel with WHO flags able to be supervised because of major security concerns (e.g. group “t”) have remained with a high SD. This is also clearly shown by comparison of the data obtained by 3 different survey protocols at approximately the same time in countries in West Africa . The reduction in SD over time by the agencies that implemented SMART methods and the failure to reduce the SD when older methods have persisted or supervision has been poor, confirms that the SD is a useful measure of the care with which the teams have collected and recorded the measurements. This is reinforced by the different performance of the var - ious agencies. Despite adequate guidelines, nutrition sur- veys are still not always done with methodological rigour by some agencies; and “remote” supervision from head- quarters nearly always leads to poor quality data (this was the problem with agency “r”). Our data demonstrate that agencies get different mean SD values from others. Such differences cannot be ascribed to variations in the popu - lations being surveyed but reflect upon the degree of staff training, supervision and application of recommended methods. The WHO standards are based upon centiles which have been converted into Z-scores; these are different Fig. 6 The moments of skewness for anthropometric variables from the use of the term Z-score in the statistical lit- by time. All survey data except for that contributed by agency erature because the numerical difference between 0 and “t”. The skewness of height-for-age (HAZ), weight-for-age ( WAZ), − 1Z is not the same as between − 1 and − 2Z etc. In this weight-for-height/length ( WHZ), MUAC-for-age (MUACageZ), way the slight positive skewness of most populations has MUAC-for-height (MUAC HtZ) and absolute MUAC (MUAC Abs), by been “normalised” to a Gaussian distribution using the date of conducting the survey. The upper panel shows the data applying SMART flags and the lower panel with WHO flags LMS (lambda-mu-sigma) procedure  and the data are expected to be normally distributed. The reference Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 10 of 13 population has been selected from 6 populations from assessment and reporting were all automated in the soft- different continents; an undoubtedly heterogeneous ware, without the user having to understand the math- sample. It is expected that a similarly heterogeneous ematics or use the formulae involved. This was meant to population in a sample will also approximate to a normal address the severe criticisms of surveys that were being Gaussian distribution. Indeed, large heterogeneous sam- reported and used to guide policy and humanitarian ples taken with stringent control of data quality, such as intervention [19–24]. the NHANES surveys of the USA by the NCHS, approxi- Corsi et al.  and Grellety and Golden  examined mate to a Gaussian distribution with a standard deviation the differences in distribution between MICS, DHS and of 1.0 Z [18, 28]. An ethnically homogeneous popula- National Government surveys (using SMART), each of tion may thus have a lower SD than the WHO standards. which used different guidelines and methods (all using Most of the surveys included in the present analysis were WHO flags). They report that the SDs of the MICS and from ethnically homogeneous populations and yet their DHS surveys were substantially higher than the National SDs approximated to 1.00Z. It would appear that the Government surveys and frequently outside the accept- homogeneity of the population does not have a marked able range. effect upon the anthropometric parameters considered in It appears that the precision with which MUAC is assessing malnutrition. This accords with the similarity of taken has also improved. Frison et al.  suggest that the different data-sets that were combined by WHO in statistical approaches relying on the normal distribution establishing their standards. assumption can be successfully applied to MUAC. How- There are always random measurement errors and this ever, we have no data to explain why the mean SDs for the always leads to an increase in the SD of a variable . In MUAC variables are less than one. We speculate that this other words, unless errors are all trivial, the SD is always is due to ethnic differences in fat patterning as usually greater than the true SD of the population. Importantly our surveys individually came from ethnically homoge- the effect is not reduced by an increase in sample size, as neous populations whereas the standards were deliber- is sometimes assumed . Where several enumeration ately derived from heterogeneous populations. There are teams are used and one or more of the teams has a sys- greater ethnic differences on body fat distribution than in tematic bias in a measurement, this will also result in an other anthropometric measurements [32, 44]. increase in the “spread” of the data and hence an increase There is controversy over which flags should be used in the SD. For most anthropometric measurements the to avoid bias caused by including erroneous data in the SD from single surveys should lie between 0.8 and 1.2 analysis. The recommended WHO procedure makes , with about 80% between 0.9 and 1.1Z . For these the assumption that all data that is compatible with life reasons the SD has been used as a useful measurement of and biologically possible has been accurately taken and data quality [25, 29, 41]. We have used this parameter to should be included in the analysis. The proportion of the examine whether there has been a change in the quality data excluded because they are not possible measure- of surveys with the introduction of standardised meth- ments is also a good indicator of data quality. It is likely ods of conducting surveys. Prior to 1992 there were rela- that the higher the proportion of impossible data the tively few anthropometric surveys performed. With the higher the proportion of erroneous measurements that introduction of Epi-info incorporating Epi-nut software, are included in the dataset. However, it is an unrealistic many more small-area surveys were performed to assess assumption that there are no errors of measurement; individual population’s nutritional status; however, there there are always errors. If these are minimised and triv- were few epidemiologists available to be involved, the ial it will make little difference to the results. However, command-line driven software required specific exper - as we have shown, the greater the error the wider the SD tise to use, sampling often used “spin-the-pen”  and and the higher the prevalence of abnormality shown by other biased sampling methods and it was thought that the analysis . Survey SDs are therefore always over- random error would not affect the results provided a suf - estimated to a greater or lesser extent; and that extent ficient sample size was achieved . In late December determines the level of over-estimation of the preva- 2002 SMART guidelines and software was introduced lence of malnutrition. This is a statistical reality. Indeed, at an international conference organised by the United the consistently high SD for HAZ because of errors of States Agency for International Development (USAID) age estimation are testimony to the difficulty in obtain - in Washington. SMART specifically addressed the gaps ing accurate data and the effect of inaccurate data. As the left by previous guidelines and was designed to allow data has improved in quality the results obtained with non-epidemiologists to sample, train, acquire, analyse WHO-flagging and SMART-flagging have converged. and report high quality nutritional data. Aspects such as This itself is an indication that the results using SMART the sampling frame, sample size calculation, data quality Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 11 of 13 flagging are more accurate than those which incorporate Conclusion all biologically possible measurements. Weight, height and MUAC based anthropometric indica- SMART flags use statistical probability to assess tors are used worldwide to characterize the nutritional whether data points are likely to be erroneous or accu- status of populations. This study shows that the mean SD rate. The flags are based on the observed population of these parameters approximate to the distribution of mean as opposed to the mean of the standards. They the WHO standards coincidentally with the introduction are set at a fixed number of standard deviations from and uptake of simplified survey guidelines, automatic this mean. Theoretically, if the SD is 1.00Z then one true data quality checks and software have been introduced data point will be outside ± 3.10 Z from the mean out of and implemented. Those agencies that have not fol - a sample of 1000 subjects. Such individuals undoubtedly lowed the guidelines obtain inflated prevalence figures exist and are remarked upon by enumerators, but the from anthropometric surveys. The results also show that false exclusion of 1/1000 of the dataset would have a triv- exclusion of data based upon SMART flag cut-off points, ial effect upon a reported prevalence. However, there are rather than including all data that is compatible with life normally many more than 1/1000 subjects outside this further improves data quality of anthropometric surveys. limit in less than well-done surveys and statistically most Agencies vary in their uptake and adherence to standard of these are errors. The SMART procedure assumes that guidelines; this is reflected in the mean SD values of the these values are errors and should be excluded. Inclusion surveys they contributed; those agencies that have fully of such erroneous values will generate a positive kurtosis embraced SMART achieve distributions of survey data (see Fig. 5) as seen when only WHO flags are used and similar to the WHO standards. Standardization tests the outliers are included in the analysis. The fact that with  should be performed and reported systematically training the mean SDs over the years using the two flag - to confirm the ability of the staff to perform sufficiently ging procedures have converged indicates the improve- precise and accurate measurements. Analysis of the qual- ment of data collection. Furthermore, the post 2007 data ity of anthropometric data is only a subset of the infor- for SD, kurtosis and skewness indicate that using a cut-off mation that is needed to assess the overall quality of a point of ± 3.100Z is appropriate, rather than using wider population-based survey. Well-defined and internation - “windows-of-inclusion”. ally accepted criteria to assess survey quality should be Crowe et al.  reported that the effect of survey’ universally applied and reported if the surveys are to be cleaning criteria on the estimation of wasting prevalence reliable, credible and form the basis for appropriate inter- with WHO flags criteria is more ‘inclusive’ (and thus vention and command donor support . tend to give higher prevalence results) whereas SMART Additional files flags are more ‘exclusive’ (and thus give lower prevalence results). We agree with Crowe’s analysis; the question to Additional file 1. Details of the surveys by agency. be answered is which gives a more reliable estimate of Additional file 2. Plots of individual survey’s anthropometric variables. the true prevalence? Our theoretical analysis  and the All survey data except for that contributed by agency “t”. XY plots of the present data indicate that using SMART flags results in a individual survey SDs against the actual date of the survey for respectively: more reliable estimate and the WHO procedure consist- WHZ, HAZ, MUAC-for-age, WAZ, MUAC-for-height, absolute MUAC (each applying SMART and WHO flags), chronological age, absolute weight and ently over-estimates the prevalence unless the survey is absolute height. The polynomial regression lines are shown in red. of very high quality. A limitation of this study is that most of the studies come from stressed African populations and children Abbreviations from Latin America, South and South-East Asia are rela- DHS: demographic and health surveys; ENA: emergency nutrition assessment; tively under represented. HAZ: height-for-age Z-score; MICS: multiple indicator cluster surveys; MUAC : mid-upper arm circumference; MUAC-AgeZ: MUAC for age z-score; MUAC- Furthermore, the surveys included were not classified HtZ: MUAC for height Z-score; NCHS: National centre for health statistics; by other measures of data quality apart from the shape of NGO: non-government organisations; NHANES: National health and nutrition the distribution. This was because for many of the studies examination survey; SD: standard deviation; SMART : standardized monitoring and assessment of relief and transitions; UN: United nations; USAID: United we did not have access to the full narrative report; it is on states agency for international development; WAZ: weight-for-age Z-score; the basis of such narrative reports that others have criti- WHO: World health organization; WFH: weight-for-height; WHZ: weight-for- cised the quality of surveys [19–24]; to our knowledge height Z-score. this is the first report to examine such a large number of Authors’ contributions surveys using the internal structure of the numerical data EG and MHG were involved in all stages from the conception and design, to assess the actual quality of the data analysed. data acquisition, analysis and interpretation. Both authors approved the final version of the article. Grellety and Golden Emerg Themes Epidemiol (2018) 15:8 Page 12 of 13 Author details 8. World Health Organization. Measuring change in nutritional status. Research Centre Health Policy and Systems - International Health, School Guidelines for assessing the nutritional impact of supplementary feeding of Public Health, Université Libre de Bruxelles, Brussels, Belgium. Department programmes for vulnerable groups. Geneva: World Health Organization; of Medicine and Therapeutics, University of Aberdeen, Aberdeen, Scotland, 1983. http://apps.who.int/iris/bitst ream/10665 /38768 /1/92415 41660 .pdf. UK. 9. Mora J. A new method of estimating a standardized prevalence of child malnutrition from anthropometric indicators. Bull World Health Organ. Acknowledgements 1989;67:133. https ://www.ncbi.nlm.nih.gov/pmc/artic les/PMC24 91240 / We sincerely acknowledge all those individuals and organizations who have pdf/bullw ho000 60-0030.pdf. generously contributed anonymous survey data over the past 20 years. They 10. Coulombier D, Pécoul B, Desvé G, Moren A. Enquêtes nutritionnelles come from many different organizations. These data were used to improve anthropométriques rapides (ENAR) en situation précaire. Cahiers d’études survey methods, develop the use of appropriate cleaning methods and exam- et de recherches francophones/Santé. 1992;2(6):377–84. ine the relationships between anthropometric variables. Most have indicated 11. Coulombier D, Pécoul B, Desvé G, Moren A. Enquêtes nutritionnelles : that they would prefer not to be individually acknowledged. The names of analyse et interprétation de l’indice poids-taille. Cahiers d’études et de the agencies that generated different quality data will remain undisclosed. EG recherches francophones/Santé. 1992;2(6):385–9. gratefully acknowledges the studentship provided by Nutriset. We would also 12. Toole M, Malkki RM. Famine-affected, Refugee and displaced popu- like to thank Professor Philippe Donnen for all the assistance he has given to lations: Recommendations for Public Health Issues, Morbidity and enable this work to be completed. Mortality Weekly Report. Centers for Disease Control (U.S.), International Health Program Office. 1992; 41/No. RR-13. https ://stack s.cdc.gov/view/ Competing interests cdc/13566 . The authors declare that they have no competing interests. 13. Binkin N, Sullivan K, Staehling N, Nieburg P. Rapid nutrition surveys: how many clusters are enough? Disasters. 1995;16:99–103. https ://doi. Availability of data and materialsorg/10.1111/j.1467-7717.1992.tb003 83.x. The data that support the findings of this study are available on request from 14. United Nations. Administrative Committee on Co-ordination. Sub- the corresponding author [EG]. 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