SHORT COMMUNICATION

European Journal of Clinical Nutrition (2005), 1–4

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SHORT COMMUNICATION Iodine nutrition among indigenous Tarahumara schoolchildren in Mexico J Mona´rrez-Espino1,2* and T Greiner1,3 1 Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden; 2Instituto Mexicano del Seguro Social, Coordinacioń de Investigacioń en Salud, Me´xico, DF, Me´xico; and 3PATH, Washington, DC, USA

This paper adds iodine data to the nutritional survey recently published in the Eur J Clin Nutr (2004;58:532–540) to identify growth retardation and micronutrient deficiencies among Tarahumara children from five selected indigenous boarding schools in Mexico. Total goiter rate (TGR) (n ¼ 384), urinary iodine concentrations (UI) (n ¼ 100), and iodine content of salt were measured. Overall, TGR was 7.0% (grade 1 ¼ 6.8%, grade 2 ¼ 0.2%). The median UI of the group was 125 mg/l, while the median UI across the schools ranged from 92.0–156.5 mg/l, with 32 and 6% of the children having UI between 50–99 mg/l and 20–49 mg/l, respectively. The iodine content in all the salt packages checked at the schools was above 25 parts per million. Based on TGR and UI, there is a marginal iodine deficiency in this sample of children, probably due to an insufficient iodine intake. These results add to existing evidence that iodine deficiency still constitutes a public health problem in certain populations living in the mountainous regions in Mexico.

European Journal of Clinical Nutrition advance online publication, 6 July 2005; doi:10.1038/sj.ejcn.1602214 Keywords: goiter; iodine deficiency; micronutrients; Mexico; schoolchildren; Tarahumara; urinary iodine

We have recently published a nutritional survey among Tarahumara children from indigenous boarding schools in an isolated mountainous area of northern Mexico (Mona´rrez-Espino et al, 2004). However, in our previous study, we made an incomplete assessment, as urinary iodine concentrations (UI) were not included. This brief report aims at adding these data. In September 2003, we returned and sampled children from the same five schools as previously surveyed (Mona´rrezEspino et al, 2004). These schools had been chosen for variation in characteristics such as location, altitude, infrastructure, size of enrolement, and accessibility. Schools I and II represented the ‘better-off’ and the ‘poor’, respectively, based on amount and quality of buildings, furniture, and other equipment; School III was designated ‘overcrowded’,

*Correspondence: Dr J Mona´rrez-Espino, Instituto Mexicano del Seguro Social, Coordinacioń de Investigacioń en Salud, Centro Me´dico Nacional Siglo XXI, Unidad de Congresos, Bloque B – 4to piso, Col. Doctores, 06725 Me´xico DF, Me´xico. E-mail: [email protected] Guarantor: J Mona´rrez-Espino. Contributors: JME was the main writer and was involved in the entire research process, and TG contributed to the study design, interpretation of the results and writing of the manuscript. Received 1 December 2004; revised 26 April 2005; accepted 23 May 2005

hosting twice the average number of schoolchildren; School IV was the ‘traditional’ school, located in an area with a strong presence of Tarahumara customs; and School V was typical of the subtropical ‘gorge’ environment, where fruits and vegetables grow. We evaluated thyroid size by inspection and palpation in all available schoolchildren aged 6–14 y (n ¼ 384; boys ¼ 179, girls ¼ 205) to calculate the total goiter rate (TGR) using the WHO simplified 3-stage classification of goiter severity (0: normal, 1: palpable, 2: visible) (ICCIDD-UNICEF-WHO, 2001). We collected casual urine specimens from a random subsample of 100 children (20 per school), stratified to obtain equal numbers of boys and girls. UI excretion has been characterized as a good marker of recent dietary iodine intake and has been recommended for the assessment of a population’s iodine nutrition (ICCIDD-UNICEF-WHO, 2001). The children urinated in clean plastic containers and this was transferred to 10 ml assay tubes containing no preservatives. The tubes were tightly sealed and kept at room temperature for 2 weeks when 0.5–1.0 ml aliquots were taken for laboratory analysis at the National Institute for Diagnosis and Epidemiological Reference (INDRE) of the Secretary of Health in Mexico City, an internationally recognized reference center with high-quality laboratory control

Iodine nutrition among Tarahumara schoolchildren in Mexico J Mona´rrez-Espino and T Greiner

2 standards. Duplicate UI was determined using the Sandell and Kolthoff method (Dunn et al, 1993). In addition, the iodine content of salt used for food preparation at the selected schools was checked using a colorimetric method (Mannar and Dunn, 1995). Salt samples from the kitchens and storerooms were tested in each school using a field test kit (UNICEF, 600017 Madras, India). The iodine content was estimated by comparing the color with a visual scale for 25, 50, 75, and 100 parts per million (p.p.m), with an accuracy of 710 p.p.m. Median UI was 122.5 mg/l (boys 129.0; girls 116.5) ranging from 92.0 mg/l in the traditional school to 156.5 mg/l in the overcrowded school. Overall, 38 and 6% of the sampled children had UI below 100 and 50 mg/l, respectively, but there was a mixed pattern across the schools, with a better status in the overcrowded, poor, and better-off schools compared to the gorge and traditional schools, where more than half of the children had UI o100 mg/l (Table 1). The traditional school also had the highest proportion of children with UI suggestive of mild or moderate deficiency (45 and 15%, respectively), and the overcrowded school had the smallest proportions (15 and 0%, respectively). TGR in the whole sample (n ¼ 384) was 7.0% (grade 1 ¼ 6.8%; grade 2 ¼ 0.2%), ranging from 5.5% in the poor school to 8.2% in the traditional and better-off schools, with girls (7.8%) and boys (6.1%) similarly affected (Table 2). These results are very similar to those previously reported (TGR 5.4%; grade 1 ¼ 5.1%, grade 2 ¼ 0.3%) (Mona´rrezEspino et al, 2004). According to the epidemiological criteria for assessing the severity of iodine deficiency, based on median UI (Dunn et al, 1993), only the traditional and gorge schools could be classified as having mild iodine deficiency. On the other hand, all five schools presented a prevalence of goiter between 5 and 19%, which is the criteria to define a mild

public health problem (Dunn et al, 1993). Traditional, gorge, and better-off schools with the highest TGR (B8%) also had the highest proportion of children with UI o49 mg/l (5–15%). Thus, this study adds to other evidence that iodine deficiency still constitutes a public health problem in certain populations living in mountainous regions in Mexico (Martıńez-Salgado et al, 2002; Va´squez-Garibay et al, 2002). Diets based on foods grown in mountainous regions, such as those inhabited by the Tarahumara, often provide inadequate iodine in the normal diet (Koutras et al, 1985). This can be corrected by iodizing salt. In this survey, the iodine content in the salt packages checked at the schools sampled was above 25 p.p.m. However, the detrimental effects of cooking practices common at the boarding schools could partially explain these relatively low UI levels. It has been estimated that

Table 2 Prevalence of goiter and total goiter rate (TGR)a in Tarahumara schoolchildren aged 6–14 y stratified by school and sex, northern Mexico, 2003 Goiter classification—n (%) Stratified group

0: No goiter

School Better-off Poor Overcrowded Traditional Gorge

45 68 107 45 92

Sex Boys Girls Total

168 (93.8) 189 (92.2) 357 (93.0)

1: Palpable

(91.8) (94.4) (93.8) (91.8) (92.0)

3 4 7 4 8

(6.1) (5.5) (6.1) (8.1) (8.0)

10 (5.5) 16 (7.8) 26 (6.7)

2: Visible 1 0 0 0 0

TGR(%)

(2.0) (0) (0) (0) (0)

8.1 5.5 6.1 8.1 8.0

1 (0.5) 0 (0) 1 (0.2)

6.1 7.8 7.0

a

TGR: palpable þ visible goiter (ICCIDD-UNICEF-WHO, 2001).

Table 1 Distribution of urinary iodine concentration (UI) in casual morning samples (in mg/l) among Tarahumara schoolchildren aged 6–14 y stratified by school and sex, northern Mexico, 2003 Proportion of children by UI levela Stratified group

Median (25th–75th percentile)

200–299

100–199

50–99

20–49

n

15 15 25 10 5

55 50 60 30 45

25 35 15 45 40

5 0 0 15 10

20 20 20 20 20

School Better-off Poor Overcrowded Traditional Gorge

129.0 116.0 156.5 92.0 101.0

Sex Boys Girls

129.0 (69.0–185.7) 116.5 (82.2–148.7)

18 10

44 52

30 34

8 4

50 50

Total

122.5 (74.7–166.2)

14

48

32

6

100

a

(73.5–192.7) (73.7–188.2) (139.0–198.5) (61.7–140.2) (71.0–139.0)

The epidemiological criteria used, based on UI/iodine status, was o20 mg/l: insufficient/severe deficiency; 20–49 mg/l: insufficient/moderate deficiency; 50–99 mg/l: insufficient/mild deficiency; 100–199 mg/l: adequate/optimal; 200–299 mg/l: more than adequate/risk of iodine-induced hyperthyroidism (ICCIDD-UNICEF-WHO, 2001).

European Journal of Clinical Nutrition


3 losses during cooking can vary from 20 to 40% (ICCIDDUNICEF-WHO, 2001). Women preparing the schools’ meals could be taught ways to minimize loss of iodine, such as adding salt at the end of the cooking process. Another possible explanation for our UI findings relates to the food the children eat at home. In an earlier study (Mona´rrez-Espino et al, 2001), we used the same kits to measure the iodine content in salt from 133 Tarahumara households and found that 19.5% contained no iodine (unpublished results). Children receive meals at the boarding schools on 200 days a year (INI, 2002); thus they eat nearly half of the time at home. Therefore, improved monitoring by health inspectors may be necessary to ensure that only iodized salt is on sale to the public. The iodine content of salt needs to be periodically monitored at all levels, using test kits and being rechecked by titration, since it has been reported that such kits do not provide a reliable quantitative estimate of the iodine content, and tend to overestimate the iodine levels in salt (Pandav et al, 2000). It is also worth noting that the traditional and gorge schools were the most geographically marginalized among the five sampled, and also presented the highest risk of iodine deficiency. Therefore, families living in those isolated areas could have more difficulties reaching places where iodized salt is on sale. There is very little published data on the frequency of use of iodized salt in meals of schoolchildren living in Mexico and no data at all for the Tarahumara to be able to determine the level of iodization in discretionary salt (ie in cooking and at the table) that will be sufficient to maintain adequate iodine intakes. However, the relatively low prevalence of low UI reported from a sample of 585 children aged 5–12 y in the National Nutrition Survey of 1999 (50–99 ¼ 5.9%, 20– 49 ¼ 2%, o20 ¼ 0.5%) was attributed by the authors to the mandatory iodization of the salt Mexicans eat at their tables for the last 50 y in Villalpando et al, (2003). In the same article, the authors report that measurements on the iodine content in table salt were in the expected range; however, none of the other forms of salt available in the market had the required iodine concentration despite the official specifications for iodizing salt in Mexico (NOM-040-SSA1– 1993). Although we did not measure the amount of processed foods containing iodized salt in the children’s diet, the use of processed foods is negligible both at home and at school, as this population is largely dependent on a locally grown diet based largely on maize and beans. Most urine samples were collected in the morning between 07:00 and 12:00 h (corresponding to the nadir of UI), as proposed by Als et al (2000). This limits the variability caused by the circadian rhythmicity of UI. We did not attempt to collect urine specimens in fasting children, an issue that is still contentious (Thomson et al, 1996; Rasmussen et al, 1999). Within-day variation in UI excretion may be responsible for some of the lower values seen among these children, but since students do not drink much water during

the school hours in this dry climate, an overestimation of UI levels is the more likely diurnal bias in this relatively small sample (Dunn et al, 1993). The possibility of insufficient iodine intake cannot be ruled out since goiter was present in a small but significant proportion of the schoolchildren. However, interference from goitrogens, especially the popular local brassicas, Mekua´sare (Bye, 1981), could also contribute to the prevalence of goiter seen here. It is also possible that the enlarged thyroid glands, caused by a past history of iodine deficiency, have not normalized yet despite adequate UI. A lag between UI and thyroid volume has been noted elsewhere (Delange, 1999; Zimmermann et al, 2004). Iodine deficiency causes retarded mental and physical development, impaired intellectual function, and diminished school performance among children (Hetzel, 2000), and should therefore be given proper attention.

References Als C, Helbling A, Peter K, Haldimann M, Zimmerli B & Gerber H (2000): Urinary iodine concentration follows a circadian rhythm: a study with 3023 spot urine samples in adults and children. J. Clin. Endocrinol. Metab. 85, 1367–1369. Bye RA (1981): Quelites, ethnoecology of edible greens: past, present and future. J. Ethnobiol. 1, 109–123. Delange F (1999): What do we call goiter? Eur. J. Endocrinol. 140, 486–488. Dunn JT, Crutchfield HE, Gutekunst R & Dunn AD (1993): Methods for Measuring Iodine in Urine. Wagenigen, The Netherlands: CCIDD/ UNICEF/WHO. Hetzel SB (2000): Iodine and neuropsychological development. J. Nutr. 130, 493–495. ICCIDD, UNICEF, WHO (2001): Assessment of Iodine Deficiency Disorders and Monitoring their Elimination. Geneva: WHO. Instituto Nacional Indigenista (2002): Programas y Proyectos del Instituto Nacional Indigenista: Direccioń de Operacioń y Desarrollo. Programa de Albergues Escolares Indı´genas (alimentacioń). Me´xico: Instituto Nacional Indigenista. Internet site in Spanish at:http:// www.ini.gob.mx/ini/progra05_1.html. Koutras DA, Matovinovic J & Vought R (1985): The ecology of iodine. In: Endemic Goiter and Cretinism, Iodine Nutrition in Health and Disease eds Stanbury JB, Hetzel BS, pp 185–195. New York: Wiley Eastern Limited. Mannar MGV & Dunn JT (1995): Salt Iodization for the Elimination of Iodine Deficiency. The Netherlands: ICCIDD/MI/UNICEF/WHO. ˜eda-Limones R, Lechuga-Martıń del Martıńez-Salgado H, Castan Campo D, Ramos-Hernańdez RI, Orozco-Lo´pez M, Rivera-Dommarco J, Mendoza I & Magos C (2002): Deficiencia de yodo y otros posibles bocio´genos en la persistencia del bocio ende´mico en Me´xico. Gac. Med. Mex. 138, 149–156. Mona´rrez-Espino J, Martıńez H & Greiner T (2001): Iron deficiency anemia in Tarahumara women of reproductive-age in northern Mexico. Salud Publica Mex. 8, 251–268. Mona´rrez-Espino J, Martıńez H, Martıńez V & Greiner T (2004): Nutritional assessment of Tarahumara children at indigenous boarding schools. Eur. J. Clin. Nutr. 58, 532–540. Pandav CS, Arora NK, Krishnan A, Sankar R, Pandav S & Karmarkar MG (2000): Validation of spot-testing kits to determine iodine content in salt. Bull. World Health Organ. 78, 975–980. Rasmussen LB, Ovesen L & Christiansen E (1999): Day-to-day and within-day variation in urinary iodine excretion. Eur. J. Clin. Nutr. 53, 401–407.



4 Thomson CD, Smith TE, Butler KA & Packer MA (1996): An evaluation of urinary measures of iodine and selenium status. J. Trace Elem. Med. Biol. 10, 214–222. õVa´squez-Garibay EM, Romero-Velarde E, Na´poles-Rodrı´guez F, Nun Cosıó ME, Trujillo-Contreras F & Sańchez-Mercado O (2002): Prevalence of iron and iodine deficiency and parasitosis in children from Arandas, Jalisco, Mexico. Salud Publica Mex. 44, 195–200. Villalpando S, Garcıá-Guerra A, Ramı´rez-Silva CI, Mejıá-Rodrı´guez F, Matute G, Shamah-Levy T & Rivera JA (2003): Iron, zinc and


iodide status in Mexican children under 12 years and women 12-49 years of age. A probabilistic national survey. Salud Publica Mex. 45, S520–S529. Zimmermann MB, Hess SY, Molinari L, De Benoist B, Delange F, Braverman LE, Fujieda K, Ito Y, Jooste PL, Moosa K, Pearce EN, Pretell EA & Shishiba Y (2004): New reference values for thyroid volume by ultrasound in iodine-sufficient schoolchildren: a World Health Organization/Nutrition for Health and Development Iodine Deficiency Study Group Report. Am. J. Clin. Nutr. 79, 231–237.