Iodine is an essential micronutrient for adequate production of thyroid hormones, including triiodothyronine (T3) and thyroxine (T4). Insufficient synthesis of thyroid hormones may impair the neurodevelopment of infants and children, particularly, in the first 3 years of life(1,Reference Bougma, Aboud and Harding2) . During lactation, maternal iodine requirement increases to allow the secretion of iodine into breast milk and to maintain maternal thyroid hormone concentrations. Studies have suggested that during lactation, mammary glands are able to concentrate 20–50 times more iodine than maternal blood due to the active sodium–iodide symporter(Reference Semba and Delange3). However, limited research has investigated how iodine absorbed from the diet is partitioned for lactating women between the mammary gland, thyroid and kidney(Reference Dold, Zimmermann and Aboussad4). It is unclear whether the mammary gland varies its iodine uptake in response to changes in dietary intake and prioritises iodine intake for infants. The WHO recommends exclusive breast-feeding (EBF) during the first 6 months of life and to continue to breastfeed for up to 2 years and beyond(5). Exclusively breastfed infants rely fully on their mothers for an adequate iodine supply to synthesise sufficient thyroid hormones during the first 6 months, thereafter infants obtain additional iodine from appropriate complementary foods(Reference Eastman, Ma and Li6).
The first postpartum year is important for women to re-adjust and meet their changing iodine requirements. Few studies have investigated iodine status at different time points from early lactation to the end of the first postpartum year(Reference Eltom, Eltom and Elnagar7–Reference Manousou, Augustin and Eggertsen11). One small study of New Zealand women (n 35) prior to the government introduction of mandatory fortification of bread with iodised salt (2009) reported median urinary iodine concentrations (MUIC) of 37 µg/l, 25 µg/l and 47 µg/l at 3, 6 and 12 months postpartum (3MPP, 6MPP and 12MPP, respectively), suggesting iodine deficiency(Reference Thomson, Packer and Butler8). There continues to be a need for a more robust investigation into the iodine status of postpartum women and their infants.
New Zealand soil typically provides low levels of available iodine, which results in low iodine concentrations in local food supply(Reference Thomson12). Endemic goitre was prevalent in New Zealand in the early 20th Century, due to iodine deficiency. A voluntary salt iodisation programme was established in 1938 which dramatically reduced goitre rates by the 1950s(Reference Skeaff, Thomson and Gibson13). An analysis of twenty different retail salt products in New Zealand reported 32–64 mg of iodine/kg of iodised table salt, while non-iodised salt contained only 1–5 mg of iodine/kg of salt(Reference Thomson14). However, public health messages have led to reduced salt consumption to prevent high blood pressure and reduce the risks of other chronic medical conditions. The recent shifting from traditional home cooking with iodised salt to commercially prepared food with non-iodised salt has contributed to low use of iodised salt(Reference Ershow, Skeaff and Merkel15). Despite 70 % of retail salt sold in New Zealand being iodised(16), only 51 % of breast-feeding women used iodised salt either at table or in cooking (published results from the Mother and Infant Nutrition Investigation (MINI)(Reference Jin, Coad and Zhou17)). Other possible reasons which may reduce population iodine intake include the cessation of using iodophors as cleaning agents in the New Zealand dairy industries which resulted in a drop of iodine content in milk(Reference Pearson, Gibbs and Lau18), and the current dietary preferences of non-dairy milks made from soya, almond, rice and oat which contain low iodine < 0·02 mg/kg(19). Re-emerging iodine deficiency was reported in the 1990s for adults(Reference Thomson, Colls and Conaglen20) and schoolchildren(Reference Skeaff, Thomson and Gibson13), and also breastfed infants and toddlers(Reference Skeaff, Ferguson and McKenzie21).
To combat iodine deficiency, mandatory fortification of bread with iodised salt (25–65 mg iodine/kg salt) was introduced in New Zealand in September 2009, applicable to all commercial breads other than organic and unleavened(16). Recent studies in New Zealand have suggested that fortification has led to adequate intakes and status in the majority of schoolchildren(Reference Skeaff and Lonsdale-Cooper22,Reference Jones, Mclean and Davies23) and adults(Reference Edmonds, McLean and Williams24,25) . According to the 2016 New Zealand Total Diet survey, bread was the primary dietary source of iodine in the diet of an adult, although dairy products, fish, meat and eggs were also major contributors(Reference Pearson, Gibbs and Lau18). However, fortification was predicted to be inadequate for pregnant and breast-feeding women due to their increased requirements. Thus, in 2010, the use of government-subsidised iodine-only supplements (150 µg/d) was recommended to all pregnant and breast-feeding women in New Zealand(26). A pilot study (n 36) suggested that breast-feeding women remain deficient(Reference Brough, Jin and Shukri27) and reported mean breast milk iodine concentrations (BMIC, 63 µg/l)(Reference Brough, Jin and Shukri27) lower than that suggested for adequacy (75 µg/l)(Reference Azizi and Smyth28), although iodine status of the breastfed infants was not investigated. Our own research reported that 86 % (75/87) of women took iodine-containing supplements (ranging from 150 to 270 µg iodine/d), with 79 % (59/75) consuming the government-subsidised iodine tablet of 150 µg/d during pregnancy. During lactation, the proportion of women taking an iodine-containing supplement was only 46 % (40/87) at 3MPP (ranging from 100 to 250 µg iodine/d), with 58 % (23/40) consuming the government-subsidised iodine tablet(Reference Jin, Coad and Zhou17).
Based on the 2003/2004(Reference Vannoort and Thomson29), 2009(Reference Vannoort and Thomson30) and 2016 New Zealand Total Diet Survey(Reference Pearson, Gibbs and Lau18), the iodine concentration in infant formula increased from 0·079 mg/kg in 2003/2004 to 0·133 mg/kg in 2009 and infant formula is suggested to be the major contributor (72 %) to the iodine intake in infants aged 6–12 months(Reference Pearson, Gibbs and Lau18). The mandatory fortification of bread with iodine had the least impact on infant’s iodine intake due to low consumption of bread(Reference Pearson, Gibbs and Lau18); however, this research did not include the contribution of iodine from breast milk.
The aim of this MINI was to describe iodine status of supplement users and non-users (for both mothers and infants) at 3MPP, 6MPP and 12MPP. Further, it investigated partitioning of iodine excretion, between urine and breast milk, of EBF women at 3MPP.
Methods
Study population
MINI was an observational longitudinal cohort study spanning the first postpartum year in Palmerston North, in the North Island of New Zealand. Breast-feeding women aged 16 years and older were recruited, who had given birth to a healthy term singleton 3 months prior. Women were excluded: (1) if they had pre-existing or developed complicated health problems, such as metabolic disorders and cancer, and (2) if they had been diagnosed or treated at any time for hyperthyroidism or hypothyroidism. Recruitment spanned 19-month period between June 2016 and December 2017. Posters to promote the study were placed at selected sites (General Practitioner surgeries, midwifery clinics, pharmacies, antenatal classes, ultrasound clinics, maternal wards in hospitals, local community playgroups and early childhood centres, etc.). Local newspapers and social media sites were used to publicise the study. Local midwives, childbirth educators and lactation consultants were asked to raise awareness of the MINI study to their clients. Potential participants responded by recording an expression of interest online or via telephone/email. Prospective participants were provided with a study information sheet. Interested participants then completed a screening questionnaire to ensure eligibility. Details of the study methods have been published previously(Reference Jin, Coad and Zhou31). The first study visit for each mother–infant pair was at approximately 3MPP, and follow-up assessments took place at 6 months (second study visit) and 12 months (third study visit) postpartum. Written informed consent was obtained from all participants before their enrolments in the study. Mothers also gave the written consent to their infants’ participation in the study.
Ethics approval
All procedures performed in the MINI study involving human participants were in accordance with the ethical standards of the Health and Disability Ethics committee. The MINI study was approved by the Health and Disability Ethics Committee (reference: 15/NTA/172) in December 2015.
Sample size
The main outcome measure was UIC, and the sample size was calculated using G*Power 3.1 (Heinrich Heine University, Dusseldorf)(Reference Faul, Erdfelder and Buchner32) based on data (mean values and standard deviation) from a preliminary study of breast-feeding women(Reference Brough, Jin and Shukri27). The analysis utilised one-way ANOVA with two groups (95 % power, alpha = 0·05, two-tailed) and three repeat measures. Eighty participants were sought, using expected mean daily UIC of 140 and 100 µg/l for iodine supplement users and non-users, respectively, with a sd of 60.
Assessment of iodine status
During each study visit, non-fasting spot urine samples were collected from each participating woman and her infant to assess iodine and creatinine excretion. A paediatric urine bag was placed inside the diaper and checked every 10 min during the study visit to collect infant urine samples. Women were asked to provide a breast milk sample (approximately 30–50 ml) using an electric breast pump if needed. Breast milk samples could be collected before, during or after a feed. All samples were collected before 12 noon on the study visit day. Samples were stored without preservative at –20°C. Breast milk samples were analysed for iodine concentration, allowing for estimations of daily excretion and infant iodine intake(Reference da Costa, Haisma and Wells33). The use of iodine-containing supplements was only determined within 24 h of the time of biological sample collections at each time point of the study visit (3MPP, 6MPP and 12MPP). Self-reported habitual use of these supplements was only assessed at 3MPP, 46 % (40/87) of women took iodine-containing supplements (ranging from 100 to 250 µg iodine/d), with 58 % (23/40) consuming the government-subsidised iodine tablet(Reference Jin, Coad and Zhou17).
Iodine concentrations of urine and breast milk samples were determined by Hill Laboratories, Hamilton, New Zealand, using inductively coupled plasma MS(Reference Fecher, Goldmann and Nagengast34). Quality Control procedures included analysis of blanks, analytical repeats and spiked samples in order to ensure accuracy and precision. Calibration standards and checks were undertaken on every run with the limit of detection at 0·001 mg/l. Standard uncertainty was calculated for each sample; mean values and standard deviation for maternal urine, breast milk and infant urine were 0·0082 (sd 0·0073), 0·0033 (sd 0·0037) and 0·0070 (sd 0·0094), respectively. Each batch (twenty-five samples) of urinary samples was analysed together with an external reference standard (Seronorm Trace Elements Urine, L-2) giving a mean iodine concentration of 286 (sd 12) µg/l (published value: 297 µg/l) with a CV of 4·2 % (n 14). Creatinine was measured in maternal urine using the Jaffe Method Flexor (Randox Assayed Multisera levels 2&3) at Massey University Nutrition Laboratory in Palmerston North. Each batch of breast milk samples was analysed together with an external reference standard (Skimmed milk powder, Elements in organic matrix, European) giving a mean iodine concentration of 1·603 (sd 0·029) mg/l (published value: 1·78 mg/l), with a CV of 4·9 % (n 6).
Iodine deficiency in a population is defined by a MUIC below 100 µg/l for lactating and non-lactating non-pregnant women, and children younger than 2 years(1). The WHO (2007) also recommends that for a population to be iodine sufficient, no more than 20 % should have a UIC <50 µg/l(1). There is no universal consensus on the optimal concentration for BMIC; however, >75 µg/l has been suggested to be sufficient for adequate infant iodine intake(Reference Azizi and Smyth28). There are no recommended cut-offs for lactating women to categorise excessive iodine intake; however, a median UIC ≥ 300 µg/l in infants was considered to indicate a risk of excessive iodine intake(1).
Infant anthropometry
At the initial visit, infant recumbent length was measured crown to heel using an infant length board and recorded to the nearest mm. Infant weight (without clothing and diapers) was measured, using a baby weighing scale (Nagata Scale Co. Ltd), and recorded to the nearest 10 g. Infant’s weight-for-age Z-score and height-for-age Z-score were calculated by entering the data into WHO-Anthro software (https://www.who.int/childgrowth/software/en/) (35), using the formula: (observed value − median value of the reference population) divided by the standard deviation value of reference population(Reference De Onis and Blössner36). The median values for weight-for-age and length-for-age were based on the WHO child growth standards(Reference De Onis, Onyango and Borghi37).
General demographic and health information
At the initial visit, mode of infant feeding, maternal general health and demographic information (including age, ethnicity, educational attainment, household size and income) were collected. Potential changeable information including mode of infant feeding and general health was also sought at the second and third visits. EBF was defined as follows: infants fed only breast milk since birth with no water, formula or liquid supplements (excluding essential medication). Non-breast-feeding was defined when infants were not fed with any breast milk at the time of questioning; partial breast-feeding was defined when infants were fed with a mixed diet consisting of breast milk, infant formula and/or complementary food. Infants’ birth information including gestational age at birth, date of delivery, method of delivery, birth weight and sex was collected at the first visit, from the ‘Well Child Tamariki Ora’ book (New Zealand child health record). Recorded date of delivery was used to calculate the age of infants on the day of study visit.
Statistical analysis
Data were analysed using IBM SPSS (Statistics Package for the Social Sciences; IBM) version 20. Data were tested for normality using Shapiro–Wilk test. Non-parametric data were expressed as median with interquartile range (25th, 75th percentile) and parametric data expressed as mean (standard deviation). Bivariate correlations were tested using the non-parametric Spearman’s rho correlation coefficient. Non-parametric data were natural log-transformed for further analysis. A one-way mixed ANOVA with two groups was used to compare the mean differences between UIC of iodine-containing supplement users and non-users (based on iodine-containing supplement use at 3MPP) with a repeated measure at 3MPP, 6MPP and 12MPP. Differences in iodine status for women who were breast-feeding at all three time points, determined by UIC, urinary iodine:creatinine ratio and BMIC between three measurement points, were tested by one-way repeated-measures ANOVA.
For EBF women, their daily maternal iodine excretion in urine was estimated based on 1·5 litres of urine/d(38). Total estimated daily iodine excretion was the sum of urinary and breast milk iodine excretions. The fractional excretions of iodine in urine and breast milk were calculated as percentages of total daily iodine excretions(Reference Dold, Zimmermann and Aboussad4). Assuming 92 % of iodine consumed is excreted into urine and breast milk together(38), total estimated maternal iodine intake was calculated. The estimated total daily iodine intake of their exclusively breastfed infants was calculated based on daily urine volume assumed at 0·5 litres, with an assumption of 87 % iodine consumed is excreted in infants’ urine(Reference Dold, Zimmermann and Baumgartner39). Independent t test was used to compare natural log-transformed maternal UIC, maternal urinary iodine:creatinine ratio and BMIC between EBF women who used iodine-containing supplements and non-users.
Results
Characteristics of mothers and their infants
In total, eighty-seven mother and infant pairs were recruited at 3MPP and followed up at 6MPP (n 78) and 12MPP (n 71). At 3MPP, the mean maternal age was 31·5 (sd 4·2) years. Most participants (77 %) were Caucasian and achieved tertiary education (Table 1). The majority had a vaginal delivery (78 %), and 44 % were delivering their first infant. All women were breast-feeding at 3MPP, and 96 % of women continued to breastfeed their infants at 6MPP, but only 46 % continued breast-feeding at 12MPP.
Table 1. Description of breast-feeding participants and their infants at 3 months postpartum (3MPP) (n 87)
(Mean values and standard deviation; numbers and percentages)
* Median annual household income based on Statistics New Zealand was 75 995 New Zealand dollars for the year ended June 2016(53).
Maternal iodine status at 3, 6 and 12 months postpartum
Maternal MUIC (25th, 75th percentile) at 3MPP (82 (46, 157) µg/l), 6MPP (85 (43, 134) µg/l) and 12MPP (95 (51, 169) µg/l) < 100 µg/l suggest iodine deficiency. Further, >20 % of women had a UIC below 50 µg/l: 29 % at 3MPP; 27 % at 6MPP and 23 % at 12MPP. Median (25th, 75th percentile) BMIC was below the suggested concentration at all three time points (69 (52, 119) µg/l), (59 (39, 108 µg/l) and (35 (26, 54) µg/l). BMIC was moderately correlated with urinary iodine:creatinine ratio at all three time points (r = 0·441, P < 0·001 at 3MPP; r = 0·552, P < 0·001 at 6MPP; r = 0·577, P = 0·001 at 12MPP; online Supplementary Table). No significant differences between maternal iodine status measures were found among EBF, partial breast-feeding or non-breast-feeding women (Table 2).
Table 2. Maternal markers of iodine status during the first postpartum year by mode of infant feeding
(Numbers; medians and 25th and 75th percentiles)
3MPP, 3 months postpartum; 6MPP, 6 months postpartum; 12MPP, 12 months postpartum; EBF, exclusive breast-feeding; PBF, partial breast-feeding; NBF, none breast-feeding; UIC, urinary iodine concentration; BMIC, breast milk iodine concentration.
Overall, among women who completed the study, 46 % (33/71) took iodine-containing supplements with 24 h of urine sampling at 3MPP; this reduced markedly to 11 % (8/71) at 6MPP, and 6 % (4/71) at 12MPP. Defining women as supplement users or non-users at 3MPP showed that there was no significant main effect of time points on natural log UIC (F (2,138) = 0·500, P = 0·607, partial η 2 = 0·007), with participants showing similar mean natural log UIC at 3MPP (4·36), 6MPP (4·97) and 12MPP (4·49). However, there was significant interaction between iodine supplement use and time points on the mean of natural log UIC (F (2,138) = 3·550, P = 0·031, partial η 2 = 0·049) (Fig. 1). At 3MPP, iodine-containing supplement users showed a higher MUIC (111 µg/l) when compared with non-users (66 µg/l). The subgroup of women who were breast-feeding at the three time points showed a significant reduction in BMIC from 3MPP to 6MPP to 12MPP (Table 3). However, there were no significant variations in UIC or maternal urinary iodine:creatinine ratio over the three time points.
Fig. 1. Urinary iodine concentration of women who completed three study visits (n 71). 
Users; 
Nonusers. Median urinary iodine concentration: 3 months postpartum: 111 µg/L (users) vs 66 µg/L (non-users); 6 months postpartum: 71 µg/L (users) vs 89 µg/L (non-users); and 12 months postpartum: 98 µg/L (users) vs 93 µg/L (non-users).
Table 3. Markers of maternal iodine status of continuous breast-feeding women
(Numbers; medians and 25th and 75th percentile, n 33)
3MPP, 3 months postpartum; 6MPP, 6 months postpartum; 12MPP, 12 months postpartum; UIC, urinary iodine concentration; BMIC, breast milk iodine concentration.
* One-way ANOVA.
Iodine status of infants aged 3, 6 and 12 months
In the current study, infant MUIC at the age of 3, 6 and 12 months were all above 100 µg/l with fewer than 20 % below 50 µg/l (Table 4), suggesting adequate iodine status. However, at 6 months, infants who were EBF had an MUIC (80 µg/l, n 13) which was below the 100 µg/l cut-off and significantly lower than infants who were mixed-fed with complementary food (147 µg/l, n 29, P = 0·033). Exclusively breastfed infants at 3 months of age had a lower infant MUIC than those who were partial breast-feeding, but this was not statistically significant (Table 4). Infant UIC was significantly, moderately correlated with BMIC at 3MPP, 6MPP and 12MPP (r = 0·598, P < 0·001; r = 0·602, P < 0·001; r = 0·656, P = 0·011, respectively; online Supplementary Table).
Table 4. Infant urinary iodine concentration (UIC) from infants aged 3, 6 and 12 months
(Numbers; medians and 25th and 75th percentile)
EBF, exclusive breast-feeding; PBF, partial breast-feeding; NBF: none breast-feeding.
* Mann–Whitney U test.
Iodine status of exclusive breast-feeding women and their infants at 3 months postpartum
The MUIC for EBF women was 78 µg/l, below 100 µg/l, suggesting iodine deficiency (Table 2). Median BMIC was 68 µg/l also below the suggested 75 µg/l. Median estimated maternal iodine intake was 212 (138, 331) µg/d (Table 5), below the recommended dietary intake of 270 µg/d, and 46 % (33/72) had intakes below the estimated average requirement of 190 µg/d(40). Only 44 % (32/72) of EBF women took iodine-containing supplements (range 150–250 µg iodine/d). Women who used iodine-containing supplements showed significantly higher MUIC (105 v. 66 µg/l, P = 0·027), urinary iodine:creatinine ratio (173 v. 94 µg/l, P < 0·001) and BMIC (84 v. 61 µg/l, P < 0·001), when compared with those who did not use iodine-containing supplements.
Table 5. Estimated daily iodine excretions and intakes in mothers and their infants at 3 months postpartum (3MPP)
(Median values and 25th and 75th percentiles)
EBF, exclusive breast-feeding; UIC, urinary iodine concentration; BMIC, breast milk iodine concentration.
* Calculated for each mother as UIC × 1·5 litres (the assumed daily urine volume in lactating women)(Reference Dold, Zimmermann and Aboussad4).
† Calculated for each infant as (UIC × 0·5 litres (the assumed daily urine volume in infants aged 0–6 months))/0·87 (the assumed iodine intake excreted in urine with negligible excretion in faeces)(Reference Dold, Zimmermann and Aboussad4).
Based upon a visual inspection of the scatter plot of the partitioning of maternal UIC and BMIC in total daily iodine excretion (Fig. 2), it demonstrates when total daily iodine excretion was below 300 µg, an increased partitioning of BMIC (the highest proportion of 60 %) was observed, together with a reduced fractional iodine excretion in urine (the lowest proportion of 40 %). When total daily iodine excretion was higher than 300 µg, a constant proportion of excretion was observed in urine (80 %) and breast milk (20 %).
Fig. 2. Fractional iodine excretion in urine and breast milk in relation to total estimated daily iodine excretion (n 72). Blue bubble indicate proportion of iodine in breastmilk and green bubble indicate proportion of iodine in urine
Discussion
Iodine sufficiency and deficiency during the first postpartum year
The MINI study found women who used iodine-containing supplements at 3MPP had a significantly higher MUIC than non-users (111 v. 68 µg/l). A post-fortification study of Australian breast-feeding women (n 60) at around 3 months after parturition showed a similar significant positive effect of taking iodine-containing supplements on maternal MUIC (206 v. 97 µg/l)(Reference Axford, Charlton and Yeatman41). However, in the current study, there was no difference in MUIC at 6MPP and 12MPP based on supplement use at 3MPP. This is unexpected, although could be due to the low proportion of women actually using iodine-containing supplements in later lactation 11 % (8/71) at 6MPP and 6 % (4/71) at 12MPP. The low use is unsurprising, and the lack of awareness of the need for iodine supplementation during lactation in this population has been reported(Reference Jin, Coad and Zhou17). The low use of iodine-containing supplements during later breast-feeding is especially concerning for women who do not consume iodine-rich foods and those who become pregnant again. In Morocco, a randomised double-blinded placebo-controlled trial (n 241 mother–infant pairs) compared the effectiveness of using maternal supplementation, either with a single dose of 400 mg iodised oil or supplementing infants (aged ≤ 8 weeks) directly with a single dose of 150 mg. This study found that maternal supplementation is more effective in ensuring adequate infant iodine status and maintaining BMIC levels until at least 6MPP(Reference Bouhouch, Bouhouch and Cherkaoui42). Achieving adequate maternal iodine status throughout lactation is critical for infants’ growth(Reference Ellsworth, Mccaffery and Harman43) and also optimal fetal neurodevelopment(Reference Velasco, Bath and Rayman44).
Overall iodine deficiency was present in a group of women during the first postpartum year based on the WHO epidemiology criteria(1). The UIC did not change significantly over the three time points. Our results showed an improvement of maternal iodine status, when compared with the results reported in a pre-fortification study of postpartum women in the South Island of New Zealand in 2001 (37 µg/l, 25 µg/l and 47 µg/l at 3MPP, 6MPP and 12MPP, respectively)(Reference Thomson, Packer and Butler8). The trend for increase in MUIC across three time points in the MINI study was also found in a study of Sudanese breast-feeding women (n 47) living in an area with 17·5 % goitre rate, where MUIC increased from 3 (51 µg/l) to 9 (63 µg/l) months postpartum(Reference Eltom, Eltom and Elnagar7). Similarly, a recent large Norwegian longitudinal study of postpartum women (n 915) reported the lowest MUIC at 6 weeks postpartum (57 µg/l), which increased through 6, 12 and 18 months postpartum (70 µg/l, 79 µg/l and 87 µg/l, respectively)(Reference Aakre, Morseth and Dahl10). The Norwegian authors suggested that the increase was possibly due to an assumed decrease of iodine excretion in breast milk during the postpartum period. However, these studies on Norwegian and Sudanese women did not measure BMIC.
In the current study, among women who continued to breastfeed, iodine secreted into breast milk significantly decreased from the highest concentration of 71 µg/l at 3 months, to 61 µg/l at 6 months, and with the lowest concentration of 35 µg/l at 12MPP. This pattern suggests reduced transport of iodine to breast milk. Similar observations were made in a cohort of New Zealand iodine-deficient lactating women without iodine supplementation during the first 6MPP in 2004–2005 decreasing from 43 µg/l in week 1 to 25 µg/l in week 24(Reference Mulrine, Skeaff and Ferguson45). A reduction of BMIC from 3 months (60 µg/l) to 9 months (26 µg/l) was also reported in Moroccan mothers who were supplemented with one oral dose (400 mg) of iodine after delivery(Reference Bouhouch, Bouhouch and Cherkaoui42). Research has reported a sharp decrease of iodine concentration from colostrum to mature milk, which could be due to the low volume of colostrum(Reference Dror and Allen46). The further reduction of BMIC from 6MPP to 12MPP observed in the current study must be interpreted with caution due to the small number of samples at 12 months. However, for breastfed infants, breast milk is still an important iodine source. Therefore, it is important for lactating women to achieve adequate iodine status.
Adequate infant iodine status was observed at three time points of this current study, using the WHO epidemiological criteria(1). However, the calculated iodine intake from a UIC of 100 µg/l is 57 µg/d (based on approximately 0·5 litres daily urine volume and 87 % of dietary iodine excreted into urine)(Reference Dold, Zimmermann and Aboussad4). This is much lower than the Institute of Medicine suggested adequate intake of 110 µg/d for infants up to age of 6 months(47). Delange suggests that infant MUIC between 180 and 225 µg/l(Reference Delange48) are necessary to achieve the WHO recommended iodine intake of 90 µg/d(1). Further, results from a recent dose–response crossover iodine balance study of euthyroid term Swiss infants with iodine sufficiency suggested 125 µg/l as a cut-off for infant MUIC (based on the estimated average requirement of 72 µg/d for infants aged 2–5 months)(Reference Dold, Zimmermann and Baumgartner39). Using this cut-off, the MUIC for infants aged 3 (115 µg/l) and 6 months (120 µg/l) in the current study would indicate iodine deficiency, which was consistent with the estimated suboptimal intake from BMIC. Further, infants aged 6 months who were exclusively breastfed had an MUIC (80 µg/l) lower than 125 µg/l suggesting iodine insufficiency, which was significantly lower than those who were partially breastfed (147 µg/l). This shows the importance of adequate maternal iodine status for those infants who are exclusively breastfed at 6 months of age.
In the present study, despite differing amounts of breast-feeding and ages of infants, BMIC was moderately correlated with infant UIC. This finding is supported by a systematic review of fourteen eligible studies(Reference Dror and Allen46), which suggested BMIC was the primary indicator of iodine status in breastfed infant iodine status due to the positive association between BMIC and infant UIC. In the current study, median BMIC at 3MPP and 6MPP (69 µg/l and 59 µg/l, respectively) suggested inadequate infant iodine intake. Further analysis from a South Australia post-fortification study in 2017 found that infants from mothers with lower BMIC (<100 µg/l) were less likely to achieve adequate iodine status (infant UIC > 100 µg/l), when compared with those with higher BMIC (≥100 µg/l)(Reference Huynh, Condo and Gibson49). The Australian authors suggest that achieving adequate iodine status for lactating women is essential to ensure sufficient iodine supply to their breastfed infants.
Iodine status of exclusive breast-feeding women and their infants at 3 months postpartum
This current MINI study found iodine deficiency was present in EBF mothers at 3MPP. The current MUIC remained similar to the value (74 µg/l in 2011) previously reported from the same region in New Zealand(Reference Brough, Jin and Shukri27), although it showed a marked improvement from 34 µg/l in 2009 (prior to government interventions)(Reference Brough, Jin and Shukri27). Women who reported consuming iodine-containing supplements at 3MPP were more likely to achieve adequate iodine status when compared with those who did not use such supplements, this has been discussed in detail previously(Reference Jin, Coad and Zhou17). Exclusively breastfed infants fully rely on their breast milk intake for thyroid function. The MUIC of exclusively breastfed infants at 3 months of age was 111 µg/l, below the suggested cut-off of 125 µg/l(Reference Dold, Zimmermann and Baumgartner39) indicating iodine deficiency. Lack of iodine intake may interrupt the motor and neurodevelopment of these infants at this crucial time.
The present study suggests that among this cohort of EBF women who were iodine-deficient, increased partitioning of iodine secretion into breast milk (the highest proportion of 60 %) occurred when total daily iodine excretion was low (<300 µg/d). This partitioning potentially provides a protective effect to ensure iodine supply to their breastfed infants. In comparison, a similar partitioning pattern (increased fraction of iodine into breast milk but decreased iodine in urine when total daily iodine excretion < 300 µg/d) was observed from a large multi-centre study of lactating women (iodine sufficient based on median BMIC) in China (n 386), Philippines (n 371) and Croatia (n 109)(Reference Dold, Zimmermann and Aboussad4). This pattern may be due to an enhanced capacity of sodium–iodide symporter transportation by mammary glands during early lactation(Reference Vermiglio, Presti and Battiato50), which may ensure adequate iodine supply to exclusively breastfed newborn infants(Reference Dold, Zimmermann and Aboussad4). However, in the MINI study, when total daily iodine excretion was higher than 300 µg, a constant partitioning of excretion was observed in urine (80 %) and breast milk (20 %), which differed from the previous multi-centre study showing a continuous decreased excretion in breast milk but a measurable increase in urine(Reference Dold, Zimmermann and Aboussad4). This may be due to the smaller number of participants in the current study whose total iodine excretion was above 300 µg/d; thus, the current results need to be interpreted with caution.
Strengths and limitations
This study is the first longitudinal cohort study in New Zealand to assess the iodine status simultaneously of both mothers and infants, subsequent to the introduction of mandatory fortification of bread with iodised salt (2009) and the recommended government-subsided iodine supplement (150 µg/d) for breast-feeding mothers (2010).
The study examined the iodine status of mother–infant pairs during the transitional period from exclusive, to partial, and in some cases, cessation of breast-feeding throughout the first postpartum year, which enhances the existing available knowledge of iodine status throughout postpartum period. Maternal iodine status was measured in both urine and breast milk to provide a thorough measure of each participant’s iodine status. The study also contributes to the limited knowledge on the fractional uptake of iodine from the mammary gland in response to variations in iodine intake while EBF.
To examine the impact of iodine supplements on iodine status, participants were defined as iodine-containing supplement users or non-users based on data collected at 3MPP; this may have diluted the effect of iodine supplements, as fewer women were taking iodine supplements after 3MPP. Although the use of iodine-containing supplements within the last 24 h was likely to be reflected in their UIC, this method could incorrectly classify habitual users who did not use the supplement on the day of assessment into the non-user group. Other limitations of this study also include that the self-selected participants were predominantly well-educated with a relatively high household income; thus, the sample may not be representative of the overall New Zealand population. If these women were iodine-deficient, iodine status of women who are less educated and of low income may be of even greater concern. In addition, the use of a spot urine samples may introduce intra-individual variability due to the variation in maternal hydration status and substantial variation in daily iodine intake. Urinary creatinine values were used to reduce the variation due to maternal hydration. To determine habitual intake, using repeated measuring could have better predicted iodine status(Reference Konig, Andersson and Hotz51). Newborn TSH can be used as another indicator of infants’ iodine status by following a standardised protocol(Reference Li and Eastman52). However, potential confounding factors including maternal iodine status, mode of delivery, sampling time and maternal exposure to iodine-containing antiseptics may limit the use of newborn TSH measurement(Reference Li and Eastman52).
Conclusions
In conclusion, after two New Zealand government interventions in 2009 and 2010, this cohort of women throughout the first postpartum year was iodine-deficient irrespective of the amount or duration of breast-feeding. Despite that an increased fractional iodine excretion into breast milk was observed in lactating women with low iodine intake, the low use of iodine-containing supplements during later breast-feeding is concerning, especially for lactating women on a diet containing few iodine-rich foods and those who become pregnant again. Iodine status of their breastfed infants aged 3 and 6 months may be inadequate. For breastfed infants, breast milk is still an important iodine source. Therefore, it is crucial for lactating women to achieve adequate iodine status throughout lactation. Further studies to assess maternal and infants’ iodine status with their thyroid function, and infant neurodevelopment outcomes are needed, to ensure optimal health of both mothers and their future offspring.
Acknowledgements
We thank the MINI team, including Anne Broomfield for her technical support. We would like to thank the women and their infants who volunteered their time and assistance for this study.
This work was supported by the Massey University Research Fund; School of Food and Advanced Technology postgraduate fund. The funding bodies had no role in the design, analysis or writing of this article.
Y. J.: Conceptualisation, methodology, investigation, data curation, formal analysis, visualisation, writing-original draft preparation and writing-reviewing and editing. J. C.: Conceptualisation, methodology, funding acquisition, supervision and writing-reviewing. S. S.: Resources and writing-reviewing. S. J. Z.: Resources and writing-reviewing. L. B.: Conceptualisation, methodology, funding acquisition, formal analysis, supervision, writing-reviewing and editing.
There are no conflicts of interest.
