Observed BLLs in the present study are slightly higher than those of other ‘non-exposed’ children in Sub-Saharan LMICs, and generally higher than global LMICs and LMICs in other regions. Our BLL data agree closely with literature data for similar non-exposed/background childhood (0-6 yr) populations in low-income countries, and are higher than those groups in more wealthy nations. Therefore, the population studied here may be considered to be representative of that in other urbanizing, low-income areas, especially in Sub-Saharan Africa (e.g., median and geomean data from the present study lie in the 50th percentile of pooled mean data for Sub-Saharan Africa as compiled by Ericson et al. 2021).
Several risk factors were identified by the survey and significantly related to elevated BLL status using crude ORs (here with discussion focusing on ≥5 µg/dL unless otherwise noted). Male gender (OR: 1.57) was associated with elevated BLLs as previously observed (Filigrana and Mendez, 2012, Morales et al., 2005), owing potentially to distinct behavior patterns that increase exposure (e.g., playing outside more often, pica/geophagy). Living near a railway (OR: 2.80) or major roadway (OR: 3.25) was significantly associated with risk of elevated BLL status; proximity to major roadway was also significantly associated at the 10 µg/dL threshold (OR: 2.30). Despite a country-wide phaseout of leaded gasoline beginning around 2005, it is plausible that stocks of leaded fuel may still be in use, or that marine-grade fuels contribute to this potential exposure source (Lin and Lin, 2006). Also, this more recent phase-out of leaded fuel, and an estimated ~15 year half-life of lead in soil (Mielke et al., 2019), suggests that lead contamination of soil is a likely on-going source of exposure as observed in other LMICs (Pan et al., 2018, Shabanda et al., 2019). Additionally, the use of low-grade, so-called “Africa-quality” fuels in poorly-maintained vehicles and machinery, often lacking pollution control devices, is common in Madagascar (Global Alliance on Health and Pollution, 2018). Children are especially prone to lead exposure from contaminated soil given their propensity for hand-to-mouth activities. Presence of bamboo flooring (OR: 4.71), as opposed to tile, a metric previously used to identify homes with higher SES (Arias and De Vos, 1996), was identified as a significant factor for elevated BLL status. Less expensive flooring (e.g., bamboo here) has been previously related to higher BLLs in Indonesian children (Albalak et al., 2003).
Daily consumption of beans was significantly associated with elevated BLL (OR: 6.58), owing potentially to the ubiquitous use of aluminum pots in this community. The extended cooking time required for this staple compared to foods requiring different preparation (e.g., grilled foods) may result in leaching of lead into solution, especially in acidic solution (e.g., with vinegar) (Weidenhamer et al., 2017); fresh beans (vs. dried) require reduced cooking times, but are more expensive, and so lower SES may in part drive exposure through this route. Rice was significantly associated with elevated BLL (OR: 2.14), potentially for this same reason; rice was also significantly associated at the ≥10 µg/dL threshold (OR: 2.71). Lead sorbs to starches such as rice (Sharma et al., 2021), and as the concentration of lead in water increases, the contribution of overall lead exposure owing to consumption of starches increases (Akers et al., 2019). Anecdotally, it is common for there to be a grey/silver residue observed on top of the cooked rice, potentially from the cooking vessel, or from hardness of the water. Export of these cooking pots have been banned from Madagascar to Réunion Island owing to analyses confirming high lead content.
Consumption of vegetables was also significantly associated with elevated BLL status (OR: 1.59). Unwashed vegetables may serve as an ingestion source for lead, especially if sold near highly-trafficked areas where lead-contaminated soil and dust may serve as exposure routes, as previously observed in Tanzania (Magoha et al., 2008); vendors in this community typically reside near major roadways. Legacy lead contamination of soil here is plausible as the half-life of lead in soil is on the order of ~15 years (Mielke et al., 2019). Additionally, vegetables may be cooked in a similar manner to beans and rice, therefore likely resulting in lead leaching into the cooked product. Additional diet terms identified as significant at the ≥10 µg/dL threshold included fruit (OR: 1.64) and meat/fish (OR: 1.63). If unwashed, fruit may serve as a similar exposure route as vegetables. Aforementioned results of the geospatial analyses (e.g., distances from railways and major roadways) support the importance of legacy soil contamination from leaded fuel use. Interestingly, consumption of baby food was a protective factor against elevated BLL status (OR: 0.24). Baby food (here, a fortified porridge) is used to supplement breastfeeding for malnourished infants in this community. Additionally, breastfeeding can be a key lead exposure route for infants in LMICs (Lozoff et al., 2009) due to mobilization of bone-stored lead in nursing mothers (Téllez-Rojo et al., 2002); however our survey data included a question specific to breastfeeding, and found no relationship to elevated BLLs.
Regarding potential occupational or ‘take-home’ exposures (i.e., those associated with occupational exposures but affecting a home environment, an important contributor to lead exposures in LMICs) (Williams et al., 2021), the maternal occupation of laundry-person was significantly related to elevated BLL status (OR: 4.71); the same association was observed at the ≥10 µg/dL threshold as well. This finding may be related to the typically lower SES of this occupation, or potentially to exposures owing to use of local river water for washing; these rivers (e.g., the Pangalan) may contain mining tailing from nearby cobalt-nickel operations. Additionally, the paternal occupation of metal/seeker (i.e., either someone who finds scrap metal at disposal/construction sites, or who works with metal soldering) was significantly related to elevated BLL status at ≥10 µg/dL (OR: 8.42), owing potentially to exposures to co-produced/recycled materials/metals containing lead (Obeng-Gyasi, 2019, UNICEF and Pure Earth, 2020).
In terms of adjusted ORs (Table 5), only the diet consumption of vegetables (OR: 2.66) was associated with elevated BLL at the ≥5 µg/dL threshold. This finding further supports the hypotheses of cooking vessels (i.e., aluminum pots in this community), and contamination of foods sold by roadside vendors owing to legacy soil contamination by leaded fuel use. At the ≥10 µg/dL threshold (Table A4), living near a major roadway (OR: 4.06), daily consumption of meat/fish (OR: 2.25), paternal occupation of metal seeker/worker (OR: 24.74), and maternal occupation of laundry-person (OR: 11.39) were associated with elevated BLL. The risk associated with living near a major roadway aligns with legacy soil contamination. The relationship between elevated BLL and the diet term associated with meat/fish is unclear, though previous work has associated higher BLLs with frequent consumption of fish (Birgisdottir et al., 2013). Finally, the occupational terms of metal seeker/worker and laundry-person may be related to direct exposures and overall lower SES, respectively.
Strengths of the present study include novel measurement of BLLs in Madagascar, one of the world’s least developed nations, as well as use of established statistical approached to relate BLL data to results of an environmental risk factor survey. Additionally, comparison against recently compiled and published global BLL data allowed for an understanding of BLLs in the target community in the context of other Sub-Saharan African and low-income nations. Limitations of the study included relatively limited sample size, and use of a point-of-care vs. reference-grade instrument. Future work with larger sample sizes may also explore interaction terms (e.g., in terms of daily diet combinations).
In summary, more than two-thirds (68%) of the children in our study were at or above the CDC threshold of 5 µg/dL, higher than the 49% estimated by Ericson and colleagues for children in LMICs with published BLL data. More than one-quarter (27%) were above 10 µg/dL, compared to 32% as estimated by Ericson and colleagues. In addition to the lead-containing hand pumps in the community, there likely exist multiple exposure routes including air, soil, food, and those associated with parental occupations and infrastructure near the home. Air quality data are limited in the country, but sampling in Antananarivo in 2007-2008 (the capital city, located 350 km west of Toamasina) determined lead concentrations in PM2.5 to be well below the WHO guideline (0.5 µg/m3) following the phase-out of leaded gasoline (Rasoazanany et al., 2012); therefore exposures to lead in the air may be minimal unless there is a source not accounted for in Toamasina (a port-city, and location of a mine tailing storage site).
However, legacy use of leaded fuel in the country likely results in continuous daily exposures via contaminated dust and soil (with relatively long lead contamination half-life), as confirmed by our geospatial analyses. The practice of pica and geophagy observed in some Sub-Saharan African communities, and especially among children (girls in particular), may contribute to elevated lead exposures in these younger populations (Msoffe et al., 2019, Nchito et al., 2004). Regarding ingestion however, the use of recycled aluminum pots for cooking is a likely contributor to lead exposure in this community, where staple foods requiring extended cooking times (e.g., rice) are common (82% of respondents consume rice daily); previous modeling efforts by our team have highlighted the importance of rice consumption in Madagascar as a potential lead exposure route (especially at elevated pump water lead levels) (Akers et al., 2019), and additional work should be conducted to assess contributions of the dietary exposure route in this community.
Finally, nearly half (47%) of Madagascar’s children suffer from chronic malnutrition (US AID, 2018), and more than one-third of adults are anemic. Iron deficiency has been extensively linked to elevated BLLs (Kwong et al., 2004), owing to similar biological pathways of iron and lead. Therefore, nutritional interventions may serve as secondary prevention in this community. However, sources of lead linked to exposed children must be the priority of any intervention here. Proposed lead exposure interventions must occur over extended time periods and involve multiple sectors/approaches (e.g., regulatory, environmental, educational) (Pfadenhauer et al., 2014).