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. 2026 Feb 17;38(2):e70219. doi: 10.1002/ajhb.70219

Impaired Intestinal Function Among Indigenous Shuar Children of Amazonian Ecuador: Evidence From Lactulose:Mannitol Tests of Absorption and Permeability

Marcela Pfaff‐Nash 1,✉, Alejandro J Ramirez 2, Elizabeth Y Kim 3, Hannah N Cantrell 4, Melissa A Liebert 5, Felicia C Madimenos 6, J Josh Snodgrass 4,7, Lawrence S Sugiyama 4, Samuel S Urlacher 1
PMCID: PMC12914155  PMID: 41703973

ABSTRACT

Objectives

Intestinal function is an important but often overlooked aspect of human biological variation, with the intestines serving as both a barrier against external pathogens/contaminants and the primary conduit of nutrient extraction from food. Impaired intestinal function among children is viewed as a key contributor to growth faltering globally. However, few studies have investigated children's intestinal function in rural settings or beyond infancy. To address this limitation, we conducted a pilot study to describe the intestinal function of school‐age Indigenous Shuar children of Amazonian Ecuador and to assess the feasibility of implementing the widely utilized lactulose:mannitol (L:M) test of absorption and permeability with this group.

Methods

The urinary L:M test was performed with 23 rural‐living Shuar children aged 4–12 years. Ultra‐performance liquid chromatograph–high‐resolution mass spectrometry was used to determine L:M ratios, lactulose recovery, and mannitol recovery. Age and sex patterns were investigated using linear regression models.

Results

Children's mean L:M ratio was 0.33 ± 0.32, a ratio comparable to values reported for children in other low‐ and middle‐income settings. 35%–91% of children were categorized as having impaired intestinal function using common cut‐off values. Children's lactulose (0.14% ± 0.17%) and mannitol (2.60% ± 2.22%) recoveries did not differ by sex but increased with age (p < 0.05) and indicated diminished intestinal absorptive capacity and increased permeability.

Conclusions

Intestinal function appears to be considerably impaired among school‐age Shuar children living in a low‐resource, rural setting. Children living in unsanitary, non‐industrialized contexts may routinely experience intestinal permeability‐related immune activation and malabsorption‐related energy/nutrient loss. More research is needed to explore the breadth of global variation in children's intestinal function and to investigate its many evolutionary and public health implications.

Keywords: dual sugar test, enteropathy, environmental enteric dysfunction, gut function, leaky gut

1. Introduction

Intestinal function is a critical aspect of human biology (Vancamelbeke and Vermeire 2017). The small intestine is the primary locale for the absorption of nutrients and energy from consumed food. The intestines also serve as a physical barrier against pathogens and contaminants that enter the digestive tract, preventing them from passing into the bloodstream. Despite these key roles and potential impacts on phenotype and health, intestinal function is often overlooked in studies of human biological variation. The recent identification of environmental enteric dysfunction (EED, an acquired subclinical condition of damage to the small intestine) as a key contributor to childhood growth faltering (Budge et al. 2019) has generated new interest in global variation in children's intestinal function (Urlacher 2023). However, relatively few studies to date have investigated children's intestinal function in non‐industrialized settings or beyond the age of 5 years.

To address this limitation, we conducted a pilot study to describe the intestinal function of school‐age Indigenous Shuar children of rural Amazonian Ecuador using the lactulose:mannitol test (L:M). Heavy enteropathogen burdens have been described among the Shuar (Cepon‐Robins et al. 2019); however, assessments of intestinal function remain limited, restricting our ability to evaluate the consequences of pathogen exposure on intestinal health. This pilot study also allowed us to assess the feasibility of implementing the L:M test in this population. The L:M test, also called the dual‐sugar test, is a minimally invasive approach that has been used extensively for over two decades to evaluate children's intestinal function (Denno et al. 2014; Lunn 2000). It involves the assessment of excretion rates in urine of both an ingested large sugar (lactulose, C12H22O11) and small sugar (mannitol, C6H14O6). Because lactulose is normally not absorbed by an intact intestinal barrier and mannitol is readily absorbed, their excretion rates are commonly interpreted as reflecting intestinal permeability and absorptive capacity, respectively. The L:M ratio is therefore widely used as a composite indicator of intestinal function.

2. Materials and Methods

2.1. Study Population and Sample

The Shuar are a large Indigenous population living in Amazonian Ecuador and Peru. Like many other Indigenous Amazonian groups, they are experiencing varying degrees of market integration and transition from a forager‐horticulturalist lifestyle. More detailed background on the Shuar is provided elsewhere (e.g., Urlacher et al. 2016).

The present study was performed as part of the Shuar Health and Life History Project (https://www.shuarproject.org/). Data were collected in 2024 from one rural Shuar community located in the relatively remote “cross‐Cutucú” geographic region of Ecuador. The community was accessible only by canoe and had no running water and only minimal access to electricity. Prior research by the SHLHP in this community has provided evidence for pervasive intestinal infection with soil‐transmitted helminths among children (Cepon‐Robins et al. 2019) and high levels of childhood growth faltering (Urlacher et al. 2018). A convenience sample of 23 school‐age Shuar children aged 4–12 years (mean age = 8.5 ± 3.1 years; 48% females) with no reported gastrointestinal symptoms was recruited to participate. Participation was voluntary, and parental written informed consent with child informed assent was obtained from all participants. Study methods and procedures were approved and conducted in accordance with guidelines set by community leaders and the Baylor University IRB.

2.2. Lactulose:Mannitol Test and UPLC‐HRMS Lab Analysis

Complete information on the test collection procedures and UPLC‐HRMS analysis details are provided in the Supporting Information.

Urinary L:M test data were collected using standard procedures (Lauer et al. 2018). All families invited to participate in the study completed the L:M test. Following an overnight fast, children consumed a dose of 5 g lactulose (MiLab lactulose solution) and 1 g mannitol (Thermo Scientific) dissolved in 20 mL water. The dose was well tolerated, and children liked the sweet taste. Total urine production was then collected for the following 2 h, and total volume was recorded. Children were allowed to drink water but not to eat during the urine collection period; breakfast was provided upon completion of the test. Completed samples were treated with two drops of chlorhexidine preservative, aliquoted in 2 × 2 mL polypropylene cryovials and stored at −20°C using a portable freezer until shipment on dry ice to Baylor University for long‐term −80°C storage and analysis.

Lactulose and mannitol concentrations were quantified at the Baylor University Mass Spectrometry Center using ultra‐performance liquid chromatograph–high‐resolution mass spectrometry (UPLC‐HRMS, Vanquish UPLC coupled to an Orbitrap Exploris 120 HRMS, Thermo Fisher Scientific). Samples were injected (5 μL) onto a Luna NH₂ column (15 cm × 2.0 mm, 5 μm; Phenomenex) and eluted with a 5‐min binary gradient (acetonitrile/water with 0.1% formic acid) at 600 μL min−1 and 40°C. Lactulose and mannitol were detected by high‐resolution (60 000 FWHM) negative‐mode HESI Orbitrap MS with internal calibration.

2.3. Data Analysis

Lactulose:mannitol ratios (L:M) were calculated using the excreted urine concentrations (g/mL) of each sugar. Lactulose and mannitol excretion percentages (L% and M%, respectively) were calculated by multiplying the measured concentration of each sugar by total urine volume and dividing by the administered dose. Fractional excretion ratios (LMER) were then calculated as the ratio of percent lactulose to percent mannitol recovered. One participant was excluded from data analysis owing to values that fell outside the physiologically plausible range. For regression modeling, L:M, L% and M% were natural log‐transformed for normality, with sex and age investigated as predictors. Analyses were performed in RStudio (v.2025.05.1), with significance set at p < 0.05.

3. Results

Descriptive results and distribution plots from L:M testing are presented in Table S1 and Figure S1, respectively. Children's mean ± SD and median (IQR) L:M ratio were 0.33 ± 0.32 and 0.23 (0.11, 0.47), respectively. Using commonly applied L:M thresholds of 0.10 and 0.15 in low‐ and middle‐income settings (LMICs) (Galpin et al. 2005; Regassa et al. 2023), 91% and 71% of children, respectively, were categorized as having impaired intestinal function (Figure 1A). Children's mean L% recovery was 0.16% ± 0.18% and mean M% was 2.70% ± 2.19%. Children's mean ± SD and median (IQR) LMER were 0.09 ± 0.12 and 0.05 (0.02, 0.09), respectively. Applying commonly used LMER thresholds of 0.03 and 0.07 (Lee et al. 2017; Quadro et al. 2000), 65% and 35% of children, respectively, were categorized as having impaired intestinal function.

FIGURE 1.

FIGURE 1

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(A) Distribution of children's L:M values (violin plot). Values on top right box indicate L:M mean ± SD (95% confidence interval). Providing evidence for common intestinal function impairment, 91% of values lie above the common impairment cut‐off value of 0.10 (dashed red line). (B) Children's L:M is not related to age, indicating persistent intestinal function impairment throughout childhood. (C) Children's L% (lactulose recovery) is positively related to age, indicating increased intestinal permeability at older ages. (D) Children's M% (mannitol recovery) is positively related to age, indicating increased absorptive capacity at older ages. Shading indicates 95% confidence intervals. Panels B, C and D use log‐transformed outcomes plotted on a log scale, with y‐axis labels reported in absolute values for interpretability.

Parameter estimates for regression models investigating age and sex effects are provided in Table S2. Children's age was not a significant predictor of L:M (Figure 1B; p = 0.722). However, age positively predicted both L% (Figure 1C; β = 0.14, SE = 0.07, p = 0.045) and M% (Figure 1D; β = 0.16, SE = 0.06, p = 0.010). Sex was not a significant predictor in any model.

4. Discussion and Conclusions

This study is one of few to investigate children's intestinal function in a low‐resource, rural setting and beyond infancy and early childhood. The mean L:M ratio of 0.33 observed for school‐age Shuar children is comparable to values reported for children in several LMICs and indicates that considerable intestinal function impairment is common in non‐industrialized contexts (Figure 2). While appropriate caution is needed comparing values across studies (see below), Shuar children's L:M ratio is dramatically elevated compared to that reported for US children (mean L:M: 0.11; McOmber et al. 2010), and somewhat greater than those reported for Ethiopian children (mean L:M: 0.27; Regassa et al. 2023). Comparisons based on LMER values reveal a similar pattern. Shuar children (mean LMER: 0.09 and median: 0.05) exhibit higher values than Italian children and adolescents (mean LMER: 0.01; Giorgio et al. 2014) and have comparable values to those reported for rural Peruvian children (mean LMER: 0.09; Lee et al. 2017) and Brazilian children (median LMER: 0.05; Moore et al. 2020). However, Shuar children exhibit lower LMER values than those observed among rural Malawian children (mean LMER: 0.2; Weisz et al. 2012). These comparisons underscore the existence of substantial global variation in children's intestinal function. They also highlight a general pattern of diminished intestinal function among rural and subsistence‐based populations that persists well beyond the first 5 years of life. The expanding body of literature on EED, which documents increased childhood intestinal damage in unsanitary, high‐pathogen contexts (Budge et al. 2019; Lin et al. 2013), supports this interpretation.

FIGURE 2.

FIGURE 2

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Global variation in childhood L:M values from key studies using the same dosing protocol as the present study. Shuar children exhibit higher L:M ratios than those reported for children in industrialized countries and cluster more closely with values from LMICs. Additional studies are provided in Table S3. *Mean ± standard deviation. § Median (1st quartile, 3rd quartile). + Mean (95% confidence interval).

Shuar L% and M% recovery values provide additional insight into the nature of intestinal impairment among children living in low‐resource, rural settings. When individual sugar recoveries are compared with those reported for Peruvian children studied using the same dosing protocol and urine collection duration (Lee et al. 2017), elevated L:M ratios among Shuar children appear to be driven primarily by higher L% (0.16 in Shuar children vs. 0.08 in Peruvian children; Figure 2). Although Shuar children also exhibit higher M% than Peruvian children (2.70 vs. 0.86), the Peruvian sample comprised younger children (3–5 years), and differences in M% may reflect body size–related differences in intestinal absorptive surface area. At the same time, elevated recoveries of both L% and M% among Shuar children may indicate greater severity of enteropathy despite similar LMER in the two populations (mean LMER: 0.09). This interpretation is consistent with recent evidence showing that L% and M% often change in parallel rather than inversely, particularly in settings characterized by moderate to severe enteropathy (Besa et al. 2026; Ordiz et al. 2018). In such contexts, loss of size selectivity in intestinal pathways may allow both sugars to traverse overlapping routes resulting in parallel increases in recovery while maintaining relatively stable L:M ratios. Together, these findings suggest that reliance on L:M ratios alone may obscure important variation, emphasizing the need to consider individual L% and M% recoveries when evaluating intestinal function.

Results further indicate that M% and L% recoveries increase with age, while overall L:M ratios remain relatively stable. The developmental pattern observed in this study contrasts with findings from Gambian children, among whom L% and L:M ratios improve with age while M% remains largely unchanged (Campbell et al. 2002). One possible explanation for this difference relates to methodological differences: the use of standard sugar doses in the present study may result in greater recovery of both sugars as body size and intestinal surface area increase with age. Consequently, higher recoveries with age likely reflect increased body size rather than true improvements in absorptive efficiency and may indicate persistently altered intestinal function across age.

The L:M test represents an important tool for human biologists investigating questions of intestinal health. However, cross‐study comparisons should be interpreted cautiously, as the application of the test varies widely across research groups (Denno et al. 2014). For example, dosing protocols differ substantially, with some studies using weight‐adjusted doses (Andrews‐Trevino et al. 2022) and others using standard doses (as in this study), but with varying amounts of lactulose and mannitol. Such dosing differences are particularly problematic for comparing L:M ratios as well as L% and M% recoveries. Urine‐collection duration also varies considerably, ranging from 2 to 6 h (Giorgio et al. 2014). When the same dose is used, L:M ratios may be comparable, but L% and M% recoveries are not, as longer collection periods typically yield higher excretion values (Musa et al. 2019). In addition, discrepancies exist in how L:M results are calculated and reported. While there is some consensus regarding calculation of individual sugar recoveries [(sugar concentration (mg/mL) × urine volume (mL))/sugar ingested (mg)], methods for calculating L:M vary: some studies report ratios of percent recovery, whereas others report ratios of total sugar excretion. More problematically, many studies do not specify how L:M values are calculated. Together, these methodological inconsistencies hinder efforts to characterize global variation in intestinal function.

Most evidence linking intestinal function impairment with growth and developmental outcomes comes from studies of infants and young children (Crane et al. 2022; Lauer et al. 2018). Much less is known about whether intestinal impairment in school‐age children has meaningful consequences for health and growth, and addressing this gap represents an important next step for future research. We propose that, in pursuing this work, continuous measures of L:M are likely to be more informative than categorical thresholds that define “normal” intestinal function, as they better capture the full range of variation across populations and contexts (Wiley 2020).

This pilot study among the Shuar highlights global variation in childhood intestinal function and supports the position that children living in low‐resource, rural contexts routinely experience diminished intestinal barrier integrity and absorptive capacity. Links to documented patterns of heavy enteropathogen burden (Cepon‐Robins et al. 2019) and linear growth faltering (Urlacher et al. 2018) among Shuar children are indicated but require direct testing. Future work in human biology should identify the socioecological factors (e.g., market integration‐related changes to environment and lifestyle) shaping children's intestinal function and seek to understand the impact of variation in intestinal function on children's energetics, development, and lifelong health.

Funding

This work was supported by Baylor University.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Data S1: ajhb70219‐sup‐0001‐Supinfo.docx.

AJHB-38-e70219-s001.docx (111.6KB, docx)

Acknowledgments

We thank Shuar participants and their families for their support and hospitality.

Pfaff‐Nash, M. , Ramirez A. J., Kim E. Y., et al. 2026. “Impaired Intestinal Function Among Indigenous Shuar Children of Amazonian Ecuador: Evidence From Lactulose:Mannitol Tests of Absorption and Permeability.” American Journal of Human Biology 38, no. 2: e70219. 10.1002/ajhb.70219.

Data Availability Statement

The complete de‐identified dataset supporting this article will be made available to qualified researchers, clinicians, and others upon request and agreement to privacy and data use expectations that conform to IRB requirements, the welfare of study participants, and their agreements to participate in research. This process is streamlined, and requests for data can be easily made via an online form on the Shuar Health and Life History Project website (https://www.shuarproject.org/).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Data S1: ajhb70219‐sup‐0001‐Supinfo.docx.

AJHB-38-e70219-s001.docx (111.6KB, docx)

Data Availability Statement

The complete de‐identified dataset supporting this article will be made available to qualified researchers, clinicians, and others upon request and agreement to privacy and data use expectations that conform to IRB requirements, the welfare of study participants, and their agreements to participate in research. This process is streamlined, and requests for data can be easily made via an online form on the Shuar Health and Life History Project website (https://www.shuarproject.org/).

Articles from American Journal of Human Biology are provided here courtesy of Wiley

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