INTRODUCTION

Stunting is a condition of growth retardation in children characterized by excessive shortness for one’s age. Specifically, stunting is indicated by a length or height-for-age that falls below -2 standard deviations from the median of the World Health Organization (WHO) child growth standards [1]. This form of malnutrition is a major public health concern, especially in developing countries, and is implicated in approximately 45% of deaths among children under 5 years old [2-4]. Stunting has detrimental effects on health in both the short and long term, becoming irreversible after the age of 2 years. The consequences of stunting can persist throughout an individual’s life and even impact future generations [5]. Global estimates indicate that nearly 150 million children under 5 years old, or about 22%, were affected by stunting in 2020. In Indonesia, the prevalence of stunting remained relatively high, at 21.6%, in 2022 [6].

Stunting is not solely the result of chronic malnutrition, which is particularly impactful during the first 1000 days of life, but is also influenced by recurrent infectious diseases [1]. These diseases contribute to nutritional deficiencies by reducing appetite, disrupting nutrient absorption (malabsorption), directly depleting micronutrients, and increasing the body’s metabolic rate [7,8]. Additionally, infectious diseases stimulate the production of proinflammatory cytokines, which can inhibit growth hormone activity and ultimately impede linear growth [9,10]. Considering the impact of infectious diseases on child growth, strategies to prevent and control these diseases, including immunization, play a role in promoting better growth outcomes in children [2,7,8].

Immunization has been identified as a key nutrition-related intervention to combat the direct causes of stunting [11]. While immunization is acknowledged as one of the most successful and cost-effective public health initiatives, global immunization coverage has largely stagnated over the past decade. The coronavirus disease 2019 pandemic and the resulting disruptions to healthcare systems have exacerbated this issue. In 2021, estimates suggest that approximately 25 million children under 1-year old did not receive basic immunizations [12]. Surveys such as the 2018 Indonesia Basic Health Survey and the 2019-2021 Indonesia National Socio-Economic Survey indicate that immunization coverage in Indonesia remains below the desired level, with less than 70% coverage [13,14]. Approximately 1.5 million children in Indonesia did not receive complete immunization between 2017 and 2021 [15].

Furthermore, several studies have demonstrated that incomplete immunization increases the risk of stunting and other forms of malnutrition [8,16-18]. However, research examining the association between basic immunization status and stunting in Indonesia has yielded inconsistent results. Most studies have been limited by factors such as inadequate sample sizes, failure to account for confounding variables, and the inclusion of participants under 9 months old, who are ineligible for complete basic immunization status. Furthermore, the use of ecological studies in certain research has introduced the potential for ecological fallacy bias.

Consequently, this study aimed to examine the relationship between basic immunization status and the incidence of stunting in Indonesian toddlers aged 12 months to 59 months. It utilized a larger sample size, controlled for confounding variables, and employed a more appropriate type of analysis than prior research. We hope that this study will serve as a reference or evidence base for implementing priority activities to reduce stunting and will inform the public about the importance of complete immunization among children.

METHODS

Data Sources and Participants

This study employed a cross-sectional design and utilized secondary data from the 2021 Study of Indonesia’s Nutritional Status (SSGI-2021). The SSGI-2021, a national health survey conducted by the Ministry of Health of the Republic of Indonesia, aimed to provide a detailed overview of the nutritional issues and their determinants among Indonesian children under 5 years old. Sampling for the SSGI-2021 was performed using a stratified 2-stage sampling method across 34 provinces, covering 514 districts/cities in Indonesia. The first stage of the SSGI-2021 was designed to estimate the prevalence of nutritional problems at the provincial level, while the second sought to determine the prevalence at the district/city level. The range of variables gathered during the second stage regarding the determinants of nutritional problems was not as extensive as that collected in the first. Consequently, this study only incorporated data from the first stage of the SSGI-2021, as this phase included a more complete set of variables.

The sample for the first stage of the SSGI-2021 included 95 911 children under 5 years old, drawn from 9500 census blocks. To be included in this study, children had to be between 12 months and 59 months old at the time of SSGI-2021 data collection, have a measured height, have no severe or chronic illness, and have complete data for all variables. Of the initial sample, 8224 children (11.7%) did not meet these inclusion criteria. Consequently, 70 267 children (88.3%) were eligible for the study.

Outcome Variable

The primary outcome variable in this study was stunting, defined as a height-for-age z-score less than −2 standard deviations from the median of the WHO Child Growth Standards for the child’s age and sex [1]. Trained personnel conducted anthropometric measurements of the children using standardized equipment that was regularly calibrated.

Independent Variable

The primary independent variable was basic immunization status, which referred to the vaccinations recommended for infants before the age of 1-year [19]. Information on immunization history was obtained from existing records or reports provided by the mother or caregiver. Complete basic immunization was defined as a child having received the following: 1 dose of the hepatitis B vaccine; 1 dose of the Bacillus Calmette –Guérin (BCG) vaccine; 4 doses of the oral polio vaccine plus 1 dose of the inactivated polio vaccine (IPV), or 3 doses of IPV alone; 3 doses of the combined diphtheria, pertussis, tetanus, hepatitis B, and Haemophilus influenzae type b (DPT-HB-Hib) vaccine; and 1 dose of the measles-rubella vaccine [19,20]. In this study, immunization status was categorized into 3 groups: complete immunization, partial immunization, and no immunization. We also considered a range of covariate variables that could potentially confound or modify the results. These included the child’s age, sex, area of residence, history of infectious diseases, dietary diversity, consumption of animal protein, economic status, birth weight, mother’s education level, mother’s occupation, sanitation, and quality of drinking water.

Statistical Analysis

Cox regression analysis was employed, with the results reported along with 95% confidence intervals (CIs), to analyze the relationship between basic immunization status and stunting. To account for potential model misspecification and ensure valid standard errors, the robust variance estimator was used. All analyses were conducted using Stata version 14.1 (StataCorp., College Station, TX, USA) with a significance level of 0.05. Cox regression can be adapted for cross-sectional studies to estimate prevalence ratios (PRs) rather than hazard ratios. In cross-sectional studies, time-to-event data are inherently absent, as the design captures data at a single point in time. Thus, applying Cox regression to calculate PR in this context requires the assumption that the time to event is the same for all participants. Multivariable analysis was conducted to determine the effect of basic immunization status on stunting after controlling for other confounding variables. Backward elimination was applied for variable selection. The adjusted prevalence ratio (aPR) was estimated from the model that included variables identified as confounders or effect modifiers. A variable was considered a confounder if the difference in PR between the reduced and full models in the multivariable analysis exceeded 10%, or if it was deemed substantively important [21]. “Substantively important” refers to variables considered critical based on theoretical frameworks, prior research, or domain expertise. These variables were included in the analysis regardless of their statistical significance because they were thought to meaningfully influence the outcome or to be essential for controlling confounding in the context of this study.

Ethics Statement

This research received ethical approval from the Health Research and Development Agency of the Ministry of Health under the approval No. LB.02.01/2/KE.248/2021.

RESULTS

The prevalence of stunting among toddlers aged 12 months to 59 months was 23.1%. Regarding basic immunization status, 74.9% of toddlers had completed basic immunizations, 22.9% had received only partial immunization, and 2.2% had not received any basic immunizations. In terms of covariate variables, most respondents were male, resided in rural areas, had no history of infectious disease in the past 6 months, had no history of low birth weight (LBW), consumed a diet with adequate diversity, and consumed 1 type to 2 types of animal protein. Furthermore, participants tended to have mothers with low to medium levels of education, mothers who were not employed, access to good sanitation, and access to clean drinking water.

The results of the bivariate analysis (Table 1) show that all variables, including basic immunization status and other covariates, were significantly associated with the incidence of stunting (p<0.05). Toddlers aged 12 months to 59 months who had either incomplete or no basic immunization were at a higher risk of stunting compared to those with complete basic immunization. Regarding covariate variables, an increased risk of stunting was observed in male toddlers as well as those with a history of infectious disease, a history of LBW, a rural area of residence, a diet lacking in food diversity, and inadequate sanitation and drinking water facilities. Maternal education also played a role; the lower the mother’s education level, the higher the risk of stunting in the child. Regarding economic status, the lower the economic quintile, the higher the risk of stunting. Finally, the risk of stunting was lower in children who consumed a greater variety of animal proteins.

Table 2 presents the results of a multivariable analysis examining the association between basic immunization status and stunting, adjusted for covariates. Toddlers who had received no basic immunizations exhibited a 1.27-fold increased risk of stunting, while those with incomplete immunizations had a 1.18-fold increased risk, compared to toddlers with complete basic immunizations. These associations remained significant after adjusting for maternal education, household economic status, and birth weight, with p-values <0.001 for each comparison. To evaluate the robustness of our findings, we performed a sensitivity analysis by systematically excluding different covariates from the model. Initially, all variables were included, resulting in an aPR for incomplete immunization of 1.18 (95% CI, 1.14 to 1.22). Upon excluding certain variables to arrive at the final model, the aPR for incomplete immunization remained at 1.18 (95% CI, 1.15 to 1.22). This consistency suggests that the association between immunization status and stunting is stable.

DISCUSSION

The results indicated that toddlers who had not received any immunizations were at the highest risk of stunting, with an aPR of 1.27 (95% CI, 1.17 to 1.37). Toddlers who had received some, but not all, immunizations (partial immunization) had an aPR of 1.18 (95% CI, 1.15 to 1.22). Bivariate analysis yielded similar findings; the greatest risk of stunting was observed in toddlers with no immunizations, followed by those with partial immunization.

These findings align with a study conducted by Semba et al. [18] in Indonesia, which revealed that among toddlers aged 12 months to 59 months, those who received complete, incomplete (partial), or no immunization exhibited stunting prevalence rates of 37%, 47%, and 54%, respectively. While the study did not report the strength of the association, manual calculations yield a crude PR of 1.27 for children who were not fully immunized and a crude PR of 1.46 for children who received no immunization at all [18].

The potential link between immunization status and stunting can be explained as follows. First, immunization is key to the formation of a child’s immune system. Children who are fully immunized tend to have robust immunity, which helps them avoid infectious diseases [22]. A meta-analysis indicated that incomplete immunization is a risk factor for acute respiratory infection, the most common infectious disease among children under 5 years of age (pooled odds ratio, 1.83; 95% CI, 1.32 to 2.52) [23]. Furthermore, immunizations, especially those involving live vaccines such as BCG and measles, have been shown to exert non-specific effects that can lower overall mortality rates in children, not solely mortality from the diseases targeted by the vaccines [24]. The findings of this study align with a report by Berendsen et al. [25] who suggest that immunization could improve children’s general health and potentially reduce the risk of stunting through non-specific vaccine effects. The underlying mechanism may be mediated by innate immune memory, also known as trained immunity, and lymphocyte cross-reaction [24,26]. Second, immunization not only prevents diseases and mortality in children but also serves as an indicator of a child’s access to adequate basic health ser-vices, which may offer a protective effect against malnutrition [16]. Third, the relationship between immunization and stunting may be further explained by the observation that the same social, economic, and cultural factors that contribute to stunting also affect parental attitudes and practices towards child immunization [27].

In this study, no statistical confounding variables were identified, as indicated by a change in PR greater than 10%. Nevertheless, in the final multivariable analysis model, we retained the variables of economic status, maternal education, and child birth weight because they were substantively important and exerted the greatest impacts on PR. The crude PR value observed was 1.29, whereas the aPR was lower at 1.19. This suggests that economic status, maternal education, and child birth weight acted as positive confounders, which could lead to an overestimation of the strength of the association if not controlled or adjusted.

The findings of this study indicate that a lower economic status is linked to an increased risk of stunting in toddlers. Data from 30 low-income and middle-income countries revealed that children under 5 from the poorest households were twice as likely to display stunting compared to those from the wealthiest households [28]. A study in West Java revealed that children from households in the lowest wealth quintile were more likely to experience stunting, with an adjusted odds ratio (aOR) of 2.30 (95% CI, 1.43 to 3.68) relative to households in the highest quintile [29]. Economic status also influences the likelihood of children receiving complete basic immunization. Children from middle to upper economic status households were 1.98 times more likely to receive complete basic immunization compared to those from households with low economic status (aOR, 1.98; 95% CI, 1.04 to 3.78) [30].

The findings of this study also demonstrated that the level of maternal education significantly influenced a child’s risk of stunting. Education is associated with maternal knowledge, which can affect maternal attitudes and behaviors in child-rearing practices. Multiple studies have shown that lower levels of maternal education correspond to a higher risk of stunting in children [31,32]. Mothers with higher education levels may have a better understanding of health behaviors, hygiene practices, and the nutritional needs of their children. Additionally, education influences maternal attitudes and behaviors in providing immunizations; more highly educated mothers tend to exhibit greater awareness of the importance of immunization and more effectively utilize healthcare services. A further analysis of data from the 2020 Indonesia National Socio-Economic Survey showed that mothers with at least a high school education had a 2.39 times greater likelihood of having babies with complete basic immunization compared to mothers with a junior high school education or less (aOR, 2.39; 95% CI, 1.18 to 4.84) [30].

Research conducted by Utami et al. [33] and Aryastami et al. [34] has indicated that LBW is a dominant risk factor for stunting in children. Birth weight reflects the adequacy of nutritional intake during pregnancy [33,34]. Additionally, LBW may influence a child’s basic immunization status. The hepatitis B vaccine is typically administered shortly after birth and is a criterion for a child to be considered fully immunized. For infants weighing less than 2000 grams born to mothers who test negative for the hepatitis B surface antigen, hepatitis B vaccination is postponed until the child is 1-month old [35]. This delay can increase the risk of a missed opportunity for hepatitis B immunization, particularly if immunizations occur at a different location from the place of birth.

The results of this study provide evidence that immunization is associated with stunting in Indonesia. This information could be a valuable reference for implementing priority activities aimed at reducing stunting. Such activities include providing support to families at risk of stunting, conducting audits of stunting cases, and managing such cases. Counseling and communication efforts, as well as information and education campaigns supporting families at risk of stunting, should clearly communicate the factors that contribute to stunting and the preventive measures that can be taken, including the importance of complete immunization [36]. Stunting case audits are proactive efforts to identify risk factors for stunting as a means of preventing similar cases in the future. During these audits, one critical aspect to investigate is the child’s immunization history [37]. According to the national guidelines for medical services regarding stunting cases, when taking an anamnesis, healthcare providers should inquire about potential risk factors for stunting that the child may have encountered, including their immunization history. For children who exhibit stunting, immunizations must be provided and completed if not done so already. In general, the administration of immunizations in stunting cases has no contraindications. Since children with stunting are particularly susceptible to infectious diseases, immunization is especially crucial [38].

We can conclude that basic immunization status affects the incidence of stunting in toddlers between the ages of 12 months and 59 months. Those with incomplete or no basic immunization are at a greater risk of stunting compared to their fully immunized counterparts. Thus, parents must ensure that their children’s immunizations are completed according to the recommended schedule and to increase parental awareness of health services, disease prevention, and the nutritional requirements of toddlers.

Strengths and Limitations

Compared to previous studies examining the relationship between basic immunization status and the incidence of stunting in Indonesia, this study had several advantages. First, it utilized a large sample size, which can reduce random errors. Second, it evaluated key variables that were suspected to be confounding factors and incorporated the IPV vaccine into the operational definition of complete basic immunization. However, while this study indicated a link between basic immunization status and stunting, it is not possible to infer temporal relationships or causality (temporal ambiguity) due to its cross-sectional design. Additionally, the strength of the association found in this study may be influenced by other unassessed variables, such as the history of exclusive breastfeeding, complementary feeding practices, advanced immunization status, maternal nutritional status, and other factors, due to limitations in the research data sources.

Notes

Conflict of Interest

The authors have no conflicts of interest associated with the material presented in this paper.

Funding

None.

Acknowledgements

The authors would like to express their gratitude to the Head of the Health Policy and Development Board at the Ministry of Health, Republic of Indonesia, for granting permission to access, analyze, present, and publish the data that were instrumental in this study.

Author Contributions

Conceptualization: Purwanti ED, Ronoatmodjo S. Data curation: Purwanti ED, Masitoh S. Formal analysis: Purwanti ED, Masitoh S. Funding acquisition: None. Methodology: Purwanti ED, Masitoh S, Ronoatmodjo S. Project administration: Purwanti ED, Masitoh S. Visualization: Masitoh S. Writing – original draft: Purwanti ED, Masitoh S, Ronoatmodjo S. Writing – review & editing: Purwanti ED, Masitoh S, Ronoatmodjo S.

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References

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