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Urban Forestry & Urban Greening 74 (2022) 127667

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Urban Forestry & Urban Greening


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How does the presence of greenspace related to physical health issues


in Indonesia?
Aji Kusumaning Asri a, Hsiao-Yun Lee b, Chih-Da Wu a, c, *, John D. Spengler d
a
Department of Geomatics, National Cheng Kung University, Tainan 70101, Taiwan
b
Department of Leisure Industry and Health Promotion, National Taipei University of Nursing and Health Sciences, Taipei 112, Taiwan
c
National Institute of Environmental Health Sciences, National Health Research Institutes, Miaoli 35053, Taiwan
d
Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA 02115, United States

A R T I C L E I N F O A B S T R A C T

Handling Editor: Nadja Kabisch There have been many studies associating various aspects of greenspaces with physical health. Very few of these
investigations are available for developing countries such as Indonesia. Our study focused on evaluating the
Keywords: association between greenspace and the incidence rate of non-communicable diseases (NCDs) in terms of
Chronic non-communicable diseases (NCDs) ischemic heart disease (IHD), diabetes mellitus (DM), rheumatoid arthritis (RA), and chronic kidney disease
Developing country, greenspace
(CKD). Greenspace was presented by satellite-derived normalized difference vegetation index (NDVI) and forest-
Indonesia
related green cover datasets to define exposures to the resolution of 250-m. The Institute for Health Metrics and
Physical health diseases
Socioeconomic factors Evaluation provided age and gender incident data of NCDs at the province level. A generalized additive mixed
model coupled with sensitivity test was used to evaluate the exposure-outcome association. Stratified analyses
were also employed. After adjusting for covariates, there was a significant negative association for incidence of
NCDs and greenspace. We found that an interquartile unit increase of NDVI, and a percentage of forest were
closely related to a decrease in the risk of NCDs by 0.3–9.4% and 0.6–6.2%, respectively. Stratified by exposure
level, a greater effect of greenspace on reducing NCDs risk occurred in high exposure areas. Considering the
socioeconomic factors, greenspace could influence on reducing NCD risks in high urbanization, low-high poverty,
and low-high literacy areas. An increment unit of greenspace was associated with a decreased risk of NCDs. This
study underscores important health benefits associated with exposures to nature supporting efforts to preserve
greenspaces in Indonesia.

1. Introduction (Purnamasari, 2018). Specifically, the Demographic and Epidemiolog­


ical Transition Review confirmed stroke, ischemic heart disease (IHD),
Indonesia is one of the countries in Southeast Asia experiencing rapid and diabetes mellitus contribute to the high number of
urbanization (The World Bank, 2016). Urbanization often leads to disability-adjusted life years (DALY) in Indonesia (Setyonaluri and
regional economic development but also has some consequential nega­ Aninditya, 2019). It also highlighted from 2006 to 2016 the health
tively impacts such as environmental degradation and reductions in burden due to diabetes mellitus increased by 54.9% and IHD by 10.5%,
human health (Moore et al., 2003; Sasana et al., 2019). Along with in addition to increases in the prevalence of depression, chronic kidney
modernity comes profound changes in lifestyle, diets, environmental diseases (CKD), and rheumatoid arthritis (RA).
exposures that are associated with a shift in disease burden. For The development of NCDs in Indonesia has been examined with a
Indonesia, as with other developing economies, there has been a pro­ focus on associated risk factors (Adisasmito et al., 2020; Idris et al.,
nounced increase in physical health problems in terms of 2018; Fitria et al., 2020; Muhith et al., 2018; Schröders et al., 2017).
non-communicable diseases (NCDs) (Indonesian Ministry of Health, What follow is an overview of the literature to date: a systematic review
2016). The 2016 Indonesian Health Profile Report’s confirmation of by Schröders and colleagues (2017) identified the risk factors related to
NCDs as the leading cause of mortality, especially for middle-age groups chronic NCDs morbidity, mortality, and coping strategies and linked

* Correspondence to: No. 1 University Road, Tainan 70101, Taiwan.


E-mail addresses: p68107021@gs.ncku.edu.tw (A.K. Asri), hsiaoyun07@ntunhs.edu.tw (H.-Y. Lee), chidawu@mail.ncku.edu.tw (C.-D. Wu), spengler@hsph.
harvard.edu (J.D. Spengler).

https://doi.org/10.1016/j.ufug.2022.127667

Available online 3 July 2022


1618-8667/© 2022 Elsevier GmbH. All rights reserved.
A.K. Asri et al. Urban Forestry & Urban Greening 74 (2022) 127667

them to the social determinants of health in Indonesia. Considering vegetation) (Weier and Herring, 2000). In this study, green NDVI data
geographic and socioeconomic disparities, a study in Indonesia revealed from 2000 to 2014 with acquisition times approaching the middle sea­
that chronic cardiovascular disease is increasing in areas with higher son have been calculated in June and December; the determination of
income and educational attainment (Adisasmito et al., 2020). Further, a the data periods was made because there are two main seasons in
study by Idris et al. (2018) confirmed gender, living area, employment Indonesia, the dry season and the rainy season (Asri et al., 2021).
status, obesity, hypertension, and dyslipidemia are contributing factors Furthermore, to avoid bias in estimation due to other natural effects,
to diabetes mellitus related to NCDs. In addition, several previous such as proximity to water, we eliminated NDVI with a negative grid.
studies discussed risk factors for NCDs, such as the influence of envi­ The average estimates of NDVI from 2000 to 2014 for the provincial
ronmental and occupational factors on chronic kidney disease (Fitria boundaries were spatially linked to the NDVI image to estimate the
et al., 2020) and the influence of genetics on conditions of chronic joint greenspace exposure of the population in each province. As an index
inflammation such as rheumatoid arthritis (Muhith et al., 2018). estimate, Fig. S2 showed the spatial distribution of NDVI in the baseline
Several recent studies report proximities to the green environments period 2000.
as having positive effect on general health (Kondo et al., 2018; Maas
et al., 2006) and, specifically, can reduce the health burden of chronic 2.2. Incidence rate of chronic non-communicable diseases
NCDs (De la Fuente et al., 2020; Kim et al., 2019; Park et al., 2021;
Stanhope et al., 2020). In terms of providing beneficial effect on car­ Four chronic non-communicable diseases (NCDs) that routinely are
diovascular disease such as IHD, a Korean study reported that an among the leading causes of mortality in Indonesia were selected as the
interquartile unit increment of NDVI was associated with 3.64% health outcomes. They include ischemic heart disease–IHD, diabetes
decrease in IHD mortality (Kim et al., 2019). The proximity to green­ mellitus-DM, rheumatoid arthritis-RA, and chronic kidney disease-CKD
space were also linked with lower risks of developing diabetes mellitus (Setyonaluri and Aninditya, 2019; Indonesian Ministry of Health,
(De la Fuente et al., 2020). Another study confirmed that a 0.1-unit 2016). Some of the factors underlined this study only focused on these
increment of greenspace (NDVI) within 250-m to 1250-m could four diseases including (1) cardiovascular diseases in terms of ischemic
decreased ESRD patient visits and all-cause death risk due to chronic heart disease and diabetes mellitus are the health burdens that cause the
kidney disease by up to 13.2% (Park et al., 2021). Additionally, research highest mortality not only in Indonesia but also in the world (Setyona­
has identified exposure to greenspace as potentially helpful in reducing luri and Aninditya, 2019; World Health Organization, 2019), followed
the global burden of pain from autoimmune-inflammatory disorders by an increment of chronic kidney disease and rheumatoid arthritis; (2)
(Stanhope et al., 2020). The various pathways for how greenspace can Diabetes mellitus as a disease suffered by most Indonesian people is also
reduce the risk of physical health problem in terms of NCDs have pre­ known as a comorbid for cardiovascular and kidney diseases (Einarson
viously been studied and reported (Shen and Lung, 2016; Wang et al., et al., 2018); (3) From the aspect of data availability, these four health
2019). outcomes have complete data for all provinces during the study period;
Indonesia, like many countries with developing economies, is in and (4) There is support from previous studies that confirmed the as­
transition with rapid urbanization. There is a need to understand the sociation between greenspace and reduced health burden due to these
potential health benefits of green infrastructure in the context of four chronic diseases (De la Fuente et al., 2020; Kim et al., 2019; Park
expanding cites in developing countries since up until now much of the et al., 2021; Stanhope et al., 2020). In this regard, several pathways were
evidence is derived from research conducted in developed countries identified including reducing risk factors and building capacities to
(Zhang et al., 2020). This study addresses this scientific gap. 15 years of encourage better physical movements (Markevych et al., 2017).
province-level disease specific occurrence data, (i.e., ischemic heart We used province level data provided by the Institute for Health
diseases, diabetes mellitus, rheumatoid arthritis, and chronic kidney Metrics and Evaluation’s 2019, Global Burden of Disease Study. As the
disease), was linked to green land cover data and satellite derived measuring unit of analysis, for each chronic NCD we calculated inci­
sensing of vegetation (NDVI) and adjusted for social and economic dence rates per 10 000 population. This province-level health data is
variables in a multi-level statistical. available annually from 2000 to 2014. For specific definitions, chronic
non-communicable diseases analyzed in this study were defined using
2. Materials and methods International Classification of Diseases 10th revision codes; ICD-10 I20-
I25 for ischemic heart disease, ICD-10 E10-E14 for diabetes mellitus,
2.1. Indicator of greenspace ICD-10 M05-M06 for rheumatoid arthritis, and ICD-10 N00-N19 for
chronic kidney disease. Considering that this study used a similar 15-
Exposure to greenspace was determined using green land cover year main exposure and outcome database, Fig. 1 depicted the spatial
dataset provided by the Geospatial Information Agency of Indonesia and distribution of the average exposure to green NDVI and the incidence
assessment by satellite-derived vegetation index obtained from the US rate of NCDs from 2000 to 2014 in 34 provinces in Indonesia.
National Aeronautics and Space Administration. First, we extracted the
coverage of forest (last updated in 2014) as one of the green indicators in 2.3. Additional risk factors
our main analysis (Fig. S1). We considered forest to represent green­
space because the Global Forest Resources Assessment reported that Province-level risk factors associated with the development of stud­
forest is the dominant green cover in major parts of Indonesia (FAO-­ ied physical diseases were including: (a) demographic adjusted for
GeoNetwork, 2015). Furthermore, an Indonesia that is forest-rich over population density and sex represented by females; (b) urban circum­
the long term would contribute to a reduction in air pollution, which is stances examined for proportion of population in poverty, unemploy­
harmful to health, especially chronic diseases (Diener and Mudu, 2021; ment rate, and the percentage of literacy; (c) unhealthy behavior in
Ratnaningsih and Suhesti, 2010). terms of smoking (Martini et al., 2021); (d) health status such as the
Next, considering for continuous exposure effect, we collected green percentage of the population who activated the national health insur­
vegetation index data represented by moderate resolution imaging ance and the percentage of population with chronic disease symptoms
spectroradiometer - normalized difference vegetation index (MODIS identified from clinical visits (Kristina et al., 2018); (e) meteorological
NDVI, MOD13Q3 V6 product) with 250 × 250 m spatial resolution that factor such as temperature and humidity (He et al., 2021; Lee et al.,
was generated every 16 days. NDVI is an approximate green index based 2020). In detail, all information related risk factors were described in
on the visible light and near-infrared light reflected by the surface. Table S1. Furthermore, as our preliminary analysis to investigate the
Values range from − 1 to + 1 (index ≤ 0.1 indicate snow, water, sand, or two-way association between the risk factors and the studied diseases,
barren lands; 0.2–0.3 indicate shrub, grass; > 0.3 indicate green we conducted a bivariate test using Spearman algorithm. The results

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A.K. Asri et al. Urban Forestry & Urban Greening 74 (2022) 127667

Fig. 1. Spatial distribution of the average exposure to green NDVI and the incidence rate of NCDs in 34 provinces.

reported in Table S2. two sensitivity tests to observe changes in the estimated coefficient. In
this case, we assumed that there is no significant change indicating
robustness in the developed models. Sensitivity model 1 was adjusted for
2.4. Sequence of statistical analysis population density, sex, urbanization, divorce, health insurance, and
meteorological factors. While sensitivity model 2 was adjusted for
As the preliminary analysis to interpret the characteristics of all population density, sex, urbanization, divorce, smoking, health insur­
adjustment variables, descriptive statistics were calculated. In per­ ance, symptoms, and meteorological factors. Second, the sensitivity test
forming the estimated greenspace, the percentage of the forest by the was also evaluated by considering all risk factors but removing data
total area of study location and NDVI represented by an interquartile from Java and Bali provinces as rapid urban regions (model 3) and
metric (IQR = 0.09) were assessed. A generalized additive mixed model sensitivity model 4 by examining the data from high-urbanized prov­
(GAMM), which controls for fixed and random effect variables was inces. This adjustment was carried out to ensure that the exposure-
applied to examine the link between greenspace exposure and all four outcome relationship remained significant even though it omitted or
physical diseases that were analyzed (i.e., IHD, DM, RA, and CKD). only considered data from urbanized provinces.
Before the association model using GAMM was generated, we checked Recognizing that urban circumstances have influenced changes in
for variance-inflation factors and assured that the values for each vari­ environmental degradation, people’s lifestyles, and socioeconomic
able were < 4, indicating there is no multicollinearity effect among (Oliveira et al., 2020), which in turn increase the burden of
adjusted risk factor variables (Asri et al., 2021; Helbich et al., 2018) non-communicable diseases (The Lancet Diabetes and Endocrinology,
(Table S3). To overcome the temporal correlation issue that causes bias 2017), we conducted multilevel analyses to investigate the effects of
estimates due to repeated computations at the same location (15 years greenspace in various urban settings. By using the median value of each
main datasets), we used the ID of the province as a random intercept in socioeconomic data, our stratified analyses distinguished the relation­
generating the association models. A continuous-time first-order autor­ ship between greenspace and chronic NCDs at various levels of urban­
egressive model was employed to adjust for the annual temporal ization (median of urban population: 36.90%), economic status (median
variance-covariance structure. The gaussian setting was considered to of poverty: 9.53%), and literacy (median of educated population:
control for the variability of data distribution. Further, knowing that the 96.07%). Stratified analyses were performed for each province with
meteorological conditions in Indonesia varied in each region (Faradiba, different levels of greenspace.
2021), the regression spline for temperature and humidity were
adjusted. In this study, the smoothing spline for centroid 3. Results
longitude-latitude coordinates of the province was also examined to
address spatial autocorrelation that may occurs in the model when 3.1. Statistical characteristics of dataset
spatial data are included from distinct areas (Davies et al., 2006; Lee
et al., 2020). Finally, Global Moran’s Index was then estimated to The statistical characteristics of all analyzed variables from 2000 to
identify whether a spatial autocorrelation problem (p-value <0.1) was 2014 were displayed in Table 1. Examining demographic factors, the
found for the residuals of association model (Leung et al., 2019). average province-level population density was 695 (per km2), with the
In the main model, we controlled for all risk factor variables. To test proportion of females (49.72%) not significantly different than the
the strength of the causality model, sensitivity analyses were performed. proportion of males. Assessing the main exposure for 15 years, this study
First, we evaluated the model using different variable settings across the

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A.K. Asri et al. Urban Forestry & Urban Greening 74 (2022) 127667

Table 1 10.23 (SD ± 2.18). Considering the control variables related to health­
Statistical characteristics of all examined variable from 2000 to 2014. care status, 27.5% of the population had proper health insurance. As for
Variable Mean ( ± SD) Min Median Max physical health status, 66.6% of the population had some symptom of
the included diseases. For urban circumstances, the literary rate was
Greenspace exposures
NDVI (IQR = 0.09) 0.69 (0.08) 0.08 0.71 0.80 94.05%, the average poverty rate was 10.40%, the population living in
Forest (%) 45.87 (23.02) 1.24 44.16 91.39 urban areas was 41.28%, the unemployment rate was 6.84%, and the
Meteorological factors divorce rate was 2.96%. In addition, the rate of chronic non-
Temperature (ºC) 27.38 (1.20) 23.20 27.00 30.46 communicable diseases was spatially clustered in the provinces of
Humidity (g/m3) 79.41 (5.59) 54.20 80.80 97.80
Chronic noncommunicable diseases (NCD)
Java Island, illustrated in the distribution map of Fig. S3.
Ischemic Heart Disease 5.57 (2.40) 2.51 4.85 19.01
(IHD)
Diabetes Mellitus (DM) 16.13 (3.34) 9.41 15.61 27.76 3.2. Main association models and sensitivity analyses
Rheumatoid Arthritis (RA) 3.88 (0.28) 3.41 3.84 4.84
Chronic Kidney Disease 10.23 (2.18) 6.63 9.88 17.77
The estimated coefficients and relative risks (RR) of the statistical
(CKD)
Demographic characteristics and urban circumstances association model between greenspace and chronic non-communicable
Population density (per 695.00 (2522.00) 8.00 95.00 15,015.00 diseases were presented in Table 2. After controlling for all risk fac­
km2) tors, the main model revealed that greenspace, represented by both
Sex (% of female) 49.72 (1.17) 46.84 49.65 52.60 NDVI and forest, exhibited a significant negative association with the
Literacy (%) 94.05 (5.37) 66.18 96.07 99.59
Poverty (%) 10.40 (5.93) 0.00 9.53 30.44
four chronic non-communicable diseases. This study identified that
Urbanization (%) 41.28 (19.29) 19.30 36.90 100.00 green NDVI and forest exhibited a significant negative relationship with
Unemployment (%) 6.84 (3.71) 0.00 6.44 17.32 the incidence rate of IHD, as risk ratios were 0.973 (95% CI =
Divorce rate (%) 2.96 (0.75) 1.82 2.91 5.58 0.951–0.996) and 0.964 (95% CI = 0.933–0.996), respectively. A sig­
Smoking (%) 29.48 (2.9) 22.96 29.30 34.12
nificant negative relationship was exhibited between DM-NDVI, and a
Health Insurance (%) 27.51 (13.41) 1.55 27.43 58.03
Population with symptoms 66.56 (9.10) 47.45 65.58 89.89 marginally negative relationship was exhibited for forest-related DM, as
(%) the estimated risk was 0.906 (95% CI = 0.851–0.964) and 0.951 (95%
CI, =0.901–1.004), respectively. Our investigation revealed a significant
negative relationship between greenspace and the incidence rate of RA,
yielded a mean NDVI value of 0.69 (SD ± 0.08) with an interquartile as the risk ratio for NDVI was 0.997 (95% CI = 0.995–0.999) and for
range (difference between Q3 and Q1) of 0.09. For another greenspace, forest was 0.994 (95% CI = 0.990–0.997,). Lastly, a significant negative
the average proportion of forest was 45.87% (SD ± 23.02). Regarding relationship was confirmed for the association between greenspace and
health outcomes, the mean incidence rate for IHD was 5.57 (SD ± 2.40), the rate of CKD, as the risk ratio values were 0.980 (95% CI =
DM was 16.13 (SD ± 3.34), RA was 3.88 (SD ± 0.28), and CKD was 0.964–0.990) and 0.938 (95% CI = 0.909–0.968) for NDVI and forest,

Table 2
Association of green exposure (i.e., NDVI and forest) and chronic non-communicable diseases.
Green Index (NDVI) † Forest
Models Coef. Estimation (95% CI) RR (95% CI) Coef. Estimation (95% CI) RR (95% CI)
Ischemic Heart Disease (IHD)
a
Main Model -0.026 (¡0.049, ¡0.003) * 0.973 (0.951, 0.996) * -0.035 (¡0.068, ¡0.003) * 0.964 (0.933, 0.996) *
Model 1b -0.027 (− 0.051, − 0.019) * 0.974 (0.950, 0.997) * -0.036 (− 0.066, − 0.006) * 0.965 (0.936, 0.994) *
Model 2c -0.027 (− 0.051, − 0.002) * 0.974 (0.950, 0.998) * -0.031 (− 0.061, − 0.001) * 0.969 (0.940, 0.998) *
Model 3d -0.020 (− 0.040, − 0.000) * 0.981 (0.961, 0.999) * -0.026 (− 0.058, − 0.000) * 0.975 (0.943, 0.999) *
Model 4e -0.040 (− 0.078, − 0.002) * 0.960 (0.924, 0.997) * -0.064 (− 0.098, − 0.030) *** 0.937 (0.906, 0.970) ***
Diabetes Mellitus (DM)
a
Main Model -0.098 (¡0.161, ¡0.035) ** 0.906 (0.851, 0.964) ** -0.049 (¡0.103, 0.004)● 0.951 (0.901, 1.004)●
Model 1b -0.083 (− 0.149, − 0.018) ** 0.919 (0.862, 0.982) ** -0.054 (− 0.107, 0.000)● 0.948 (0.899, 1.000)●
Model 2c -0.083 (− 0.148, − 0.018) ** 0.919 (0.861, 0.982) ** -0.051–0.104, 0.002)● 0.950 (0.900, 1.001)●
Model 3d -0.105 (− 0.178, − 0.032) ** 0.900 (0.837, 0.969) ** -0.071 (− 0.157, 0.005)● 0.931 (0.855, 1.005)●
Model 4e -0.085 (− 0.167, − 0.001) * 0.918 (0.845, 0.998) * -0.078 (− 0.157, 0.000)● 0.925 (0.855, 1.000)●
Green Index (NDVI) Forest
Models Coef. Estimation (95% CI) RR (95% CI) Coef. Estimation (95% CI) RR (95% CI)
Rheumatoid arthritis (RA)
a
Main Model -0.002 (¡0.004, ¡0.001) * 0.997 (0.995, 0.999) * -0.006 (¡0.009, ¡0.003) *** 0.994 (0.990, 0.997) ***
Model 1b -0.002 (− 0.004, − 0.000) * 0.998 (0.996, 0.999) * -0.006 (− 0.010, − 0.003) *** 0.994 (0.991, 0.997) ***
Model 2c -0.002 (− 0.004, − 0.000) * 0.998 (0.996, 0.999) * -0.006 (− 0.010, − 0.003) *** 0.993 (0.990, 0.996) ***
Model 3d -0.002 (− 0.004, − 0.000) * 0.998 (0.996, 0.999) * -0.004 (− 0.007, − 0.001) ** 0.996 (0.993, 0.999) **
Model 4e -0.010 (− 0.021, 0.001)● 0.990 (0.979, 1.001)● -0.006 (− 0.012, − 0.001) * 0.993 (0.988, 0.999) *
Chronic Kidney Disease (CKD)
Main Modela -0.020 (¡0.037, ¡0.003) * 0.980 (0.964, 0.990) * -0.063 (¡0.095, -¡0.032) *** 0.938 (0.909, 0.968) ***
Model 1b -0.016 (− 0.033, − 0.001) * 0.984 (0.967, 0.999) * -0.069 (− 0.098, − 0.039) *** 0.934 (0.907, 0.961) ***
Model 2c -0.016 (− 0.033, − 0.001) * 0.984 (0.967, 0.999) * -0.068 (− 0.097, − 0.038) *** 0.935 (0.908, 0.962) ***
Model 3 -0.016 (− 0.035, − 0.000) * 0.984 (0.966, 0.999) * -0.040 (− 0.069, − 0.010) *** 0.961 (0.933, 0.990) ***
Model 4 -0.021 (− 0.046, − 0.000) * 0.978 (0.955, 0.999) * -0.091 (− 0.132, − 0.051) *** 0.913 (0.876, 0.950) ***

CI = Confidence Interval; NDVI = Normalized Difference Vegetation Index; RR = Risk Ratio


† Interquartile of NDVI = 0.09

p-value < 0.1;*p-value < 0.05;** p-value < 0.01; *** p-value < 0.001
a
Controlling for all covariates
b
Adjusting for population, sex, urbanization, divorce, health insurance, temperature, humidity, and spatial-temporal autocorrelation.
c
Adjusting for population, sex, urbanization, divorce, smoking, health insurance, symptoms, temperature, humidity, and spatial-temporal autocorrelation.
d
Adjusting all covariates but excluding data from provinces in Java and Bali Island.
e
Adjusting all covariates but excluding data from provinces categorized as low-urbanization areas.

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respectively. In short, analysis of the statistical relationships between


exposure-outcome established that each interquartile unit increase of
greenspace to NDVI was estimated to reduce the health risks of studied
chronic NCDs by up to 0.3–9.4%. Meanwhile, exposure to green land
cover, which is represented by forest, may reduce the risk of NCDs by up
to 0.6–6.2%. The detail estimated risk ratio of each adjusted variable in
the main model was presented in Fig. 2 and Table S4.
To evaluate the performance of the developed association model, the
sensitivity models with different adjusted risk factors were examined.
From the sensitivity tests, we identified a robust model performance as
indicated by no significant difference in estimated results with the main
model, estimated both for the coefficient and risk ratios. Even after
omitting and/or considering data from high urbanization areas, the as­
sociation model still showed a significant relationship. In addition, the
main association model also deals with spatial autocorrelation problem,
as identified from the results of the Moran’s I test with an insignificant p-
value (p-value > 0.1) (Table S5).

3.3. Relationship of varying greenspace exposure levels to chronic non-


communicable diseases

The linkages between the selected chronic non-communicable dis­


eases and varying levels of greenspace exposure are listed in Table 3.
After considering all control variables, we conclude that, compared to
areas with low levels of greenspace (set as reference), areas with higher
levels of greenspace are significantly negatively associated with the
incidence rate of chronic NCDs. Additionally, there is a significant
negative association with the incidence rate of NCDs in areas with
moderate and high forest exposure, with risk ratios of 0.725 (95% CI =
0.749–0.860) and 0.850 (95% CI = 0.725–0.997), respectively. There
was a marginally significant negative association between green NDVI
and the IHD rate. Regarding the relationship between greenspace
exposure and DM, a significant negative relationship was only found for
high forest exposure, with a risk ratio of 0.757 (95% CI = 0.565–0.999).
For RA, areas with high greenspace exposure had a significant negative
association with the burden of the disease, compared to areas with low
greenspace exposure, with risk ratios of 0.976 (95% CI = 0.955–0.997)
and 0.977 (95% CI = 0.955–0.997) for NDVI and the presence of forest,
respectively. Regarding the effects of greenspace on CKD risk, it was
confirmed that, compared to areas with low greenspace, areas with
moderate and high greenspace for both NDVI and forest had a significant
negative association with CKD, with risk ratios of 0.817 (95% CI =
0.678–0.985) and 0.754 (95% CI = 0.625–0.908), respectively - calcu­
lated for high exposure to greenspace.

3.4. Socioeconomic settings and the relationship between greenspace and


chronic non-communicable diseases

The results of a stratification analysis based on socioeconomic status


in this study indicate the availability of green exposure may have an
effect on chronic diseases and that this effect varies according to so­
cioeconomic conditions (Fig. 3). The results of our stratification analysis
based on the level of urbanization revealed that in areas with high urban
status greenspace, in terms of NDVI and forest (per unit increment) was
estimated to reduce the risk of IHD by 4% and 6.3%, respectively. For
DM, green NDVI had a significant effect in areas with a high level of
urbanization, with a risk reduction of 8.9%, while this effect was only
marginally significant for forest. Additionally, significant negative as­
sociations were found for both green NDVI and forest exposure with RA
and CKD in highly urbanized areas, reducing the risk by 1% and 0.7%,
for RA, and by 2.2% and 8.9%, for CKD (Table S7-a).
A stratified analysis based on economic status with poverty level as
the threshold also was performed. This analysis revealed nearly all Fig. 2. The relative risk of main association model between green exposure and
analyzed chronic non-communicable diseases, (a) IHD, (b) DM, (c) RA, and
greenspace had a beneficial effect on reducing chronic NCDs risk in
(d) CKD.
areas with high indications of poverty. In detail, greenspace has a
significantly negative relationship with IHD in areas with high poverty

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Table 3
Association of greenspace and chronic non-communicable diseases for different levels of green exposure.
Low exposure Moderate exposure High exposure

Coefficient (95% CI) RR (95% CI) Coefficient (95% CI) RR (95% CI)

Ischemic Heart Disease


NDVI Reference -0.150 (− 0.327, 0.026) 0.860 (0.720, 1.027) -0.159 (− 0.331, 0.012)● 0.852 (0.717, 1.012)●
Forest 0.150 (− 0.287, − 0.013)* 0.725 (0.749, 0.860)* -0.162 (− 0.321, − 0.002)* 0.850 (0.725, 0.997)*
Diabetes Mellitus
NDVI Reference -0.264 (− 0.548, 0.018) 0.767 (0.578, 1.018) -0.152 (0.428, 0.123) 0.858 (0.651, 1.131)
Forest -0.139 (− 0.388, 0.109) 0.869 (0.677, 1.116) -0.278 (− 0.570, − 0.000)* 0.757 (0.565, 0.999)*
Rheumatoid Arthritis
NDVI Reference -0.017 (− 0.039, 0.004) 0.982 (0.960, 1.004) -0.024 (− 0.045, − 0.002)* 0.976 (0.955, 0.997)*
Forest -0.018 (− 0.037, 0.000)● 0.981 (0.963, 1.000)● -0.022 (− 0.044, − 0.000)* 0.977 (0.956, 0.999)*
Chronic Kidney Disease
NDVI Reference -0.198 (− 0.389, − 0.007)* 0.819 (0.677, 0.992)* -0.201 (− 0.387, − 0.014)* 0.817 (0.678, 0.985)*
Forest -0.172 (− 0.333, − 0.011)* 0.841 (0.716, 0.988)* -0.282 (− 0.468, − 0.095)** 0.754 (0.625, 0.908)**

CI = Confidence Interval; NDVI = Normalized Difference Vegetation Index; RR = Risk Ratio



p-value < 0.1;*p-value < 0.05;**p-value < 0.01; ***p-value < 0.001
Controlled for all covariates.

rates, with a risk reduction of 4.1% and 7.8% for a unit increment of reported that diabetes mellitus is a chronic comorbid disease that is
NDVI and forest, respectively. There was a negative relationship be­ suffered by many Indonesian people and is experienced by populations
tween green NDVI and DM, and the relationship did not differ between of various backgrounds. Related to the distribution of health outcomes,
low and high poverty areas. In areas categorized as high poverty, NDVI we found a spatial cluster of these four diseases in the provinces of Java
reduced the risk of DM by up to 8.4%, while for low poverty it reached Island. We speculate that this spatial cluster occurred due to the high
9.8%. A beneficial effect of greenspace was yielded in association with incidence rate of diseases in these provinces. In addition, Java Island is a
RA and CKD even in the absence of significant differences between areas densely populated region and is well-known as the center of urbaniza­
of low and high economic status. Results of the analysis indicate NDVI tion in Indonesia (Mardiansjah and Rahayu, 2019). This condition is a
can reduce the risk of RA by 0.3% and forest can reduce the risk of RA by potential possibility that affects this area to have a high case of health
0.7–0.9%. As for CKD, green NDVI and forest can also reduce the risk by burden.
2.6% and 15.2%, respectively, in high poverty areas. Further, there was Ischemic heart disease (IHD), diabetes mellitus (DM), rheumatoid
a marginal association between forest and CKD in low poverty areas arthritis (RA), and chronic kidney disease (CKD) are among the leading
(Table S7-b). cause of mortality in Indonesia (Setyonaluri and Aninditya, 2019;
A stratified analysis based on one factor of education was performed. Indonesian Ministry of Health, 2016). The significant negative associa­
Dividing the analysis by low-high literacy status, there was a significant tion between long-term greenspace exposure (i.e., NDVI and forest) and
negative relationship between green NDVI and IHD in areas of low lit­ the incidence rate of these chronic non-communicable diseases are
eracy, with an estimated reduction in the risk ratio of 3.2%. There was a intriguing findings implying that the existence of greenspace mitigates
beneficial effect of greenspace (i.e., NDVI and forest) on DM in both low the risk of non-communicable diseases to some degree. Extensive
and high literacy areas. In areas with low literacy, there was a significant sensitivity testing with demographic, socioeconomic, and meteorolog­
negative relationship, with a reduced risk of DM of 9% for NDVI and of ical variables left central estimates virtually unchanged. In an additional
7.7% for forest. Meanwhile, in areas with high literacy, the risk reduc­ analysis, we tried to convert the reduced risk of NCDs for each increase
tion was up to 12.6% and 10.7% for NDVI and forest. Further, there was in forest area in Jakarta (the state capital of Indonesia) and found a
a significant negative relationship between greenspace and chronic decrease in NCDs risk of 0.09–0.94% for an increase in 1-km of forest
NCDs in both low and high literacy in relation to a reduced risk of RA area (Table S6). Others have reported similar associations (Asri et al.,
and CKD. The association model assessed that NDVI reduced the risk of 2020; Dalton and Jones, 2020; Levine, 2019; Liang et al., 2021). A recent
RA and CKD in areas of low literacy, a marginally significant effect, and global analysis by Asri et al. (2020) analyzed population data in 183
was significantly associated with a reduced risk in areas of high literacy. countries and reported a significant negative association between
Specifically, the risk reduction was 0.4% for RA and 2.6% for CKD greenspace exposure and disease burden related to IHD, especially in
(Table S7-c and d). Forest was also identified as reducing the risk of RA low-middle income countries. A cross-sectional study in the United
by 0.6% in low literacy areas and 1.2% in high literacy areas. Kingdom reported a similar result, where individuals living in the
greenest areas had a 7% lower risk hazard relative to less green areas of
4. Discussion experiencing cardiovascular disease including IHD (Dalton and Jones,
2020). The significant negative relationship between residential green­
We focused on the impact of greenspace on ischemic heart disease space and CKD prevalence also was confirmed by a study in China (Liang
(IHD), diabetes mellitus (DM), rheumatoid arthritis (RA), and chronic et al., 2021). Lastly, our study confirmed greenspace’s positive impact
kidney disease (CKD) because these four chronic non-communicable on RA prevalence, which has been reported in previous study by Levine
diseases have been identified as the leading causes of mortality in and colleagues (2019).
Indonesia (Setyonaluri and Aninditya, 2019; Indonesian Ministry of Our primary findings still could have a significant negative associa­
Health, 2016). Together, these four NCDs contribute to 20.6% of the tion even taking into account various risk factors. It has been argued that
global mortality (Roth et al., 2018). Providing further justification for access to greenspaces encourages physical activity, which could reduce
selecting these diseases, a report by the World Health Organization the risk of IHD, DM, RA, and CKD (Richardson et al., 2013; Swärdh et al.,
(2019) noted cardiovascular disease in terms of ischemic heart disease 2021; Wang et al., 2019). In detail, how exposure to greenspace could be
was the leading cause of mortality globally, followed by diabetes mel­ associated with a reduced risk of physical diseases was also explained in
litus, which is a comorbidity. Examining the health outcomes of the four a theoretical study by Markevych and colleagues (2017). In this case,
chronic diseases analyzed, we identified diabetes mellitus as the disease our findings meet a pathway where greenspace could reduce harm such
with the highest incidence rate in Indonesia. This result was confirmed as decreasing air pollution concentration, heat, and noise, which are the
by the Indonesian Ministry of Health Information Center (2014), which risk factors for chronic disease (Al-Kindi et al., 2020; Dehghan et al.,

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A.K. Asri et al. Urban Forestry & Urban Greening 74 (2022) 127667

2017; Yang et al., 2018). In addition, green space as building capacities


can encourage people to have better physical movement and facilitate
social interaction. Then, for the question of how greenspace exposure
could be related to reducing the risk of chronic non-communicable
diseases in Indonesia, this study emphasizes the existence of green na­
ture serves a potential role in the community’s attempt to fulfill its daily
needs. Indonesia is an interesting case since around 33.4 million people
work as farmers (The Indonesian Central Bureau of Statistics, 2018) and
60.0 million people depend on forest resources (World Resources Insti­
tute, 2018). These occupations utilize greenspaces and require strenuous
physical activities. To the extent that our greenspace indicators include
forest and agricultural land, it could be a proxy for access to
high-nutrient foods which will reduce NCDs rates.
Since the presence of greenspace varies in each area, a multilevel
analysis by considering greenspace levels was assessed. We identified a
significant negative relationship between non-communicable diseases
and greenspace in high-exposure areas, although it was dependent
across vegetation types. Referring to IHD, our findings were corrobo­
rated by Wang and colleagues’ study (2019) which showed that the
highest greenspace was correlated with a 20% decreasing IHD risk
(Wang et al., 2019). This beneficial impact also prevailed to diabetes
mellitus, rheumatoid arthritis, and chronic kidney diseases, where
greater exposure to greenspace was linked with a lower case of type 2
diabetes mellitus, chronic kidney disease, and autoimmune associated
with chronic inflammatory diseases (Park et al., 2021; Tsai et al., 2021;
Von Hertzen et al., 2015). Interestingly, the potential role of forest
presence at both moderate and high exposure areas in reducing the risk
of chronic NCDs was also highlighted. A report by the FAO (2020)
confirmed that forests contribute to the health of people living nearby. It
was explained that forest offer edible products or foods that redound
macro and micronutrients to a healthy diet and contribute to dietary
diversity, which increases the gut microbiome diversity for better
health. A Japanese study also identified an NCD-associated blood
pressure-lowering effect of experiencing the forest atmosphere or forest
bathing (Ideno et al., 2017).
Recognizing that living in cities has been associated with increased
risk of health burdens especially chronic non-communicable diseases for
a variety of complex reasons (Angkurawaranon et al., 2014), we inves­
tigated in the relationship of greenspace to NCD across several strata of
urbanization. Greenspace either by NDVI or forest measures still had a
significant negative association with all four chronic non-communicable
diseases. This finding aligns with a previous investigation which
concluded that in areas with high urbanization greenspace was closely
associated with a reduced risk of ischemic heart disease, diabetes mel­
litus, rheumatoid arthritis, and chronic kidney disease (James et al.,
2016; Khan et al., 2021; Wang et al., 2019). Greenspace in cities could
promote more physical activity as suggested by Pradipta (2020).
Further, we also found a beneficial effect of greenspace in low-urban
areas for diabetes mellitus and rheumatoid arthritis, although margin­
ally significant. However, given higher population densities it is even
more important to have access greenspaces in cities.
Next, we assessed the relationship of greenspace and NCDs based on
economic status as represented by the poverty rate. Corroborating pre­
vious findings (Asri et al., 2020; Labib et al., 2020), we identified that an
increase in the green index is associated with a decreased risk of NCDs in
areas falling in the high poverty category. We also identified a reduction
in the risk of several physical health diseases in low-poverty areas,
although not as large as areas with high poverty levels. Furthermore, the
livelihoods of Indonesians living in low-middle income areas tend to
depend on the existence of natural resources, such as forest and other
green lands, and this could serve additional benefits through them
having continuous interactions with nature to satisfy their basic needs
Fig. 3. Stratified analyses by socioeconomic factors, (a) ischemic heart disease, (Njurumana and Octavia, 2020; World Resources Institute, 2018). In
(b) diabetes mellitus, (c) rheumatoid arthritis, and (d) chronic kidney disease.
addition, it is known that areas with high exposure to greenspace are
mostly rural areas with high poverty rates, thus, the presence of sus­
tainable greenspace may provide free health care in supporting the

7
A.K. Asri et al. Urban Forestry & Urban Greening 74 (2022) 127667

quality of life of the population (Purnamasari, 2018). Funding


Lastly, we examined the education factor in a multilevel analysis. For
ischemic heart disease, there was a significant negative relationship This study was funded by the Ministry of Science and Technology, R.
with the green index in areas classified as low literacy. This result is O.C. (MOST 110- 2628-M-006 -001 -MY3).
plausible positing that a low level of education likely will coincide with a
lower economic and healthcare status, so the risk of IHD and its CRediT authorship contribution statement
comorbidities will be high as has been suggested in previous studies
(Kelli et al., 2019; Oshio and Kan, 2019). As for diabetes mellitus, Aji Kusumaning Asri, Chih-Da Wu, John D. Spengler: Conceptu­
rheumatoid arthritis, and chronic kidney diseases, there were not any alization. Aji Kusumaning Asri, Chih-Da Wu: Methodology. Aji
significant differences in the effects of greenspace at the two levels of Kusumaning Asri, Chih-Da Wu: Formal analysis. Aji Kusumaning
literacy. In this regard, our results suggest a significant beneficial effect Asri, Hsiao-Yun Lee: Writing – original draft. Aji Kusumaning Asri,
of greenspace in reducing NCDs risk in areas with low and high literacy. Hsiao-Yun Lee, Chih-Da Wu, John D. Spengler: Writing – review &
We had predicted the percentage reduction effect in risk would be editing. Chih-Da Wu, John D. Spengler: Supervision. Chih-Da Wu:
greater in areas with a high literacy rate than in areas with a low literacy Funding acquisition.
rate, since this result was yielded in Maas’s study (2006). A possible
reason for their finding is that the high incidence rate of chronic NCDs Declaration of Competing Interest
among educated people may influence the greater beneficial effect of
greenspace on risk reduction. Lifestyle-related behaviors of educated The authors declare that they have no known competing financial
people likely have affected the development of NCDs risk, with increases interests or personal relationships that could have appeared to influence
in body weight from an overindulgent diet and increases in sedentary the work reported in this paper.
behavior resulting from less physical activity at work (Deforche et al.,
2015; Olatona et al., 2018). Acknowledgments
We acknowledge the limitations of this study. The main drawback is
in the application of the study design which was only a population scale This study was funded by the Ministry of Science and Technology, R.
analysis. Second, evaluating population-level data, this study does not O.C (Taiwan). This study was supported by the Institute for Health
have individual-level health data information that may improve the Metrics and Evaluation (IHME), who provided the health database; the
causality effect. But, in the case that this study has never been conducted National Aeronautics and Space Administration (NASA), which pro­
for Indonesia, the results of this study can be used as a reference for a vided global greenspace - NDVI data; the Geospatial Information Agency
more complete follow-up study. Third, many of the considered risk of Indonesia, which provided the green land-cover datasets; the Central
factors were related to socioeconomic and urban circumstances, so Bureau of Statistics, which provided demographic data and pertinent
variables remain that have not been considered, such as genetic factors, risk factor databases; and the Indonesian Ministry of Health, which
comorbidities, family history, and other variables that are risk factors for provided health status databases at a province-level.
each selected NCD with consistent period of datasets. Hence, other risk
factors that have not been examined should be the focus for develop­ Appendix A. Supporting information
ment in future studies. Fourth, due to the lack of data, the scope of this
study is only at the provincial level, we suggest that further studies Supplementary data associated with this article can be found in the
consider data on a better scale accuracy, such as the city or township online version at doi:10.1016/j.ufug.2022.127667.
level. Fifth, we have not considered the spatial scale in analyzing the
relationship between greenspace and health outcomes. In this case, References
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