Literature DB >> 33075086

Prevalence of metabolic syndrome among adult population in India: A systematic review and meta-analysis.

Yuvaraj Krishnamoorthy1, Sathish Rajaa1, Sharan Murali1, Tanveer Rehman1, Jayaprakash Sahoo2, Sitanshu Sekhar Kar1.   

Abstract

OBJECTIVE: This review was done to determine the prevalence of metabolic syndrome (MS) among adult general population in India. We also wanted to find the gender, setting, and region-wide distribution of MS in India.
METHODS: We conducted systematic searches in various databases including Medline, ScienceDirect, Cochrane library and Google Scholar from inception until August 2019. We included studies conducted in India reporting the prevalence of MS among adults aged 18 years or more. We used the Newcastle Ottawa scale to assess the quality of included studies. We carried out a meta-analysis with random-effects model and reported pooled prevalence with 95% confidence intervals (CIs). We used the Funnel plot to assess publication biases.
RESULTS: In total, we analysed 113 data from 111 studies with 133,926 participants. Majority of the included studies (76 out of 111) had low risk of bias. We found significant heterogeneity among the included studies (p<0.001). We also found a symmetrical funnel plot indicating an absence of publication bias. The prevalence of MS among adult population in India was 30% (95%CI: 28%-33%). There was a steady increase in the burden across the age groups from 13% (18-29 years group) to 50% (50-59 years). We also found that people living in urban areas (32%; 95%CI: 29%-36%) had higher prevalence when compared to tribal (28%; 95%CI: 21%-36%) or rural adults (22%; 95%CI: 20%-25%). Gender distribution of MS showed that the females had higher prevalence (35%; 95%CI: 31%-38%) when compared to males 26% (95%CI: 22%-29%).
CONCLUSION: Almost one in three adults in India suffer from MS. Females, people living in urban areas and in northeast region had higher prevalence of MS. Development and implementation of policies and protocols for the screening of MS would enable us in early diagnosis and treatment with special focus towards the vulnerable and high-risk groups.

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Mesh:

Year:  2020        PMID: 33075086      PMCID: PMC7571716          DOI: 10.1371/journal.pone.0240971

Source DB:  PubMed          Journal:  PLoS One        ISSN: 1932-6203            Impact factor:   3.240


Introduction

Disease patterns around the globe are undergoing rapid structural changes over the last three decades, with a sudden increase in the burden of Non-Communicable Diseases (NCDs) and a decreasing trend of communicable diseases [1]. The Global Burden of Disease (GBD) study, brings to light this phenomenon of epidemiological transition in India, with a 62.7% of the total mortality in 2016 contributed by the NCDs. Key elements contributing to the development of these NCDs have been identified and are studied together under the heading of Metabolic Syndrome (MS) [2]. Metabolic syndrome is a constellation of interconnected physiological, biochemical, clinical and metabolic factors that directly increases the risk of cardiovascular diseases, type 2 diabetes mellitus (DM) and all-cause mortality. It is constituted by abdominal obesity, insulin resistance, hypertension, and hyperlipidemia [3]. Various diagnostic criteria have been proposed for quantifying MS. But the most widely used ones are from the International Diabetic Federation (IDF) and the National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) [4, 5]. Metabolic syndrome increases the risk of developing type 2 DM and cardiovascular diseases over the next 5 to 10 years by five and two-fold respectively [3]. Furthermore the patients with MS have, an average four-fold increased risk of developing stroke & myocardial infarction and a two-fold risk of dying from a similar event compared with those without MS, regardless of previous history of cardiovascular events [6]. Identifying the individuals with (or) at risk of developing MS would help to inform the probabilities of worse outcomes and thus an urgent need for a promotive, preventive or curative action. A recent study from the United States reported the prevalence of MS to be around 22.9% [7]. Various population-based studies were conducted in India too, to quantify the same and the results ranged from 10 to 30 percentage [8]. A study conducted in the eleven large urban cities of India during 2006–2010 reported the prevalence of MS as high as 35% [9]. Owing to the behavioural habits, urban population, seem to be the most vulnerable group for developing MS [10]. Prevalence of MS, thus, seems to vary greatly from region to region and from ethnicity to ethnicity. Even though evidences are being generated on MS from different parts of the country, there is no nationwide pooled estimate to comment on the burden of MS in the Indian subcontinent, which could drive policy action [11]. With almost one third of the total population living in the urban areas, and with 40% of the population aged between 30 and 70 years, understanding the overall prevalence of MS in India becomes essential for predicting the future burden of type 2 DM and cardiovascular diseases [12]. While the NCD care in the country is segregated under the broad headings of Diabetes, and Cardiovascular diseases, MS informs us the need to look at the picture as a whole. Results from this study would, thus, help guide national policy making process to give due importance to prevention and treatment of MS in the community and clinical settings. This could thus be an essential key to keep a check on the ever-increasing burden of the NCD epidemic in the country. Hence, this review was conducted to generate a pooled prevalence estimate for MS in India.

Methods

Design and registration

We conducted a systematic review and meta-analysis of cross-sectional studies. We have obtained approval from the JIPMER Scientific Advisory Committee (JSAC). We have also obtained exemption from Institutional Ethics Committee (IEC). We have registered our protocol on the international prospective register of systematic review (PROSPERO). PROSPERO Registration Number is CRD42019147277. We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist for reporting systematic reviews incorporating meta-analyses for reporting our review.

Eligibility criteria

Type of studies

We included studies conducted in India reporting the prevalence of MS for the current review. There was no restriction related to study design, communities (rural/urban) or age groups. We included the studies irrespective of the setting in which the study was conducted (community or facility based or workplace based). Studies reported as full text were included while unpublished data were excluded from the review.

Type of participants

We included studies conducted among adults aged 18 years or more. We excluded the studies conducted among specific diseased population.

Type of outcome measure

Studies reporting the prevalence of MS and diagnosed it as per the NCEP ATP III or IDF guidelines were included to obtain the pooled prevalence estimate for MS in India.

Search strategy

We conducted extensive electronic search in the following databases: Medline, ScienceDirect, Cochrane library and Google Scholar. Combination of medical subject heading (MeSH) and free text terms were used for carrying out literature search. The detailed search strategy used to search the Medline database has been reported in . Similar strategies were used in Cochrane Library, ScienceDirect and Google scholar for literature search of published studies. Search was conducted in all the databases from inception of the database to August 2019 with English language restriction for publication. We also checked the reference list of primary studies obtained through electronic search and relevant articles were included in the review and analysis.

Selection of studies

Two independent investigators (YK and TR) independently performed the literature search and screened the title, abstract and keywords of all the studies identified for possible inclusion in the review. Full text article was obtained for those studies that are found to be relevant. Further screening of abstract and full text of the retrieved articles was done independently by two investigators (YK and TR) to select the studies which satisfy the eligibility criteria of the current review. Any disagreements during the entire selection process between two authors were resolved either through consensus or consultation with third investigator (SR). Quality of the overall review process was monitored by the third investigator (SR).

Data extraction and management

Primary investigator (YK) extracted the relevant study characteristics for the review from the included studies using the Cochrane Public Health group Data extraction and Assessment Template. Following data were extracted:

General information

Author, Study title, Publication year.

Methods section

Study design, study period, study setting (community/workplace/facility), community (urban/rural/tribal), geographical region, state, sample size, sampling technique, diagnostic criteria, outcome assessment and statistical tests employed.

Outcome section

Mean age, non-response rate and their characteristics, prevalence of MS. Primary investigator (YK) transferred the obtained data into the software STATA version 14. Data entry was double checked for correct entry by another investigator (SR) through comparison of data presented in review and included study reports.

Risk of bias assessment in included studies

Two independent authors (SR and SM) assessed the quality of all the included studies using the Newcastle-Ottawa (NO) scale adapted for cross sectional studies [13]. Two criteria (selection and outcome) were used to assess the risk of bias. Following domains were used for assessing the risk of bias under selection criteria: representativeness of the sample, justification of sample size, rate of non-respondents and their characteristics and use of validated measurement tool. Under Outcome criteria, outcome assessment and statistical test employed were used to assess the risk of bias. Each of these outcomes was rated as high (1 point) or low (0 points) based on the quality of evidence and availability of information. Studies scoring more than or equal to 3 points were considered to have high risk of bias.

Statistical analysis

Meta-analysis was performed with the selected studies using STATA 14.2 (StataCorp, College Station, TX, USA). For each of the studies, standard error was calculated using the reported prevalence of MS and total sample size. “Metaprop” function was used for performing analysis of the current review [14]. To minimize the effect of extremely small or large prevalence on the overall estimate, Freeman Tukey double arc-sine transformation was done to stabilise the variance [14]. Final pooling of data was done with random effects model and reported as proportion with 95% confidence interval. Evidence of between-study variance due to heterogeneity was assessed through following methods: Chi square test for heterogeneity and I2 statistics to quantify the inconsistency. I2 less than 25% was mild, 25–75% was moderate and more than 75% was considered as substantial heterogeneity [15]. Sub-group analysis was performed based on age group, gender, geographical region (North/South/West/East/Northeast/Central), study setting (community/workplace/facility), diagnostic criteria, waist circumference measurement, year of publication, quality of studies, representativeness of the sample and urban/rural/tribal communities. Potential covariates for meta-regression were study setting, region, diagnostic criteria, representativeness of the sample, year of publication, mean age and quality of evidence. We performed multivariable meta-regression analysis by including the study level factors with p value less than 0.2 in the univariate model. We performed sensitivity analysis to assess the robustness of the results by excluding the studies conducted exclusively on elderly (≥60 years), studies having high risk of bias or not conducted on a representative sample, and studies conducted before 2007. Study specific prevalence estimates and pooled estimates were graphically represented through forest plot for both combined and subgroup analysis. Publication bias was assessed and graphically represented by funnel plot; asymmetry of the plot was tested using Egger’s test and p value less than 0.10 was considered as statistically significant publication bias [16].

Results

Study selection

We conducted a systematic search to find studies that report the prevalence of MS from the dates of database inception until August 2019. During the first stage of screening (title, abstract and keywords), we retrieved 310 studies from the following databases: Medline, ScienceDirect, Cochrane library and Google Scholar. After removal of duplicates, we reviewed 249 articles’ full texts against our eligibility criteria for the possible inclusion in the review. We reviewed the bibliographies of the retrieved articles and found four more relevant studies. Finally, we analysed 111 studies with 133,926 participants satisfying the inclusion criteria () [17-127].

Characteristics of the included studies

lists the characteristics of the studies analysed. Most of the studies (46) were conducted in Southern states like Andhra Pradesh, Karnataka, Kerala and Tamil Nadu. The mean age of study participants ranged from 19.6 to 69.4 years. Coming to the study setting, 83 were from community-based studies followed by 21 from facility-based studies and 9 from workplace-based studies. The sample sizes in the studies varied from 60 to 9,886. Majority of the studies (49 out of 111) have reported separate estimates for urban region, while 34 studies reported for rural and 4 studies for tribal region. Rest of the studies did not provide separate estimates for urban, rural or tribal regions because of the study setting (facility or workplace-based studies). Majority (82 out of 111) studies have reported estimates for female burden of MS while 76 studies have reported estimates for male adult population. NCEP ATP III–National Cholesterol Education Program Adult Treatment Panel III. IDF–International Diabetes Federation. NA–Not applicable.

Methodological quality of the included studies

We performed assessments of risk of bias for all the included studies using NO scale. First, selection bias domains were assessed and it was found that 64 out of 111 studies (58% of studies) had high risk of bias related to representativeness of the sample for our review, 80 (72%) studies did not report proper justification for sample size, 69 (62%) studies did not report non-response rate or their characteristics. All the studies reported use of validated measurement tool. Under the outcome domain, only one study did not independently assess the outcome; nine studies did not report the statistical methods used in the study. Almost one-third i.e. 35 (31.5%) of the included studies had high risk of bias as per NO scale.

Burden of metabolic syndrome in India

Pooled estimate was calculated after adjusting for population size weights and graphically depicted in . The overall pooled prevalence of MS among adult population in India was 30% (95%CI: 28%-33%). State wise analysis of MS showed that the maximum prevalence of MS was reported in Madhya Pradesh (50%) followed by New Delhi (43%), Odisha (43%) and Telangana (42%). Least pooled prevalence of MS was found in Jammu & Kashmir (15%) followed by Haryana (18%) and Punjab (21%). There was a significant heterogeneity found among the studies included in our review (I2 = 99.1%; p<0.001). Additional subgroup analysis was performed to explore the source of heterogeneity and obtain separate estimates based on age group, gender, study setting, geographical area and regions, year of publication, representativeness of sample, waist circumference measurement, quality of studies and diagnostic criteria (.

Age wise distribution of metabolic syndrome in India

The pooled prevalence of MS differed significantly across the age groups (p<0.001). There was a steady increase in the burden across the age groups from 13% (18–29 years group) to 50% (50–59 years). There was significant heterogeneity among the studies reporting prevalence across all the age groups with I2>90% and p<0.001.

Gender distribution of metabolic syndrome in India

In total, 82 studies have reported prevalence of MS among female adult population while 76 studies have reported for males. The pooled prevalence of MS among adult females in India was 35% (95%CI: 31%-38%); while for males, the pooled prevalence was 26% (95%CI: 22%-29%). There was significant heterogeneity among the studies reporting prevalence in females and males (I2 = 98%, p<0.001).

Urban vs rural vs tribal

Overall, 49 studies have reported separate estimates for urban region, 34 for rural and 4 for tribal region. The pooled prevalence of MS among adult urban population in India was 32% (95%CI: 29%-36%); while in rural population, the pooled prevalence was 22% (95%CI: 20%-25%) and in tribal population, it was 28% (95%CI: 21%-36%). Significant heterogeneity was found among the studies reporting prevalence across urban, rural and tribal regions (p<0.001).

Study setting (community vs facility vs workplace)

Subgroup analysis based on study setting showed that the facility-based studies showed higher prevalence (38%; 95%CI: 30%-47%) followed by community based (29%; 95%CI: 26%-32%) and workplace-based studies (28% 95%CI: 22%-35%). However, this difference was not statistically significant (p = 0.08). There was significant heterogeneity among the studies reporting prevalence of MS irrespective of the study setting (p<0.001).

Geographical regions

North India. In total, 31 studies reporting the burden of MS were from Northern region. The pooled prevalence of MS in North India was 30% (95%CI: 25%-35%). There was a significant heterogeneity found among the studies conducted in North India (I2 = 99.2%; p<0.001). Among the 31 studies, 15 reported separate estimates for urban and 10 for rural regions. Prevalence of MS in urban North India was 35% (95%CI: 27%-44%; I2 = 99.3%; p<0.001) while for rural North India, the pooled prevalence was 21% (95%CI: 15%-27%; I2 = 97.4%, p<0.001). We also checked for gender wise distribution of MS in North India. The prevalence of MS among adult females in North India was 33% (95%CI: 26%-40%; I2 = 98.9%, p<0.001); while for adult male population, it was 26% (95%CI: 20%-34%; I2 = 99%, p<0.001) (. Central India. Ten studies have reported prevalence of MS in Central India. The pooled estimate for prevalence of MS in Central India was 27% (95%CI: 17%-39%; I2 = 98.4%, p<0.001). Only one study was conducted in urban community of Central India. It reported a prevalence of 25% with 95%CI: 18%-33%. Three studies were conducted in the rural community of Central India, with which we found a pooled prevalence of 14% with 95%CI: 9%-20%. Gender wise distribution showed that the prevalence of MS was higher among adult females in Central India (30%; 95%CI: 17%-46%; I2 = 97.3%, p<0.001) when compared to males (21%; 95%CI: 12%-33%; I2 = 97.2%, p<0.001) ( Western India. In total, 7 studies from Western India were included in our review. The pooled prevalence of MS in Western India was 30% (95%CI: 19%-44%; I2 = 99%, p<0.001). There was a significant urban-rural difference in the prevalence of MS in Western India. The prevalence of MS in urban Western India was 37% (95%CI: 21%-55%, I2 = 98.1%, p<0.001); while in rural Western India, it was 13% (95%CI: 12%-15%). Gender wise distribution of MS showed that the prevalence was higher among females (32%; 95%CI: 15%-51%; I2 = 98.3%, p<0.001) when compared to males (25%; 95%CI: 14%-35%; I2 = 95%, p<0.001) (. Eastern India. Eleven studies have reported the prevalence of MS in Eastern India. The pooled prevalence of MS in Eastern India was 33% (95%CI: 23%-43%; I2 = 99.1%, p<0.001). The prevalence was higher among urban Eastern India (38%; 95%CI: 31%-45%; I2 = 90.3%, p<0.001) when compared to rural Eastern India (29%; 95%CI: 18%-40%; I2 = 98.5%, p<0.001). Gender distribution of MS showed that the burden was higher among the females (39%; 95%CI: 27%-53%; I2 = 98.8%, p<0.001) when compared to males (23%; 95%CI: 12%-36%, I2 = 98.5%, p<0.001) (. Southern India. In total, 46 studies reporting the burden of MS were from Southern region. The pooled prevalence of MS in South India was 30% (95%CI: 26%-33%). There was a significant heterogeneity found among the studies conducted in South India (I2 = 98.6%; p<0.001). Prevalence of MS in urban South India was 30% (95%CI: 25%-34%; I2 = 98.1%; p<0.001) while for rural South India, the pooled prevalence was 25% (95%CI: 20%-30%; I2 = 97.9%, p<0.001). Gender wise prevalence of MS in South India was also checked. The prevalence of MS among adult females in South India was 34% (95%CI: 28%-40%; I2 = 98.1%, p<0.001); while for adult male population, it was 26% (95%CI: 21%-31%; I2 = 97.9%, p<0.001) (. Northeast India. Only 4 studies were conducted in Northeast India to determine the prevalence of MS. The pooled prevalence of MS in Northeast India was 35% (95%CI: 25%-46%). There was a significant heterogeneity found among the studies conducted in South India (I2 = 96.9%; p<0.001) (. There was no sufficient number of studies to see the urban-rural and gender-based differences in the burden of MS.

Additional subgroup analysis and sensitivity analysis

Subgroup analysis based on diagnostic criteria revealed a statistically significant difference in the pooled estimate between NCEP ATP-III and IDF criteria (29% vs 34%; p = 0.05). However, we did not see any statistically significant difference in the burden of MS based on year of publication, difference in measurement of waist circumference, quality of studies or representativeness of sample. We performed sensitivity analysis by excluding the studies conducted exclusively on elderly (≥60 years), studies having high risk of bias or not conducted on a representative sample, and studies conducted before 2007. This is to provide robust and latest estimate on the burden of MS among adult population in India. In total, 47 out of the 111 studies satisfied these criteria and included in the sensitivity analysis. The pooled prevalence of MS obtained in sensitivity analysis was still almost similar to the overall findings (29%; 95%CI: 25%-33%) indicating that the estimate is robust to the changes in age group, year, and quality of studies.

Meta-regression

First, we conducted univariate meta-regression with individual study level factors such as study setting, geographical region, diagnostic criteria, year of publication, mean age, representativeness of the sample and quality of studies (. We found significant association with mean age and study setting. However, we performed multivariable meta-regression with factors having p value less than 0.2 such as study setting, mean age, and diagnostic criteria used. The adjusted model was able to explain 24.5% of the between-study variability and the model was statistically significant (p = 0.004).

Publication bias

Egger’s test was performed for the assessment of publication bias. There were no small study effects with non-significant coefficient value (Co-efficient: 0.78; 95%CI: -0.95 to 2.52; p = 0.372) which shows lack of evidence of publication bias. Graphical representation of the test of publication bias was depicted through funnel plot in . Funnel plot also showed symmetric plot indicating the absence of publication bias.

Discussion

We have conducted this review to obtain a comprehensive estimate of burden of MS among adult population in India. We have also captured the gender distribution, urban-rural-tribal differences and geographical region wise estimates to find any significant difference in the estimates of MS. In total, we analysed data from 111 studies with 133,926 participants. Majority of the studies were conducted in Southern states followed by Northern states. Majority (83) were from community-based studies. Out of these, 49 have reported separate estimates for urban region, 34 for rural and 4 for tribal region. Majority of the included studies (76 out of 111) had low risk of bias. The prevalence of MS among adult population in India was 30% (95%CI: 28%-33%). Similar reviews published from other low middle income countries in Middle East, South East Asia and Latin American region also reported that almost one third of general population have MS [128-130]. This recent upsurge in the prevalence of MS among low middle income countries including India might be directly linked with rapid economic development and urbanization in the country. This rapid industrialization can influence drastic changes in lifestyle patterns and nutrition [131-133]. We also found that people living in urban areas (32%; 95%CI: 29%-36%) were found to have higher prevalence of MS when compared to people living in tribal (28%; 95%CI: 21%-36%) or rural areas (22%; 95%CI: 20%-25%). These findings were in line with the studies conducted in neighbouring low middle-income countries [129]. Unhealthy lifestyles, better socio-economic status, decreased physical activity, stress, excessive salt and red meat consumption might be the contributory factors influencing the higher prevalence of MS in urban areas [134]. Age wise distribution showed that there is a steady rise in the burden of MS with increase in age groups and it differed significantly (p<0.001). Gender distribution of MS showed that the females had higher prevalence (35%; 95%CI: 31%-38%) when compared to males 26% (95%CI: 22%-29%). Similar reviews in Eastern Mediterranean [135], South East Asian [136], and Western pacific [137] regions abide by our findings. Major reason for this finding could be the gender specific risk factors such as menopause, polycystic ovarian syndrome and use of hormonal contraceptives among women [138]. Other probable reasons could be the excess risk women carries in terms of elevated body weight, increased waist girth, and low high density lipoprotein cholesterol when compared to men [139-142]. Highest prevalence of MS was reported in Madhya Pradesh (50%) followed by New Delhi (43%), Orissa (43%) and Telangana (42%). Stratified analysis across the geographical regions showed that people living in Northeast India (35%) have highest prevalence of MS followed by Eastern India (33%), regions with unique lifestyle and culture [142]. This highlights the need of understanding the influence of sociocultural, ethno-geographical factors in determining the risk of MS. This high prevalence among the north eastern states could also be due to lesser number of studies (n = 4) from the region. Hence, the current review may not be representative of the entire north eastern population. Further studies should be carried out in this region to have conclusive evidence on the burden of MS. The major strength of the study is that we have tried to provide the first comprehensive review on burden of MS among adult general population in India. We also provided estimates based on gender, study setting, community and geographical regions. Test for publication bias have found that there was no significant bias in the current review. However, our review has certain limitations. Summarizing and concluding the burden of MS as 30% among adults in India with demographic and socio-economic differences is difficult because of the inherent heterogeneity. We have tried to overcome this limitation by conducting subgroup analysis based on study setting, geographical regions and provided individual prevalence estimates. The chi square test for heterogeneity also revealed significant variability across the national and region wise included studies. Hence, we tried to explain the between-study variability using meta-regression and found the potential sources of heterogeneity. In spite of these limitations, current review provides important baseline information on the burden of MS among adult population in India. Our review has showed a higher prevalence among women, people living in urban areas and in specific geographical pockets. The findings of our review highlight that MS is a major public health problem in India. It is necessary for the government to allocate adequate resources and establish appropriate cost-effective interventions to tackle the burden of MS. Development and implementation of policies and protocols for the screening (focusing on population level screening strategies) would enable us in early diagnosis and treatment. Special focus should be given towards the vulnerable and high-risk groups. A wholesome comprehensive health care approach encompassing various levels of health care is necessary to achieve better management of MS. This crucial step would not only enable us to reduce the mortality imposed by its individual components but also to curtail the out-of-pocket expenditure incurred by these conditions. Further comprehensive meta-analysis on population-based studies is necessary to find the factors responsible for MS which will help the policy makers, especially in the low and low middle-income regions to devise region specific interventions.

PRISMA 2009 checklist.

(DOC) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in North India a) North India–Male b) North India–Female c) North India–Urban d) North India–Rural. (TIFF) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in Central India a) Central India–Male b) Central India–Female c) Central India–Rural. (TIFF) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in Western India a) Western India–Male b) Western India–Female c) Western India–Urban d) Western India–Rural. (TIFF) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in Eastern India a) Eastern India–Male b) Eastern India–Female c) Eastern India–Urban d) Eastern India–Rural. (TIFF) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in South India a) South India–Male b) South India–Female c) South India–Urban d) South India–Rural. (TIFF) Click here for additional data file. Forest plot showing the setting wise and gender wise distribution of metabolic syndrome in Northeast India a) Northeast India–Male b) Northeast India–Female. (TIFF) Click here for additional data file.

Search strategy.

(PDF) Click here for additional data file. (DTA) Click here for additional data file.
Table 1

Characteristics of the studies included (N = 111).

S.N.Author and yearStateGeographical RegionSettingUrban/Rural/TribalAge group (years)GenderSample sizeDiagnostic criteriaPrevalence (95%CI)
1.Bal 2011ChandigarhNorthFacilityNA25–50Males & Females440NCEP ATP -III37% (32%-42%)
2.Bandella 2017Andhra PradeshSouthCommunityUrban, rural and tribal20–60Males & Females1032NCEP ATP -III32% (29%-35%)
3.Bansal 2009New DelhiNorthFacilityNA≥18Males & Females1905NCEP ATP -III48% (45%-50%)
4.Bansal 2017Uttar PradeshCentralFacilityNA30–70Males & Females350NCEP ATP -III17% (13%-21%)
5.Bansal A 2015New DelhiNorthCommunityUrban35–65Males & Females406NCEP ATP -III75% (71%-79%)
6.Barik A 2017West BengalEastCommunityRural≥18Males & Females9886NCEP ATP -III16% (15%-17%)
7.Basha 2018Andhra PradeshSouthCommunityUrban≥18Males & Females802NCEP ATP -III32% (29%-35%)
8.Bhagat 2017ChandigarhNorthCommunityUrban18–25Males & Females611IDF18% (15%-22%)
9.Bhat R 2010Jammu & KashmirNorthFacilityNA≥18Males & Females500NCEP ATP -III9% (6%-11%)
10.Bhattacharya 2016TelanganaSouthFacilityNA≥60Males & Females114NCEP ATP -III42% (33%-52%)
11.Bhutia 2017SikkimNortheastFacilityNA≥20Males & Females361IDF34% (29%-39%)
12.Chakraborty 2015West BengalEastCommunityUrban≥18Males & Females690NCEP ATP -III33% (29%-36%)
13.Chhabra 2014Not mentionedNorthCommunityUrban & Rural25–60Females200NCEP ATP -III33% (27%-40%)
14.Chinawale 2018GujaratWestCommunityNot mentioned20–80Males & Females473IDF41% (37%-46%)
15.Chow 2007Andhra PradeshSouthCommunityRural≥30Males & Females4535NCEP ATP -III25% (23%-26%)
16.Das 2011West BengalEastCommunityUrban & Rural≥30Males & Females350NCEP ATP -III48% (43%-54%)
17.Das 2017West BengalEastCommunityNot mentioned18–24Males & Females397IDF5% (3%-7%)
18.Das M 2011West BengalEastCommunityUrban & Rural≥30Males & Females448NCEP ATP -III29% (25%-34%)
19.Deedwania 201411 cities in IndiaIndiaCommunityUrban≥20Males & Females6198NCEP ATP -III36% (35%-37%)
20.Deepa M 2006Tamil NaduSouthCommunityUrban≥20Males & Females2350NCEP ATP -III18% (17%-20%)
21.Deshmukh 2012MaharashtraCentralCommunityRural≥18Males & Females300NCEP ATP -III17% (13%-22%)
22.Dhabriya 2015RajasthanNorthCommunityUrban≥18Males & Females1130IDF23% (20–25%)
23.Goyal 2013UttarkhandNorthFacilityNA≥18Males & Females380IDF21% (17%-26%)
24.Gupta 2012RajasthanNorthCommunityUrban≥20Males & Females6106NCEP ATP -III26% (25%-27%)
25.Gupta A 2004RajasthanNorthCommunityUrban≥20Males & Females1091NCEP ATP III32% (29%-34%)
26.Gupta R 2007RajasthanNorthCommunityUrban≥20Males & Females644NCEP ATP III47% (43%-51%)
27.Gupta R 2012RajasthanNorthCommunityUrban20–60Males & Females739NCEP ATP III23% (20%-26%)
28.Harikrishnan 2018KeralaSouthCommunityUrban & Rural≥20Males & Females5063NCEP ATP III24% (23%-25%)
29.Ismail 2016KeralaSouthCommunityTribal≥18Males & Females120NCEP ATP III28% (20%-37%)
30.Jain 2015MaharashtraCentralFacilityNA18–25Males & Females668NCEP ATP III11% (9%-14%)
31.Jeyasheela 2018Tamil NaduSouthFacilityNA≥45Females154IDF64% (56%-72%)
32.Jones 2016Andhra PradeshSouthCommunityRural≥18Males & Females6217NCEP ATP III14% (13%-15%)
33.Kamble 2010MaharashtraCentralCommunityRural≥18Males & Females300NCEP ATP III9% (6%-13%)
34.Kandpal 2016UttarkhandNorthCommunityTribal20–60Males & Females288NCEP ATP III39% (34%-45%)
35.Kanjilal 2008Karnataka, MaharashtraSouth & CentralFacilityNA≥20Males & Females2315NCEP ATP III58% (56%-60%)
36.Kapil 2018UttarkhandNorthCommunityRural≥60Males & Females979IDF29% (26%-32%)
37.Kaur J 2014PunjabNorthCommunityUrban & Rural≥20Males & Females351NCEP ATP III17% (14%-22%)
38.Kaur P 2010Tamil NaduSouthWorkplaceNA≥20Males1077IDF41% (38%-44%)
39.Kaushal 2016Uttar PradeshCentralCommunityUrban≥20Males & Females127NCEP ATP III37% (29%-46%)
40.Kempegowda 2011KarnatakaSouthCommunityRural≥20Males & Females495NCEP ATP III20% (16%-23%)
41.Khan 2018Uttar PradeshCentralFacilityNA≥20Males & Females420NCEP ATP III41% (36%-46%)
42.Kotokey 2013AssamNortheastCommunityUrban≥20Males & Females502IDF33% (29%-37%)
43.Kunti 2019West BengalEastFacilityNA≥18Males & Females330NCEP ATP III64% (58%-69%)
44.Lakshmipriya 2012Tamil NaduSouthCommunityUrban≥20Males & Females1875IDF28% (26%-30%)
45.Lateef 2007Andhra PradeshSouthCommunityUrban≥20Males & Females1519NCEP ATP III24% (22%-27%)
46.Lavanya 2012Andhra PradeshSouthCommunityUrban≥20Males & Females350NCEP ATP III23% (19%-28%)
47.Madan G 2016MaharashtraWestCommunityUrban & Rural18–65Males313IDF40% (34%-46%)
48.Madhav 2013Andhra PradeshSouthWorkplaceNA≥20Males180IDF22% (16%-28%)
49.Mahadik 2007MaharashtraWestCommunityUrban & Rural≥20Males & Females1071NCEP ATP III24% (22%-27%)
50.Mahajan 2012New DelhiNorthCommunityUrban & Rural≥20Males & Females7174NCEP ATP III57% (56%-58%)
51.Mahanta 2013AssamNortheastCommunityUrban & Rural≥35Males & Females297NCEP ATP III27% (22%-32%)
52.Mahanta 2017AssamNortheastCommunityUrban & Rural20–60Males & Females3372NCEP ATP III48% (46%-49%)
53.Majumdar 2011KarnatakaSouthCommunityNot available18–75Males & Females441NCEP ATP III28% (24%-32%)
54.Majumdar 2017Andhra PradeshSouthCommunityUrban≥60Males & Females112IDF54% (45%-64%)
55.Mangat 2010ChandigarhNorthCommunityUrban & Rural≥18Males & Females605NCEP ATP III39% (35%-43%)
56.Manjunath 2014Andhra PradeshSouthCommunityUrban18–25Males & Females473NCEP ATP III4% (2%-6%)
57.Mini 2018KeralaSouthWorkplaceNA18–64Males & Females2287NCEP ATP III19% (18%-21%)
58.Misra 2011HaryanaNorthCommunityRural≥20Males & Females307NCEP ATP III12% (9%-16%)
59.Mittal 2018Uttar PradeshCentralCommunityUrban & Rural≥20Males & Females125IDF35% (27%-44%)
60.Mohan 2007Tamil NaduSouthCommunityUrban & Rural≥20Males & Females1736NCEP ATP III17% (15%-19%)
61.Mohan 2009Tamil NaduSouthCommunityUrban & Rural≥20Males & Females541NCEP ATP III37% (33%-41%)
62.Nag 2015West BengalEastCommunityRural≥20Males & Females1007IDF26% (23%-29%)
63.Naik 2016Andhra PradeshSouthCommunityUrban≥60Males & Females295IDF35% (29%-40%)
64.Nithya 2015Tamil NaduSouthCommunityRural≥60Males & Females514NCEP ATP III20% (17%-24%)
65.Pai 2019KarnatakaSouthCommunityUrban & Rural≥20Males & Females420NCEP ATP III4% (2%-6%)
66.Pandey 2010MaharashtraWestCommunityUrban35–65Females498IDF57% (52%-61%)
67.Parale 2008KarnatakaSouthWorkplaceNA≥30Males & Females700NCEP ATP III27% (24%-30%)
68.Patel 2016GujaratWestFacilityNA25–65Males & Females478NCEP ATP III26% (22%-30%)
69.Pathak 2018HaryanaNorthCommunityRural≥20Males & Females1200IDF9% (8%-11%)
70.Pemminati 2010KarnatakaSouthCommunityUrban≥20Males & Females451IDF30% (26%-34%)
71.Prabhakaran 2005New DelhiNorthWorkplaceNA20–59Males2120NCEP ATP III35% (33%-37%)
72.Prabhakaran 2007New DelhiNorthCommunityUrban & Rural35–64Males & Females4044NCEP ATP III33% (32%-35%)
73.Pradeepa 2016Tamil NaduSouthCommunityUrban≥60Males & Females222IDF37% (31%-44%)
74.Prakash 2013Uttar PradeshNorthFacilityNA≥18Males & Females1340NCEP ATP III32% (30%-35%)
75.Prasad 2012OrissaEastCommunityUrban20–80Males & Females1178IDF43% (40%-46%)
76.Rajput 2014HaryanaNorthCommunityUrban & Rural≥20Males & Females3042IDF29% (27%-31%)
77.Ramachandran 2003Tamil NaduSouthCommunityNot mentioned20–75Males & Females475NCEP ATP III41% (37%-46%)
78.Ramachandran 2008Tamil NaduSouthWorkplaceNA≥20Males & Females2499NCEP ATP III29% (27%-31%)
Ramachandran 2008Tamil NaduSouthCommunityUrban≥20Males & Females3278NCEP ATP III41% (37%-46%)
79.Randhwa 2015PunjabNorthCommunityRural25–55Females300NCEP ATP III26% (21%-31%)
80.Ravikiran 2010ChandigarhNorthCommunityUrban & Rural≥20Males & Females2225NCEP ATP III45% (43%-47%)
81.Roopa 2010Tamil NaduSouthCommunityUrban≥20Males & Females358NCEP ATP III35% (30%-40%)
82.Sachdev 2009New DelhiNorthCommunityUrban26–32Males & Females1492IDF25% (23%-27%)
83.Sarkar P 2016KarnatakaSouthCommunityRural≥30Males & Females448NCEP ATP III26% (22%-30%)
84.Sarkar S 2006West BengalEastCommunityTribal≥20Males & Females588NCEP ATP III25% (22%-29%)
85.Sarma 2015Andhra PradeshSouthCommunityRural30–50Females60NCEP ATP III20% (11%-32%)
86.Sawant 2011MaharashtraWestCommunityUrban≥20Males & Females548NCEP ATP III20% (16%-23%)
87.Selvaraj 2012Tamil NaduSouthCommunityRural30–50Females150NCEP ATP III31% (23%-39%)
88.Selvaraj 2019Tamil NaduSouthCommunityRural20–40Males360NCEP ATP III17% (13%-21%)
89.Shalini 2013KarnatakaSouthCommunityUrban & Rural≥18Females1023NCEP ATP III57% (54%-60%)
90.Sharma MK 2018Uttar PradeshCentralCommunityUrban & Rural20–55Males & Females290NCEP ATP III20% (16%-25%)
91.Sharma R 2019Jammu & KashmirNorthCommunityNot mentioned≥18Males & Females210NCEP ATP III35% (29%-42%)
92.Sharma S 2016ChandigarhNorthFacilityNA45–55Females350NCEP ATP III63% (57%-68%)
93.Sharma S 2016KarnatakaSouthWorkplaceNA20–50Males & Females210NCEP ATP III12% (8%-17%)
94.Singh 2016HaryanaNorthCommunityRural≥20Males & Females1700IDF27% (25%-29%)
95.Singh 2017Uttar PradeshNorthCommunityUrban≥25Males & Females2002NCEP ATP III19% (18%-21%)
96.Sinha N 2016TelanganaSouthCommunityUrban≥60Males & Females114IDF42% (33%-52%)
97.Sinha S 2012New DelhiNorthCommunityUrban≥20Females226NCEP ATP III30% (24%-36%)
98.Srimani 2017West BengalEastCommunityRural45–70Females222IDF46% (39%-53%)
99.Srimani 2018West BengalEastCommunityRural45–70Females509IDF38% (34%-42%)
100.Srinivasan 2016KeralaSouthFacilityNA≥20Males & Females432NCEP ATP III61% (56%-66%)
101.Subramani 2018Madhya PradeshCentralFacilityNA20–79Males & Females1190NCEP ATP III50% (47%-53%)
102.Tandon 2010Jammu & KashmirNorthCommunityRural≥45Females500NCEP ATP III13% (10%-16%)
103.Tharkar 2010Tamil NaduSouthCommunityUrban≥20Males & Females2021NCEP ATP III32% (30%-34%)
104.Tharkar S 2008Tamil NaduSouthWorkplaceNA≥30Males & Females318IDF57% (52%-63%)
Tharkar S 2008Tamil NaduSouthCommunityUrban≥30Males & Females410IDF28% (23%-32%)
105.Thayyil 2012KeralaSouthWorkplaceNA≥30Males823NCEP ATP III17% (14%-19%)
106.Thiruvagounder 2010Tamil NaduSouthFacilityNA≥20Males & Females1568NCEP ATP III29% (27%-31%)
107.Thyagi 2013Uttar PradeshCentralFacilityNA25–65Males & Females405NCEP ATP III43% (38%-48%)
108.Vatakanchery 2019KeralaSouthFacilityNA20–60Males & Females520IDF76% (72%-80%)
109.Venugopal 2019PondicherrySouthCommunityRural≥30Males & Females489IDF40% (35%-44%)
110.Wani 2014Jammu & KashmirNorthFacilityNA20–60Males & Females500NCEP ATP III9% (6%-11%)
111.Zafar 2017Uttar PradeshWestCommunityRural18–55Males & Females2982NCEP ATP III12% (11%-13%)

NCEP ATP III–National Cholesterol Education Program Adult Treatment Panel III.

IDF–International Diabetes Federation.

NA–Not applicable.

Table 2

Summary of findings and subgroup analysis of studies reporting prevalence of metabolic syndrome in India.

CharacteristicNumber of studies pooledPooled ES# (95% CI)I2P for heterogeneity/trend
Pooled prevalence of Metabolic syndrome in India = 30% (95%CI: 28%-33%)
AGE GROUP
18–29 years1213% (8%-18%)93.3%<0.001
30–39 years1132% (24%-41%)96.7%
40–49 years1141% (33%-48%)95.9%
50–59 years1050% (43%-57%)94.3%
≥60 years1741% (34%-49%)97.3%
GENDER
Male7626% (22%-29%)98.6%0.04
Female8235% (31%-38%)98.8%
URBAN VS RURAL VS TRIBAL
Urban4932% (29%-36%)98.9%<0.001
Rural3422% (20%-25%)97.7%
Tribal428% (21%-36%)88.4%
STUDY SETTING
Community8329% (26%-32%)99.1%0.08
Facility2138% (30%-47%)99.1%
Workplace928% (22%-35%)98.2%
GEOGRAPHICAL REGION
North3130% (25%-35%)99.2%0.83
South4630% (26%-33%)98.5%
East1133% (23%-43%)99.1%
West730% (19%-44%)99%
Central1027% (17%-39%)98.4%
Northeast435% (25%-46%)96.7%
DIAGNOSTIC CRITERIA
NTEP-ATP III8129% (26%-32%)99.2%0.05
IDF3234% (30%-39%)98.3%
WAIST CIRCUMFERENCE MEASUREMENT
Tip of iliac crest3429% (25%-33%)98.6%0.67
Midline of iliac crest & costal margin2232% (26%-39%)99%
YEAR OF PUBLICATION
2003–2006530% (22%-39%)98.2%0.62
2007–20102632% (27%-36%)98.9%
2011–20143027% (23%-33%)99.1%
2015–20195231% (27%-36%)99.1%
SAMPLING (REPRESENTATIVENESS)
Random4729% (25%-33%)99.30.37
Non-random6431% (27%-35%)98.8%
QUALITY OF STUDIES
Low3532% (28%-36%)98.4%0.40
High7629% (26%-33%)99.2%
Table 3

Univariate and multivariate meta-regression performed to explore the heterogeneity between the studies (N = 113).

CharacteristicsUnadjusted Co-efficientUnadjusted p-ValueAdjusted Co-efficientAdjusted p-value
Mean age0.00690.0020.00680.002
Study setting
CommunityRef-Ref-
Facility0.100.0060.100.04
Workplace-0.0040.930.040.49
Diagnostic criteria
IDFRef-Ref-
NCEP-ATP-0.050.10-0.070.11
Year of publication{Not included in the multivariate model}
2003–2006Ref-
2007–20100.020.75
2011–2014-0.010.82
2015–20190.020.75
Geographical region
NorthRef-
South0.050.41
East0.020.61
West0.070.40
Central0.020.63
Northeast0.030.69
Representativeness of the sample
RepresentativeRef-
Non-representative0.030.34
Quality of studies
Low riskRef-
High risk-0.020.46
  87 in total

1.  High prevalence of metabolic syndrome and its correlates in two tribal populations of India and the impact of urbanization.

Authors:  Sobhanjan Sarkar; Mithun Das; Barun Mukhopadhyay; C S Chakrabarti; Partha P Majumder
Journal:  Indian J Med Res       Date:  2006-05       Impact factor: 2.375

2.  The metabolic syndrome and associated risk factors in an urban industrial male population in South India.

Authors:  Prabhdeep Kaur; Ezhil Radhakrishnan; Sudha Ramachandra Rao; Suresh Sankarasubbaiyan; Thota Venkata Rao; Mohan Digamber Gupte
Journal:  J Assoc Physicians India       Date:  2010-06

3.  Prevalence of sleep abnormalities and their association with metabolic syndrome among Asian Indians: Chennai Urban Rural Epidemiology Study (CURES-67).

Authors:  Mahadevan Roopa; Mohan Deepa; Karunakaran Indulekha; Viswanathan Mohan
Journal:  J Diabetes Sci Technol       Date:  2010-11-01

4.  Elevated levels of C-reactive protein as a risk factor for metabolic syndrome in Indians.

Authors:  Anubha Mahajan; Alok Jaiswal; Rubina Tabassum; Avijit Podder; Saurabh Ghosh; S V Madhu; Sandeep K Mathur; Nikhil Tandon; Dwaipayan Bharadwaj
Journal:  Atherosclerosis       Date:  2011-11-02       Impact factor: 5.162

5.  Metabolic syndrome among elderly care-home residents in southern India: A cross-sectional study.

Authors:  Nirmalya Sinha; Ananta Bhattacharya; Pradeep Ranjan Deshmukh; Tanmay Kanti Panja; Shamima Yasmin; Nimmathota Arlappa
Journal:  WHO South East Asia J Public Health       Date:  2016-04

6.  Vitamin D status and metabolic syndrome in Asian Indians.

Authors:  V Majumdar; D Nagaraja; R Christopher
Journal:  Int J Obes (Lond)       Date:  2010-11-09       Impact factor: 5.095

Review 7.  Food consumption trends and drivers.

Authors:  John Kearney
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2010-09-27       Impact factor: 6.237

8.  Cardiometabolic risk factors in the Agarwal business community in India: Jaipur Heart Watch-6.

Authors:  Ritu Dhabriya; Mukta Agrawal; Rajeev Gupta; Indu Mohan; Krishna Kumar Sharma
Journal:  Indian Heart J       Date:  2015-04-30

9.  Epidemiological predictors of metabolic syndrome in urban West Bengal, India.

Authors:  Sasthi Narayan Chakraborty; Sunetra Kaviraj Roy; Md Abdur Rahaman
Journal:  J Family Med Prim Care       Date:  2015 Oct-Dec

10.  Prevalence of metabolic syndrome and its risk factors in Kerala, South India: Analysis of a community based cross-sectional study.

Authors:  S Harikrishnan; Smitha Sarma; G Sanjay; P Jeemon; M N Krishnan; K Venugopal; P P Mohanan; L Jeyaseelan; K R Thankappan; G Zachariah
Journal:  PLoS One       Date:  2018-03-27       Impact factor: 3.240

View more
  10 in total

Review 1.  Metabolic syndrome and underlying genetic determinants-A systematic review.

Authors:  Sanjeev Rana; Shafat Ali; Hilal Ahmad Wani; Qazi Danish Mushtaq; Swarkar Sharma; Muneeb U Rehman
Journal:  J Diabetes Metab Disord       Date:  2022-03-03

2.  Prevalence of Non-alcoholic Fatty Liver Disease in India: A Systematic Review and Meta-analysis.

Authors:  Anshuman Elhence; Bhavik Bansal; Hardik Gupta; Abhinav Anand; Thakur P Singh; Amit Goel
Journal:  J Clin Exp Hepatol       Date:  2021-11-25

3.  Identifying metabolic syndrome in migrant Asian Indian adults with anthropometric and visceral fat action points.

Authors:  John D Sluyter; Lindsay D Plank; Elaine C Rush
Journal:  Diabetol Metab Syndr       Date:  2022-07-15       Impact factor: 5.395

4.  Rural-Urban differentials in prevalence, spectrum and determinants of Non-alcoholic Fatty Liver Disease in North Indian population.

Authors:  Md Asadullah; Roopa Shivashankar; Devasenathipathy Kandasamy; Dimple Kondal; Garima Rautela; Ariba Peerzada; Bhanvi Grover; Ritvik Amarchand; Baibaswata Nayak; Raju Sharma; Lakshmy Ramakrishnan; Dorairaj Prabhakaran; Anand Krishnan; Nikhil Tandon
Journal:  PLoS One       Date:  2022-02-10       Impact factor: 3.240

5.  Prevalence of metabolic syndrome among the adult population in western China and the association with socioeconomic and individual factors: four cross-sectional studies.

Authors:  Xinyin Xu; Jing Zeng; Wei Yang; Ting Dong; Xin Zhang; Shuwen Cheng; Xiaobo Zhou; Maigeng Zhou; Ling Niu; Guanghui Yi; You Li; Lishi Zhang; Yin Deng; Xianping Wu
Journal:  BMJ Open       Date:  2022-04-01       Impact factor: 2.692

6.  Rural-urban and gender differences in metabolic syndrome in the aging population from southern India: Two parallel, prospective cohort studies.

Authors:  Jonas S Sundarakumar; Albert Stezin; Abhishek L Menesgere; Vijayalakshmi Ravindranath
Journal:  EClinicalMedicine       Date:  2022-04-19

Review 7.  Association Between Anthropometric Risk Factors and Metabolic Syndrome Among Adults in India: A Systematic Review and Meta-Analysis of Observational Studies.

Authors:  Yuvaraj Krishnamoorthy; Sathish Rajaa; Sharan Murali; Jayaprakash Sahoo; Sitanshu Sekhar Kar
Journal:  Prev Chronic Dis       Date:  2022-05-05       Impact factor: 4.354

8.  An examination of the prevalence of metabolic syndrome in older adults in Ireland: Findings from The Irish Longitudinal Study on Ageing (TILDA).

Authors:  Kevin McCarthy; Eamon Laird; Aisling M O'Halloran; Padraic Fallon; Deirdre O'Connor; Román Romero Ortuño; Rose Anne Kenny
Journal:  PLoS One       Date:  2022-09-14       Impact factor: 3.752

Review 9.  Metabolic syndrome and its associated factors in Ethiopia: A systematic review and meta-analysis.

Authors:  Tadeg Jemere; Belayneh Kefale
Journal:  J Diabetes Metab Disord       Date:  2021-05-09

10.  Multiomics Profiling Reveals Signatures of Dysmetabolism in Urban Populations in Central India.

Authors:  Tanya M Monaghan; Rima N Biswas; Rupam R Nashine; Samidha S Joshi; Benjamin H Mullish; Anna M Seekatz; Jesus Miguens Blanco; Julie A K McDonald; Julian R Marchesi; Tung On Yau; Niki Christodoulou; Maria Hatziapostolou; Maja Pucic-Bakovic; Frano Vuckovic; Filip Klicek; Gordan Lauc; Ning Xue; Tania Dottorini; Shrikant Ambalkar; Ashish Satav; Christos Polytarchou; Animesh Acharjee; Rajpal Singh Kashyap
Journal:  Microorganisms       Date:  2021-07-12
  10 in total

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