The combination between praziquantel treatment and fatty liver disease in relation to diabetes mellitus in Northeast of Thailand 10.55131/jphd/2024/220109

Main Article Content

Dutsadee Khaweewong
Kavin Thinkhamrop
Apiporn T. Suwannatrai
Attapol Titapun
Watcharin Loilome
Matthew Kelly

Abstract

Diabetes mellitus (DM) is a growing global public health concern, including Thailand. Prior research has established an association between fatty liver disease (FLD) and DM. Moreover, the distribution of DM was also found in liver fluke endemic areas where praziquantel (PZQ) was used prevalently. However, limited information exists regarding factors associated with DM, specifically in FLD patients undergoing PZQ treatment. Our study aimed to evaluate the association between the combination of PZQ treatment and FLD diagnosis, and DM in Northeast Thailand. We conducted the study among participants in northeastern Thailand with self-reported DM diagnosis and PZQ treatment history using health questionnaires. Additionally, FLD diagnosis was confirmed through ultrasonography from the Cholangiocarcinoma Screening Program data collected from 2013-2022. We employed multilevel mixed-effect logistic regression to assess the association between the combination of PZQ treatments and FLD diagnosis, and DM, represented as adjusted odds ratios (AOR) and their 95% confidence intervals (CI). Of 756,431 participants, the overall DM prevalence was 7%. Notably, 10.45% of individuals with FLD+ and 8.23% with PZQ+ were found to have DM. Specifically, the prevalence of DM in individuals with PZQ+ and FLD-, PZQ- and FLD+, and PZQ+ and FLD+ combinations were 7.14%, 10%, and 11.81%, respectively. In comparison to PZQ- and FLD-, participants with PZQ+ and FLD-, PZQ- and FLD+, and PZQ+ and FLD+ were associated with DM (AOR = 1.27; 95% CI: 1.24-1.30, AOR = 1.8; 95% CI: 1.76-1.85, and AOR = 2.19; 95% CI: 2.12-2.27, respectively). In conclusion, the combination of PZQ and FLD plays a crucial role in the association with DM, particularly in individuals with PZQ+ and FLD+. Our findings emphasize the importance of DM screening, with special attention to individuals with a combination of PZQ treatment and FLD diagnosis, in order to promote early detection and management of DM in Northeast Thailand.

Article Details

How to Cite
1.
Khaweewong D, Thinkhamrop K, T. Suwannatrai A, Titapun A, Loilome W, Kelly M. The combination between praziquantel treatment and fatty liver disease in relation to diabetes mellitus in Northeast of Thailand: 10.55131/jphd/2024/220109. J Public Hlth Dev [Internet]. 2024 Jan. 26 [cited 2024 Apr. 24];22(1):110-25. Available from: https://he01.tci-thaijo.org/index.php/AIHD-MU/article/view/265852
Section
Original Articles
Author Biographies

Dutsadee Khaweewong, Doctor of Public Health Program, Faculty of Public Health, Khon Kaen University, Khon Kaen, Thailand

Doctor of Public Health Program, Faculty of Public Health, Khon Kaen University, Khon Kaen, Thailand

Kavin Thinkhamrop, Health and Epidemiology Geoinformatics Research (HEGER), Faculty of Public Health, Khon Kaen University, Khon Kaen, Thailand

Cholangiocarcinoma Research Institute (CARI), Khon Kaen, Thailand

Cholangiocarcinoma Screening and Care Program (CASCAP), Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Health and Epidemiology Geoinformatics Research (HEGER), Faculty of Public Health, Khon Kaen University, Khon Kaen, Thailand

Apiporn T. Suwannatrai, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Cholangiocarcinoma Research Institute (CARI), Khon Kaen, Thailand

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Attapol Titapun, Department of Surgery, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Cholangiocarcinoma Research Institute (CARI), Khon Kaen, Thailand

Cholangiocarcinoma Screening and Care Program (CASCAP), Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Department of Surgery, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Watcharin Loilome, Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Cholangiocarcinoma Research Institute (CARI), Khon Kaen, Thailand

Cholangiocarcinoma Screening and Care Program (CASCAP), Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand

Matthew Kelly, Department of Applied Epidemiology, National Centre for Epidemiology and Population Health, Australian National University, Canberra, Australia

Department of Applied Epidemiology, National Centre for Epidemiology and Population Health, Australian National University, Canberra, Australia

References

Al-Lawati JA. Diabetes Mellitus: A Local and Global Public Health Emergency! Oman Med J. 2017;32(3):177-9. doi: 10.5001/omj. 2017.34.

Galicia-Garcia U, Benito-Vicente A, Jebari S, Larrea-Sebal A, Siddiqi H, Uribe KB, et al. Pathophysiology of Type 2 Diabetes Mellitus. Int J Mol Sci. 2020;21(17). doi: 10.3390/ijms 21176275.

Papier K, Jordan S, D'Este C, Bain C, Peungson J, Banwell C, et al. Incidence and risk factors for type 2 diabetes mellitus in transitional Thailand: results from the Thai cohort study. BMJ Open. 2016;6(12):e014102. doi: 10.1136/ bmjopen-2016-014102.

Li J, Ye Q, Jiao H, Wang W, Zhang K, Chen C, et al. An early prediction model for type 2 diabetes mellitus based on genetic variants and nongenetic risk factors in a Han Chinese cohort. Front Endocrinol (Lausanne). 2023;14: 1279450. doi: 10.3389/fendo.2023. 1279450.

Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9(th) edition. Diabetes Res Clin Pract. 2019;157:107843. doi: 10.1016/ j.diabres.2019.107843.

Aekplakorn W, Chariyalertsak S, Kessomboon P, Assanangkornchai S, Taneepanichskul S, Putwatana P. Prevalence of Diabetes and Relationship with Socioeconomic Status in the Thai Population: National Health Examination Survey, 2004-2014. J Diabetes Res. 2018;2018: 1654530. doi: 10.1155/2018/1654530.

Reutrakul S, Deerochanawong C. Diabetes in Thailand: Status and Policy. Curr Diab Rep. 2016;16(3):28. doi: 10.1007/s11892-016-0725-7.

Hanprathet N, Lertmaharit S, Lohsoonthorn V, Rattananupong T, Ammaranond P, Jiamjarasrangsi W. Increased Risk Of Type 2 Diabetes And Abnormal FPG Due To Shift Work Differs According To Gender: A Retrospective Cohort Study Among Thai Workers In Bangkok, Thailand. Diabetes Metab Syndr Obes. 2019; 12:2341-54. doi: 10.2147/DMSO. S219524.

Sae-Wong J, Chaopathomkul B, Phewplung T, Chaijitraruch N, Sahakitrungruang T. The Prevalence of Nonalcoholic Fatty Liver Disease and Its Risk Factors in Children and Young Adults with Type 1 Diabetes Mellitus. J Pediatr. 2021;230:32-7.e1. doi: 10.1016/j.jpeds.2020.10.043.

Dejkhamron P, Santiprabhob J, Likitmaskul S, Deerochanawong C, Rawdaree P, Tharavanij T, et al. Young-onset diabetes patients in Thailand: Data from Thai Type 1 Diabetes and Diabetes diagnosed Age before 30 years Registry, Care and Network (T1DDAR CN). J Diabetes Investig. 2022;13(5):796-809. doi: 10.1111/jdi.13732.

Nooseisai M, Viwattanakulvanid P, Kumar R, Viriyautsahakul N, Muhammad Baloch G, Somrongthong R. Effects of diabetes self-management education program on lowering blood glucose level, stress, and quality of life among females with type 2 diabetes mellitus in Thailand. Prim Health Care Res Dev. 2021;22:e46. doi: 10.1017/ S1463423621000505.

Golabi P, Paik JM, Kumar A, Al Shabeeb R, Eberly KE, Cusi K, et al. Nonalcoholic fatty liver disease (NAFLD) and associated mortality in individuals with type 2 diabetes, pre-diabetes, metabolically unhealthy, and metabolically healthy individuals in the United States. Metabolism. 2023; 146:155642. doi: 10.1016/j.metabol. 2023.155642.

Chen YY, Yeh MM. Non-alcoholic fatty liver disease: A review with clinical and pathological correlation. J Formos Med Assoc. 2021;120(1 Pt 1):68-77. doi: 10.1016/j.jfma.2020.07. 006.

Miller MJ, Harding-Theobald E, DiBattista JV, Zhao Z, Wijarnpreecha K, Lok AS, et al. Progression to cirrhosis is similar among all ages in nonalcoholic fatty liver disease, but liver-related events increase with age. Hepatol Commun. 2023;7(6). doi: 10.1097/HC9.0000000000000148.

Wu PH, Chung CH, Wang YH, Hu JM, Chien WC, Cheng YC. Association between nonalcoholic fatty liver disease and colorectal cancer: A population-based study. Medicine (Baltimore). 2023;102(21):e33867. doi: 10.1097/ MD.0000000000033867.

Younossi ZM, Otgonsuren M, Henry L, Venkatesan C, Mishra A, Erario M, et al. Association of nonalcoholic fatty liver disease (NAFLD) with hepatocellular carcinoma (HCC) in the United States from 2004 to 2009. Hepatology. 2015;62(6):1723-30. doi: 10.1002/hep.28123.

Wongjarupong N, Assavapongpaiboon B, Susantitaphong P, Cheungpasitporn W, Treeprasertsuk S, Rerknimitr R, et al. Non-alcoholic fatty liver disease as a risk factor for cholangiocarcinoma: a systematic review and meta-analysis. BMC Gastroenterol. 2017;17(1):149. doi: 10.1186/s12876-017-0696-4.

Toshikuni N, Tsutsumi M, Arisawa T. Clinical differences between alcoholic liver disease and nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20(26):8393-406. doi: 10.3748/ wjg.v20.i26.8393.

Haonon O, Liu Z, Dangtakot R, Pinlaor P, Puapairoj A, Cha'on U, et al. Opisthorchis viverrini infection induces metabolic disturbances in hamsters fed with high fat/high fructose diets: Implications for liver and kidney pathologies. J Nutr Biochem. 2022;107: 109053. doi: 10.1016/j.jnutbio.2022. 109053.

Summart U, Thinkhamrop B, Chamadol N, Khuntikeo N, Songthamwat M, Kim CS. Gender differences in the prevalence of nonalcoholic fatty liver disease in the Northeast of Thailand: A population-based cross-sectional study. F1000Res. 2017;6:1630. doi: 10.12688/f1000 research.12417.2.

Thinkhamrop K, Khuntikeo N, Phonjitt P, Chamadol N, Thinkhamrop B, Moore MA, et al. Association between Diabetes Mellitus and Fatty Liver Based on Ultrasonography Screening in the World's Highest Cholangiocarcinoma Incidence Region, Northeast Thailand. Asian Pac J Cancer Prev. 2015;16(9):3931-6. doi: 10.7314/ apjcp.2015.16.9.3931.

Tanase DM, Gosav EM, Costea CF, Ciocoiu M, Lacatusu CM, Maranduca MA, et al. The Intricate Relationship between Type 2 Diabetes Mellitus (T2DM), Insulin Resistance (IR), and Nonalcoholic Fatty Liver Disease (NAFLD). J Diabetes Res. 2020;2020: 3920196. doi: 10.1155/2020/3920196.

El-Kashef HA, Salem HA, Said SA, Elmazar MM. Effect of praziquantel on serum glucose and insulin levels in normal and hyperglycemic rats. Arzneimittelforschung. 1996;46(4): 433-5.

Muthukumar R, Suttiprapa S, Mairiang E, Kessomboon P, Laha T, Smith JF, et al. Effects of Opisthorchis viverrini infection on glucose and lipid profiles in human hosts: A cross-sectional and prospective follow-up study from Thailand. Parasitol Int. 2020;75: 102000. doi: 10.1016/j.parint.2019. 102000.

Saengsawang P, Promthet S, Bradshaw P. Infection with Opisthorchis viverrini and use of praziquantel among a working-age population in northeast Thailand. Asian Pac J Cancer Prev. 2013;14(5):2963-6. doi: 10.7314/apjcp. 2013.14.5.2963.

Thinkhamrop K, Khuntikeo N, Sithithaworn P, Thinkhamrop W, Wangdi K, Kelly MJ, et al. Repeated praziquantel treatment and Opisthorchis viverrini infection: a population-based cross-sectional study in northeast Thailand. Infect Dis Poverty. 2019;8(1):18. doi: 10.1186/ s40249-019-0529-5.

Thinkhamrop K, Khuntikeo N, Laohasiriwong W, Chupanit P, Kelly M, Suwannatrai AT. Association of comorbidity between Opisthorchis viverrini infection and diabetes mellitus in the development of cholangiocarcinoma among a high-risk population, northeastern Thailand. PLOS NEGL TROP DIS. 2021;15(9): e0009741. doi: 10.1371/journal.pntd. 0009741.

Htun NSN, Odermatt P, Paboriboune P, Sayasone S, Vongsakid M, Phimolsarn-Nusith V, et al. Association between helminth infections and diabetes mellitus in adults from the Lao People's Democratic Republic: a cross-sectional study. Infect Dis Poverty. 2018;7(1): 105. doi: 10.1186/s40249-018-0488-2.

Khuntikeo N, Chamadol N, Yongvanit P, Loilome W, Namwat N, Sithithaworn P, et al. Cohort profile: cholangiocarcinoma screening and care program (CASCAP). BMC Cancer. 2015;15:459. doi: 10.1186/s12885-015-1475-7.

Prathumkam P, Thinkhamrop K, Khuntikeo N, Chamadol N, Thuanman J, Kelly M, et al. Association between the Number of Repeated Praziquantel Treatments and Kidney Parenchymal Change in Northeast Thailand. Asian Pac J Cancer Prev. 2022;23(7):2397-405. doi: 10.31557/APJCP.2022.23. 7.2397.

Sripa B, Suwannatrai AT, Sayasone S, Do DT, Khieu V, Yang Y. Current status of human liver fluke infections in the Greater Mekong Subregion. Acta Trop. 2021;224:106133. doi: 10.1016/ j.actatropica.2021.106133.

Martviset P, Phadungsil W, Na-Bangchang K, Sungkhabut W, Panupornpong T, Prathaphan P, et al. Current prevalence and geographic distribution of helminth infections in the parasitic endemic areas of rural Northeastern Thailand. BMC Public Health. 2023;23(1):448. doi: 10.1186/ s12889-023-15378-4.

Cusacovich I, Sánchez-Lite I, Toribio B, González JM, Pérez-Rubio A, Andaluz-Ojeda D. Prevalence of nonalcoholic fatty liver disease in a Spanish town: a population-based study. Rev Clin Esp (Barc). 2023; 223(7):396-404. doi: 10.1016/j.rceng. 2023.04.012.

Phisalprapa P, Prasitwarachot R, Kositamongkol C, Hengswat P, Srivanichakorn W, Washirasaksiri C, et al. Economic burden of non-alcoholic steatohepatitis with significant fibrosis in Thailand. BMC Gastroenterol. 2021; 21(1):135. doi: 10.1186/s12876-021-01720-w.

Han WM, Apornpong T, Lwin HMS, Thammapiwan S, Boonrungsirisap J, Gatechompol S, et al. Nonalcoholic Fatty Liver Disease and Nonalcoholic Steatohepatitis With Liver Fibrosis as Predictors of New-Onset Diabetes Mellitus in People With HIV: A Longitudinal Cohort Study. Clin Infect Dis. 2023;77(12):1687-95. doi: 10.1093/cid/ciad433.

Cho Y, Chang Y, Ryu S, Wild SH, Byrne CD. Nonalcoholic fatty liver disease without overlapping metabolic-associated fatty liver disease and the risk of incident type 2 diabetes. Liver Int. 2023;43(11):2445-54. doi:10.1111/ liv.15661.