Abstract
The study aimed to estimate the prevalence and associated factors of undiagnosed type 2 diabetes (T2D) among adults in Morocco. Cross-sectional data were analyzed from 4779 people (≥ 18 years, mean age 41.7 years) who participated in the Morocco STEPS nationally representative survey in 2017 and had completed fasting blood glucose measurement. The results indicate that the prevalence of undiagnosed T2D was 5.9% (44.7% of total T2D), diagnosed T2D 7.3% and total T2D 13.2%. In the adjusted multinomial logistic regression analysis, older age (≥ 50 years), receipt of health care advice, and obesity were positively associated with undiagnosed T2D. Older age (≥ 50 years), urban residence, receipt of health care advice, ever cholesterol screening, moderate sedentary behaviour, obesity, hypertension, and elevated total cholesterol were positively associated with diagnosed T2D. In adjusted logistic regression analysis, older age (≥ 50 years), receipt of health care advice and cholesterol screening were negatively associated with undiagnosed T2D versus diagnosed T2D. A significant proportion of adults in Morocco had undiagnosed T2D and several associated factors were identified that can help guide interventions.
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Introduction
According to the World Health Organization1, more than one and a half million people died from diabetes in 2019; however, diabetes can be treated with diet, physical activity, medication and regular screening and management of complications. Untreated undiagnosed type 2 diabetes (T2D) may have serious consequences, including microvascular and macrovascular complications2,3 and an increased risk of mortality4,5, highlighting the crucial importance of early diagnosis. In 2021, worldwide 44.7% of adults with T2D did not know they had T2D6. In an earlier review of studies in 29 low- and middle-income countries (LMICs), the prevalence of undiagnosed T2D was 4.9%7, and in a review of 55 studies in the eastern Mediterranean region, the pooled prevalence of undiagnosed T2D was 5.45%, for example, in Tunisia 7.7% and in Iraq 6.2%8. In a small sample of urban Sahraoui women in South Morocco, the prevalence of undiagnosed T2D was 6.4% in 2001/20029. Due to 44% of the diabetes population being undiagnosed in Morocco10, the Moroccan Ministry of Health launched a public awareness campaign in 2015 on the different types of diabetes, its risk factors, warning signs and complications, the importance of screening and the adoption of a healthy lifestyle, involving health professionals and other lay persons in awareness and health education and involving the media in information and awareness on diabetes and its complications11. There is a lack of national data on undiagnosed T2D and its correlates in Morocco8,12. These data may help to assess public health interventions related to the screening and diagnosis of T2D in Morocco.
Predisposing factors associated with undiagnosed T2D included in some studies younger adults13,14,15, older adults16,17,18,19, male sex15,17, living alone 15,20, and family history of diabetes21,22. Enabling/disabling factors associated with undiagnosed T2D include rural residence13,16, in some studies lower economic status13,23, food insecurity24, and lower education14,25, and in other studies higher economic status17, and higher education23. Other enabling/disabling factors associated with undiagnosed T2D include knowing symptoms of diabetes21, no health care visit in the past 12 months15, health insurance status (having medical insurance16, and not having private insurance26 and health risk behaviours (high sedentary behaviour27, heavy alcohol use28, and high level of physical activity23.
The need factors associated with undiagnosed T2D include other chronic diseases16, hypertension status (not hypertension13,14, hypertension17,18,29,30), obesity17,18,19,21,22,28,31, low HDL-C31,32, high triglycerides31,32, dyslipidaemia22, cardiovascular disease status (not heart disease14, cardiovascular disease18), and perceived poor health16. The study aimed to estimate the prevalence and associated factors of undiagnosed T2D among people 18 years and older in Morocco.
Methods
Study design and participants
Secondary data from the ‘STEPwise approach to NCD risk factor Surveillance’ (STEPS) cross-sectional survey in Morocco in 201733 with complete measurements of fasting blood glucose were analyzed; the overall response rate was 89.0%34. STEPS focus is on “obtaining population-based data on the established risk factors that determine the major disease burden on a regular basis”33. Participants were randomly selected from the target population (18 years and older), using a multi-stage stratified sampling procedures34. Following the STEP-wise survey procedures, in Step 1 behavioural and sociodemographic data were collected. In Step 2, physical measurements and blood pressure were assessed, and in Step 3. biochemical measurements were collected to assess blood glucose and cholesterol33. Blood glucose, total cholesterol and triglycerides were measured in peripheral (capillary) blood at the data collection site; equipment used was the Cardiochek® PA (pts Diagnostics, Indianapolis, Indiana, USA) with a Chip MeMo, Blood Glucose Strips and lipids34.
Ethics approval was provided by the Biomedical Research Ethics Committee, Faculty of Medicine and Pharmacy of Rabat, Morocco, and participants provided written informed consent. All methods were performed in accordance with the relevant guidelines and regulations.
Measures
Outcome variable
Undiagnosed T2D was defined as fasting plasma glucose level ≥ 126 mg/dL among people who responded “no” to the question “Have you ever been told by a doctor or other health worker that you have raised blood sugar or diabetes?” Diagnosed T2D was defined as those who answered “yes” to the question of ever having been told by a health care worker that they had diabetes, and total T2D included those with undiagnosed and diagnosed T2D35.
Predisposing factors included age, sex, and marital status.
Enabling or disabling factors included residence status, receipt of health care advice, ever screening for cholesterol, smoking tobacco history, physical activity, and sedentary behaviour. The receipt of health care advice was assessed with the question, “During the past three years, has a doctor or other health worker advised you to maintain a healthy body weight or lose weight?” (yes/no). Smoking history was assessed with two questions, “Do you currently smoke any tobacco products, such as cigarettes, cigars or pipes?” (Yes, No) and “In the past, did you ever smoke any tobacco products?”(Yes, No)34. Self-reported physical activity and sedentary behaviour were assessed with the Global Physical Activity Questionnaire (GPAQ) and categorized by the median metabolic equivalent (METs) of performed activities as low, moderate, and high36, and sedentary behaviour defined as low (< 4 h), moderate (4 to < 8 h) and high (≥ 8 h sitting/day)37.
The need factors included BMI, hypertension, heart attack or stroke, and elevated total cholesterol. Body mass index (BMI) was classified as “underweight (< 18.5 kg/m2), normal weight (18.5–24.9 kg/m2), overweight (25.0–29.9 kg/m2), and obesity (≥ 30.0 kg/m2)”33. Hypertension was defined as “systolic BP ≥ 140 mmHg and/or diastolic BP ≥ 90 mmHg and/or previous or current treatment with antihypertensive drugs”38. History of heart attack or stroke included self-reported “Have you ever had a heart attack or chest pain from heart disease (angina) or a stroke (cerebrovascular accident or incident)? (Yes, No)”34. Elevated total cholesterol was classified39 as: “being on antilipidemic medication or having elevated total cholesterol (TC): ≥ 5.17 mmol/l (200 mg/dl)”.
Sample size calculations and data analysis
Sample size calculation. This data set had an overall N = 5429 and 4779 (88%) persons from the total sample had completed fasting blood glucose measurement. From a review in the study region, the pooled prevalence of undiagnosed T2D was 5.45%8. We calculated the sample size with Epi-Info with population 100,000, expected frequency 5.45, acceptable margin of error 5% confidence level 99.99, minimum sample size is 317. In our study we calculated that based on the existing data set of 4799 people, the sample size is sufficient.
All statistical analyses were conducted with STATA software version 14.0 (Stata Corporation, College Station, TX, USA). Analysis weights were calculated by taking the inverse of the probability of selection of each participant adjusted for differences in the age-sex composition of the sample population compared to the target population.33 Descriptive statistics are used to describe the sample. Pearson chi-square statistics were used to calculate differences in proportion. Multinomial logistic regression was used to estimate factors associated with undiagnosed T2D and diagnosed T2D (with not having T2D as reference category). Logistic regressions were used to assess the associations with undiagnosed T2D versus diagnosed T2D. Covariates in the logistic regression models included predisposing factors (age, gender, and marital status), enabling, or disabling factors (residence status, reported receipt of health care advice, cholesterol screening, education, smoking status, physical activity, and sedentary behaviour) and need factors (BMI, hypertension, heart attack or stroke, and elevated total cholesterol). Variables significant in univariable analyses were subsequently included in the multivariable models. To account for the multi-stage sample design, Taylor linearization methods were utilized. P-values < 0.05 were considered significant and missing values were discarded.
Results
Sample characteristics
The sample with complete fasting blood glucose measurement included 4779 persons (≥ 18 years), with a mean age of 41.7 years (SD = 16.5 years) in 2017. The prevalence of undiagnosed T2D was 5.9% (44.7% of total T2D), diagnosed T2D 7.3%, and total T2D 13.2%. Further sociodemographic and health characteristics of the sample by T2D status are described in Table 1.
Associations with undiagnosed and diagnosed T2D versus non-diabetic
In the adjusted multinomial logistic regression analysis, older age (≥ 50 years) (ARRR: 2.80, 95% CI: 1.80–4.35), receipt of health care advice (ARRR: 1.79, 95% CI: 1.32–2.41), and obesity (ARRR: 1.71, 95% CI: 1.19–2.46) were positively associated with undiagnosed T2D. Older age (≥ 50 years) (ARRR: 6.64, 95% CI: 3.81–11.60), urban residence (ARRR: 1.50, 95% CI: 1.12–2.00), receipt of health care advice (ARRR: 2.92, 95% CI: 2.23–3.82), ever cholesterol screening (ARRR: 2.64, 95% CI: 1.99–3.50), moderate sedentary behaviour (ARRR: 1.33, 95% CI: 1.01–1.75), obesity (ARRR: 1.56, 95% CI: 1.11–2.19), hypertension (ARRR: 1.47, 95% CI: 1.13–1.92), and elevated total cholesterol (ARRR: 2.64, 95% CI: 1.99–3.50) were positively associated with diagnosed T2D. In addition, in unadjusted analyses, male sex, higher education, and high physical activity were negatively associated, and hypertension and elevated total cholesterol were positively associated with undiagnosed T2D (see Tables 2 and 3).
Associations with undiagnosed T2D versus diagnosed T2D
In adjusted logistic regression analysis, older age (≥ 50 years) (AOR: 0.32, 95% CI: 0.16–0.64), receipt of health care advice (AOR: 0.51, 95% CI: 0.36–0.72), and ever cholesterol screening (AOR: 0.31, 95% CI: 0.20–0.47) were negatively associated with undiagnosed T2D versus diagnosed T2D. Furthermore, in the unadjusted analysis, urban residence, sedentary behaviour, obesity, hypertension, and heart attack or stroke were negatively associated with undiagnosed T2D versus diagnosed T2D (see Table 4).
Discussion
The study found a national prevalence of undiagnosed T2D (5.9%, 44.7% of total T2D), which is similar to recent global Figs. (44.7% of total T2D)6, higher than in an earlier review of studies in 29 LMICs (4.9%)7, higher than in a review of studies in the Eastern Mediterranean region (5.45%)8, and lower than in a local study among women in Morocco (6.4%)9. People with undiagnosed T2D versus diagnosed T2D showed fewer diabetes-related risk factors, such as younger age, no obesity, and no hypertension than those with diagnosed T2D. This may be explained by people with undiagnosed T2D being generally younger and healthier than those with diagnosed T2D, mostly at an earlier stage of T2D40.
Consistent with some previous research14,15,16,17,18,19, some predisposing factors (older age) were associated with undiagnosed T2D versus no T2D. According to some previous studies15,16,26, enabling / disabling factors associated with undiagnosed T2D versus diagnosed T2D included no receipt of health care advice (to lose weight) in the past three years, and had never been screened for cholesterol. People with receipt of health care advice and cholesterol screening are more likely to use health services and may consequently reduce the odds of undiagnosed T2D16. Following the T2D management guidelines in Morocco, patients with diabetes are expected to attend health care services more often41, which may explain that people with diagnosed T2D visit health care providers more often than people with undiagnosed T2D15. While some studies13,16 found an association between rural residence and undiagnosed T2D, we only found this association in unadjusted analysis. Previous studies14,23,25 found mixed results regarding the association between educational status and undiagnosed T2D, while we found no significant association.
Consistent with previous research17,18,19,21,22,28, need factors associated with undiagnosed T2D included other chronic diseases, such as obesity. Obesity is a known risk factor for diabetes21. Consistent with some research13,14,15, in unadjusted analysis, we found a negative association between hypertension, cardiovascular disease, and undiagnosed T2D versus diagnosed T2D. Unlike some previous studies22,31,32, we did not find an association between elevated total cholesterol and undiagnosed T2D. However, we found a statistically significant positive association between elevated total cholesterol and diagnosed T2D. This may be explained by people with diagnosed T2D who are generally older and less healthy, mostly at a later stage of T2D than those with undiagnosed T2D40.
Strengths and limitations
The study strengths include the use of nationally representative adult sample of all ages and standardized STEPS methodology and measures. The limitation of the study is using peripheral (capillary) blood instead venous plasma glucose42. However, Priya et al.43 showed that capillary blood glucose is a feasible alternative for screening for diabetes in epidemiological studies in developing countries where obtaining venous samples may be difficult. Some variables were evaluated by self-report, which may have biased responses, and the cross-sectional design precludes causative conclusions between the evaluated variables. The sample only included those persons who were non-institutionalized, while the inclusion of institutionalized persons would have given different estimates. Furthermore, certain variables, such as knowledge of diabetes symptoms and a family history of diabetes, were not evaluated and should be included in future research.
Implications for public health research and practice
Policy implications are that increased public awareness campaigns, and screening of T2D are needed to reduce undiagnosed T2D in Morocco. The Morocco national NCD programme includes community awareness campaigns on diabetes, screening/early detection, and integrated care for diabetes44.
Conclusion
A significant proportion of adults in Morocco had undiagnosed T2D. Predisposing factors (older age), enabling factors (receipt of health care advice) and need factors (obesity) were identified as associated with undiagnosed T2D versus no T2D, and predisposing factors (younger age), and enabling / enabling factors (no receipt of health care advice, never been screened for cholesterol) were identified as associated with undiagnosed T2D versus diagnosed T2D, which can be targeted in interventions.
Data availability
The data source is publicly available at the World Health Organization NCD Microdata Repository (URL: https://extranet.who.int/ncdsmicrodata/index.php/catalog).
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Acknowledgements
This paper uses data from the 2017 Morocco STEPS survey, implemented by the Ministry of Health with the support of the World Health Organization.
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All authors fulfil the criteria for authorship. S.P. and K.P. conceived and designed the research, performed statistical analysis, drafted the manuscript, and made critical revision of the manuscript for key intellectual content. All authors read and approved the final version of the manuscript and have agreed to authorship and order of authorship for this manuscript.
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Pengpid, S., Peltzer, K. Prevalence and correlates of undiagnosed, diagnosed, and total type 2 diabetes among adults in Morocco, 2017. Sci Rep 12, 16092 (2022). https://doi.org/10.1038/s41598-022-20368-4
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DOI: https://doi.org/10.1038/s41598-022-20368-4
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