Dyslipidemias: Prevalence and Associated Factors among Lactating Women in a Lower- and Middle-Income Country, Ghana

Background Dyslipidemia, an abnormally high level of lipids in the blood, has a negative impact on the health status of the individual and has lately emerged as a major public health concern, especially for low- and middle-income countries (LMIC) globally, including Ghana. However, it is still unclear what the burden and drivers of these lipid abnormalities are, especially among lactating women in the Upper West of Ghana. Thus, this study is aimed at determining the prevalence of dyslipidemia and its associated factors among lactating mothers in the Wa Municipality of Ghana. Methodology. A cross-sectional study was conducted from May to June 2020 in 8 health facilities within the Wa Municipality. Multistage and simple random sampling methods were used to select the facilities and the 200 study subjects. Sociodemographic data were collected using questionnaires, while blood samples were taken to determine the lipid profile of participants. Dietary patterns were also assessed using the Food Frequency Questionnaire (FFQ). Data were processed and analyzed using SPSS 17 software (SPSS, Inc., Chicago, IL). The chi-square test and multiple regression analysis were performed to determine the predictors associated with the various types of dyslipidemia, with statistical significance set at a p value < 0.05. Results The prevalence of hypercholesterolemia (LDL-C), hypo-HDL-cholesterolemia, and hypertriglyceridemia (TG) was 57%, 59%, and 22%, respectively. Chi-square and multinomial regression analysis revealed that duration of lactation (X2 = 3.95, p = 0.047), religion (AOR = 0.375, 95% CI 0.144–0.978, p = 0.045), low income (AOR = 0.116, 95% CI 0.026–0.514, p = 0.005), middle income (AOR = 0.163, 95% CI 0.044–0.600, p = 0.006), and alcohol intake (AOR = 6.312, 95% CI 1.108–35.949, p = 0.038) were associated with LDL-C, while age (AOR = 0.963, 95% CI 0.910-1.019, p < 0.001) and educational status (AOR = 0.365, 95% CI 0.140–0.954, p = 0.040) predicted HDL status. Conclusion Dyslipidemia is common among lactating mothers of Wa Municipality, and it is predicted by lifestyle factors. Furthermore, future research to look at a larger sample size on dyslipidemia during lactation is recommended.


Introduction
Dyslipidemia is the abnormal value of any of the transportable lipid forms, namely, high-density lipoprotein (HDL), low-density lipoprotein (LDL), very low-density lipoprotein (VLDL), and triglyceride (TG), in the bloodstream [1,2] or as a combination of abnormalities of lipoprotein concentration in the bloodstream [3].Dyslipidemia is of more public health burden, especially for high-and middle-income countries [4], due to its association with atherosclerosis [5] and the attendant coronary heart disease (CHD) [6] and strokes.
Dyslipidemia is categorized into primary and secondary dyslipidemia, where the primary condition refers to the overproduction, a lack of production of or excessive clearance of HDL, or the inability of the body system to clear some lipoproteins arising from genetic defects during the lipoprotein metabolism process [7], with familial hypercholesterolemia, hypertriglyceridemia, and hypocholesterolemia as examples [8].Secondary dyslipidemia is related to the acquired form of the disorder and is associated with factors such as physical inactivity and consumption of saturated fatty diets, hypothyroidism, diabetes mellitus, obstructive liver disease, hypertension, thiazide diuretics, and progestin [9].Drinking coffee, advanced age, raised fasting blood sugar, and vegetable intake have also been reported as significant predictors of dyslipidemia among a population of women using contraceptives in eastern Ethiopia [10].
The prevalence of dyslipidemia varies in different localities ranging from 66.7% to 89.0% [5,11,12], and in Ghana, its public health importance has been described with data from independent studies [13,14].A study also revealed that dyslipidemia is more prevalent among the female population relative to the male population of Turkey [15].
Pregnancy and menopause are also known to affect the blood lipid profiles of women [11].During pregnancy, the metabolic activity is physiologically adjusted to accommodate increased progesterone and estrogen serum concentrations, hence leading to an increase in the metabolism of lipids [16].Meanwhile, breastfeeding improves the lipid profile, as indicated in some studies, thereby having the potential to reduce the risk of cardiovascular diseases [17,18].This suggests breastfeeding to be an important factor in overcoming the attendant weight gain and associated problems such as hypertension, among others.
Lactation is important immediately following childbirth and is characterized by an elevation in progesterone and estrogen serum concentrations.The interaction of these hor-mones alters the physiological and hormonal balance of the mother, thus compromising their health status [19].While evaluation of dyslipidemia has been done on the general population, few studies exist to evaluate lipid abnormalities among lactating mothers, and little to no data is recorded on lactating mothers in northern Ghana.This study therefore sought to determine the prevalence of dyslipidemias and associated factors among lactating mothers in the Wa Municipality of northern Ghana, a lower middle-income country.

Methodology
2.1.Study Area.The study was carried out in the Wa Municipality of the Upper West Region (UWR), located in the northwestern part of Ghana (Figure 1).This study area was chosen for the fact that the data on this dyslipidemia among lactating mothers in the study area was scanty.The region has four boundaries, with Burkina Faso to its north and la Cote d'Ivoire to the western part of the region, while the newly created Savannah Region is with the southern boundary, with the Upper East Region on the eastern part of the UWR.

Study
Design, Target Population, and Sampling.A crosssectional design was adopted to address the objective of the study.The lactating women within Wa Municipality constituted the targeted population of the study, which was estimated to be 4,950 based on the number of annual deliveries in the municipality [20].A multistage sampling was used in selecting eight subdistricts from the ten subdistricts in the Wa Municipality, and these subdistricts were Bamahu, Charia, Dobile, Kambali, Kperisi, Kpongu, Wa  Journal of Lipids South, and Wa North.From each of these selected subdistricts, one facility that provided child welfare clinic (CWC) services was chosen.For the purpose of this study, a total of nine health facilities were selected, including eight chosen randomly: Bamahu Hospital, Adolescent Clinic, Market Clinic, Dobile South CHPS, Gbegru CHPS, Kpaguri CHPS, Konjiehi CHPS, and Dandafuro CHPS.The Wa Regional Hospital was included in this selection as it serves as a key referral hospital.Two hundred (200) medically fit, consenting lactating mothers who visited any of the nine selected health facilities for CWC services during the time of the study were recruited.Figure 2 gives the flow of the study and subject recruitment.

Sample Size Determination.
The sample size required to be representative of the population was determined using Cochran's formula for sample size determination [21] where n represents the sample size.At a confidence interval of 95%, hence, Z is equivalent to 1.96.P represents the estimated proportion, which in this case is 93.4% [11].Q is equal to 1, P is equal to 1, and 0 0934 = 0 9066.d is the margin of error, and this case was chosen as 5% since the confidence interval is 95% = 0 05.This is approximated to be 95.0.

Sub-districts
Excluded those with no birth weight of children, had a fever, did not give consent Eight sub-districts were randomly selected + Wa Regional Hospital selected purposefully Nine health facilities selected (One facility from each of the selected sub-districts + Wa regional Hospital selected purposefully) Lactating mothers randomly selected 200 medically fit lactating mothers were recruited 3 Journal of Lipids But since the source population is less than 10,000, in estimating the sample size: where n is 95 and N is 10,000.
Therefore, the minimum sample size required for the study was estimated at 95.However, a 10% upward adjustment was made to the estimated minimum sample size to accommodate an assumed 10% nonresponse rate, giving the final sample size of 104.
To ensure a fair distribution of the number of study subjects recruited, the number of participants was weighted, and the final figure was computed as indicated in Table 1.

Inclusion and Exclusion
Criteria.Only lactating women who had visited the CWC during the period of the study were medically fit, had medically fit children, and consented were included in the study.Study subjects were excluded from the study if they had no record of the birth weight of their children, had a fever, and did not consent to be part of the study.
2.5.Data Collection.Data was collected from April to May 2020, and the biochemical analysis of the blood samples was conducted in June 2020.A one-day training was given to data enumerators on how to administer the questionnaire, ensure the privacy of the participants, and ensure the confidentiality of their information.A pretested questionnaire was administered to the study participants to elicit data on sociodemographic characteristics and lifestyle characteristics, together with dietary assessments of the respondents using the Food Frequency Questionnaire (FFQ) [22].To evaluate the lipid profile of the study participants, a minimum of 2 ml of venous blood samples was taken from each study participant and given a unique code.The venous blood samples were centrifuged at 3,500 rpm for ten minutes, and the collected serum was stored at -20 °C until it was analyzed.On the day of analysis, serum samples were removed from the freezer to thaw, and serum lipid concentration was quantified using the AX-200 Automatic Biochemistry Analyzer.
2.6.Data Processing and Analysis.Microsoft Excel (2013) was used to process and clean the data that was generated, which was exported into SPSS version 17 software (SPSS, Inc., Chicago, IL, USA) for statistical analysis.The number of lactating women with elevated plasma concentrations of LDL and TG (triglycerides) and lowered plasma concentration levels of HDL were reported as proportions.The sociodemographic characteristics of the respondents such as age, marital status, and type of residence were analyzed by employing descriptive statistics.The prevalence of dyslipidemia for the independent variables (covariates) was presented as frequencies and percentages.Continuous variables were summarized using means, with standard deviations or medians, and ranges, where appropriate.Pearson's chisquare was used to test for any associations between variables.Multiple logistic regression was used to test for the predictive effects of independent variables on the dependent variable, dyslipidemia, once other covariates were controlled.A statistical significance of p < 0 05 was set for all the statistical analyses, and all odds ratios were presented with 95% confidence intervals.

Ethical Considerations. Ethical clearance was obtained from the Committee on Human Research Publication and Ethics (CHRPE) of the Kwame Nkrumah University of
Science and Technology (KNUST), Kumasi, Ghana, with ID number CHRPE/AP/178/22.An introductory letter was obtained from the Department of Nutritional Sciences, University for Development Studies (UDS), and submitted to the Wa Municipal Health Directorate for approval to conduct the study in the selected facilities.Permission was given by the administrators and in-charges of the various facilities that were randomly chosen.Participants in the study were voluntarily and randomly chosen to participate in the study after their informed consent was obtained.

Results
3.1.Background Characteristics of Respondents.In all, 200 lactating women responded to the questionnaires, and their characteristics are summarized in Table 2.The most represented age groups were 28-32 and 33-37 years (56, 28.0%), with those <18 years being the least (1, 0.5%); all respondents were married at the time of the study (200, 100%).

Lifestyle
Activities of the Respondents.Table 3 gives an overview of the lifestyle characteristics of lactating mothers.Means of transport and frequency of exercise were evaluated to assess the level of physical activity.It was observed that the majority (137, 68.5%) of the respondents used engine vehicles as their means of transport, with 63 (31.5%) on foot.
Almost half of the study participants (93, 46.5%) exercised often (at least 5 times a week), while 60 (30%) had no form of exercise.The majority (183, 91%) of the study participants did not consume alcohol.Most (148, 91.5%) of the women breastfed their children exclusively, which was done for months.One hundred and eighty (180, 90%) of the mothers had an index child with normal birth weight, and (82.0%) of the study participants had normal (i.e., via vaginal) delivery.Furthermore, the majority (184, 92.0%) of the deliveries were singletons.

Sociodemographic Characteristics and Lifestyle Activities
Relationship with Lipid Profile of Lactating Women.One hundred and fourteen (114) lactating women had elevated levels of LDL serum cholesterol (LDL-C), suggesting a 57.0%prevalence of hypercholesterolemia, while a (59.0%) prevalence of hypocholesterolemia was also observed due to a low level of high-density lipoprotein cholesterol (HDL-C) (Figure 3).Furthermore, 44 (22.0%) of study participants were observed to have high levels of triglycerides (TG).

Discussion
While dyslipidemia in the general population and pregnant women has been documented, little is known about this condition in lactating mothers, especially in the study area, the UWR of Ghana.Even though dyslipidemia was common among the lactating mothers in the study area, it was significantly less associated with certain lifestyle and sociodemographic characteristics.
Dyslipidemia is of great public health concern due to its association with atherosclerotic plaques and consequent CHD and strokes.Thus, the various dyslipidemia types observed in the current study call for a more proactive approach among lactating mothers to reduce mortalities and disabilities linked with lipid metabolism.Elevated levels of LDL-C and hypertriglyceridemia (TG) observed in this study implicate CVD, fat embolisms, and other related ailments of atherosclerosis.LDL that has not been oxidized will not lead to foam cell formation; however, lipid peroxidation of LDL, as it accumulates, makes the LDL a target or ligand for certain receptors, including the scavenger receptor and   (2-tailed).* Near (place of residence close that they can walk to the health facility), far (need to take a vehicle to health facility).* * High income (>GHS1,000.00),middle income (GHS500.00-1,000.00),and low income (<GHS500.00).# Engine vehicle = motorbikes or cars.## Exercise level is defined as any form of physical activity (walking, farming, etc.): often (at least five times a week), maybe (at least two times a week).Hypocholesterolemia = serum concentration levels of HDL lower than 1.0 mmol/L; hypercholesterolemia = serum concentration levels of LDL greater than 3.3 mmol/L; hypertriglycerides = serum concentration levels of triglycerides higher than 2.2 mmol/L [23].The values in bold means those analysis was statistically significant.
8 Journal of Lipids    11 Journal of Lipids perhaps a specific receptor for oxidized LDL.These events generate cholesterol-laden foam cells, and oxidized LDL in the cell wall enhances the production of cytokines and growth factors, resulting in monocyte recruitment and the proliferation of smooth muscle cells [24].
The high prevalence (59%) of hypocholesterolemia (HDL-C) in this study gives cause for concern in relation to the physiology of the lactating mother.Higher rates of hypocholesterolemia (HDL-C) were also observed in other studies (60.91%, [25]; 64%, [26]; 72%, [13]; and 61%, [14]).HDL-C functions to scavenge any excess cholesterol within the body; thus, being low is a high risk for cardiovascular disease (CVD) for the participants in this study.
Age was associated with hypocholesterolemia in the current study; however, such was not the case with any of the dyslipidemia types studied in other studies ( [27] but varies with [28][29][30]).Meanwhile, studies have shown that older persons have a higher tendency to develop dyslipidemia [28,31].The explanation is that, as one age, the level of physical activity decreases, thus increasing the risk of developing dyslipidemia.Furthermore, the study participants in the current study were relatively younger generation (86% < 37 years).
Enani et al. [32] did not observe any association of religion with dyslipidemia as reported in the current study.Meanwhile, the majority of the study population were Muslims, who are noted to have a strict diet with minimal fat, as noted by the kind of diet reported in this study.Studies have shown that while a higher education level is associated with an increased level of physical activity, low-nutrient and high-calorie food consumption is often noted in women with lower level of education [33].Such unhealthy practices are high-risk factors for CVD.Thus, the association of education with low-level HDL-C (hypocholesterolemia) in this study and elsewhere [28,34] is of public health concern.Education provides an opportunity for awareness of 13 Journal of Lipids safe life habits and independence over one's health decisions, thus boosting self-confidence to have control of one's health style choices.
Individuals with high-income levels were observed to be at higher risk for dyslipidemia [34].The understanding is that they are accustomed to sedentary lives with less physical activity.It is not clear why hyperlipidemia was associated more with low-and middle-income earners in the current study.It has been established that alcohol intake is associated with increased HDL for those with moderate alcohol intake [35,36].However, in other studies, alcohol intake is associated with increased LDL-C [37] and TG [38][39][40], as observed in the current study.These have implications for public health.Hyperlipidemia is a metabolic defect in diabetics due to the accelerated breakdown of lipid molecules into acetyl-CoA molecules in an attempt to make energy available to the body.Consequently, lipids are resynthesized in the blood from the acetyl-CoA molecules that accumulate in the bloodstream, narrowing the blood vessels and resulting in atherosclerosis and associated CVD.Meanwhile, diabetes was not studied in the current study, which can be explored in further studies.
Physical exercise remains one of the recommendations for those being affected by dyslipidemia.However, no relationship between dyslipidemia and physical exercise was revealed in the current research, while other studies report an association [29,41].Although the degree or intensity of exercise was not evaluated, it is important to recommend to lactating mothers that they engage in the types of exercise that will increase metabolism.
The benefits of breastfeeding and its duration in relation to dyslipidemia need to be explored further.This is due to the conflicting opinions being reported regarding the link between the duration of breastfeeding and dyslipidemia.While our study observed dyslipidemia to be associated with a longer duration of breastfeeding as reported elsewhere [28], another study found no time-dependent association between breastfeeding (lactation) and metabolic risk [42].Meanwhile, central adiposity is known to be associated with high dyslipidemia.This is possible due to the accumulation of visceral fat instead of the subcutaneous fat being linked to hyperlipidemia.Thus, to prevent or reduce lipid metabolism disorders, it is important and necessary to reduce abdominal fat and increase lipid metabolism, hence the need to encourage appropriate exercise for these lactating mothers.
The results of this current study in relation to diet and its association with dyslipidemia were explored, but these were not significant and were in contrast to other studies [32,43,44].The results of those studies also established that the consumption of butter and eggs was associated with hypercholesterolemia, while hypertriglycerides were associated with fish, butter, eggs, and milk consumption.These observations confirm the role of diet in the health of an individual, particularly the development of dyslipidemia, irrespective of the geographical location of the study or individual.It is a known fact that there are some fish types and eggs that will impact the lipid pattern in the body of an individual, either resulting in hyperlipidemia or hypolipidemia.This study, however, did not investigate the food types, which should be explored in further studies.Meanwhile, grains, fish, vegetables, and fruits contain fiber which decreases the absorption of fat and sugar in the small intestine, helping to lower the number of triglycerides in the bloodstream.This should be recommended for lactating women.
Although some limitations were observed in the study, it has several strengths.This is the first of its kind to be conducted in the study area and has provided sound knowledge in the study area.The use of FFQ in accessing their dietary pattern may pose a limitation.Dietary intake is difficult to measure, and any single method cannot assess dietary exposure perfectly.Nutritional biomarkers are valid for objective estimates of dietary exposures in anthropometric and clinical assessments, while the 24HR, DR, dietary history, and FFQ are subjective estimates.Notwithstanding the discussed limitation, FFQs are still widely used as the primary dietary assessment tool in epidemiological studies.Recently, it has been suggested that a combination of methods, such as the FFQ with DRs (or 24HR) or the FFQ with biomarker levels, be used to obtain more accurate estimates of dietary intakes than those of individual methods.Considerable efforts to improve the accuracy and feasibility of large epidemiological studies are still ongoing.In summary, dietary assessment methods should be selected with caution while considering the research objective, hypothesis, design, and available resources [22].

Conclusions
This study shows that dyslipidemia is prevalent among the lactating mothers of Wa Municipality, which is predicted by some lifestyle factors (age, alcohol intake, income status, religion, and duration of lactation).It is recommended that future studies consider a larger sample size for dyslipidemia during lactation.

Figure 2 :
Figure2: Flow diagram of the study procedure.Medically fit are those without fever or no medical problem for which they will have to be referred to the medical doctor for treatment.

Figure 3 :
Figure 3: Prevalence of the various types of dyslipidemias.

Table 1 :
Proportionate distribution of sample size by health facility.

Table 4 :
Chi-square analysis of factors associated with the various types of dyslipidemias.

Table 5 :
Chi-square analysis of dietary factors associated with various types of dyslipidemias.
p is analyzed by multinomial logistic regression analyses and considered significant at <0.05 (2-tailed).The reference category is normal.b Parameter considered redundant and set to zero.B: regression coefficient; ExpB: exponentiation of B, which is the same as AOR; AOR: adjusted odds ratio; 95% CI: 95% confidence interval.The values in bold means the analysis were statistically significant.