Associations between green tea drinking and body mass index, serum lipid profile and prostate-specific antigen in a Ghanaian population: a cross-sectional study

Abstract

Background

Prostate cancer (PCa) is a major malignancy that affects men worldwide. Obesity, dyslipidemia and elevated serum PSA are common risk factors. Green tea is a popular beverage in some West African communities with a relatively low incidence of PCa. However, the associations of green tea consumption with these PCa risk factors in that population remain unknown. This study therefore aimed at investigating the associations between green tea intake and the serum lipid profile, body mass index (BMI), and serum PSA.

Methods

An analytical cross-sectional survey was conducted to compare the serum lipid profile, BMI and serum PSA between green tea drinkers (GTD) and non-tea drinkers (NTD). A total of 415 men, 40 years or older, who gave their consent were assigned to four groups on the basis of age: 40–49 years, 50–59 years, 60–69 years, and 70 + years. BMI, serum lipid profile (total cholesterol, HDL-c, LDL-c, and triglycerides), and serum PSA level were determined and compared between GTD and NTD.

Results

Compared with the NTD group, the GTD with normal BMI were significantly greater across all age groups, and the odds of being overweight (obese) were significantly lower in the GTD group than in the NTD group. Compared with those in the NTD, significantly fewer atherogenic lipids in the GTD were observed across all age categories. Furthermore, the odds of dyslipidemia in GTD groups were lower than those in NTD groups across all age groups. A significantly lower mean serum PSA level was observed in the older GTD age groups (60–69 and 70+) than in the NTD group, and significantly lower odds of elevated serum PSA were detected in the GTD group than in the NTD group. However, there were no differences in the mean PSA between the GTD and NTD groups in the younger age groups. Weak positive correlations between serum PSA and BMI were observed in the NTD group regardless of the age category. However, a significantly strong negative correlation between the serum PSA concentration and BMI was observed in the older age GTD group compared with the NTD group.

Conclusions

Consumption of green tea was associated with reduced atherogenic serum lipids and improved BMI independent of age. Furthermore, GTD was significantly associated with reduced serum PSA in older men but not in younger adults.

Background

Prostate cancer is the second most diagnosed cancer in men globally and the fifth leading cause of death worldwide [1, 2]. Men of African ancestry suffer the most aggressive type of this cancer, leading to the highest mortality-to-incidence rate ratios globally compared with other ethnicities [3, 4]. Prostate cancer (PCa) has therefore become a remarkable public health concern in Africa, as the majority of new diagnoses are advanced/metastatic cancers, with poor prognoses and low chances of long-term survival [5]. There is no evidence yet on how to prevent PCa; however, some modifiable risk factors have been identified [6, 7]. Obesity and elevated serum lipids in men are strongly associated with PCa development and recurrence after treatment [8, 9]. A growing body of evidence indicates that an aberrant serum lipid profile in obesity is associated with increased PCa risk and worse outcomes of radical prostatectomy [10, 11]. Therefore, a high BMI and dyslipidemia are considered major risk factors for PCa in men [7, 8, 12, 13]. Available reports indicate that elevated triglyceride (TG), low serum levels of high-density lipoprotein (HDL) and elevated serum cholesterol levels are strongly associated with high-grade PCa [14,15,16,17]. Earlier reports indicate that patients with high serum cholesterol levels are more likely to have high-grade PCa or recurrence. However, in addition to unhealthy body mass index (BMI) and atherogenic dyslipidemia, increased serum PSA increases one’s risk of PCa [18]. Given the age-adjusted geographical variations in PCa incidence reported in Global Cancer Statistics, there is increasing interest in nutrition and non-nutrient diets as relevant factors in the etiology and pathogenesis of PCa. Although the literature on plant-based nutrients and non-nutrient phytochemicals and PCa has been somewhat inconsistent, there are reports on inverse associations between PCa risk and plant-based diets [19,20,21]. In addition to micronutrients and dietary fiber, diet-derived polyphenols have received tremendous attention for their health-promoting effects and chemopreventive benefits [22]. Green tea is a rich source of polyphenols from dried unfermented leaves of Camellia sinensis that contain diverse polyphenols and alkaloids with numerous health-promoting effects, including cancer chemoprevention [23,24,25]. However, data from earlier epidemiological studies and randomized control trials that assessed the impact of green tea intake on PCa risk have been inconclusive [26]. Another challenge with most of the earlier studies is that most of those studies were carried out in Asian populations characterized by a high intake of green tea, thus limiting the generalizability of the findings to other populations. Therefore, studies in other populations, such as in sub-Sahara Africans, are needed to assess the benefits or otherwise of green tea consumption on the aforementioned prostate cancer risk factors to assess the generalizability of the potential beneficial effects of green tea consumption. Considering the potential effects of BMI, atherogenic serum lipids and PSA levels on the risk of prostate cancer, this study investigated the associations between the consumption of green tea and BMI, serum lipid profile and serum PSA level dynamics in a sub-Saharan population.

Materials and methods

Study population, design and sample size

The study was a community-based one conducted at Ayigya Zango. This community of Muslims shares a common culture as a way of life. For example, dietary patterns, clothes, religion, educational level and occupation are just a few (supplementary dat Fig. 1 and Fig. 2b). The study employed an analytical cross-sectional observational survey method from April 2021 through April 2022. The sample size was determined via OpenEpi Info software (Open Source Epidemiologic Statistics for Public Health) version 3.01, which was developed by the Centre for Disease Control and Prevention (https://www.openepi.com/SampleSize/SSCC.htm). This online software calculates the sample size via the design effect, population size, estimated proportion and desired absolute precision. Systematic random sampling was used, where starting from 1, only odd-numbered individuals were selected as study participants. All even-numbered individuals were excluded from the study. Therefore, a design effect of 1 was used for estimating the sample size. The study used an estimated proportion of 50%, which is the default percentage when the researcher is unsure of the exact percentage of the population that will respond to the outcome variable and a desired absolute precision of 5%. The current population of the suburb (Ayigya Zango) stands at 48419 [27], and the national percentage of the adult population (above 18 years old) is 55.2%. On the basis of the latest national demographic statistics, the male population accounts for 49.87% of the total population. This resulted in an adult male population of 13,264 men in the suburb. The recommended minimum sample size was therefore 347 men. The formula used for calculating the sample size was as follows:

$$\begin{gathered}Sample\,size\,n\, = \,\left[ {DEEF*Np\left( {1 - p} \right)} \right] \hfill \\\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,\,/\left[ {\left( {{d^2}/{Z^2}_{1 - \alpha /2}*\left( {N - 1} \right) + p} \right.*\left( {1 - p} \right)} \right] \hfill \\ \end{gathered} $$

Population size (N): 13,264.

Hypothesized % frequency of the outcome factor in the population (p): 50%+/-5.

Confidence limits as % of 100(absolute +/- %)(d): 5%.

Design effect (for cluster surveys-DEFF): 1.

Confidence Level (%): 95%.

Sample size: 374.

Inclusion and exclusion criteria

The study population was defined as all male Ayigya residents aged 40 years or older (men at risk of PCa) [28] with no confirmed prostate cancer or disease of the prostate. In addition, men with a prior history of prostate surgery or urinary tract infection/obstruction within the past 12 months were also excluded. This was to eliminate a major confounder in the assessment of the serum PSA levels. Residents who drink green tea daily were recruited, and those who did not have a culture of drinking green tea were selected as controls for comparison.

Approximately 200 green tea-drinking (GTD) and 200 nontea-drinking (NTD) men who consented to be part of this study were recruited, after which a semistructured questionnaire was administered to obtain their sociodemographic information, health history, and green tea-drinking status. Both the GTD and NTD participants were stratified into 10-year age groups: 40–49, 50–59, 60–69, and 70 years and older (70+) [29]. The study was approved by the Committee on Human Research, Publication and Ethics of the Kwame Nkrumah University of Science and Technology, KNUST, Ghana (Ref: CHRPE/AP/151/21). All participants provided their informed consent to participate in the study after being informed of its design both orally and in writing.

Anthropometric measurements

All measurements were performed by the same operator who followed standard procedures. The subjects’ heights were measured during the selection phase to the nearest 0.5 cm with a stadiometer. After voiding and while wearing light clothing, each participant’s body weight was measured to the nearest 0.01 kg on a digital scale (Harson. Model H89). The body mass index of the participants was calculated using the formula BMI = weight (kg)/height ^2 (m) [30].

Biochemical analysis

Blood samples were collected from a peripheral vein early in the morning after at least a 12-h overnight fast. Total cholesterol (TC), triglyceride (TG) and high-density lipoprotein (HDL)-cholesterol (HDL-c) levels were measured via a MindRay BS230 Chemistry Analyzer (China). The low-density lipoprotein cholesterol (LDL-c) level was calculated according to the Friedewald et al. Equation [31]. The normal reference ranges used were as follows: TC < 5.2 mmol/L (200 mg/dL), HDL-c ˃ 1 mmol/L (40 mg/dL), LDL-c < 3.4 mmol/L (130 mg/dL), and TG < 1.7 mmol/L (150 mg/dL) [32, 33]. The total serum prostate-specific antigen (PSA) concentration was determined via the electrochemiluminescence method (Cobas e411 Analyzer, Roche Diagnostics, Germany).

Statistical analyses

The primary focus of the study was to assess the associations of green tea intake with BMI (normal/abnormal), lipid profile (normal or high) and serum PSA (normal or high). Descriptive statistics were generated by comparing data on measured biomarkers between the NTD and GTD groups using a t-test. The biomarker variables were further stratified into normal (equal to or less than the upper limits of normal) and abnormal (higher than normal): BMI, normal (18.5–24.9 kg/m²) or overweight (≥ 25 kg/m²), normal total cholesterol (TC) ˂ 5.2 (200 mg/dl) or high TC ˃ 5.2 (200 mg/dl), normal or high triglyceride (TG) ˃ 1.7 (150 mg/dl), normal or high low-density lipoprotein cholesterol (LDL-c) ˃ 3.4 mmol/ml and normal or low high-density lipoprotein cholesterol (HDL-c) ˂ 1 mmol/ml. Additionally, data on serum PSA were also stratified as normal (PSA ˂ 2.5 ng/ml) or elevated (PSA ˃ 2.5 ng/ml) [34]. The resulting data was analyzed using unconditional logistic regression to examine the associations between GTD and each biomarker measured. Finally, Pearson correlation was used to assess the correlation between measured biomarkers and serum PSA to estimate PCa risk between the NTD and GTD. The correlation coefficient, r, was calculated using a correlation bivariate test. All tests were performed using a critical significance level of 5%. Analyses were carried out using MS Excel and GraphPad Prism 5.0 (GraphPad, San Diego, CA, USA).

Results

Age distribution

A total of 415 eligible participants selected for this study were stratified into 10-year age groups: 40–49 years, 50–59 years, 60–69 years and 70 + years, based on the Age-specific PSA reference ranges [28, 35]. The mean ages were not significantly different between the GTD and NTD groups (Table 1).

BMI

Based on the WHO Expert committee recommendation on BMI, (i.e., normal weight, 18.5–24.9 kg/m²; overweight, 25–29.9 kg/m²; obesity, 30 kg/m² and above), the mean BMIs of GTD in all age groups were normal compared with those of the NTD groups (Table 1). Furthermore, we observed significantly lower odds for all the GTD groups to be overweight (or obese) than for the NTD subgroups (Table 2a–5d).

Lipid profile

Comparison of atherogenic lipids (triglycerides, total cholesterol and low-density lipoprotein cholesterol) between the GTD subgroup and NTD age-specific subgroup revealed significantly lower atherogenic lipids in the GTD subgroup than in the NTD subgroup (Table 1). Except for the 50–59-year-old group, which presented a significantly higher mean HDL-c in the GTD, there were no differences in HDL-c across the other groups (Table 1). Our association analysis revealed significantly lower odds of the GTD subgroup being hyperlipidemic than the NTD subgroup was (Table 2a–5d).

Prostate-Specific antigen

In this study, none of the age-specific subgroups presented serum PSA levels greater than 4 ng/ml, although the authors reported significantly lower mean serum PSA levels in the older GTD subgroups (60–69 and 70+) than in the NTD subgroups (Table 1). However, we noted a decreasing trend in the serum PSA levels in the GTD subgroup compared with those in the NTD 40–59 years subgroup, but the differences were not significant. This finding most likely suggests a differential response of prostate tissue to green tea polyphenols in the elderly population compared with the relatively younger adult population. Association analysis between green tea consumption and serum PSA levels revealed significantly lower odds of elevated serum PSA levels in the GTD older adult subgroup than in the respective NTD subgroup (Table 4c − 5d). Even though our subgroup analysis revealed a tendency toward reduced odds of having elevated serum PSA levels in the GTD group than in the NTD group, the associations were not significant.

Correlation of PSA with BMI and the serum lipid profile: Our subgroup analysis revealed a weak nonsignificant positive correlation between the serum PSA level and atherogenic serum lipid level in the NTD subgroup younger than 70 years. However, our study revealed significant positive correlations between atherogenic lipid TC and LDL-c levels and serum PSA levels within the 70 + year subgroup (Table 6a). Intriguingly, the analysis of serum PSA levels and nonatherogenic serum lipids (HDL-c) revealed a negative correlation, although it was not significant (Table 6a). Among the GTD subgroups younger than 70 + years, there were generally weak negative correlations between serum PSA levels and atherogenic serum lipids and positive correlations between serum PSA levels and HDL-c nonatherogenic lipids; only the 50–59-year subgroup was significant. However, in the GTD 70 + year group, although the analysis revealed a positive correlation between the serum PSA level and all the serum lipids, none of the correlations were statistically significant (Table 6a). Furthermore, when the data from all age-specific subgroups were pooled and correlation analysis was carried out, positive correlations between the serum PSA level and atherogenic lipids were detected in the NTD group. However, the association with TG was not significant (Table 6b). This result may suggest an increase in one’s PCa risk with increasing levels of serum atherogenic lipids. Our analysis of the pooled data revealed a negative correlation between the serum PSA level and the nonatherogenic lipid HDL-c, although the correlation was not significant (Table 7b). However, for the pooled data from the GTD group, the correlations between the serum PSA level and the serum lipid level were not significant.

Finally, our correlation analysis between serum PSA levels and body mass index (BMI) revealed a weak positive correlation between the two variables in both the NTD subgroup and the GTD 40–59 years subgroup. Nevertheless, the correlation between the serum PSA concentration and BMI in the 60–70 + year NTD subgroup was strongly positive, whereas that in the GTD 60–70 + subgroup was negative (Table 6a). These results may suggest a selective potential benefit of green tea intake in reversing the positive correlation between BMI and serum PSA levels in older nongreen tea-drinking men, i.e., a reduction in the potential risk of increased serum PSA in older men with higher BMIs who drink green tea.

Table 1 Comparisons of age, BMI, lipid profile and serum PSA between the study groups

Table 2 a. Analysis of association of obesity, dyslipidaemia and elevated PSA among GTD compared with NTD men aged 40–49 years

Table 3 b. Analysis of association of obesity, dyslipidaemia and elevated PSA among GTD compared with NTD men aged 50–59 years

Table 4 c. Analysis of association of obesity, dyslipidaemia and elevated PSA among GTD compared with NTD men aged 60–69 years

Table 5 d. Analysis of association of obesity, dyslipidaemia and elevated PSA among GTD compared with NTD men aged 70 years and older

Table 6 a. Analysis of the associations (correlations) between serum PSA levels and serum lipid profile and BMI among the GTD and NTD groups

Table 7 b. Pearson correlation between serum prostate-specific antigen and serum lipids (pooled data)

Discussion

To the best of our knowledge, this is the first study in a sub-Saharan African country to assess the associations of green tea intake with body mass index (BMI), the serum lipid profile, and serum prostate-specific antigen (PSA) levels in men. This analytical cross-sectional survey revealed that a greater proportion of the study participants who drink green tea (GTD) had a healthy body weight (normal BMI) and lower atherogenic lipids than did those in the nongreen tea drinking (NTD) group. This study also revealed generally lower serum PSA in the GTD group than in the NTD group. Nevertheless, this difference was significant in the older GTD adult subgroups (60–60 and 70 + years) compared with the NTD subgroup. The findings of this study agree with those of previous reports suggesting that green tea consumption reduces atherogenic serum lipids and improves BMI [36,37,38]. The mechanism behind the favorable associations of green tea intake with the serum lipid profile, BMI and serum PSA level remains to be fully elucidated; however, many reports have attributed the effects to the high content of catechins present in green tea [39]. One study attributed the antidyslipidemic mechanisms of green tea to its ability to reduce intestinal cholesterol absorption [40]. The predominant catechin in green tea, epigallocatechin gallate (EGCG), is reported to interfere with the biliary micelle system in the lumen of the intestine by forming insoluble coprecipitates of cholesterol and increasing the fecal excretion of cholesterol [41]. In addition, a decrease in hepatic production of cholesterol [42] and the modulation of LDL-c receptors in the liver have been reported as other mechanisms of green tea catechins [43]. Furthermore, additional studies have reported that the activation of adenosine monophosphate kinase by catechins in green tea inhibits adipocyte differentiation, suppresses the expression of lipogenic molecules and induces fatty acid oxidation [44].

The findings of this study indicate that not only is green tea consumption associated with reduced atherogenic serum lipids, especially in older adults, but it is also associated with healthy BMI among GTD patients compared with NTD patients. Overweight is defined as a body mass index (BMI) of ≥ 25 kg/m² [33], and in the past few decades, several studies have reported that a high BMI is a major risk factor for diabetes, cardiovascular diseases, and many forms of cancer, including PCa [45]. Earlier studies reported the antiobesogenic effects of green tea [46], although little is known about the exact underlying mechanism(s). Some studies have attributed the bioactives found in green tea to be responsible for alterations in the expression of genes involved in obesity [47]. In addition to the beneficial effects of green tea polyphenol-induced alterations in obesity-related gene expression, there are reports that green tea intake also regulates appetite and the absorption of calories (Huang et al., 2018). Additional reports indicate that green tea consumption increases fat oxidation and energy expenditure due to its high concentration of EGCG [48]. EGCG inhibits catechol-o-methyltransferase (COMT), an enzyme that degrades Norepinephrine. This consequently increases lipolysis and fat oxidation [49]. Taken together, the combination of reported mechanisms of green tea bioactive substances, whose action tends to reduce fat mass associated with obesity, could explain the observations of lower atherogenic serum lipids and healthy BMI among green tea-drinking men in this study.

The relationships among intake of green tea, serum lipids, BMI and prostate cancer risk remain complex. Although there are reports of direct inhibitory effects of the major catechin in green tea, EGCG, on androgen receptor signaling during PCa development [50, 51], a possible indirect effect of green tea catechins on PCa risk via the modulation of risk factors associated with PCa development, such as dyslipidemia and high BMI, could be a plausible alternative mechanism. Our findings on the associations of green tea consumption with improved serum lipids and healthy weight are supported by evidence from recent systematic reviews and meta-analyses on the effects of green tea intake on serum lipids and obesity [39]. Furthermore, the influence of dyslipidemia and obesity on increasing the risk of PCa and PCa progression is also supported by the work of David et al. [52], who reported that high serum atherogenic lipids reprograms prostate cell metabolism and accelerate disease progression by mimicking MYC overexpression in a mouse model. Thus, alteration of the lipid profile in favor of dyslipidemia might be associated with increased PCa risk. Therefore, the findings of our work suggest that the association of green tea with lower atherogenic lipids and improved BMI, most likely, translates into decreased PCa risk. Our conclusion is based on our observation of reduced mean PSA, a biomarker of the prostate, in the GTD group compared with the NTD group, especially in the older age groups. The decreased serum PSA levels in the GTD groups observed in this study are consistent with the findings of other studies [53, 54], which reported a strong association between green tea intake, reduced serum PSA and an actual reduction in the incidence and progression of PCa [55].

The authors of this study recognize some limitations of this study. Firstly, an obvious limitation of this study is that men with prostate cancer and benign prostate hyperplasia were not included to ascertain the actual associations of the studied variables in patients with these conditions.

Second, although the overall sample size was adequate, the subgrouping based on age-specific ranges for PSA interpretation resulted in small sample sizes for comparison. However, it should be noted that the age-specific PSA range subgroupings made the comparison and interpretation of results that focused on serum PSA dynamics meaningful. This is because the knowledge that PSA generally increases with age in people without prostate cancer has led to the consensus that the threshold above which a serum PSA level should be considered elevated should be made on the basis of the age range [28]. Thirdly, this study was unable to carry out a dietary pattern assessment of the participants. Even though Zango Muslims generally have a common dietary patterns, not carrying out a 24-hour dietary recall and determining the nutritional composition or nutrient loads of the study participants and factoring in the data analysis remains a notable limitation of the current study.

However, this study has demonstrated a link between green tea intake and improved body mass index, serum lipid profile, lower serum PSA levels, and possibly lower PCa risk, especially in older adult men in a sub-Saharan population. The insight from this study advances our understanding of the relationships between green tea intake and serum lipids, BMI and serum PSA levels.

Conclusions

This study revealed that the consumption of green tea was associated with reduced atherogenic serum lipids and improved BMI independent of age. Furthermore, green tea consumption was associated with reduced serum PSA in older adult men. Taken together, the results of this study revealed that green tea consumption had beneficial effects on improving the serum lipid profile, BMI, the vital index of prostate health, and the serum PSA level in a sub-Saharan population.