Participants percentage distribution.
\r\n\t
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Ismail is currently an Associate Professor and Chairman of the Department of Mechanical Engineering, Lakehead University, Thunder Bay, Ontario, Canada. In 2004, Prof. Ismail earned his Ph.D. degree in Mechanical Engineering from McMaster University, Hamilton, Ontario, Canada. From 2004 to 2005, he worked as a Postdoctoral researcher at McMaster University. His specialty is in engineering heat transfer, engineering thermodynamics, and energy conversion and storage engineering. Dr. Ismail’s research activities are theoretical and applied in nature. Currently, his research areas of interest are focused on green engineering technologies related to alternative and renewable energy systems for power generation, heating and cooling. Dr. Ismail was the leading research investigator in a collaborative project (2007-2010) with Goldcorp-Musselwhite Canada Ltd. and Engineering of Lakehead University. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"68869",title:"Metformin in Cervical Cancer: Metabolic Reprogramming",doi:"10.5772/intechopen.88930",slug:"metformin-in-cervical-cancer-metabolic-reprogramming",body:'The malignant transformation results in a specific rearrangement of metabolic processes called metabolic reprogramming of tumor cell. The altered metabolism causes a selective advantage to a transformed cell by facilitating its survival in a harsh environment and promoting the spread of tumor cells within the body.
Malignant cells very effectively adapt to high proliferation rate, metastasis, and invasion. Several molecular mechanisms were pointed out to drive such metabolic adaptation of cancer cells. The critical aspects of metabolic reprogramming in tumor cells substantially contribute to the Warburg effect [1], an increased catabolism of glucose to lactate in the presence of oxygen [2]. The altered metabolism of tumors results in elevated biosynthesis of macromolecules such as proteins, carbohydrates, and lipids and, in consequence, supports high proliferation rate of malignant cells [3].
In particular, the regulation of mitochondrial processes in cancer cells differs from normal counterparts, and it may be specific to the stage of tumor [4]. Therefore, cancer cells are sensitive to drugs that disrupt energy homeostasis, such as Metformin (1,1-dimethylbiguanide, Met) [5].
A generic drug, Metformin, has been widely used for treatment of diabetes mellitus in humans. However, it exerts pleiotropic effect in human organism. In particular, a great interest has been paid to Met, since retrospective analyses demonstrated that it significantly decreased the relative risk of cancer incidence in diabetic patients when compared with patients treated with other drugs. Clinical trials confirmed the epidemiological observations that Met exerted anticancer effects in humans [6]. It has been established that Met inhibits proliferation of various neoplastic cell lines in vitro, including breast, prostatic, colon, gastric, and cervical cancers [7, 8]. Currently, there is an intense ongoing research focused on molecular mechanisms behind these effects, since the implications of Met action in tumor cell are not completely understood [9].
To date, several molecular mechanisms were reported to play critical role in anticancer activity of Met. In particular, it was established that Met may affect energy metabolism of cancer cells by inhibition of complex I of mitochondrial electron transport chain (ETC) in mitochondria, which results in adenosine-5′-triphosphate (ATP) depletion and remodeling of the network of biosynthetic processes within the cell [9]. Met may act as an anticancer drug through the activation of the main energy regulator within the cell, adenosine 5′-monophosphate (AMP)-activated protein kinase (AMPK) [7], and inhibition of mechanistic target of rapamycin complex-1 (mTORC1) [10] in tumor cells. Some of the pharmacological effects of Met seem to be independent of its action on glycemia homeostasis. Several reports demonstrated that treatment of tumor cells with Met results in cell cycle perturbations and apoptosis [11, 12]. The intracellular targets affected by Met were comprehensively reviewed by Ikhlas and Ahmad [9] and Pierotti et al. [13].
Along with the advent of human papillomavirus (HPV) vaccines, the primary prevention of cervical cancer has become more successful, but cervical malignancy still remains the significant cause of cancer mortality in women worldwide. Currently, chemotherapy using cytostatic drugs (mainly cisplatin, cis-dichlorodiammineplatinum (II)) is still the primal regimen, despite low specificity and substantial toxicity in patients [14].
Aerobic glycolysis has been recognized as the most common metabolic feature of malignant cells. The alterations in metabolism of cancer cells combined with the overexpression of oncogenes (c-Myc) and transcription factors (hypoxia-inducible factor 1a, HIF 1a) confer a great advantage to malignant cells to avoid apoptosis induced by reactive oxygen species (ROS). In this study we focused on the effects of Met on metabolism of metastatic cervical tumor cells. Based on recent data, we reported that Met inhibited glycolytic phenotype of aggressive cervical cancer cells by regulation of expression of oncogenes and their downstream proteins, which led to cellular death. Furthermore, Met regulated mitochondrial metabolism, especially via supplementation of tricarboxylic acid cycle (TCA cycle, Krebs cycle) with pyruvate and glutamine. Met, by targeting epithelial and mesenchymal markers of tumor cells, alleviated invasive properties of cervical cancer cells.
This review summarizes recent findings on Met and cervical cancer underscoring new implications of this drug in regulation of peculiar metabolism of tumor cells. We discuss new perspectives about targeting specific alterations in cervical tumor metabolic pathways using Met.
A growing evidence suggests that the screening for molecular targets for anticancer therapeutic treatments should take into account the existing differences in tumor cell phenotypes. Therefore, the metabolic effects exerted by Met were studied using SiHa cells (American Type Culture Collection, ATCC designation HTB-35) originating from aggressive cervical tumor, which acquired malignant characteristics [15]. The regulation of apoptosis pathways in HTB-35 (SiHa) cells highly reflects the specificity of cervical tumor in vivo [16]. HTB-35 cells, even unstimulated with cytokines, have mesenchymal-like characteristics, especially high vimentin expression, along with enhancement of cell scattering and ability to move [17]. Another cell line, C-4I cells (ATCC, designation CRL1594) with epithelial phenotype, was derived from primary in situ tumor [18]. HTB-34 cells (ATCC designation MS751) were isolated from metastatic site in lymph node [19]. HTB-35, C-4I and HTB-34 are human squamous cell cervical carcinoma lines and it is worth noting that squamous cell cancer is the most common cervical cancer and accounts for almost 80% of cervical carcinomas in patients [14]. HeLa human cervical cancer cells (ATCC designation CCL2), which have been extensively used in mechanistic studies, expressed epithelial traits and were derived from adenocarcinoma [8].
The reliance on glucose supply is linked to the aggressiveness of malignant cells. Such reprogrammed metabolism makes migrating cancer cells more robust and independent of environmental conditions. The dysregulation of glucose metabolism is caused by alterations in functioning of several oncogenes. Malignant cells may gain metabolic plasticity by upregulation of only few oncogenes, such as c-Myc, p53, phosphoinositide 3-kinase (PI3K) and the mammalian target of rapamycin (mTOR) [20]. Additionally, the activation of transcription factors, such as HIF-1α, makes malignant cells more resistant to hypoxia (decreased oxygen level in microenvironment), which is one of the main factors affecting tumor growth [20]. The activation of HIF-1α is one of the crucial processes that promote glycolysis to generate ATP along with the decrease of mitochondrial pathways’ activity in aggressive tumors. What is more, the migrating tumor cells may avoid oxidative stress by relying on glucose catabolism. As a result, tumor cells have higher chance to survive detachment from extracellular matrix (ECM), whereas normal cells undergo programmed death due to anoikis in the absence of attachment to ECM [21]. Following detachment from primary tumor bed and transportation to plasma and lymph, malignant cells may spread within the body and form secondary tumors. Therefore, the reprogrammed metabolism plays a crucial role in facilitating tumor metastasis.
We found that Met may regulate glycolysis in aggressive cervical cancer cells. The glycolytic phenotype of tumor cells is triggered mainly by a master regulator HIF-1α and its downstream proteins. Our study showed that Met alleviated the hypoxia-induced activation of HIF-1α, which was followed by decreased expression of HIF-1α downstream protein effectors in HTB-35 cells, as demonstrated in [22]. In particular, Met downregulated GLUT transporters (solute carrier family 2 member receptors, SLC2A), specifically GLUT1 and GLUT3. Additionally, Met inhibited the regulatory enzymes of the glycolytic pathway, hexokinase 2 (HK2), bifunctional enzyme 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 4 (PFKFB4), pyruvate kinase (PKM), and lactate dehydrogenase (LDH) (Figure 1). Met exerted greater effect on regulatory proteins in HTB-35 cells exposed to decreased oxygen level in the air than normal conditions.
Metformin inhibits glycolytic phenotype of cervical carcinoma cells (↑—activation, Ⱶ—inhibition) [11, 12, 21, 22].
Recent studies have reported that overexpression of c-Myc oncogene plays a significant role in the formation of cervical cancer. The enhanced expression of c-Myc is also of particular relevance to promoting invasive phenotype of cancer cells. What is more, the upregulated c-Myc may collaborate with HIF to effectively induce glucose and glutamine consumption in tumor cells. As a result, mitochondrial oxidative phosphorylation decreases. In particular, the upregulated c-Myc enhances glutamine catabolism in tumor cells, since the oncogene controls glutaminase (GLS) expression [23]. As measured using qPCR analysis, Met decreased c-MYC transcript level in HTB-35 cells [22], which was in compliance with inhibition of GLS protein expression [11]. The treatment of cervical tumor cells with Met decreased mRNA level for another c-Myc downstream protein, CCND1 (cyclin D1), which regulates cell cycle progression [22]. Zhang et al. [24] reported that Met caused a substantial decrease of cyclin D1 expression in bladder cancer cells. The overexpression of oncogene cyclin D1 is positively correlated with chemotherapeutic resistance and apoptosis avoidance in squamous cell cancers [23]. The inhibition of CCND1 expression in aggressive cervical tumor cells resulted in enhanced apoptosis [22].
Met triggered another pro-apoptotic mechanism in cervical carcinoma cells via regulation of Bcl-2 (B-cell lymphoma 2) protein family members’ expression [22]. Bcl-2 proteins are key players in the regulation of mitochondrial-dependent programmed cell death. The activation of BAX protein leads to disruption of mitochondrial membrane potential and apoptosis, whereas Bcl-2 acts as an apoptotic suppressor. The counterbalancing pro- and anti-apoptotic effectors of Bcl-2 protein family play a crucial role in the regulation of the mitochondrial apoptotic cascade within the cell and constitute another important apoptotic checkpoint [25]. However, the disturbance of BAX/Bcl-2 pathway may result in the resistance to apoptosis by inducing compensatory mechanisms, thereby influencing the efficacy of some therapeutic regimens [26]. The exposition of cervical tumor cells to Met significantly upregulated BAX transcript. It was found that the expression of BAX under hypoxic conditions was greater than in normoxia [22]. Additionally, Met downregulated transcript for BCL-2 in HTB-35 cells in both, normoxic and hypoxic conditions.
The study using cervical cancer cells with metastatic phenotype cells showed that the downregulation of oncogenes/downstream regulatory proteins, together with the upregulation of pro-apoptotic BAX/Bcl-2, elucidated mitochondrial-dependent apoptosis in tumor cells. The obtained data suggest that Met was highly effective in facilitating cell death in cervical tumor cells [22], since it exerted its effect targeting independent events controlling mitochondrial apoptosis including the induction of ROS [11], the regulation of Bcl-2 protein family expression, and downregulation of cyclin D1. It should be emphasized that Met induced cell death solely in tumor cells, without causing detrimental effects to normal cells [11].
The reprogrammed metabolism of tumor cells not only meets high energetic demands but also provides intermediates for intensive proliferation. Therefore, glycolysis and mitochondrial oxidative phosphorylation may operate simultaneously in cancer cells. Many tumors may even switch between these pathways accordingly to the current requirements. Recent studies showed that most cancer cells have metabolically efficient mitochondria to provide intermediates for biosynthesis, generate reductive power (nicotinamide adenine dinucleotide phosphate, NADPH), and restore cofactor pool (e.g., nicotinamide adenine dinucleotide, NADH). In highly proliferating cancer cells, mitochondrial TCA cycle is active enough to sustain the biochemical reactions. Currently, the precise regulation of anabolic pathways and keeping their activities at adequate level is thought to play a key role in determination of “flexible” metabolic phenotype of cancer cells that enables their rapid division. Moreover, oxidative phosphorylation (OXPHOS) may represent a significant contribution to energy generation within malignant cell. On the other hand, inevitable products of OXPHOS are ROS and oxidative stress due to ROS overproduction may kill tumor cells [27].
It was demonstrated that the process of detachment of migrating squamous cancer cells from extracellular matrix (ECM) results in reprogramed metabolism toward glycolysis, particularly by PDH complex inhibition and following suppression of glucose respiration in mitochondria. Such metabolic phenotype of tumor cell enables efficient production of energy without excessive ROS generation. On the other hand, the stimulation of PDH activity may lead to increased anoikis sensitivity and attenuation of metastatic potential of cancer cells [28].
We found that Met may precisely regulate PDH metabolic checkpoint in cervical tumor cells (Figure 2). Met had great potency to activate oxidative decarboxylation of pyruvate to acetyl-CoA in HTB-35 cells expressing invasive phenotype, and it occurred via activation of PDH complex [11]. PDH complex plays a determinant role in the overall glucose disposal within the cell, since it funnels mitochondrial TCA cycle instead of lactate formation in cytosol. PDH activity is precisely regulated via covalent modification by the action of specific enzyme pyruvate dehydrogenase kinase (PDK). Several PDK activators were found to expand potent antitumor effect, also in cervical tumor HeLa cells [29]. We showed in aggressive cervical cancer HTB-35 cells that Met suppressed both PDK activity and the expression of gene encoding tumor-specific isoenzyme PDK1 [22]. This finding may have practical implications, since the screening strategy for PDK inhibitors should recognize the specificity among the PDK isoenzymes in order to avoid side effects in vivo [30]. Under hypoxic conditions inside tumors, the activation of HIF-1α decreases mitochondrial metabolism, which prevents the cell from oxidative stress and helps cancer cells avoid apoptosis [20, 23]. Our study showed that in aggressive cervical cancer cells Met counteracted these metabolic alterations by inhibiting PDK1, which is at the same time HIF-1α prime downstream effector. Furthermore, Met downregulated PDK1 gene expression also in normoxia [22].
Metformin regulates mitochondrial metabolism of cervical carcinoma cells (↑—activation, Ⱶ—inhibition) [11, 13, 22, 27, 30].
In tumor cells that have functional mitochondria, the generation of oxidative stress may become an important therapeutic target [27, 30]. The imbalance of metabolic regulation and the resulting overproduction of ROS in mitochondrial ETC cause oxidative stress, which, at some point, becomes toxic to cancer cells, and that escalation of ROS elicits apoptosis-inducing factors and triggers death program through multiple mechanisms. In compliance, it has been newly reported that Met significantly increased ROS level, altered apoptosis-associated signaling, and induced cell death in human gastric adenocarcinoma cells [31] and human cervical cancer HeLa cells [32]. We found that in HTB-35 cervical cancer cells, Met caused excessive generation of mitochondrial ROS and elicited apoptosis [11, 22]. As shown in [22], the effect of Met was specific to tumor cells, and the formation of mitochondrial ROS was not affected in normal cells exposed to Met.
Met concomitantly targeted cytosolic glycolysis and mitochondrial pathways in HTB-35 cells, which increased apoptosis and suppressed survival of cervical tumor cells under normoxic and hypoxic conditions [22].
Glutamine may provide precursors to feed TCA cycle under limited flux of pyruvate from cytosolic glycolysis within tumor cells. The facilitated use of glutamine is a significant metabolic adaptation of cancer cell, besides enhanced glucose catabolism, and it provides intermediates sufficient for intensive biosynthesis and energy production [20]. Glutaminase (GLS) is a key regulator of glutamine entry to TCA [33], and the inhibition of the enzyme may suppress tumor cell growth [25].
As shown in [11], the exposition of cervical cancer cells with invasive phenotype to Met downregulated the expression of GLS, thereby protecting mitochondrial anabolism from additional carbon supply for synthesis of macromolecules. Additionally, the effect of Met on GLS expression was specific toward cervical cancer cells, and in normal cells drug did not change the expression of the enzyme [11].
Glutamine entry to tumor cell not only improves carbon supply for macromolecules buildup, but it also replenishes the pool of cellular NADPH, since the conversion of malate to pyruvate catalyzed by malic enzyme 1 (ME1) is accompanied by the reduction of NADP+ (Figure 2). NADPH is used for biosynthesis, but it also plays a significant role in the antioxidant protection of tumor cell by reducing glutathione molecule. Met downregulated expression of ME1 and alleviated generation of NADPH in cells, which, in conditions of limited supplementation of HTB-35 cells with glucose (suppressed expression of GLUTs), resulted in hampering of biosynthesis and alleviation of ROS detoxification [11, 22].
Furthermore, Met treatment caused acute drop in ATP concentration in HTB-35 cells. This is in compliance with data obtained by Parker et al. [34] who demonstrated that non-small cell lung cancer (NSCLC) cells may be uniquely sensitized to metabolic stresses by the action of other biguanide, phenformin (1-(diaminomethylidene)-2-(2-phenylethyl)guanidine). The inhibition of ATP generation may block biosynthesis in cervical tumor cells which results in restraining of cell proliferation.
The facilitated fatty acid (FA) de novo synthesis together with upregulated glycolysis was recognized as one of the prime metabolic alterations in such tumor cells [35]. The enhanced FA biosynthesis meets high demands of rapidly proliferating malignant cells (generating components for cell membranes and signaling molecules). We found that Met decreased unsaturated lipid content in aggressive cervical cancer cells (Figure 2). The mechanism of Met action included downregulation of regulatory enzyme elongase 6 (ELOVL6), which catalyzes elongation of fatty acid molecule. Met also suppressed stearoyl-CoA desaturase (SCD1), which controls desaturation of FA. It was shown by Fritz et al. [36] that pharmacologic inhibition of SCD1 activity impaired unsaturated FA synthesis, which resulted in decreased proliferation of both androgen-sensitive and androgen-resistant prostate cancer cells. The treatment of cervical cancer cell lines [22, 37] with Met decreased cervical tumor cell proliferation, but Met did not affect the growth of normal cells [11].
Emerging data indicate that the enhanced activity of enzymes regulating lipid de novo synthesis may contribute to activation of EMT process in tumor cells [36]. The activation of EMT program in epithelial cancer cells facilitates tumor progression, invasion, and metastasis. It has been shown in independent studies that Met inhibits EMT in various cancer cell lines [8, 37]. Recently, it has been reported that Met reversed EMT phenotype induced with transforming growth factor beta 1 (TGF-β1) in breast, lung, and cervical cancer cells by targeting the mechanisms regulating the expression of E-cadherin. The exposition of tumor cells to Met resulted in suppression of their metastatic properties [8, 38].
In our study, EMT process was induced upon 48 h incubation of cervical cancer cells with 10 ng/mL of cytokine TGF-β1, as described in detail in [17]. HTB-35 cells, even unstimulated, expressed mesenchymal-like characteristics, and the incubation with TGF-β further enforced expression of mesenchymal marker, vimentin, along with enhancement of cell scattering and ability to move [17]. The study showed that Met was an effective suppressor of mesenchymal phenotype and, in particular, downregulated vimentin in HTB-35 cells (Figure 3). Recently, it was reported by Laskov et al. [39] that Met downregulated the expression of vimentin in endometrial cancers in vitro and in vivo in diabetic patients. The incubation of cervical cancer cell lines with Met reduced cells’ ability to move, as shown using functional scratch test in C4-I and HTB-35 cells stimulated with TGF-β1 [17]. Mechanistic study revealed that Met inhibited the expression of transcription factors Snail-1, ZEB-1, and Twist-1. These mesenchymal markers facilitate EMT progress in cervical cancer cells.
Metformin inhibits TGF-β1-induced EMT phenotype of cervical carcinoma cells (↑—activation, Ⱶ—inhibition) [8, 17, 40].
Cheng and Hao [8] proposed another mechanism of Met action in cervical carcinoma cells via inhibition of mTOR/p70s6k signaling pathway and downregulation of glycolytic regulatory protein pyruvate kinase, isozyme M2 (PKM2), in HeLa cell line.
In order to clarify the molecular action of Met in cervical tumor cells with aggressive characteristics, the effect of the drug was tested in the hypoxic conditions. In cervical cancers, hypoxia and concomitant enhanced lactate formation result in acidification of microenvironment, which may promote the ability of metastatic cells to rapidly spread in tissue [41]. In such conditions, the activation of HIF1α induces its downstream protein carbonic anhydrase IX (CAIX). By regulation of tumor milieu pH, CAIX acts as a survival factor protecting malignant cells against enhanced acidification of microenvironment. As a result, lactate damages adjacent normal cells and does not harm tumor cells [42]. Due to its relevant role in cell invasion, CAIX was proposed as a potential therapeutic target, also in cervical cancers [41, 42]. We showed that the exposition of HTB-35 cells to Met under hypoxia suppressed HIF-1α, which resulted in decreased transcription of CAIX gene, thereby alleviating invasive properties of cervical malignant cells [17].
Recently, numerous beneficial activities of Met were reported. Met was shown to improve cardiovascular outcomes in humans [43], and the ability of Met to extend life-span in mammals has attracted great attention [44]. Emerging data indicate that Met may be applied as adjuvant in therapies aiming at combating diseases with high mortality rate, also in cervical cancer [45]. The clinical benefits of the use of Met in gynecologic oncology in humans were reviewed by Irie et al. [46] and Imai et al. [47]. Met also reduced the incidence of endometrial tumors and improved survival of patients with diagnosed local or advanced endometrial cancer [48]. Several clinical trials showed the potential of Met to elicit apoptosis in the uterus and prostate cancers in humans [49].
The potential pathological effects of Met have been well studied in long term in human population. One of the most undesirable effects in the context of peculiar metabolic alterations of cancer cell is the enhanced generation of lactic acid caused by biguanides. In fact, the application of phenformin (1-(diaminomethylidene)-2-(2-phenylethyl)guanidine) was associated with a much higher risk of lactic acidosis in patients, than Metformin. Therefore, the former drug was withdrawn from clinical use. Currently, the contraindication for the use of Met in patients is renal failure, since this group has greater risk of lactic acidosis. However, the concerns over lactic acidosis were shown to be largely unfounded, unless kidney disease was advanced. Yet, based on the recent data, Met can be safely used in patients with mild renal dysfunction, provided that patients are monitored appropriately [43, 50].
The exposition of aggressive cervical cancer cells to Met restrained the function of HIF-1α master regulator and downregulated HIF-1α downstream glycolytic genes. Met also downregulated glycolytic phenotype of HTB-35 cells through inhibition of oncogene c-MYC expression, which resulted in impairment of metabolic plasticity of cervical tumor cells, especially via downregulation of GLS.
Met precisely regulated PDH and GLS metabolic checkpoints in cervical tumor cells. In particular, in tumor cells Met targeted supplementation of mitochondrial pathways in pyruvate by downregulation of PDK1 gene expression and decreasing PDK activity. As a result, Met effectively enhanced TCA cycle flux in normoxic and hypoxic conditions. The downregulation of GLS and ME1 resulted in decreased regeneration of NADPH, the factor essential both for biosynthesis and cell protection against oxidative stress. The metabolic alterations of mitochondrial pathways caused by Met caused excessive generation of ROS which led to apoptosis. In cervical cancer cells, Met additionally induced apoptosis via upregulation of pro-apoptotic BAX protein expression and by downregulation of cyclin D1, oncogene c-MYC downstream protein. Met exerted its pro-apoptotic effect both in normal and decreased oxygen availability. This aspect of Met action may be important when designing anticancer therapies targeting cells in hypoxic milieu inside solid tumors.
It is also important to highlight another cellular mechanism of Met action, namely, the suppression of EMT process in cervical tumor cells. EMT seems implicated into invasiveness and metastasis of cancer, and Met was able to inhibit EMT pathways. In cervical tumor cells stimulated with TGF-β1 as well as in unstimulated ones, Met decreased the expression of the main mesenchymal marker vimentin and reduced motility of cells. In addition, Met downregulated adaptive enzyme CAIX in tumor cells under hypoxia. CAIX promoted migration of malignant cells and acted as an important survival factor, and thus it has recently been proposed as therapeutic target in cervical cancers. Met might be considered as a potential factor targeting CAIX to hamper cervical tumor invasiveness.
These findings provide a new insight into regulation of glycolysis and mitochondrial pathways in cervical tumor cells using nontoxic and well-studied drug, Metformin, indicating the future prospect about utilization of this molecule in clinical oncological routine. The identification and targeting of specific alterations in tumor metabolic pathways may constitute a sole basis to design new precise therapeutic strategies in cervical malignancy. To date, very few innovative therapies against cervical malignancy are being tested in clinical trials; thus more specific and effective intervention is highly required.
The artworks were prepared using elements from Servier Medical Art.
Human hygiene is considered as one of the most effective ways of preventing diseases, and germs. Center for diseases control and prevention (CDC) associated many diseases and sicknesses to poor body hygiene [1, 2]. One key body part that requires constant and continuous hygiene to prevent human infection from germs and diseases is hands. In 2004, one of the US FDA studies revealed that food establishments were frequently out of compliance with the food code requirements for proper and adequate handwashing. In the study, the percentage of food establishments observed to be out of compliance with handwashing requirements ranged from 34% in hospitals to 73% in full-service establishments [3]. Our world today faces alarming rates of diseases related to hygiene and the quick spread of germs via contact of improper hand hygiene. According to the CDC [4], it is established that keeping hands clean is one of the most important steps to avoid sickness and spreading of germs and diseases to others. Hand hygiene is the most effective measure for interrupting the transmission of microorganisms, which cause infection both in the community and in the healthcare setting. Therefore, using epidemiology model, transmission of diseases and germs through poor hand hygiene practices could be reduced in the society. The use of restrooms and other everyday activities regularly expose a human to germs; therefore, the need to explore other factors surrounding handwashing for hygiene purposes is essential.
The knowledge of handwashing as a measure of hand and personal hygiene is not new, as it has been successfully transferred from generations to generations. Handwashing has been linked to culture and religion, see Staub [5]. The United States of America officially recommended that healthcare workers (HCWs) should wash their hands with soap for 1–2 min before and after patient contact, see Coppage [6]. In 1975, CDC released handwashing guidelines and practice in the healthcare (hospitals) and later modified the original version in 1985 [7, 8]. Research has revealed that the revised CDC handwashing guideline has been expanded for better practice in all organizations [9, 10, 11].
While we can say training people on the handwashing routine is important and it has helped improving hand hygiene practice, the attention to hand hygiene in health and safety should go beyond educating people commonly known in the healthcare industry. According to Jang et al. [12], healthcare workers’ workload, other job interruptions, and overly conservative guidelines make it difficult to adhere to hand hygiene. The same authors concluded that it is imperative to study other factors on proper handwashing practice to make handwashing hygiene a lifestyle other than a routine. The process of hand hygiene could be regarded as cumbersome and demanding for many people due to workload and other conditions like availability of toiletries, environmental and structural conditions. It is no doubt that many people know that hand hygiene what is the most effective measure to prevent microbial pathogen cross-transmission and other healthcare-associated infections but wasn’t enough to get people to do it and practice the routine that leads to good handwashing practice. World Health Organization (WHO) reported that several continuous evaluations and good team methodologies have helped compliance but are yet to sustain in specific critical communities and healthcare areas [13]. The study further shows that mentoring aside other handwashing routines could be an excellent way to make hand hygiene a lifestyle.
Experts have proven that hand hygiene is the most effective measure for interrupting the transmission of microorganisms, which cause infection both in the community and in the healthcare setting. Using hand hygiene as a training measure of reducing disease is unlikely to be successful when other factors in infection control, such as environmental hygiene, crowding, staffing levels, and education, are inadequate. Therefore, the way people use restrooms and regularly exposed to germs in everyday activities makes it essential to explore other factors surrounding handwashing that could encourage hand and body hygiene in general.
The lack of appropriate infrastructure, religious beliefs, and workplace conditions were the major influencers on the low compliance to handwashing hygiene among the health professionals [14, 15, 16]. It is about time to start focusing on the influencers on low complaint rates.
About 1.8 million children under the age of 5 die due to diarrhea and pneumonia every year [17]. Diarrhea and pneumonia are the top two killers among children all over the world [17]. The same study showed how handwashing is the most effective way to prevent people in the world from dying through diseases and much other life-threatening conditions from hand contamination. Handwashing with soap has a strong capability to protect and shield about one out of every three young children who get sick with diarrhea [18, 19], and practically one out of five young children with respiratory infections like pneumonia [19]. Another research shows handwashing in educational institutions and access to water and soap in schools could improve student health [20, 21]. Children’s exposure to proper handwashing from early life might help to improve their development in some settings [22]. If hand washing could affect children around the world this much, then, proper handwashing should be included in all organization culture.
If hand hygiene can be included in daily human behavior, it automatically becomes a lifestyle and not just a routine, because humans can tire of routine with time, but a lifestyle is part of human behavior that cannot be easily broken. In 2005, Jumaa highlighted areas needed for further research on proper handwashing, which include environmental conditions, people acts etc. and further concluded that cultural and behavioral issues also contributed to the poor practice of hand hygiene. This study investigated other factors influencing public’s poor handwashing habits, suggested better restroom designs, and provided recommendations for improvement.
Objectives of the study
Develop a questionnaire that captures public opinion on the use of public restrooms or school restrooms.
Propose a better design structure based on survey feedback and design of prototype.
Evaluate prototype from user perception.
This study was conducted in a university environment. The university is in Hammond and Westville, Northwest Indiana US. Data were collected through survey. The survey was a self-developed questionnaire adapted from a standardized resource online. Survey was reviewed by three experts, two health practitioners, and one safety specialist to validate the contents for the purpose of the research. The questions were presented in the form of Likert scale options. The IRB office of the university where the study was conducted approved the protocol before survey distribution. The survey was distributed via email to all students, faculty, and all the university employees. Four hundred and twenty-seven (427) participants, including 246 students, 109 university employees, and 72 faculty, participated in the study. Participants include 147 males, 270 females, and 9 people who preferred not to indicate their gender. All the participants took the same survey with the same preferences given to all. The research was divided into three parts. The first part is the questionnaire, research on appropriate solutions and redesign for appropriateness. The survey questions focused on the toilet’s settings, design, user habit, and toiletries availability.
Data compilation was done with the use of Excel® version 365 ProPlus. The use, cleanliness, structure, and factors that affect handwashing practices were evaluated using simple descriptive statistics and inferential statistics (Welch T-tests). Descriptive statistics was used to assess the differences in the proportions of participants reporting specific handwashing practices by gender. At the beginning of the analysis, the data were checked for normality. As expected, the percentage who had used the college restrooms one time or more was found to be 100% (out of which 35% were male, 64% female, and 2% preferred not to say). Table 1 details the frequency distribution of the participants in percentage. Analysis shows that the percentage of those who used the restrooms always was the highest with 71% compared with those who sometimes or rarely used the restroom, that is, 14%.
Level | Responses | |
---|---|---|
Gender | Male | 35% |
Female | 63% | |
Prefer not to say | 2% | |
Category | Student | 58% |
Faculty | 17% | |
University employee | 25% | |
Age | 18–25 | 40% |
25–30 | 8% | |
30+ | 52% |
Participants percentage distribution.
The percentage of those who are comfortable using the school restroom was 44% based on different levels of comfortability while the percentage of those who are rarely or not comfortable is 34%. About 88% of the participants reported to always wash their hands after the use of restrooms. Approximately 99% agreed to have seen someone at some point walking out of the restroom without washing their hands, 85% strongly agreed that hand and body hygiene is paramount after the use of public and private restrooms. Furthermore, 72% strongly agreed that proper handwashing will prevent one from many diseases and sicknesses, 22% agreed to some degree while only 3% somewhat disagreed. In another question, participants were asked if they have received any form of hand hygiene training in the last 3 years. The responses show that 50% had received different forms of training in the last 3 years. The use of alcohol-based hand rub for hand hygiene also shows about 67% at different level of agreement.
Only 215 participants responded to the open-ended question, the responses showed 48.8% strongly suggested restroom redesign to improve hand hygiene and reduce germs transmission. Approximately 14% believe that automated hand-sanitizer machines should be installed in the restrooms. Further, only 3% of the participants responded that the inclusion of handwashing training as part of the school curriculum and regular cleaning of the university community restrooms would improve hygiene practices.
Survey questions were divided into two categories, the first part focused on individual hand hygiene and the second part focused on restroom restructure or redesign for health safety purposes of the community. Figure 1 is the graphical representation that shows the significances of some major factors that could potentially affect college restrooms and handwashing hygiene among college students:
Graphical representations of survey responses.
The purpose of this study is to investigate factors influencing poor handwashing practices in the community, especially among the younger generation. These days, poor handwashing practices and inadequate body hygiene have been attributed to different illnesses around the world and have increasingly expanded the spreading of the present pandemic case called COVID-19. Therefore, the results of this study could be instrumental to promote good handwashing practices. Promotion of good handwashing will prevent viral infection and reduce exponential chances of spreading any illness outbreak. Handwashing hygiene should be taken beyond restrooms, but also to prevent viral infections, especially those that spread through droplets from coughs and sneezes. In this situation, proper handwashing is the first line of measure.
Four survey questions that specifically addressed restroom redesign and restructure were separately analyzed using descriptive and inferential statistics (Welch T-test). Participants’ responses on the question “Do you think public restrooms should be structured and well designed for Heath safety?” were analyzed. The participants that neither agreed nor disagreed (in-between) were eliminated in order to define the significance of those that agreed or disagreed. The number of people in this category was found to be 10, constituting 2% of the total participants. Group 1 was considered people who disagreed and group 2 as people who agreed with restroom redesign.
Table 2 shows that only two participants disagreed to the opinion that public restrooms on campus should be restructured and well redesigned for health safety of the users, while 416 agreed to the opinion that university community restrooms should be restructured and redesigned for health safety (Table 3).
Categories | Participants’ answer |
---|---|
Disagree | 2 |
Neither nor | 9 |
Agree | 416 |
Total | 427 |
Participants response to question 4.
Groups | Categories | Response | Percentage % |
---|---|---|---|
G1 | Disagreed | 2 | 0.5 |
G2 | Agreed | 416 | 99.5 |
Total | 418 |
Participants’ response to question 4 in percentages.
G1 = Group 1; G2 = Group 2.
Based on the descriptive analysis of the user’s opinion, it is concluded that restrooms should be redesigned for health safety. Figure 2 reveals the relationship between the participants that agreed and disagreed that restrooms’ redesign would improve the health safety of the users.
Graphical representation of participants’ response to question 4.
Questions 3, 6, and 12 were analyzed using Welch t-test to further determine the significance of redesigning and restructuring university community restrooms for health safety. As shown in Table 4, participants’ response to question 3 reveals (t = 1.967903, df = 300; p < 0.0001) to question 6 (t = 1.99006, df = 80; p < 0.0001) and to question 12 (t = 1.97462, df = 163; p < 0.0001).
Summary of the Welch unpaired T-test.
From the participant’s opinions, visual and auditory alerts will be necessary for most of the public restrooms to enhance user’s awareness of handwashing after use.
Redesign of most restrooms was another issue raised by the respondents if proper hygiene levels must be reached for safety purposes.
Automated handwashing devices like an automated sink with soap dispenser, auto sensor water, and hand sanitizer pump dispenser were also recommended to be made available.
A redesign of the restroom doors to be touchless (auto open and close) without touch or ergonomical design (i.e., pull to go in and push to exit) as the participants felt that touching might increase the chances of contacting germs.
A high percentage of the participants also believe that the current hand dryer is unhealthy, breeds germs, and is against proper hygiene and health safety.
Respondents also mention the inclusion of hygiene training into college’s education curriculums in all levels of education.
Ergonomically redesign doors/restroom system was suggested in order to fit the operating process of the restroom to the users’ capability. This could be perfect as stated in Fasanya and Shofoluwe’s [23] finding that fitting job to worker capability improved worker performances.
After a careful review of the findings, it is decided that the inclusion of auditory and visual alert sensor in the urinal bowl area and toilet compartment will improve the handwashing practice.
The visual and auditory alerting signals will assist in reminding restroom users to wash their hands after use. Visual and auditory alerts have been known for being vital reminders of activity in different areas of life such as in traffic control (transportation industry). Visual and alert methods have also played important roles in many other situations relating to alerting and reminding users. It has been used in the airplane for almost everything possible, especially in alerting, reminding, and giving the passengers directions when needed. According Papastavrou and Lehto [24], visual and auditory alerts help in the detection of anticipated stimuli. This study suggested for the design shown in Figure 3 to ensure proper reliabilities and the alerts required for the safe use of the restrooms. The design is a computer-based script that senses restroom flush and gently nudges and reminds the users to wash their hands. The process involves the following.
Message display.
It involves designing a computer screen algorithm that will help to auto-sense sides. The machine design can be achieved by using C# combined with light and sound using sensor fusion with computer vision to sense flushing sound and press of restroom flushes. Figure 3 also shows the sample of visual message that would be displayed on the screen.
This device is an auditory and visual alert device coded with C# and with a motion and sound sensor to sense either the motion or flush sound before displaying a message as shown in Figure 3.
The visual and auditory alert system design would be placed in two locations as shown in the Figure 4—the device with the “Message Area” caption here is a LED Message display board designed and computer coded for auditory and visual alert for the users at the sound of restroom flush. The device should be a computer coded with the passive infrared (PIR) sensor to sense and detect body heat (infrared energy) and the most widely used motion sensor, at the sound of the flush. Pleasant messages are to be included in the alert to remind the users to wash their hands: messages like “Do you know handwashing hygiene increases health safety? Don’t forget to wash your hands? Washing Hands prevents from deadly diseases, etc.” The application that controls the device is suggested to be designed with C# and designed with LED message display board and passive infrared sensor. It is important for it to be both visual and auditory to accommodate visually or aurally challenged individuals.
Restroom message display design.
Findings from this study had led the university management to include in all restrooms hand soap dispensers and gradually work on how to restructure the rooms to be ergonomically fit for the users. From the management comments, less attention has been given to restroom designs of all things in the academic environment. Meanwhile, the outcome of this study has proved that less important things in management perspective might be a huge factor to promote health and safety of both students and the employees.
Different studies have concluded that there are other factors affecting hand hygiene behavior. For example, Zimakoff et al. [25] concluded by identifying few other factors affecting hand hygiene such as skin irritation and dryness as the leading factors affecting handwashing in health care. The same authors affirmed that there are other possible factors not covered in the scope of the research. Likewise, in 1982, Larson and Killien concluded that it is imperative to identify factors that are the antecedents to whether the individual decides to wash one’s hands or not as they are critical in the prevention or intervention plans to improve handwashing practice. The same authors further ascertained that most emphases are placed on the importance of handwashing instead of other factors affecting people’s behavior toward handwashing compliance. The results of this study supported that there are other factors different from training people and showing people how to practice hygiene properly. Researchers are now focusing on the growing literature about the other factors affecting hand hygiene behavior.
Day by day, researchers are focusing on other factors that could affect hand hygiene behavior, none or few have looked into the structure and redesign of restrooms. This study investigated the people’s experience in the restroom, why handwashing compliance is low, and other factors, which could affect hand hygiene behavior. A significant proportion of the participants requested for restroom redesign for their health safety. A significant finding from this study is that about 83% of the participants suggested alert systems to remind restroom users to wash hands after use. The participants also reported the significance of other factors like an automated sink, soap dispenser, water dispenser, dryer devices as well as ergonomically designed doors. The participants unanimously believe that ergonomically designed door (pull and push type) would reduce touch and greatly enhance health safety. The above data results reflect restroom equipment, structure, cleanliness, and comfortability have significant effects on hand hygiene behavior. The results from this study supported other researchers who found that there are other factors affecting hand hygiene behavior, rather than just training and those factors should be focused on in order to improve handwashing practices.
The handwashing procedure is a little monotonous, especially for healthcare professionals, and can be frustrating or become things of no interest when relevant factors are not available and very challenging in different ramifications. The low compliance of handwashing is a significant issue around the world as reported in several literatures. Appropriate handwashing practices can reduce the risk of foodborne illness and prevent transmission of viral infections, especially those that spread through droplets from coughs and sneezes. Besides, among many other hygiene practices, poor handwashing is the most common practice among the younger generation. The message and the information about handwashing or hand hygiene has been around for over 200 years, yet the level of compliance is low as revealed from this study. Thus, this study details another factor affecting handwashing hygiene after the use of public restrooms and suggests how hand hygiene could be improved in human daily behavior. The findings of this study revealed that restroom designs and structures have significant effects on hand hygiene behavior based on participant’s opinions from the survey. Redesign to include visual and auditory alerts will be necessary for most of the public restrooms to enhance user’s awareness for handwashing after use. Findings from this study suggest for a restroom redesign to include auto-sensor soap and water dispenser, dryers, and touchless doors. Findings further revealed that inclusion of hygiene training in all college’s education curriculums at every level would encourage user’s handwashing hygiene lifestyle and behavior. The findings from this study could help identify the design structures for ensuring more compliance with handwashing hygiene and health safety practice among the public. Further research is needed in this direction to investigate how other factors aside from the aforementioned could potentially discourage individuals from making hand hygiene a daily behavior.
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