Building a Biopsychosocial Conceptual Framework to Explore Pressure Ulcer Pain for Hospitalized Patients

Although pressure ulcers are a prevalent condition, pain associated with pressure ulcers is not fully understood. Indeed, previous studies do not shed light on the association between pressure ulcer stages and the experience of pain. Especially, pain characteristics of suspected deep tissue injury, which is a new category that was recently added by the National Pressure Ulcer Advisory Panel, are yet unknown. This is concerning because the incidence of pressure ulcers in hospitalized patients has increased exponentially over the last two decades, and health care providers are struggling to ensure providing adequate care. Thus, in order to facilitate the development of effective interventions, this paper presents a conceptual framework to explore pressure ulcer pain in hospitalized patients. The concepts were derived from a biopsychosocial model of pain, and the relationships among each concept were identified through a literature review. Major propositions are presented based on the proposed conceptual framework, which integrates previous research on pressure ulcer pain, to ultimately improve understanding of pain in hospitalized patients with pressure ulcers.


Introduction
Pressure ulcers are a significant and highly prevalent health care problem in the United States, especially among hospitalized patients. The number of hospitalizations related to pressure ulcers has increased by 86.4% between 1993 and 2008. Moreover, pressure ulcers affected 503,300 hospitalized patients and cost more than $11 billion in 2006 alone [1]. The incidence of hospital acquired pressure ulcers was 4.5% between 2006 and 2007 [2], and the costs of hospitalization for Stage III and IV pressure ulcers was $43,180 per case [3].
In response to the incidence and rising costs, in 2008 the Centers for Medicare and Medicaid Services (CMS) identified advanced pressure ulcers acquired during hospitalization as preventable conditions, rendering hospitals unable to receive Medicare payments or private insurance reimbursement for the care of patients with advanced stages of pressure ulcers [4]. As a result of this policy, the Agency for Healthcare Research and Quality estimated a 23% decrease in hospital acquired pressure ulcers from 2011 to 2014, which led to a savings of approximately $5,270,000,000 as well as a 22,444 death reduction in hospitals [5]. Despite decreasing incidence and costs of hospital acquired pressure ulcers, this improvement reflects only a short term period.
According to statistics from the National Center for Health Statistics (NCHS) posted by the Center for Disease Control and Prevention (CDC), 159,000 nursing home residents in the United States have pressure ulcers, which is approximately 11% of the total nursing home population [6]. Many of these pressure ulcers go untreated. In fact, in patients with a Stage II or higher pressure ulcer, only 34% of ulcers and provide a conceptual framework to promote the development of therapeutic interventions to decrease pain in populations with pressure ulcers.

Method
In order to develop a conceptual framework to explain pain experiences in patients with pressure ulcers, we first identified relevant concepts and the relationships among the concepts through an extensive literature review. Next, we conducted an extensive literature search for theories with relevant concepts and selected a parent model. Finally, we established relationships between concepts and the parent theory, and modified the parent model to build the theoretical framework.
Concepts were identified from the literature review that explain pain phenomena. Literature was searched in CINAHL and PubMed using the key word "pain" along with the words "physical", "psychological", "cultural", and "pressure ulcers". The inclusion criteria were peer reviewed articles published before 2015 in English. The identified concepts were labeled as meanings under related constructs. The methods supported the aim of the conceptual framework: (1) to describe pain experiences related to pressure ulcers; (2) to explain the predictors and moderators of pain experiences based on existing evidence; and (3) to predict pain characteristics in patients with different stages/categories of pressure ulcers [24]. Several conceptual models which were able to explain pressure ulcer pain were found: the gate theory [25], the nociceptive theory [26], the pain assessment model [27], the lens model [28], and the biopsychosocial model of pain [29]. After reviewing related literature, the biopsychosocial model of pain [29] was chosen as the parent conceptual model. The parent model was selected based on meaning, logical adequacy, usefulness, generality, parsimony, and testability [24].
The biopsychosocial model of pain was chosen because it contains the most relevant concepts to explain pressure ulcer pain. Indeed, it depicts pain as a unique, individual experience, and a consequence of complex, biopsychosocial interactions. The three main constructs of the biopsychosocial model of pain are: (1) biological factors such as tissue damage, genetic factors, and endogenous pain inhibition; (2) sociocultural factors such as ethnicity, family history, and cultural factors; and (3) psychological factors such as anxiety, depression, coping strategies, and social learning ( Figure 1). The diagram explains individual variability in pain perception and experiences as a consequence of interactions among the variables. After selecting the parent model, we revised the biopsychosocial model of pain by adding environmental factors (e.g., nurse/patient ratio, nurse educational level, frequency/type of wound dressing) and modifying psychological factors (i.e., we added anger, stress, sleep, fatigue and catastrophizing, and withdrew social learning), biological factors (i.e., we added comorbidity, inflammation, infection, and age, and withdrew tissue damage) and social cultural factors (i.e., we added discrimination and social support, and withdrew family history and cultural factors).
Healthcare 2016, 4, 7 3 of 17 pressure ulcers and provide a conceptual framework to promote the development of therapeutic interventions to decrease pain in populations with pressure ulcers.

Method
In order to develop a conceptual framework to explain pain experiences in patients with pressure ulcers, we first identified relevant concepts and the relationships among the concepts through an extensive literature review. Next, we conducted an extensive literature search for theories with relevant concepts and selected a parent model. Finally, we established relationships between concepts and the parent theory, and modified the parent model to build the theoretical framework.
Concepts were identified from the literature review that explain pain phenomena. Literature was searched in CINAHL and PubMed using the key word "pain" along with the words "physical", "psychological", "cultural", and "pressure ulcers". The inclusion criteria were peer reviewed articles published before 2015 in English. The identified concepts were labeled as meanings under related constructs. The methods supported the aim of the conceptual framework: (1) to describe pain experiences related to pressure ulcers; (2) to explain the predictors and moderators of pain experiences based on existing evidence; and (3) to predict pain characteristics in patients with different stages/categories of pressure ulcers [24]. Several conceptual models which were able to explain pressure ulcer pain were found: the gate theory [25], the nociceptive theory [26], the pain assessment model [27], the lens model [28], and the biopsychosocial model of pain [29]. After reviewing related literature, the biopsychosocial model of pain [29] was chosen as the parent conceptual model. The parent model was selected based on meaning, logical adequacy, usefulness, generality, parsimony, and testability [24].
The biopsychosocial model of pain was chosen because it contains the most relevant concepts to explain pressure ulcer pain. Indeed, it depicts pain as a unique, individual experience, and a consequence of complex, biopsychosocial interactions. The three main constructs of the biopsychosocial model of pain are: (1) biological factors such as tissue damage, genetic factors, and endogenous pain inhibition; (2) sociocultural factors such as ethnicity, family history, and cultural factors; and (3) psychological factors such as anxiety, depression, coping strategies, and social learning ( Figure 1). The diagram explains individual variability in pain perception and experiences as a consequence of interactions among the variables. After selecting the parent model, we revised the biopsychosocial model of pain by adding environmental factors (e.g., nurse/patient ratio, nurse educational level, frequency/type of wound dressing) and modifying psychological factors (i.e., we added anger, stress, sleep, fatigue and catastrophizing, and withdrew social learning), biological factors (i.e., we added comorbidity, inflammation, infection, and age, and withdrew tissue damage) and social cultural factors (i.e., we added discrimination and social support, and withdrew family history and cultural factors).

Results
Concepts of pain experiences and the relationships between concepts were derived from the biopsychosocial model of pain. The key concepts of the proposed conceptual framework are pressure ulcer stages/categories as inputs and pain experiences as an outcome. Other concepts are sociocultural, psychological, and biological factors, which may moderate the pain associated with pressure ulcers. Similarly, environmental factors have been added because the target population is hospitalized patients.
The proposed conceptual framework contains the following concepts ( Figure 2): (1) pressure ulcer stages/categories as inputs; (2) pain experiences as an outcome; (3) comorbidities, genetic factors, endogenous pain inhibition, inflammation, infection, and age as biological factors; (4) ethnicity, discrimination, and social support as sociocultural factors; (5) anxiety, depression, anger, stress, sleep, fatigue, catastrophizing, and coping strategies as psychological factors; and (6) nurse/patient ratio, nurse educational level, and frequency/type of wound dressing as environmental factors. The definitions of these concepts are summarized in Table 1. The detailed discussion of the empirical indicators is beyond the scope of this paper. This paper is focused on the presentation and relationships among concepts.

Results
Concepts of pain experiences and the relationships between concepts were derived from the biopsychosocial model of pain. The key concepts of the proposed conceptual framework are pressure ulcer stages/categories as inputs and pain experiences as an outcome. Other concepts are sociocultural, psychological, and biological factors, which may moderate the pain associated with pressure ulcers. Similarly, environmental factors have been added because the target population is hospitalized patients.
The proposed conceptual framework contains the following concepts ( Figure 2): (1) pressure ulcer stages/categories as inputs; (2) pain experiences as an outcome; (3) comorbidities, genetic factors, endogenous pain inhibition, inflammation, infection, and age as biological factors; (4) ethnicity, discrimination, and social support as sociocultural factors; (5) anxiety, depression, anger, stress, sleep, fatigue, catastrophizing, and coping strategies as psychological factors; and (6) nurse/patient ratio, nurse educational level, and frequency/type of wound dressing as environmental factors. The definitions of these concepts are summarized in Table 1. The detailed discussion of the empirical indicators is beyond the scope of this paper. This paper is focused on the presentation and relationships among concepts.

Pain Quality, Intensity, and Sensitivity
Pain is an unpleasant sensory and emotional experience evoked by tissue damage [30]. It is an outcome variable in the proposed conceptual framework, which uses pain quality, intensity, and sensitivity to measure pain phenomena in patients with pressure ulcers. In 2011, Gorecki and colleagues [17] stated that descriptions of pressure ulcer pain vary according to pressure ulcer stages: "tender" and "burning" are used to describe all stages of pressure ulcers; "sore" is used to describe Stages II and III; "stinging" is used to describe Stages II and IV; and "stabbing" is used to describe Stages III and IV. Similarly, Girouard and colleagues [18] and others described pressure ulcer pain as a burning sensation, and stated that patients with pressure ulcers experience various levels of pain from pressure ulcers [9,10,19,20]. Experimental pain sensitivity using quantitative sensory testing (QST) is used often to study patients with pain; however, QST has not been frequently used in studies about pressure ulcer pain. QST may be a useful way to measure pain hypersensitivity caused by central sensitization in patients with pressure ulcers [19]. Thus, in order to describe individual pain experiences related to pressure ulcers, future studies are recommended to include detailed measurements of pain. This conceptual framework gives clear and comprehensive understanding of pain related to pressure ulcers. Thus it will facilitate research for measurement of pain in pressure ulcer population.

Sociocultural Factors
Sociocultural factors, such as ethnicity, discrimination, and social support, influence pain [31]. Ethnicity, which refers to discrete groups of people with similar behaviors, culture, and biophysical characteristics [32], is one of the sociocultural contextual factors that influence an individual's health-related beliefs and behaviors [33]. Indeed, studies have shown that pain responses vary across ethnic groups and that racial and ethnic minorities have higher experimental pain sensitivity and clinical pain intensity compared to Caucasians [34][35][36].
Another sociocultural factor, discrimination, refers to unfair or different treatment based on membership in a group [37]. In the clinical setting, health care providers may discriminate against patients by prescribing treatments based on ethnic group stereotypes. For example, in their literature review, Garbez and Puntillo [38] reported that inappropriate pain management may be related to demographic factors such as age, gender, and ethnicity. Significantly, Black patients were 31% less likely to receive opioids compared to Caucasian patients (odds ratio (OR) = 0.69, p < 0.001) among 18 million ED visits during 2003 to 2006 [39]. In a similar study that included 153,891 patients in the emergency department, Pletcher and colleagues [40] reported that white patients are more likely to receive opioids than black, Hispanic, and Asian patients (adjusted odds ratio [OR] 0.66, 0.69, and 0.79 respectively).
The last sociocultural factor, social support, refers to the availability of resources from others who are connected by social networks to an individual [41]. Lee and colleagues [42] suggested that social support may buffer pain among the elderly who have chronic pain symptoms; this is because elderly patients with higher social support reported lower pain (regression coefficient (β) =´0.04, p < 0.05) in a study that included 299 participants in a retirement community in central Florida. Similarly, Takai and colleagues [43] reported social support is an effective long term strategy with pharmacotherapy and physical activity for the management of chronic pain. Finally, Ferreira and Sherman [44] described that social support affected pain (r =´0.28, p < 0.05) among 72 older adults with chronic pain [44].
Based on the above findings, sociocultural factors have significant influences on pain experiences. Health care providers should be aware of individual ethnicity and consider available social support and possible discrimination in healthcare when they manage pain in pressure ulcer population.

Biological Factors
Biological factors (e.g., comorbidity, genetic factors, endogenous pain inhibition, inflammation, infection, and age) influence pain. Comorbidity is defined as "two or more coexisting medical conditions or unrelated disease processes" [45]. Indeed, among a half million hospitalized patients with pressure ulcers in 2006, 90% of adults were hospitalized for treatment of other primary conditions, rather than treatment for pressure ulcers [1]. Onubogu [46] found that a higher number of comorbidities was significantly correlated with more severe bodily pain (r = 0.13, p = 0.001) in 1592 community-dwelling older adults with chronic pain. In a study that included 29,132 participants with chronic pain, Caporali and colleagues [47] reported that pain was significantly worse (p < 0.0001) when patients had two or more comorbidities. Comorbidity interferes with the pain experience in pressure ulcer population. It decreases pain perception or intensifies pain. It is difficult to differentiate the origin of pain in hospitalized patients. Therefore, healthcare providers should approach pain associated with pressure ulcers as a complex experience.
Currently, pain research involving genomics suggests that genes may affect pain a patient's experience of pain [48]. Indeed, emerging evidence suggests that genetic factors are related to pain experiences. For example, the catechol-O-methyltransferase gene (COMT) and mu-opioid receptor gene (OPRM1) may be associated with pain-induced mu-opioid receptor binding [49], experimental pain sensitivity [50,51], and risk of developing chronic pain [52].
Individual differences in endogenous pain inhibition are assumed to provide a plausible mechanistic predictor of pain experiences. For example, Bruehl and colleagues [53] found that individual differences in endogenous opioid inhibition of chronic pain were associated with the magnitude of acute reductions in pain ratings after pain medication administration. Gene and endogenous pain inhibition is highly individualized and cannot be generalized. Gene and endogenous pain inhibition support importance of customized pain management. Healthcare providers should always apply specific patients' needs when managing pain in the pressure ulcer population.
Another biological factor, inflammation, may influence pain [54]. Indeed, several studies reported that inflammation mediators (e.g., cytokines) are closely involved with and regulate the pain process. Inflammation is defined as "the protective response of body tissue to irritation or injury" [45]. For example, in a study that included 32 participants, Starkweather and colleagues [55] reported that women with chronic pain had a higher level of C-Reactive Protein (p < 0.01), interleukin-13 (p < 0.02), and interleukin-7 (p < 0.02) than women having no pain. Similarly, the literature review by DeVon and colleagues [56] reported that higher levels of proinflammatory markers (e.g., C-reactive protein, tumor necrosis factor-alpha, interleukins) were associated with greater pain.
Infection is defined as the invasion of the body by pathogenic microorganisms that reproduce and multiply, causing disease by local cellular injury, secretion of a toxin, or antigen-antibody reaction in the host [45]. Infection occurs when microorganisms invade the host tissue, causing injury to cells and host immunological reactions that defeat the host's defensive mechanisms [57]. In a study with 44 participants with post burn, Juozapaviciene and colleagues [58] reported that patients with wound infections in the acute hospitalization period experienced chronic wound pain (p = 0.03). Tengvall and colleagues [59] reported that the severity of infection was significantly related to pain intensity (p < 0.01). Healthcare providers should consider infection or inflammation affects not only pressure ulcer wound but also pain experience.
Age is closely related to incidence of pressure ulcers. Older patients tend to have a higher incidence of pressure ulcers [60,61]. Among the 6.2 million ED admissions per year, elderly patients were at a higher risk of developing pressure ulcers [62]. For example, in one study by Baumgarten and colleagues [63], researchers found that elderly patients admitted to the emergency department had a significantly higher incidence of pressure ulcers (6.2% among 3233 elderly patients who were over age 62). To explain these findings, Jaul and colleagues [64] analyzed factors such as dementia (OR = 3.0, p < 0.002), urinary catheter usage (OR = 2.25, p < 0.03), low body mass index (OR = 0.92, p < 0.02), and anemia (OR = 0.7, p < 0.004) to determine if they were associated with pressure ulcer incidence in the elderly. Pressure ulcers are also prevalent in hospitalized children ages 0 to 18 (35% (N = 412)), with Stage I being the most common (54%), especially in pediatric patients who use external medical devices (40%) [65]. Kottner and colleagues [66] reported varied prevalence of pressure ulcers (between 2% and 28%) in pediatric patients who use medical devices. According to these reports, elderly and pediatrics who were hospitalized may have high incidence of pressure ulcers and experience higher level of pain related to pressure ulcers. Health care providers should have more consideration about preventive care of pressure ulcers when providing care to elderly and pediatrics.
Age also affects experiences related to pain. In one study, older adults were perceived as being more sensitive to pain than middle-aged adults (p < 0.001) and younger adults (p = 0.00) [67]. In response to stimuli of pressure pain, the elderly were shown to have lower pain thresholds [68,69]. Therefore, pain perception varies according to age groups. Lillie and colleagues [70] have reported that pain is under assessed or undertreated in older adults. In a study by Ahn et al. (2015), age was able to predict pain intensity in a population with pressure ulcers (OR = 0.97, p < 0.001) [19]. However, Baharestani and colleagues [71] reported a lack of tools to assess pressure ulcer pain in the neonatal or pediatric population. Collectively, these studies reveal that pain may be inadequately managed in certain age groups. According to the above characteristics of the elderly, their pain level may be expressed lower than their actual pain. Therefore, health care providers should consider age specific characteristics when they manage pain in the pressure ulcer population.

Psychosocial Factors
Pain phenomena are affected by psychological status, stress, sleep, fatigue, catastrophizing, and individual coping styles. Gorecki and colleagues [17] stated that anticipating pain may lead to negative moods, emotions, and anxiety in patients, and that these emotions influence the experiences of pain in patients with pressure ulcers. Anxiety is defined as the "anticipation of impending danger and dread accompanied by restlessness, tension, tachycardia, and breathing difficulty not associated with an apparent stimulus" [45]. In a qualitative study regarding quality of life among patients with pressure ulcers, Gorecki and colleagues [17] described how patients with pressure ulcers experienced emotional distress and anxiety related to their wounds. Similarly, Smeijers and colleagues [72] reported a strong association between anxiety and pain. Indeed, patients with high anxiety levels were more likely to experience pain than controls (OR = 3.09, 95% confidence interval [CI]: 1.52-6.27, p = 0.002) even after adjusting for demographic factors among 1279 participants [72].
Depression is "a condition of loss of interest or pleasure in life activities" that leads to "significant impairment in social, work, or other important areas of functioning" [73]. Depression has been studied for several decades as a predictor of pain and a factor that contributes to increased pain. Zakoscielna and Pamrmelee [74] explored predictors of pain variability, and found that more severe baseline depression was related to higher pain variability (β = 0.308, p < 0.02). In addition, Ligthart and colleagues [75] reported that depression was strongly associated with more frequent pain and multiple pain sites in 11,787 twin adults.
Several studies found that anger is a strong predictor of pain. Anger refers to "an emotional reaction characterized by extreme displeasure, rage, indignation or hostility" [45]. A literature review by Bruehl and colleagues [76] reported that participants who responded more angrily to pain stimuli had higher levels of chronic pain. In addition, van Middendorp and colleagues [77] reported that people who responded angrily to an event experienced more severe pain (β =´0.09, p < 0.001) in a study of 333 women with chronic pain over a period of 28 days.
Stress refers to any stimulus or event that evokes a physiologic stress response [78]. Psychosocial stress plays an important role as a predictor of pain [79,80]. The study of Osteras and colleagues [81] determined a strong association between pain intensity and stress (r = 0.40, p < 0.01; OR = 1.68, 95% CI: 1.42-1.99) among young people. Hannibal and Bishop [78] reported that exposing chronic physiologic stressors to patients may prolong their pain experiences. Hospitalization causes emotional and physical crisis. Anxiety, stress, and anger are common in hospitalized patients. According to above findings, emotional crisis along with physical crisis may often magnify their pain experience. Emotional crisis influences pain in a similar manner in the hospitalized pressure ulcer population.
Sleep is closely related to pain outcomes. Sleep is defined as "a state marked by reduced consciousness, diminished activity of skeletal muscles, and depressed metabolism" [45]. Sivertsen and colleagues [82] found that insomnia significantly increased the risk of reduced experimental pain tolerance in 10,412 participants. Insomnia often reduced cold pressor pain tolerance (hazard ratio (HR) = 1.52, 1.39, and 1.24 when insomnia occurred once a week, weekly and monthly respectively) [82]. Smith and colleagues [83] discussed that continuous sleep disturbance increased pain and reduced endogenous pain inhibitors among 32 healthy females. Schuh-Hofer and colleagues [84] reported that sleep disturbance increased sensitivity to heat stimuli (p < 0.05), blunt pressure stimuli (p < 0.05), cold stimuli (p < 0.01), and pinprick stimuli (p < 0.05) in 14 healthy participants. Schrimpf and colleagues [85] reported that sleep deprivation increased pain perception (p = 0.015) among 266 healthy participants through meta-analysis.
Fatigue is "a nonspecific, common subjective feeling of low vitality that disrupts daily functioning" [86]. The relationship between pain and fatigue has been explored in many studies. Pain and fatigue were strongly related (p < 0.05) in a population of 250 elderly people with chronic pain [87]. Sturgeon and colleagues [88] described fatigue as a significant factor that increased pain among a chronic pain population of 2487. Van Dartel and colleagues [89] reported that pain and fatigue had a significant positive relationship (β = 2.04, p < 0.0001) in 198 patients with chronic pain. Creavin and colleagues [90] investigated the co-occurrence of pain and fatigue, and found that 60% of the 451 participants with chronic pain reported persistent fatigue. In addition, these researchers found that 33% of the 809 participants with persistent fatigue reported chronic pain among 2447 community dwelling Dutch adults. Hospitalized patients commonly experience sleep deprivation and fatigue due to 24 h ongoing care. Sleep and fatigue are closely related to each other. Above findings support that sleep deprivation and fatigue may intensify pain experiences in hospitalized pressure ulcer population.
Catastrophizing is defined as "a negative cognitive and affective process involving magnification of pain-related symptoms, helplessness, pessimism, and rumination about pain" [91]. Quartana and colleagues [92] reported that pain catastrophizing has a significant influence short and long term adverse outcomes of pain. Indeed, it alters the hypothalamic pituitary response, magnifies the activity of the neural region, and decreases endogenous pain inhibition [92]. In addition, using multivariate regression analyses in 59 patients undergoing the treatment of pain, George and Hirsh [93] reported that pain catastrophizing affects pain intensity (β = 0.43, p < 0.01) [93].
Coping refers to the cognitive and behavioral adjustments that an individual uses to confront and manage health and daily-life stressors [94]. An individual's coping strategy is a significant factor in the regulation of pain perception. Moore and colleagues [95] conducted a study to compare pain tolerance between participants who used either acceptance or distraction as a coping method. Their findings suggested that acceptance was associated with better pain tolerance than distraction (t(13) = 2.18, p < 0.05) [95]. Rejeh and colleagues [96] explored relaxation as an effective technique to decrease pain (t =´4.68, p = 0.004) in a study of 124 participants over age 65 undergoing surgery. According to above findings, individual pain experiences vary depending on the coping toward their situation. Hospitalization is certainly a crisis for the patients and family. Pressure ulcers are chronic condition and require longer medical treatments. Therefore, coping and catastrophizing may have significant influence in pressure ulcer population and their pain experience.

Environmental Factors
Nurses play an important role in the prevention and treatment of pressure ulcers and any related pain. In one study by Park and colleagues (2014), researchers examined the relationship between staffing and hospital acquired pressure ulcers, and found that increased registered nurse (RN) staffing was associated with a lower rate of pressure ulcers (OR = 0.952-0.950, p < 0.011), using the national database of nursing quality indicators from 2008 to 2010 [97]. Their findings were supported by a study by Choi and Staggs [98] that RN-perceived staffing adequacy was significantly associated with unit acquired pressure ulcers (odds = 0.782, 95% CI: 0.647-0.944) in the 57,223 National Database of Nursing Quality Indicators (NDNQI) RN Survey in 2011.
Similarly, Castle and Anderson (2011) reported relationships between staffing variables and quality measures in 2839 nursing homes from 2003 to 2007. Results showed that an increase in RN staffing was related to a decrease in pressure ulcers (´0.46, p < 0.001) and improved pain management (´0.53, p < 0.05) [99]. These findings indicate that patients' mobility, activity, and perfusion are facilitated by nurses during hospitalization. In the systematic review of Coleman and colleagues [100] reported that adequate mobility, activity, and perfusion may prevent the development of pressure ulcers. Based on these reports, it is clear that nurses play an important role in the prevention of pressure ulcers and the provision of appropriate pain management in hospitalized patients. Therefore, the nurse/patient ratio should be regarded as one of the environmental factors that affects pain experiences in hospitalized patients with pressure ulcers.
Nurse education and quality of care have been demonstrated to affect the management of pressure ulcers. For example, Aydin and Karadag [101] reported that the educational background of nurses (p < 0.004) significantly influenced the prevention and management of sDTI and Stage I pressure ulcers among 243 nurses in Ankara and Turkey. Similarly, Pancorbo-Hidalogo and colleagues [102] reported that knowledge of prevention intervention (p < 0.001) and treatment intervention (p < 0.001) was greater in RNs with a university degree than in LPNs among 740 nurses in Spain. Based on these reports, it is clear that nurse education level is an environmental factor that can affect the pain experiences of hospitalized patients with pressure ulcers.
During hospitalization, patients may experience pain as a result of pressure ulcer wound treatments and dressings. For example, the negative pressure vacuum assisted system, which is used to treat pressure ulcers, may cause pain [103], as well as wound debridement and cleansing [104]. During treatments such as dressing changes or interventions, patients may experience varying levels of pain [12]. Pieper and colleagues [11] reported that dressing changes cause severe pain and their frequency affects the overall comfort level of patients. Woo and Sibbald [104] also reported that dressing changes aggravate pain in local wounds. Thus, frequency and type of pressure ulcer dressing changes should be included as an environmental factor for hospitalized populations.
In summary, the proposed conceptual framework derived from the biopsychosocial model explains pain in pressure ulcers. Biological, psychological, sociocultural, and environmental factors influence the experience of pain. Possible components in each factor are identified by the literature review for this conceptual framework.

Major Propositions of the Proposed Conceptual Framework
The concepts presented in the proposed model are connected by relational statements. The proposed conceptual framework enables the investigation of concepts using appropriate empirical indicators and provides systematic knowledge of pain phenomena. Several possible hypotheses from the proposed conceptual framework include:

‚
If other predictors are controlled, pressure ulcer stages/categories will be significantly associated with pain experiences.
‚ Sociocultural factors, including ethnicity, discrimination, and social support, will moderate pain experiences associated with pressure ulcers.
‚ Psychological factors, including anxiety, depression, anger, stress, sleep, fatigue, catastrophizing, and coping strategies, will moderate pain experiences associated with pressure ulcers.
‚ Environmental factors, including nurse/patients ratio, nurse educational level and frequency/type of dressing changes, will moderate pain experiences associated with pressure ulcers in hospitalized patients.

‚
These biological, sociocultural, psychological, and environmental factors are assumed to combine in a sequence to influence pain experiences with pressure ulcers.

Discussion
The proposed conceptual framework, adapted from the biopsychosocial model of pain, uses a multidimensional approach to include possible moderators that influence pain experiences in patients with pressure ulcers. This proposed conceptual framework explains pain phenomena in pressure ulcers in detail. In addition, a future study using this proposed conceptual framework will present empirical evidence that explains the clear association between pain experiences and pressure ulcer stages/categories. The proposed conceptual framework contains factors that affect the pain experiences of hospitalized patients with pressure ulcers. This framework will help health care providers determine the best intervention to prevent, manage, and treat pain related to pressure ulcers. Furthermore, the proposed conceptual framework may be modified to apply to other chronic pain populations as well.
The parent model, which is the "biopsychosocial model of pain", depicts a bidirectional relationship among the biological, sociocultural, and psychological factors that influence pain. This model uses a multidimensional approach to explain the complexity and variability of pain experiences. It describes pain as a result of complex processes of biopsychosocial interactions. However, it is difficult to define how much these factors may affect pain experiences associated with pressure ulcers. The proposed conceptual framework tries to explain how each factor influences pain experiences associated with pressure ulcers using a linear structure. In addition, environmental factors aimed at hospitalized patients were added to the proposed conceptual framework, which describes a more clear relationship between pain experiences and other concepts related to pressure ulcers in hospitalized patients. The framework also presents possible modifying factors that may contribute to a decrease in pain experiences for this population.
Gorecki and colleagues [17] presented a model that explains how pressure ulcer pain affects a patient's daily life and how the management of pain is influenced by communication through qualitative and quantitative systematic review. The model presented by Gorecki and colleagues suggested a biopsychosocial approach to pressure ulcer pain and improvements in communication with patients for effective pain management. Our proposed conceptual framework is consistent with their model in terms of how pressure ulcer pain is described from a biopsychosocial perspective. However, the model suggested by Gorecki and colleagues focuses on factors influencing pain management, whereas our conceptual framework focuses on factors that influence the pain experiences of patients in hospital settings, and includes both biopsychosocial and environmental perspectives. Our framework is consistent with the chronic wound associated with pain model suggested by Woo and colleagues [104] because individualized pain is affected by psychological factors, biological factors, and wound treatments. The model proposed by Woo and Sibbald used a variety of chronic wounds to explain pain in general, whereas our proposed conceptual framework focuses on pain associated with pressure ulcers.
Our proposed conceptual framework provides a foundation for future research and practice. First, this conceptual framework directs research by identifying current knowledge regarding the relationship between pressure ulcers and pain, and reducing the number of alternative explanations for findings. In addition, research based on a conceptual model contributes to a more coherent and comprehensive body of knowledge, whereas research without a theory produces isolated information [105][106][107]. Second, future studies that explore the most effective pressure ulcer pain management programs are needed, and these studies should examine pharmacological and non-pharmacological treatment programs (e.g., culturally sensitive, cognitive-behavioral therapy). Third, health care providers who use the proposed conceptual framework will be better able to identify patients who are at risk of experiencing high levels of pain associated with pressure ulcers. Finally, the proposed conceptual framework suggests applicable interventions to decrease pain experiences by manipulating factors such as environmental factors (establishing appropriate nurse/patient ratios and nursing educational levels, and selecting appropriate types of dressings to decrease the frequency of dressing changes), some biological factors (preventing infection and decreasing inflammation), psychological factors (decreasing anxiety and depression, maintaining quiet time to improve sleep quality, and promoting appropriate coping strategies) and sociocultural factors (supporting individual cultural aspects and facilitating family support).
The proposed conceptual framework has limitations. This conceptual framework was built through an extensive literature review and concepts were derived from the biopsychosocial model of pain. Thus, our preliminary conceptual framework aims to provide a comprehensive understanding of the pain experiences of hospitalized patients, and it needs to be tested with hospitalized patients with pressure ulcers. Although it will be difficult to test all factors in this conceptual framework simultaneously, certain factors may be tested in a select sample from the target population.
In terms of pain associated with pressure ulcers, our proposed conceptual framework identifies the important role that healthcare providers play in the prevention, management, and treatment of pressure ulcers and any related pain. Also, the proposed conceptual framework is consistent with current guidelines for the treatment of pressure ulcers, including adequate pain assessment and management [22]. Therefore, healthcare providers should be aware of pain associated with pressure ulcers when they provide care to hospitalized patients with pressure ulcers.

Conclusions
A comprehensive understanding of pain experiences associated with pressure ulcers is required to increase health related quality of life in patients with pressure ulcers. To date, there is no clear conceptual framework to explain pain experiences associated with pressure ulcers. Based on the review of literature, the proposed conceptual framework was generated from the biopsychosocial model of pain, existing evidence was reviewed based on the biopsychosocial model of pain, and environmental factors were added for the target population. Based on this conceptual framework, several strategies were suggested to decrease the pain experiences of hospitalized patients with pressure ulcers. The proposed conceptual framework will provide an advanced understanding of pain phenomena in hospitalized populations with pressure ulcers. Furthermore, it will guide the development of effective nursing interventions by modifying significant factors that may decrease pain experiences for patients with pressure ulcers and promote their quality of life.