Oral Health Problems Among Palliative and Terminally Ill Patients

An Integrated Systematic Review

Munikumar Ramasamy Venkatasalu; Zaidah Rizidah Murang; Divya Thirumalai Rajam Ramasamy; Jagjit Singh Dhaliwal

BMC Oral Health. 2020;20(79)

Abstract and Introduction

Abstract

Background: High incidence of treatable oral conditions has been reported among palliative patients. However, a large proportion of palliative patients lose their ability to communicate their sufferings. Therefore, it may lead to under-reporting of oral conditions among these patients. This review systematically synthesized the published evidence on the presence of oral conditions among palliative patients, the impact, management, and challenges in treating these conditions.

Methods: An integrative review was undertaken with defined search strategy from five databases and manual search through key journals and reference list. Studies which focused on oral conditions of palliative patients and published between years 2000 to 2017 were included.

Results: Xerostomia, oral candidiasis and dysphagia were the three most common oral conditions among palliative patients, followed by mucositis, orofacial pain, taste change and ulceration. We also found social and functional impact of having certain oral conditions among these patients. In terms of management, complementary therapies such as acupuncture has been used but not well explored. The lack of knowledge among healthcare providers also posed as a challenge in treating oral conditions among palliative patients.

Conclusions: This review is first in its kind to systematically synthesize the published evidence regarding the impact, management and challenges in managing oral conditions among palliative patients. Although there is still lack of study investigating palliative oral care among specific group of patients such as patients with dementia, geriatric or pediatric advanced cancer patients, this review has however provided baseline knowledge that may guide health care professionals in palliative settings.

Introduction

High incidence of oral conditions were often reported among palliative patients either direct or indirect primary cause such as salivary gland dysfunction in non-Hodgkin's lymphoma or fatigue which may affect patient's ability to undertake oral care hygiene.^[1,2] Medical management of palliative conditions such as chemotherapy were often reported which can produce oral complications among these patients.^[2] For example, the National Cancer Institute at the National Institutes of Health, United States of America reported that 80% of patients receiving myeloablative chemotherapy will develop oral complications, and palliative drugs such as bisphosphonates and analgesics were associated with oral mucositis and taste disturbance.^[3]

Early diagnosis and treatment of oral conditions among palliative patients could minimize their pain and suffering.^[2] However, evidence shows that 40% of palliative patients lose their ability to communicate their oral health needs. Therefore, they may suffer treatable oral conditions for a prolonged period of time,^[4] or they may not complain of discomfort in their oral cavity which they believe to be an inevitable effect of their treatment.^[5] This may contribute to under-reporting as well as underestimation of oral conditions among palliative patients, which may result in failure among health professionals to completely appreciate the problem. A literature review of oral care for cancer patients in 2001 reported that oral care is given by junior staffs with less experience and the practice needs to be transferred to oncology nurses.^[6] Furthermore, a survey of international supportive health care providers (n = 212) (with 35% response rate) recommended to develop evidence-based practice protocol for oral care management.^[7]

This systematic review aimed to synthesize the published evidence on oral conditions among palliative patients, impact, management and challenges in managing oral conditions among palliative patients.

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Table 1. Details of data sources
Research team	A palliative nurse (MRV) A dentist (JSD) A medical doctor (DR) \ A healthcare researcher (ZR)
Data bases	Sciencedirect, PubMed, Google scholar, Ovid and EBSCOhost
Other resources	Reference list and manual search in key journals
Search time	January 2000 to December 2017
Language	Primary studies in English language
Search terms	"oral condition" OR "oral disease" OR "dental disease" OR "mouth disease" OR "mouth condition" OR mucositis OR stomatitis OR candidiasis OR cheilitis OR xerostomia OR "periodontal disease" OR halitosis OR thrush OR "angular cheilitis" OR "denture stomatitis" OR gingivitis OR periodontitis OR "mouth ulcer" OR "aphthous ulcer" AND palliative OR terminally-ill OR "terminally ill" OR "advanced disease" OR "advanced illness" OR dying OR end-of-life OR hospice OR cancer AND treatment OR intervention OR therapy OR management OR "oral care" OR "mouth care" OR "dental management" AND "end-of-life care"

Table 2. Summary of included studies
Author(s)/Year	Title	Purpose	Setting	Participants	Study design	Oral conditions present
Nakajima/2017	Characteristics of Oral Problems and Effects of Oral Care in Terminally Ill Patients With Cancer	To investigate oral problems in terminal stage of cancer and improvement of dry mouth by oral care.	Japan	Terminally-ill cancer patients	Quantitative descriptive	1. Dry mouth 2. Stomatitis 3. Candidiasis
Fischer et al./2014	Oral health conditions affect functional and social activities of terminally ill cancer patients	To characterize oral conditions in terminally ill cancer patients to determine the presence, severity, and the functional and social impact of these oral conditions.	United States of America	Terminally-ill cancer patients	Quantitative descriptive	Using standardized oral examination: 1. Salivary hypofunction 2. Mucosal erythema 3. Ulceration 4. Fungal infection Using Oral Problem Scale (OPS): 1. Xerostomia 2. Orofacial pain 3. Taste change
Amodio et al./2014	Oral health after breast cancer treatment in postmenopausal women	To characterize oral health in postmenopausal breast cancer survivors.	Brazil	Post-menopausal breast cancer survivors	Quantitative descriptive	1. Chronic periodontal disease
Qutob et al./2013	Implementation of a hospital oral care protocol and recording of oral mucositis in children receiving cancer treatment	To implement a standardized hospital oral care protocol and record the incidence of oral mucositis for inpatients with childhood cancer.	Australia	Pediatric patients with cancer	Quantitative descriptive	1. Mucositis
Velten et al./2017	Prevalence of oral manifestations in children and adolescents with cancer submitted to chemotherapy	To evaluate changes in oral lesions during follow-up of children and adolescents in chemotherapy	Brazil	Children and adolescents with cancer	Quantitative descriptive	1. Mucositis 2. Xerostomia 3. Cold sores 4. Candidiasis
Ezenwa et al./2016	Caregivers' perspectives on oral health problems of end-of-life cancer patients	To determine caregivers' perspectives on oral health problems in cancer patients at the end of life and explore factors that contribute to those perspectives.	United States of America	Advanced cancer patients	Quantitative descriptive	1. Xerostomia 2. Orofacial pain 3. Taste change
Mercadante et al./2015	Prevalence of oral mucositis, dry mouth, and dysphagia in advanced cancer patients.	To determine the prevalence and the characteristics of oral symptoms in a large population of advanced cancer patients.	Argentina	Advanced cancer patients	Quantitative descriptive	1. Mucositis 2. Dry mouth 3. Dysphagia
Matsuo et al./2016	Associations between oral complications and days to death in palliative care patients	To investigate the associations between the incidence of oral problems and the days to death (DTD) in patients receiving palliative care.	Japan	Patients receiving palliative care	Quantitative descriptive	1. Dental caries 2. Gingival inflammation 3. Tongue coating 4. Candidiasis 5. Tongue inflammation 6. Dry mouth 7. Bleeding spots
Kvalheim et al./2016	End-of-life palliative oral care in Norwegian health institutions. An exploratory study.	To explore circumstances surrounding procedures and knowledge regarding oral care for terminal patients in Norwegian healthcare institutions.	Norway	Nurses for end-of-life patients	Quantitative descriptive	1. Dry mouth 2. Plaque 3. Food particles and fungus Infections 4. Sores and scab 5. Viscous ropy saliva and chapped lips 6. Reduced appetite and pain 7. Dysphagia 8. Halitosis 9. Coughing and problems using dentures
Bogaardt et al./2015	Swallowing problems at the end of the palliative phase: incidence and severity in 164 unsedated patients.	To establish the incidence of swallowing problems and related problems in the dying phase	Netherlands	Dying patients	Quantitative descriptive	1. Swallowing problems 2. Frequent coughing 3. Problems with oral secretions
Meidell et al./2009	Acupuncture as an optional treatment for hospice patients with xerostomia: an intervention study	To investigate the feasibility of conducting a 5-week acupuncture intervention in a hospice, and the effect of acupuncture on xerostomia, dysphagia and dysarthria in patients with terminal cancer.	Sweden	End-of-life patients	Quantitative comparative	1. Xerostomia 2. Dysphagia 3. Dysarthria
Lagman et al./2017	Single-Dose Fluconazole Therapy for Oral Thrush in Hospice and Palliative Medicine Patients.	To assess the efficacy of a single-dose fluconazole 150 mg for oral thrush.	United States of America	Palliative and hospice patients with advanced cancer and have a clinical diagnosis of oral thrush	Quantitative descriptive	1. Oral thrush
Momo et al., 2017	Assessment of indomethacin oral spray for the treatment of oropharyngeal mucositis-induced pain during anticancer therapy	To assess the efficacy and safety of indomethacin (IM) oral spray (OS) as a pain control therapy for oropharyngeal mucositis due to anticancer chemo- and radiotherapy	Japan	Patients with head and neck carcinomas and haematological tumours	Quantitative comparative	1. Mucositis
Ling & Larsson/2011	Individualized pharmacological treatment of oral mucositis pain in patients with head and neck cancer receiving radiotherapy	To assess the effect of pharmacological treatment in head and neck cancer patients with OM-induced pain and swallowing difficulties.	Sweden	Patients with head and neck cancer undergoing radiotherapy	Quantitative descriptive	1. Mucositis 2. Pain 3. Swallowing difficulties
Gligorov et al./2011	Prevalence and treatment management of oropharyngeal candidiasis in cancer patients: results of the French CANDIDOSCOPE study.	To evaluate the prevalence of oropharyngeal candidiasis (OPC) in cancer patients treated with chemotherapy and/or radiotherapy.	France	Cancer patients treated with chemotherapy and/or radiotherapy	Quantitative descriptive	1. Oropharyngeal candidiasis 2. Mucositis 3. Xerostomia 4. Taste changes 5. Pain
Davies et al./2006	Oral candidosis in patients with advanced cancer	To determine the epidemiology, aetiology, clinical features and microbiological aspects of oral candidosis in a cohort of cancer patients receiving specialist palliative care.	United Kingdom	Cancer patients receiving specialist palliative care.	Quantitative descriptive	1. Oral yeast carriage 2. Oral candidiasis 3. Xerostomia
Wilberg et al./2012	Oral health is an important issue in end-of-life cancer care.	To assess the prevalence of oral morbidity in patients receiving palliative care for cancers outside the head and neck region and to investigate if information concerning oral problems was given.	Norway	Cancers patients outside the head and neck region	Qualitative interview	1. Xerostomia 2. Mucosal friction 3. General oral discomfort 4. Taste changes 5. Candidiasis
Rydholm & Strang/2002	Physical and psychosocial impact of xerostomia in palliative cancer care: a qualitative interview study	To explore the global effects of xerostomia, with a specific focus on psychological and social consequences.	Sweden	Patients with advanced malignancies and symptomatic xerostomia	Qualitative interview	1. Subjective discomfort 2. Dryness or burning sensation 3. Loss of function e.g. articulation or swallowing 4. Increased infection (oral thrush and ulcerations)
Rohr et al./2010	Oral discomfort in palliative care: results of an exploratory study of the experiences of terminally ill patients.	To examine oral discomfort from the perspective of terminally ill patients.	Australia	Terminally-ill patients	Qualitative interview	1. Xerostomia 2. Bouts of ulceration and infection

Table 3. Studies addressing the impact of oral conditions among palliative patients
Study	Findings associating oral conditions and its social and/or functional impact
Study	Social	Functional
Fischer et al.	Orofacial pain and salivary hypofunction had significant associations with social impact (p < 0.001) such as worrisome that affected the patients' social interactions.	Xerostomia (p < 0.001), orofacial pain (p < 0.001), salivary hypofunction (p < .001) and taste change (p = 0.042) had significant associations with functional impact, which was possibly related to food enjoyment.
Ezenwa et al.	Xerostomia, orofacial pain and taste change had social impact of feeling worried, bothered, not wanting people around and a feeling of less satisfying life, with percentage agreement ranged from 41 to 64% between caregivers and care recipients. However, a significant difference in the means of the social impact subscale was reported between the two groups (p = 0.02), with caregivers overestimating social impact.	Xerostomia, orofacial pain and taste change had functional impact which include swallowing difficulty, speaking difficulty, eating difficulty, food restriction, dryness and pain, with significant correlation between caregivers' and care recipients' ratings (p < 0.001)
Rydholm & Strang	Xerostomia was reported to have psychosocial effects, including shame, increased feelings of being a patient rather than a person and a tendency to avoid social contact, resulting in loneliness.	Xerostomia was reported to be associated with loss of oral function, such as in articulation and swallowing.
Rohr et al.	Orofacial pain prevent patient from sharing and enjoying meals with friends and family, which limit their social outings and participation at special occasions. Participants were more 'tentative' in holding a conversation with others due to speech difficulties, hence avoiding 'close physical contact' with their loved ones.	Xerostomia was described as 'constantly there', causing swallowing difficulties and loss of taste. Difficulty of swallowing was also described as 'unbearable at times'.
Wilberg et al.	Xerostomia and taste alterations were associated with anxiety (p = 0.04) and depression (p = 0.34)	n/a

*n/a not available

Table 4. Studies addressing the management of oral conditions among palliative patients
Oral condition	Study	Management	Effectiveness
Xerostomia	Mercadante et al.	Drug medication • Opioids • Corticosteroids • Diuretics • Benzodiazepines • Anticonvulsants • Neuropletics • Nonsteroidal anti-inflammatory drugs Medical treatment • Chlorexidine • antifungal drugs • Benzydamine • Natural agents	n/a
	Kvalheim et al.	Lubricating lips • Eucerin liniment • Glycerol • Vaseline • Blisex • Lypsyl • Lip stick • Lip cream Lubricating mucosa • Glycerol • Glycerol solution 17% • Glycerol solution 50% • Glycerol solution 70% • Glycerol with peppermint oil • Glycerol and Chlorhexidine • Xylocaine/Lidocaine viscous • Xylocaine/Lidocaine viscous • Paracetamol mixture and cream • Panodil mixture and cream 1:1 • Pure cream • Zendium saliva • Zendium gel • Groundnut oil • Saliva gel • Oralbalance • Mouth moisturiser	n/a
	Meidell & Rasmussen	Acupuncture treatment twice a week for 5 weeks – a total of ten treatments.	Measurements were using visual analogue scale (VAS), consisted of a horizontal line, 0–10 cm, where 0 represented no problem or discomfort and 10 represented severe problems and discomfort. The feeling of dryness of the mouth declined for all the participants as the series of treatment proceeded. In most cases a substantial improvement could not be noted until after fifth treatments. VAS decreased from 7.5 to 4.8 after fifth treatments (P < 0.001). Between the sixth and tenth treatments, the VAS decreased from 4.8 to 3.3 (P < 0.001). The VAS decreased from 7.5 before the baseline to 3.3 before the tenth treatment (P < 0.001).
	Nakajima	Standard oral care by nursing staff of the wards, which include moisturizing, brushing, and oral cleaning (such as tongue coating removal) or oral massage performed by ward staff on a regular basis to resolve dry mouth). Intervention by specialist oral care team (specialist oral care) was performed as needed.	The rate of dry mouth improvement by oral care intervention was investigated by the severity (Grade 1, 2 and 3). All grade 1 cases were improved by standard oral care (100%). Grade 2 dry mouth was improved by standard oral care in 85% in good oral intake group (oral food intake was 30% or more) and 71% in poor oral intake group (oral food intake was less than 30%). Six ineffective cases of poor oral intake group were treated with specialist oral care, resulting in an improvement rate of 83%. Grade 3 dry mouth was improved by standard oral care in 40% in good oral intake group, and 2 ineffective cases were treated with specialist oral care, resulting in an improvement rate of 80%. In poor oral intake group, improvement was achieved by standard oral care in 67%, and 8 ineffective cases were treated with specialist oral care, resulting in an improvement rate of 81%. Thus, these interventions improved dry mouth in 80% or more of the patients both in good oral intake group and in poor oral intake group.
Candidiasis	Lagman et al.	A single-dose fluconazole 150 mg via mouth	Majority had complete response, except 2 who did not respond to treatment. Probable side effects of the medication included nausea in 4 patients, abdominal pain in 1, and diarrhea in 1. Both the change in the number of symptoms and the symptom scores before and after treatment decreased significantly (P < 0.001).
Candidiasis	Gligorov et al.	Local antifungal treatments were prescribed in 123 (75%) patients. Amphotericin B mouthwashes were administered in 67 (54.5%) patients, miconazole mucoadhesive buccal tablet in 36 patients (29.3%), and nystatin mouthwashes in 20 (16.3%) patients. Fluconazole, an oral systemic treatment, was prescribed in 41 (25%) patients at a dosage of 50 mg/day, 100 mg/day, and 200 mg/day in 7 (17.7%), 22 (53.7%), and 10 (24.4%) patients, respectively. Concomitant non-antifungal treatments were prescribed in 57 (35%) patients, mainly sodium bicarbonate mouthwashes in 45 patients.	Miconazole MBT was reported to be "efficacious" or "very efficacious" in 25 of 32 patients (78.1%) vs. 39 of 51 (76.5%) for amphotericin B, and 9 of 15 60%) for nystatin. The nonefficacy reported by the patients was related to noncompliance to treatment; 30% of noncompliant patients vs. 14.3% of those compliant rated amphotericin B as "slightly efficacious or not efficacious."
Dysphagia	Meidell & Rasmussen	Acupuncture treatment twice a week for 5 weeks – a total of ten treatments.	Measurements were using visual analogue scale (VAS), consisted of a horizontal line, 0–10 cm, where 0 represented no problem or discomfort and 10 represented severe problems and discomfort. A substantial improvement of dysphagia was not obvious until after fifth treatments when the VAS had decreased from 5.6 to 4.1 (P < 0.001). Between the sixth and tenth treatments, the VAS decreased from 4.1 to 3.7 (P = 0.81). The VAS decreased from 5.6 before the baseline to 3.7 before the tenth treatment (P = 0.01).
Dysphagia	Ling & Larsson	Step-based pharmacological intervention 1. Acetaminophen 2. NSAID 3. Opioids 4. Adjuvant medication - Amitryptilin, gabapentin, or pregabalin were considered due to neurotic pain, mainly tumor-related. - Betametasone was considered for optimized anti-inflammatory effect, impaired general condition, or antiemetic effect. Topically acting drugs - Lidocain and benzydamine were prescribed at RT start by the dental services at the hospital to all patients with an irradiated mouth.	Soreness in the mouth showed unexpectedly significant worsening (P = 0.001) between baseline (TQ1) and 1 week later (TQ2). Significant worsening was found for three swallowing questions about liquids (P = 0.007) and solid food (P = 0.004), choking when swallowing (P = 0.018).
Mucositis	Ling & Larsson	Step-based pharmacological intervention 1. Acetaminophen 2. NSAID 3. Opioids 4. Adjuvant medication - Amitryptilin, gabapentin, or pregabalin were considered due to neurotic pain, mainly tumor-related. - Betametasone was considered for optimized anti-inflammatory effect, impaired general condition, or antiemetic effect. Topically acting drugs Lidocain and benzydamine were prescribed at RT start by the dental services at the hospital to all patients with an irradiated mouth.	Four oral mucositis (OM) grades were used: 0: No reaction 1: Hyperaemia, impressions, soreness, edema 2: Erythema, occasional ulcers, soreness 3: Painful erythema, larger fibrin-coated ulcers 4: Widespread ulcerated areas, easily bleeding, very painful In the early intervention (EI) group, the OM grade increased between baseline (TQ1) and 1 week later (TQ2) (P < 0.001). In the late intervention (LI) group, the OM grade was unchanged between TQ1 and TQ2 (P = 0.059).
Mucositis	Momo et al.	Indomethacin (IM) oral spray (OS)	Pain relief was achieved in 93% patients at 25 (5–60) min after applying the IM-OS preparation (15.6 ± 3.4 μg/kg) and analgesic effects were maintained for 120 (10–360) min. The pain was significantly decreased after using the spray (3.6 ± 0.7 vs. 2.4 ± 0.9, p < 0.01). Moreover, urinary IM excretion rates after applying the IM spray preparation were 1.8 ± 0.8% of the IM oral spray dose (130.5 ± 77.7 μg/kg/day), which was markedly lower than that following oral administration of IM (60%). No adverse events were observed following application of the spray.

*n/a not available

Table 5. Studies addressing the challenges in treating oral conditions among palliative patient
Study	Challenges
Kvalheim et al.	• Lack of knowledge/experience/routine (43%) • Lack of patient cooperation (38%) • Oral problems were not prioritised (22%) • Difficult access to the mouth (11%), • Lack of resources by (8%) • Retching (3%).
Bogaardt et al	• Nursing staff rated the incidence and severity of swallowing problems lower than the relatives (p < 0.0001) • Nursing staff rated the median severity of frequent coughing (p = 0.012) and loss of appetite (p = 0.001) significantly lower compared to the relatives'