Oral health status among 65-year-olds in Oslo, Norway; periodontitis, chemosensory disorders, and oral health-related quality of life

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Oral health status among 65-year-olds in Oslo, Norway; periodontitis, chemosensory disorders, and

oral health-related quality of life

Anne Thea Tveit Sødal

Department of Cariology and Gerodontology Faculty of Dentistry

University of Oslo 2022

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© Anne Thea Tveit Sødal, 2023

Series of dissertations submitted to the Faculty of Dentistry, University of Oslo

ISBN 978-82-8327-069-3

reproduced or transmitted, in any form or by any means, without permission.

Print production: Graphics Center, University of Oslo.

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Acknowledgments

This work has been carried out during my years as a PhD student at the Faculty of Dentistry, University of Oslo. I am grateful to the Faculty of Dentistry for the funding and research facilities that made this project possible to implement. The work in this thesis is a result of collaboration and great effort from many people.

First, I want to express my greatest gratitude to my main supervisor Lene Hystad Hove for all the support and guidance, but also for the freedom to work independently through my time as a PhD student. I would also like to thank Lene Hystad Hove and Rasa Skudutyte-Rysstad for introducing me to the joy of research when they supervised me during the work with my Master’s Degree in Dentistry.

I am grateful to my co-supervisors Rasa Skudutyte-Rysstad, Odd Carsten Koldsland and Preet Bano Singh for the support, guidance and constructive comments at all stages in this project.

Their knowledge has been invaluable both in planning the study, the data collection and the writing of the articles.

My Tien Diep, my dear colleague and friend, thank you for all your support, valuable discussions and friendship. Without you, these years would have been a lot less fun.

To all my other colleagues at the Department for Cariology and Gerodontology, thank you for a pleasant working atmosphere and valuable discussions. A special thanks to Alix Young Vik for taking the time to carefully read this thesis and give constructive feedback on language and content.

I am also grateful to other departments and staff at the Faculty of Dentistry who have contributed to this project. Aud Jorid Kjellsbøl Hole and Anita Smedstuen Thorkildsen, thank you for the extra effort you made atthe Department of Maxillofacial Radiology during the data collection.

I would like to thank all the 65-year-olds participating in the study. Without you, there would have been no study.

Finally, I would like to thank my family and friends for their invaluable support, everlasting encouragement and care.

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List of papers

The work in this thesis was funded by, and conducted at, the Faculty of Dentistry, University of Oslo. The first and third papers have been published in international peer-reviewed journals, and the second study is in manuscript and has been submitted.

I. Sødal ATT, Hove LH, Diep MT, Skudutyte-Rysstad R, Koldsland OC. Periodontal conditions in a 65-year-old population and prevalence of periodontitis

according to three different bone level thresholds. BMC Oral Health. 2022 Jun 21;22(1):246. doi: 10.1186/s12903-022-02276-1. PMID: 35729603; PMCID:

PMC9215064.

II. Sødal ATT, Skudutyte-Rysstad R, Diep MT, Koldsland OC, Hove LH. Periodontitis in a 65-year-old population: risk indicators and impact on oral health-related quality of life. Submitted to BMC Oral Health 2022 Sep 01

III. Sødal ATT, Singh PB, Skudutyte-Rysstad R, Diep MT, Hove LH. Smell, taste and trigeminal disorders in a 65-year-old population. BMC Geriatr. 2021 May 8;21(1):300. doi: 10.1186/s12877-021-02242-6. PMID: 33964881; PMCID:

PMC8105933.

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Abbreviations

BW Bitewing

BoP Bleeding on probing

ICC Intra-class correlation coefficient

OPG Orthopantograms

OECD Organization for Economic Co-operation and Development OHIP-14 Oral health impact profile-14

OHRQoL Oral health-related quality of life

PA Periapical

PPD Periodontal probing depth

RBL Radiographic bone loss

QoL Quality of life

SWS Stimulated whole saliva UWS Unstimulated whole saliva

VAS Visual analogue scale

WHO World Health Organization

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Background

The Organization for Economic Co-operation and Development (OECD) has defined the elderly population as people aged 65 and over (1). This lower age limit for young elderly can be discussed due to longer life expectancy (2). However, around the age of 65, individuals are often on the verge of a shift in life, from the traditional working life, to life after

retirement. This might lead to changes in social and behavioral habits. In addition, aging may be associated with a reduction in an individual’s health status due to physiological aging and the accumulation of illness. These changes will often also influence oral health. A

demographic transition has been reported both globally (2) and in Norway (3), including an increase in the proportion of elderly in the population. A greater proportion of elderly will probably lead to an increase in the need for oral healthcare in the society, exacerbated by more elderly retaining their own teeth longer (4-6). Poor oral health can have a profound bearing on general health and well-being (7-9). In addition, as a consequence of poor oral health, increased costs related to acute dental diseases that can lead to tooth loss and need for medical treatment have been identified (10). In order to be able to plan for health services in the future, oral health status data in the population are necessary.

Information regarding oral health among the elderly population in the southern parts of Norway is scarce. Repeated studies among 35-year-olds in Oslo showed an improvement in oral health between 1973 and 2003 (11, 12). More recent studies have provided data from northern Norway (13-15) and the county of Trøndelag in the central part of the country (16).

However, a study showed that there are large geographical disparities with respect to dental status in Norway (17). More research investigating oral health has been requested by the Norwegian authorities (18). The data presented in this thesis are from the project

“OsloMunn65”, a population-based study investigating a wide range of oral health aspects among residents of Oslo born in 1954 (aged 65 years). The data were collected at the Faculty of Dentistry, University of Oslo, between February 2019 and December 2019. The main rationale for the OsloMunn65 project was to provide data regarding oral health status and possible risk indicators for oral diseases in this population group that will be useful for planning dental health services for the elderly population in the years to come. Data from the present work will also be useful as a baseline for follow-up studies, and thereby offer opportunities for studying oral disease determinants. The focus of this thesis is the

epidemiological aspects of a retrieved selection of oral health-related conditions in a young elderly population that may have an impact on healthy ageing.

The World Health Organization (WHO) has pointed out oral health as a crucial and often neglected area of healthy aging (7). As one of the most common oral diseases, periodontitis is highlighted as a main indicator that reflects poor oral health (7, 19). Poor oral health-

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status may lead to pain, problems with eating, chewing, smiling and communication, and thereby have a detrimental effect on nutrition and people’s daily life (7). Another

component that may impact healthy aging is sensory impairments such as a decrease in smell and taste function (7). Reduced smell and taste function may lead to an unhealthy dietary composition and an increased intake of sugar (20), and may have a deteriorating effect on both the general and oral health. This thesis therefore describes periodontal and chemosensory status of the 65-year-olds, in addition to associated socioeconomic,

behavioral and general health factors. Furthermore, the participants’ awareness of

chemosensory disorders and also periodontitis` impact on quality of life, were investigated.

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Current knowledge

Epidemiology

Epidemiology is defined as “the study of the distribution and determinants of health-related states or events in specified populations, and the application of this study to the control of health problems” (21). Epidemiological studies can be divided further into subgroups based on the study design and purpose. While descriptive epidemiological studies are designed to investigate the occurrence of disease or other health-related characteristics in a population, analytical studies are designed to examine associations and risk factors for disease (21, 22).

Epidemiology is considered as the basic science of public health (23). The assessment of health status in a population is necessary to be able to describe the need for health care in a community. In addition, identification of disease risk indicators in a population may help to identify groups of individuals in need of information regarding increased disease risk and possible preventive measures.

Periodontal health and diseases

The periodontium consists of several components: cementum, the periodontal ligament, alveolar bone, and gingival tissue (24, 25). These connective tissues support the teeth, both by making the attachment to the bone possible, and by protecting the teeth from

periodontal pathogens (24). The cementum is a hard connective tissue that coats the roots of the teeth and function as an attachment surface for the periodontal ligament fibers (25).

Between the cementum and the alveolar bone, the periodontal ligament (a soft, specialized connective tissue) supports the teeth in their bony socket, allowing them to withstand large masticatory forces (25). This specialized soft tissue also contributes to positioning of the jaws during mastication by acting as a sensory receptor (25). In addition, the periodontal ligament functions as a cell reservoir for tissue homeostasis and regeneration (25). The epithelial gingival tissue facing the tooth (the dentogingival junction) plays a crucial role protecting the underlying periodontal tissue from the microflora and contribute in keeping the

periodontium healthy (25).

Periodontal diseases affect the supportive tissues of the teeth. The mildest form of periodontal disease, gingivitis, does not affect the underlying periodontal tissues (24, 26).

Gingivitis can be caused either by the microflora in plaque biofilm or by specific non-dental plaque-induced conditions, e.g. manifestation of systemic diseases (27). The inflammatory process in the gingiva causes edema and bleeding and is registered clinically as bleeding on probing (BoP). For epidemiological purposes, the extent of bleeding on probing is often used

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for classifying gingivitis in individuals without a history of periodontitis (27). In this case, localized gingivitis is defined as presence of BoP at 10-30% of sites, while generalized gingivitis is defined as presence of BoP at > 30% of sites (27). As gingivitis only affects the gingiva, and does not lead to degradation of the underlying connective tissue, this condition is reversible if the cause is eliminated, e.g. by plaque removal (27). Even though the

epithelium in the dentogingival junction functions as a barrier against periodontal

pathogens, these microorganisms can disturb the function of the epithelium leading to their subgingival spread in the gingival pocket. This spreading can lead to an inflammation in the periodontal tissues, with degradation of the underlying connective tissue and irreversible damage - periodontitis (26). If left untreated, periodontitis can lead to loss of tooth support and eventually tooth loss.

Periodontitis is one of the most common oral diseases (19). A global increase in the prevalence of severe periodontitis has been observed (28). Even though the prevalence of severe periodontitis is highest in low- and middle-income countries, a substantial disease burden has also been reported for the high-income country Denmark (28). Population growth has been identified as an important factor in the global increase in severe

periodontitis (28). The largest increase in prevalence of severe periodontitis cases globally from 1990-2019 was found in the age group 70-74 years (28). However, longitudinal studies from Sweden and Norway from 1973 have shown an improvement in periodontal conditions, with a reduction in the prevalence of severe periodontitis (11, 29).

In Norway, more recent epidemiological studies have reported a prevalence of periodontitis ranging from 49 to 72%, with a higher prevalence in older age groups (14-16). Stødle et al.

investigated the prevalence of periodontitis among individuals living in the county of Nord- Trøndelag and reported a prevalence of 98.5% in 60-79 year olds (16). The studies by Holde et al. (14) and Bongo et al. (15) were performed further north in the counties of Troms and Finnmark, respectively. Among individuals living in Troms the prevalence was 81.3% in the age group 65-79, and among individuals living in Finnmark the prevalence was 79.4% in the age group 65-75 years (15). These studies indicate a high prevalence of periodontitis among elderly in Norway. Recent prevalence data among young elderly in southern part of Norway are lacking.

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Oral health-related Quality of life

In the constitution of the World Health Organization (WHO), health is defined as “a complete state of physical, mental and social well-being and not just the absence of disease” (30).

Therefore, an individual´s perceived health status and its impact on life are important to include in epidemiological research investigating health status in populations. In response to this, health care researchers now give more attention to health as a multidimensional construct (31). The WHO work group on quality of life (QoL) defined QoL as “individuals' perception of their position in life in the context of the culture and value systems in which they live and in relation to their goals, expectations, standards and concerns” (32). Quality of life is considered as a valid parameter in patient assessments in several areas of physical and mental health care, including oral health care (31).

With increased focus on patient-centered care and biopsychosocial aspects in oral

healthcare, the assessment of oral health-related quality of life (OHRQoL) has gained more attention in dental research (31, 33). The concept of OHRQoL has been defined as “how oral health affects quality of life related to a) oral functioning (such as being able to chew, bite, swallow, or speak), b) psychological well-being (such as a person`s satisfaction with the appearance of their teeth and smile, and self-esteem), c) social well-being (such as the level of comfort when eating or speaking in front of others), as well as d) pain/discomfort (33).

Oral health-related quality of life has been used both as an outcome variable when evaluating the effect of specific treatments, but also in epidemiological studies to identify individual and environmental factors affecting OHRQoL (31). This has resulted in the development of several instruments to assess oral health-related quality of life (34-38).

Among existing instruments, the oral health impact profile-14 (OHIP-14), oral impacts on daily performances (OIDP) and geriatric oral assessment index (GOHAI) have been stated to be the most widely validated ones (39).

Globally, an increase in life expectancy have been observed in the last decades (2). With an increase in the life expectancy, a healthy aging is paramount for maintaining a good quality of life in the additional living years. The investigation and identification of risk indicators leading to a reduction in the oral health-related quality of life will therefore help in reducing these risk factors. Several factors are reported to be associated with reduced OHRQoL, including self-rated oral health, frequency of dental visits, number of teeth, reduced chewing ability, and xerostomia (40-42). Studies have shown an association between periodontitis and OHRQoL, however, the literature is inconsistent (41). This indicates a need for further studies investigating this association.

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Chemosensory function and disorders

The gustatory and olfactory systems that are responsible for taste and smell perception are complex. Smell perception starts when chemicals entering the nasal cavity, either through the nostrils or through the nasopharynx, trigger the olfactory epithelium in the nasal mucosa (43, 44). Olfactory receptor neurons in the epithelium then send signals to the central

nervous system through different components of the olfactory nerve (cranial nerve I, CN I) (45-47). Taste perception is induced when chemical molecules from food and beverages that are dissolved in the saliva, trigger taste buds located in the oral mucosa (48, 49). The taste buds are innervated by cranial nerves (CN VII, IX and X) which send information to the central nervous system (48). In addition to the cranial nerves mentioned above, the

trigeminal nerve (CN V) endings in the oral and nasal cavity provide tactile and nociceptive information when triggered by chemicals, a function known as chemesthesis (48, 50).

Chemesthesis plays an important role in detecting temperature, consistency and pungency of food and beverages (48, 50), and thereby contributes in flavor perception.

Disturbances in olfactory and gustatory functions may result in a reduced or distorted ability to smell and taste, and are known as chemosensory disorders. Olfactory disorders are classified as hyposmia when the sense of smell is reduced, and anosmia when complete loss of ability to smell occurs (51). Gustatory disorders are classified as hypogeusia when the sense of taste is reduced, and ageusia when the ability to taste is completely absent (52). In addition to these quantitative smell and taste disorders, some patients suffer from

qualitative disorders that can give a distortion of smell and taste, termed parosmia and dysgeusia (51, 52). A normal ability to smell is termed normosmia, and a normal ability to taste is termed normogeusia. Disorders in the trigeminal nerve may lead to a numbness or a burning sensation in the oral mucosa (53). This can be the cause of burning mouth syndrome that is characterized by burning pain or discomfort in the tongue, lips, or entire oral mucosa without an identifiable local or systemic cause (54).

Chemosensory disorders can have several causes. Since the olfactory and gustatory functions are dependent on different functional systems (43, 45-49), diseases that lead to taste and smell loss might be caused by different factors. The most common causes for olfactory disorders are upper respiratory infections, head trauma and nasal and paranasal sinus disease (51). Risk factors for disturbed taste function may be bad-tasting substances from oral conditions, oral dryness and oral candida infections, or damage of buds by local trauma (49, 52). In addition, during the recent Covid-19 pandemic, chemosensory disorders have received more attention. As common symptoms of Covid-19 disease, many people around the world were suddenly affected by these disorders (55-57).

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Reduced gustatory and olfactory functions have also been observed in older age groups (58- 62). This might be due both to diseases associated with older age and chemosensory

disorders (51, 52, 63), but also an increase in use of medications with age that can disturb chemosensory function (64-67). In addition, physiological processes in the body, such as cell regeneration, slow down (68, 69). As the proportion of older individuals in the population is increasing, medication use and the prevalence of various illnesses will almost certainly increase, leading to an increase in the prevalence of chemosensory disorders in the years to come.

Various studies from the US show that more than 50% of the population aged ≥ 65 years are affected by olfactory disorders (51, 60, 70). In Germany, olfactory and gustatory disorders were reported to be present in more than 20% of a population aged 65-74 years (71). In Scandinavia, the prevalence of olfactory disorders reported in a large population-based sample in Sweden was 19% (58), and in Norway one study investigating olfactory function among cognitive healthy adults found a prevalence of 28% (72). Another study from Norway found a prevalence of olfactory disorders of 37% among the general population (73).

Chemosensory disorders and their association with certain diseases and prevalence in specific patient groups have also been investigated (74-76). However, studies involving examinations of both olfactory and gustatory function in the elderly in Norway are missing.

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Aims

As there is a general current knowledge gap regarding oral health status in the young elderly population, the overall aim of this thesis was to investigate certain oral health parameters and their impact on oral health-related quality of life among young elderly living in Oslo.

More specifically, the aims of the papers included in this thesis were as follows:

Paper I. Periodontal conditions in a 65-year-old population and prevalence of periodontitis according to three different bone level thresholds

The aim of paper I was to describe periodontal conditions among young elderly living in Oslo using the classification decided at the 2017 World Workshop on the Classification of

Periodontal and Peri-implant Diseases and Conditions. An additional aim was to investigate to what extent different radiographic bone level cutoffs influence the prevalence of

periodontitis in this population.

Paper II. Periodontitis in a 65-year-old population: risk indicators and impact on oral health-related quality of life

The aim of paper II was to identify possible socioeconomic and behavioral risk indicators for severe periodontitis in a population of young elderly in Oslo, and to investigate how the disease impact the oral health-related quality of life.

Paper III. Smell, taste and trigeminal disorders in a 65-year-old population

The aim of paper III was to investigate chemosensory function in a population of 65-year- olds. More specifically, the aim was to determine the prevalence of taste and smell disorders, and burning mouth sensation, and furthermore evaluate possible associations between these disorders and gender, smoking, salivary secretion rate, chronic diseases and use of medications.

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Participants and methods

Study sample

The participants in this study (OsloMunn65) were Oslo residents born in 1954, randomly chosen from the Norwegian Population Register (retrieved from the Norwegian Tax Administration). Invitation letters (Appendix I) were sent by mail to eligible participants to their registered address, and they were contacted by telephone two weeks later. In accordance with the ethical approval (see Ethical considerations), a flowchart was used to ask the 65-year-olds whether they would be interested in participating in the study

(Appendix II). Of the 796 eligible individuals, 460 agreed to participate in the study. The recruitment process is shown in Figure 1, and the different samples of participants that were included in the three papers are described in Table 1.

Figure 1. Flow chart outlining the recruitment process.

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17 Table 1. Overview of participants in papers I, II and III

Paper I All 460 individuals underwent clinical and radiographic periodontal examinations. Three individuals who did not answer the questionnaire variables included in paper I and 3 individuals who had < 2 remaining teeth were excluded from the analyses, leading to a final number of 454

participants.

Paper II Of the 460 individuals, 7 were excluded from the analyses (3 due to < 2 remaining teeth and 4 due to missing relevant questionnaire variables), resulting in a final number of 453 participants.

Paper III A subsample of 225 individuals was randomly selected for chemosensory examination. One participant who did not complete the questionnaire and 1 participant who failed to complete the olfactory and gustatory test due to discomfort were excluded from the analyses. The final number of individuals included in the analyses was 223.

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Data collection

Clinical and radiographic examination

The data collection took place from February 2019 to December 2019 at the Research Clinic at the Faculty of Dentistry, University of Oslo. This interdisciplinary project required

cooperation across several departments including cariology and gerodontology, maxillofacial radiology, periodontology, endodontics, oral surgery and oral medicine and orthodontics.

Two calibrated dentist performed the clinical examinations. In addition, bitewing (BW) radiographs and orthopantograms (OPG) were taken of all participants. The clinical and radiographic parameters are all presented in Table 3 and 4.

Questionnaire

All participants answered a questionnaire in Nettskjema software (University of Oslo, Norway). A link to this questionnaire was sent by email to participants prior to their appointment at the faculty. Participants who were unable to answer the questionnaire at home filled out the questionnaire during the appointment at the faculty. The questionnaire was only available in Norwegian (Appendix IV). The questionnaire parameters that were relevant for the studies included in the present thesis are presented in Table 3. In addition to the self-administered questionnaire, the participants were interviewed regarding smell and taste function and burning mouth sensation when they attended the clinical examination (75). The participants were also asked to score their smell and taste perception on a linear visual analogue scale (VAS) from 0 to 10, where 0 = no smell perception and 10 = very good smell perception prior to the chemosensory testing.

Microdata

To be able to compare the sample population included in the present project with the study population, register data from the total population of 65-year-olds were drawn from the Microdata database collected by Statistics Norway (77). Characteristics of individuals in the sample population and the study population are shown in Table 2.

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19 Table 2. Sample population (N = 460) versus general population of 65-year-olds in Oslo (N = 6014), according to Statistics Norway (77)

Background variable

65-year- olds in Oslo

%

Study population

% Gender

Men 49.5% 51.7%

Women 50.5% 48.3%

Country of birth*

Western 82% 91%

Non-western 18% 9%

Education**

Basic 53% 33%

Higher 47% 67%

*Country of birth was dichotomized into ‘western’ (Nordic countries, Western Europe, North America, and Australia) and ‘non-western’ (the rest of the world)

**Education was dichotomized into ‘higher education’

(university/college education) and ‘basic education’ (high school, elementary school, or lower)

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20 Table 3. Overview of self-reported parameters

Self-reported outcomes Description Background characteristics Gender

- Men - Women Country of Birth

- Western - Non-western Socioeconomic status Education

- Higher - Basic

General health Diseases

Medications

Smoking habits Never smoker

Former smoker Current smoker

- < 10 cigarettes daily - ≥ 10 cigarettes daily Use of dental health care services Frequency of dental visits

- Regular - Non-regular Oral hygiene behavior Frequency of brushing

- < 2 times daily - ≥ 2 times daily

Oral health-related quality of life Oral health impact profile 14 (OHIP-14) Self-reported taste perception Rating from 0 (very bad) to 10 (very good) Self-reported smell perception Rating from 0 (very bad) to 10 (very good)

Burning mouth sensation Assessed by yes/no and specified which area in the mouth that was affected

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Table 4. Overview of clinical and radiographic parameters Clinical and radiographic

outcomes Description

Sniffin' Sticks Sniffin` Sticks-Screening test (Burghart Messtechnik GmbH, Wedel, Germany) consisting of 12 felt-tip odor pens were used for non-lateralized psychophysical testing of olfactory function (78-80).

Taste Strips Taste Strips (Burghart Messtechnik GmbH, Wedel, Germany) impregnated with solutions in four different concentrations of four different taste qualities (sweet, sour, bitter and salty) were used for whole mouth testing of gustatory function (81).

Unstimulated whole saliva (UWS) and stimulated whole saliva (SWS) secretion rates

For the UWS collection, participants were instructed to spit into a pre-weighed cup when needed for 5 min. For SWS

measurements, the participants chewed on a paraffin tablet (Ivoclar Vivadent, Schaan, Lichtenstein) and when needed spat saliva into a pre-weighed cup for 5 min. After collection of saliva the cup was weighed and secretion rate calculated as ml/min (1 g/min = 1 ml/min). Hyposalivation was defined as a secretion rate of ≤ 0.1 ml/min for UWS and ≤ 0.7 ml/min for SWS (82, 83).

Periodontal probing

depth (PPD) PPD was measured as the distance from the bottom of the periodontal sulcus to the gingival margin measured on six sites per tooth using LM 52B XSI Perio Probe (LM-Dental™, Planmeca Group, Helsinki, Finland), recorded to the nearest mm, rounded down.

Bleeding on probing (BoP) Bleeding from periodontal sulcus on probing, assessed at six sites per tooth. Recorded as bleeding/no bleeding.

Furcation involvement Measured on molars using Nabers Q2N probe (Hu-Friedy, Chicago, USA) and recorded as grade I, II, or III as defined by Hamp et al. (84).

Mobility Recorded as grade 0, I, II, or III as described by Nyman et al. (85).

Radiographic bone loss

(RBL) Detectable interproximal bone loss was recorded as the distance in millimeters from the cemento-enamel junction to the alveolar bone crest on the two most severely affected non-adjacent sites measured on BW radiographs. Percentage bone loss was

calculated for each tooth by dividing the distance from the cemento-enamel junction to the alveolar bone crest by the distance from the cemento-enamel junction to the tooth apex measured on OPGs.

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Assessment of periodontal status

Periodontal status was classified based on the classification system from the 2017 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions (27, 86, 87). Clinical and radiographic parameters are described in Table 4. The definitions used for classifying periodontal conditions, and also for staging and grading the periodontal diseases, are described in detail in Paper I.

Assessment of chemosensory function

Sniffin`n Sticks and Taste Strips (Burghart Messtechnik GmbH, Wedel, Germany) were used for quantitative testing of olfactory (smell) and gustatory (taste) function (Table 4). Based on the results from the Sniffin`n Sticks test participants were categorized into anosmic (total loss of smell function), hyposmic (reduced smell function) and normosmic (normal smell function) (88). Based on the results from the Taste Strips test participants were categorized into ageusic (total loss of taste function), hypogeusic (reduced taste function) and

normogeusic (normal taste function) (81).

Prior to the quantitative chemosensory testing, the participants were asked to score their perceived smell and taste perception separately on a linear visual analogue scale from 0 to 10, where 0 = no smell/taste perception and 10 = very good smell/taste perception (Table 3).

In addition, the participants were interviewed regarding their experience of burning mouth sensation (Table 3).

Assessment of oral health-related quality of life

Oral health-related quality of life was assessed using the shortened Norwegian version of the oral health impact profile-14 (OHIP-14) (34, 40). The questionnaire consists of 14 items divided into 7 domains. Ratings were made on a 5-point Likert scale for each item: 0 = never, 1 = hardly ever, 2 = occasionally, 3 = fairly often and 4 = very often, with sum score ranging from 0-56 and higher score indicating poorer OHRQoL. Participants reporting the response codes: 3 'fairly often' or 4 'very often' to at least one of the 14 items were categorized as having negative impact on OHRQoL.

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Statistical analyses

All clinical registrations were recorded using the Oral Data Collector sheet specifically designed for data entry in this study, developed in Microsoft Excel 2016 (Microsoft Corporation, Redmond, Washington, US) (Appendix V). Radiographic registrations were performed in ImageJ software (ImageJ 1.52a, National Institutes of Health, USA) and

registered in Microsoft Excel 2016 (Microsoft Corporation, Redmond, Washington, US). Data from the questionnaire, and clinical and radiographic examinations were imported into STATA (Stata version 16.1; College Station, TX, USA) for statistical analysis. Data were collected, stored and analyzed in the Service for Sensitive Data (TSD facilities, UiO). An overview of the statistical analyses is given in Table 5.

Table 5. Overview of statistical methods Study Statistical methods Paper I Descriptive

Paper II Chi-square test and Fisher`s exact test

Mann-Whitney U test and Kruskal-Wallis ANOVA Logistic regression

Paper III Chi-square test and Fisher`s exact test

Mann-Whitney U test and Kruskal-Wallis ANOVA

Ethical considerations

Participants signed a written informed consent (Appendix III) prior to the examination, and had the possibility to withdraw their participation at any time throughout the duration of the project. The participants were not remunerated for participation in the project, but were informed that participation would include a free thorough dental examination. After the examination, participants received a feedback form including relevant findings (Appendix VI). All data were stored in Services for Sensitive Data (TSD: Tjenester for sensitive data, University of Oslo), a secure digital system. The study was approved by the Norwegian Regional Committee for Medical and Health Research Ethics (REK 2018/1383), and was performed in compliance with the tenets of the Declaration of Helsinki.

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Results and discussion

Methodological considerations

This thesis focuses on the oral health and prevalence of oral-related diseases and associated factors in a population of 65-year-olds living in Oslo, Norway. Paper I, paper II and paper III included individuals that participated in the larger epidemiological study OsloMunn65 (OM65). A random sample of individuals born in 1954 and resident in Oslo was recruited from the general population. The response rate was 58%.

Even though the present cross-sectional study was based on a random sample of the general population of 65-year-olds in Oslo, the response rate of 58% led to a sizable proportion of non-respondents and the possibility of selection bias. Information about non-responders was not available due to restrictions from the ethical committee, and non-responders analyses were therefore not performed. However, when background characteristics about the participants were compared to register data from the total population of 65-year-olds living in Oslo, retrieved from Statistics Norway (77), individuals born in a western-country, individuals with higher education, and non-smokers were shown to be somewhat

overrepresented in the present study (Table 2). Reports from the Norwegian Institute of Public Health have shown that a lower educational level and smoking are related to poorer health status (89-91). In addition, studies indicate that non-western immigrants have a poorer oral health status than their western counterparts (92). Therefore, there is a possibility that the health status reported in the present thesis may be better than the general population of 65-year-olds in Oslo.

The reliability of the results in epidemiological studies where there is more than one examiner doing the registrations, may be influenced by variations in the precision of measurements. The clinical examinations in the present project (OsloMunn 65) were

performed by two calibrated dentists. Both examiners were present during all examinations.

Prior to the examinations, the dentists were trained by a specialist in periodontology for periodontal examinations, and by an experienced dentist for the chemosensory

examinations. For the periodontal examination, inter-rater reliability of the clinical examiners was estimated from pocket depth registrations. The intra-class correlation coefficient (ICC) (95% CI) was 0.82 (0.78–0.86) indicating good reliability (93). Intra-rater reliability for the clinical periodontal parameters and calibration of chemosensory testing was not performed because this would have required an additional visit for the participants.

Relevant radiographic registrations for the papers included in the present thesis (paper I and II) were performed by one trained dentist. Prior to the radiographic registrations, the

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examiner was calibrated with a specialist in periodontology. The specialist in periodontology and the trained dentist separately evaluated 50 radiographs. For continuous variables, intra- class coefficients were calculated and for categorical variables Cohen`s Kappa was calculated for evaluating the reliability of measurements. The results were evaluated and for the inter- examiner calibration the ICC (95% CI) was 0.79 (0.66–0.86) for % bone loss, indicating good reliability (93), and the weighted Cohen’s kappa (95% CI) was 0.72 (0.66–0.78) for stage, indicating substantial reliability (94). Furthermore, intra-examiner calibration was performed on 25 radiographs. For the intra-examiner radiographic registration the ICC (95% CI) was 0.88 (0.86–0.90) for % bone loss, indicating good reliability (93), and the weighted Cohen’s kappa (95% CI) was 0.90 (0.82–0.98) for stage, indicating almost perfect reliability (94).

In collaboration with the statistician at the Faculty of Dentistry, sample size calculations were performed. In order to detect and document oral conditions with a prevalence of 10%, and the possibility for longitudinal follow-up of the participants with a dropout rate of 50%

after 5 years, a final sample size estimate was 450 individuals. For chemosensory examinations, only half of the sample was recruited due to time limitations. Therefore, future chemosensory longitudinal analyses using data from these participants, will depend on the response rate in follow-up studies. However, for this cross-sectional study the sample size was considered sufficient. Furthermore, the study sample in the present thesis included individuals from the general population and not a group of patients with certain diagnoses.

This leads to difficulties when investigating associations with the main outcome of interest, e.g. periodontitis or chemosensory disorders, and risk indicators due to small groups and thereby low power in the statistical analyzes. In addition, in studies including samples from the general population rather than a sample of patients, classification of diseases into subgroups according to disease severity may also lead to small samples of the most severe groups of the diseases. This may lead to the need to merge groups of different disease severity in order to achieve enough power in the statistical analysis. In these cases, differences between severity groups of diseases may not be identified.

The cross-sectional design used in the present study, limits the ability to assess causality between an exposure variable and outcome variable (95). The ideal design to investigate causal relationships is a longitudinal study. However, results from cross-sectional studies can be important for generating hypothesis for further studies. In addition, data from the

present study are planned to be used as a baseline for follow up studies.

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Paper I

Periodontal conditions in a 65-year-old population and prevalence of periodontitis according to three different bone level thresholds

In this study we investigated the periodontal status based on the 2017 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions (27, 86, 87) among 454 individuals, all 65-years of age and living in Oslo. Due to the lack of a clear cutoff for case definition in the 2018 European Federation of Periodontology/American Academy of Periodontology classification system, we also explored to what extent the choice of

radiographic bone level cutoffs for periodontitis case definition influences the disease prevalence estimates.

The mean number of teeth in the present study sample was 25.6 (SD = 3.4), ranging from 4 to 28 remaining teeth. In the present study population, bleeding on probing (BoP) in ≥ 10%

of sites was present in 24.9% of the participants and 74.7% of the participants had one or more periodontal pockets that were ≥ 4 mm. According to a 3 mm radiographic bone loss (RBL) cutoff, the prevalence of periodontitis in the present study population was 52.6%. In addition, 38.1% of the participants had periodontitis and at least one PPD ≥ 5 mm, or PPD ≥ 4 mm with BoP, indicating a large proportion with periodontal treatment needs. Regarding the severity of periodontitis, 16.5% of the participants were assigned to stage II, 32.8% to stage III and 3.3% to stage IV. No participants were assigned to stage I periodontitis in the present study. Periodontitis grade based on percentage of radiographic bone loss measured on the worst affected tooth divided by age and grade modifiers (i.e., smoking and diabetes type 2) resulted in 44.7% of the participants assigned to grade B periodontitis, while 7.9% were assigned to grade C. When changing the RBL cutoff level for defining a periodontitis case from > 3 mm to > 2 mm and further to > 1 mm, the prevalence of periodontitis cases increased to 91.9% and 99.6% respectively (Figure 2).

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Figure 2. Prevalence of periodontitis according to a 3 mm (A), 2 mm (B), and 1 mm (C) radiographic bone loss cutoff

The use of different examination procedures and diagnostic classifications in different studies may lead to challenges in summarizing epidemiological research. Several different case definitions and classification systems have been used in previous studies investigating periodontal disease (96-98), which makes comparisons of prevalence across studies difficult (22, 99, 100). The consensus report from the 2017 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions, concluded that future research should “use existing databases/develop new databases that will facilitate the

implementation, validation and continuous refinement of the newly introduced periodontitis classification system“ (86). Even though the consensus report presents cutoffs with respect

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to clinical attachment loss (CAL) for staging periodontitis cases, no exact value for CAL for periodontitis case definition is given. The results in the present study showed that a change in the radiographic bone loss cutoff from 3 mm to 2 mm and 1 mm changed the estimated prevalence considerably. This indicates a need for a clearer case definition cutoff to enable comparison of prevalence across studies.

Furthermore, the present study showed that measurements necessary for assigning periodontitis stage and grade according to the consensus report are time consuming. This indicates that the consensus report in its current form is poorly applicable in large

epidemiological studies where several aspects of oral health are included. Due to time limitations in the clinical examinations, measurements necessary for calculating CAL were not performed in the present study. Therefore, the most extreme RBL measured on bite wing radiographs was used to identify periodontitis cases, however, potential bone loss in frontal areas may not have been identified. As previously described by Tonetti et al. (87), the use of RBL instead of CAL for identifying periodontitis cases may lead to underestimation of the disease prevalence. In the absence of CAL measurements, it would be preferable to use periapical (PA) radiographs for the measurement of radiographic bone loss, which also would have made it possible to include the frontal areas. Furthermore, bone loss in frontal areas used in the staging procedure of periodontitis may often be difficult to measure on OPGs. This led to some missing values where the bone level was not possible to assess.

Therefore, the use of PA radiographs in the staging procedure instead of OPGs could have led to a higher prevalence of more severe periodontitis in this population. However, taking PA radiographs of the complete dentition in all participants would have required more time and personal in the present study, and was therefore not possible to implement in the study protocol. At the same time, when considering the RBL for the case definition, BW

radiographs using parallel technique instead of OPG, probably enabled a more precise registration of bone destruction.

A clear strength of the present study method was the full mouth registration of periodontal parameters, which has been considered as a gold standard (101). In addition, reporting detailed information of both BoP and PPD were important to make it easier to compare prevalences across studies using different case definitions. However, pseudo pockets might lead to a challenge in cross-sectional studies where PPD is registered without an initial hygiene instruction prior to the measurement. It might be speculated that the use of PPD for identifying cases will lead to an overestimation in prevalence of periodontitis, however, this was not the case in the present study protocol. When classifying non-periodontitis cases as individuals with periodontal health or gingivitis cases, a challenge appeared in using the consensus report from 2018 (27). According to the consensus report, cases with both PPD >

3 mm and ≥ 10% teeth with BoP, but no radiographic bone loss > 3 mm, are categorized

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neither as gingivitis cases or periodontitis cases. In the present study, due to the lack of initial hygiene instruction, these pockets were considered as pseudo pockets, and the relevant participants were categorized as gingivitis cases.

Paper II

Periodontitis in a 65-year-old population: risk indicators and impact on oral health-related quality of life

In addition to reporting the prevalence of disease, it is important to investigate possible risk indicators and determine whether the disease has an impact on the quality of life of affected individuals. Therefore, paper II aimed to investigate risk indicators for severe periodontitis in a 65-year-old population in Oslo, Norway, and to examine how the disease impacted on their oral health-related quality of life.

In the present study, non-western birth country, diabetes type 2 and smoking were found to be significant risk indicators for severe periodontitis (stage III or IV periodontitis).

Participants with severe periodontitis reported a significantly higher OHIP-14 total score (mean: 4.7, SD: 7.4) than non-periodontitis participants (mean: 2.9, SD: 4.9). When using a cutoff for negative impact (“fairly often” or “very often” to at least one of the OHIP-14 items), no significant differences were found between individuals with severe periodontitis and non-periodontitis participants (Figure 3).

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Figure 3. Proportion of individuals reporting negative impact on oral health-related quality of life (“fairly often” or “very often” to at least one of the OHIP-14 items) among participants with stage III or IV periodontitis (A), stage II periodontitis (B) and non-periodontitis

participants (C)

Due to the risk indicators for severe periodontitis revealed in Paper II some aspects

regarding the prevalence reported in this thesis should be discussed. In the present sample population, the prevalence of current smokers was 10%, which is slightly lower than in the target population where the prevalence is 12% (based on register data from Statistics

Norway). The results in paper II showed a significant increased risk for severe periodontitis in current smokers compared to never smokers. Hence, it can be speculated that the

prevalence of severe periodontitis may be even higher in the target population than reported in the present sample population (paper I). In addition, individuals with western country of birth were overrepresented in the present sample population compared to the study population. Therefore, increased risk for severe periodontitis among individuals born

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in non-western countries shown in this study may also suggest an underestimation of the prevalence of severe periodontitis in the present sample population compared to the general population of 65-year-olds living in Oslo.

Regarding oral health-related quality of life, this study revealed some differences between participants with periodontitis and non-periodontitis participants. However, even though individuals with severe periodontitis reported a significantly higher OHIP-14 total score compared to non-periodontitis participants, there was no significant difference in the

proportion of individuals reporting a negative impact on the oral health-related quality of life in the present study. Some challenges interpreting results from OHRQoL-measurements have previously been discussed (102). Using the sum score of a scale comprised of several items, each with frequency alternatives, may lead to individuals with different response profiles being treated as the same in an analytical setting due to them having the same sum score (102). However, there may be differences in an individuals´ experience of what affects their OHRQoL. As discussed by Tsakos et al., using OHIP-14 with response alternatives

ranging from 0 to 4, an individual answering ‘Hardly ever’ (= 1) to all 14 items would be given the same total score (= 14) as an individual who responded ‘Very often’ (= 4) to three items,

‘Sometimes’ (= 2) to one and ‘Never’ (= 0) to the remaining ten items (102). Therefore,the use of a cutoff for prevalence of chosen response alternatives, and description of these prevalences, would probably give a more accurate picture of different response profiles in the study. In the present work, participants responding “Fairly often” or “Very often” were considered as experiencing negative impacts on OHRQoL.

The OHIP-14 questionnaire has been used in comparable Norwegian population samples (40, 103). However, different domain structures have been identified when factor analyses have been done in different sample populations (104-107). Due to time restrictions, a separate article discussing the methodological aspects of the OHIP-14 instrument in this sample population was not possible in this thesis. Therefore, periodontitis in relation to certain domains of OHIP-14 in the present study should be interpreted with caution. In addition, duplicate assessment of the OHIP-14 instrument to test its reproducibility in the present study sample was also not possible due to time constrains and logistics.

The literature regarding associations between periodontitis and oral health-related quality of life is inconsistent (29). However, a lower number of remaining teeth has been associated with lower quality of life (41, 108). As progression of periodontal disease may lead to a reduced number of teeth, periodontal treatment and preventive measures in early stages of the disease will be important to prevent disease progression and a possible reduction of OHRQoL in the population.

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Paper III

Smell, taste and trigeminal disorders in a 65-year-old population

In this study, chemosensory function (smell and taste) was investigated in 223 individuals (123 men, 100 women), randomly selected from study sample of the OsloMunn65 study.

The aim of the study was to determine the prevalence of smell, taste and burning mouth sensation in a 65-year-old population in Oslo, Norway, and to investigate associations between these disorders and gender, the presence of chronic diseases and use of medications, smoking, and salivary secretion rates.

According to results from the Sniffin´ Sticks test and Taste Strips test, 34% of the participants had smell disorders (28% hyposmia (reduced smell function) and 6% anosmia (total loss of smell)), 28% had taste disorders (21% hypogeusia (reduced taste function) and 7% ageusia (total loss of taste)) and burning mouth sensation was reported by 4% of the participants. A combination of both smell and taste disorders was present in 13% of the participants.

Regarding taste function, sweet taste was most often identified correctly, while sour taste was least often identified correctly in all four concentrations. In addition, the present study showed that women had more sensitive smell- and taste function than men. Self-reported smell perception was significantly lower in anosmic individuals than to hyposmic and

normosmic participants. Hyposmic individuals also scored their smell perception significantly lower compared to normosmic participants. However, the majority of affected individuals had low awareness of reduced smell and taste function, and no significant differences in self- reported taste perception were found between normogeusic, hypogeusic and ageusic participants. Furthermore, within this study population, some diseases and medications were associated with chemosensory disorders and burning mouth sensation.

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As mentioned, this study showed an overall low awareness of reduced smell and taste function among affected individuals. Furthermore, there was a low agreement between the results for self-reported smell and taste and the measured values. Since participants in this study represent the general population and not a selected group of people suffering from known chemosensory loss, participants with reduced smell perception may not have been aware of their condition. The visual analogue scale used in the present study has previously been used to investigate self-reported smell and taste perception in patients with Sjögren’s syndrome and healthy individuals (74, 75, 109, 110). Rusthen et al. found a significant positive correlation between measured and self-reported smell and taste ability in Sjögren’s patients (74). Landis et al. did not find a significant correlation between self-reported olfactory function prior to olfactory testing and measured olfactory function in healthy individuals (110). It might be speculated that the use of VAS for assessment of self-reported chemosensory function might be more suited when individuals with specific disorders are included rather than individuals from the general population. The fact that the present study showed low agreement between measured and self-reported smell and taste scores may indicate that smell and taste perception assessed by a VAS might be subject to individual interpretation. Considering this, the use of VAS for assessment for self-reported olfactory and gustatory function in a general population might be more suitable in longitudinal studies. They can be used to compare changes in VAS scores from start to follow up rather than comparing scores between individuals in a cross-sectional study.

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Regarding the examination of gustatory (taste) function, taste strips (Burghart Messtechnik GmbH, Wedel, Germany) can be used for both lateral testing of the tongue and whole mouth testing (81). The lateral test enables detection of function separately on both sides of the tongue. However, since the aim of this study was to investigate an overall prevalence of taste disorders and not disorders related to specific regions of the tongue or nerves, the whole mouth testing method was used. It can be speculated that this gives a more realistic picture of the taste perception and is more relevant for the participants who uses taste receptors throughout the oral cavity at the same time.

Olfactory function was tested using Sniffin` Sticks-Identification test (Burghart Messtechnik GmbH, Wedel, Germany) consisting of 12 felt-tip odor pens. Ideally, a test including both threshold, discrimination and identification resulting in a TDI-score (threshold,

discrimination, identification), would give a more comprehensive assessment of the

olfactory function. However, due to time limitation in this study, only identification test for screening of olfactory function was performed.

In the present study, participants were asked if they had experienced a burning sensation in the mouth. They were also asked to specify the location of the burning sensation.

Disturbances in the trigeminal nerve may often lead to a burning mouth sensation. However, for diagnosing trigeminal disorders a more comprehensive examination and recording of symptoms would have been necessary. Because the burning mouth sensation was assessed through a few questions with no further examination, we decided to not use the term burning mouth syndrome that would have required a more strict assessment to diagnose (111).

The individuals included in the chemosensory examination also answered the OHIP-14 questionnaire. A significantly higher percentage of individuals with ageusia (27%) reported negative impact on OHRQoL (“Fairly often” or “Very often” to at least one of the OHIP-14 items) compared to normogeusic participants (6%). No significant association was found between hypogeusic (15%) and ageusic or normogeusic participants. Regarding smell function, a significant larger proportion of hyposmic participants (18%) reported negative impact on OHRQoL compared to normosmic participants (6%). No significant association was found between anosmic (7%) and hyposmic or normosmic participants. However, the power in these analyses can be discussed due to small samples of individuals with different severity of smell and taste disorders. In addition, the applicability of the OHIP-14 instrument in these analyses can be discussed. Even though the chemosensory function includes physiological processes that takes place in the oral cavity and adjacent tissues, some individuals might not

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consider smell and taste function as a part of oral health when answering the oral health- related quality of life measure.

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Discussion of major findings

The results indicated a substantial need for periodontal treatment among this population of 65-year-old Oslo citizens. By reporting the stages and grades of periodontitis in the

population, this work also provides information about the proportion of individuals that requires different levels of treatment complexity, and may help for planning the resources in dental services. To be able to prevent an increase of periodontal disease in the elderly population in the years to come, it will be of importance that dental health professionals are able to both detect periodontitis at early stages, and help in the prevention of this disease.

The risk indicators for severe periodontitis revealed in this study, i.e. non-western country of birth, diabetes type 2 and smoking, are important to highlight in order to ensure awareness among high risk individuals, but also among health authorities, and medical and dental professionals, so that the necessary preventive measures are initiated. Furthermore, the results from the present work indicating that periodontitis in early stages does not have a great impact on oral health-related quality of life in affected individuals, and highlights the importance of regular dental visits so that these stages of periodontitis can be discovered and necessary treatment be initiated. It is also important for dental professionals to be able to inform and advise patients about any necessary health behavior changes. Such preventive programs have shown to have a positive effect on reducing periodontitis (112-115).

The results showed that one-third of the participants had impaired smell function and more than one fourth had impaired taste function. However, the results also showed low

awareness of chemosensory disorders among affected individuals indicating that these disorders might not have a large impact on the life of individuals in the present sample.

Nevertheless, it is important to raise awareness of possible changes in these senses throughout life, for example as a result of diseases or medications more frequent used in older age, in order to prevent any harmful consequences such as negative changes in dietary composition or difficulties of detecting smoke or other dangerous situations. Therefore, this study indicates a need for attention towards detection, diagnostics and treatment of

chemosensory disorders in the Norwegian health sector.

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Concluding remarks and future perspective

This thesis provides new knowledge about the prevalence of periodontitis and

chemosensory disorders among a large sample of 65-year-olds living in Oslo. In addition, the thesis highlights possible risk indicators for these conditions as well as the young elderly individuals´ awareness of these conditions and the possible effects on their oral health- related quality of life.

The present work showed that approximately half of the participants had periodontitis, and the majority of these had unstable, recurrent periodontitis. However, there was no

significant difference in the proportion of individuals reporting a negative impact on OHRQoL in non-periodontitis participants compared to individuals with periodontitis. The present work also indicated a low awareness of chemosensory disorders among the affected individuals. Lack of awareness in relation to diseases in general prevent individuals seeking health services until the disease has progressed to a state where more complex treatment is needed. Therefore, preventive measures and oral health advices to the population are important for preventing the progression and negative consequences of oral diseases. In addition, in order to prevent an increase in burden of diseases among the elderly in the years to come, information that strengthens the awareness of healthcare personnel,

including dentists, general physicians, and staff in nursing homes, etc., about conditions that can affect oral health will be increasingly important. Furthermore, appropriate knowledge about preventive measures that should be implemented for individuals at risk will be crucial.

In order to achieve this, interdisciplinary collaboration across different health disciplines will be important in the years to come.

At present, it can be expected that the participants in the OsloMunn65-study mostly use private dental services. According to the current subsidized scheme for dental services in Norway, patients can receive subsidized treatment in relation to certain diagnoses, e.g.

periodontitis – a diagnosis scheme. However, when individuals receive home care services or are living in a nursing home, they have the right to public dental services free of charge independent of diagnoses – a budget-based scheme. Therefore, as the proportion of elderly people in the population increases, the need for public dental services will most likely also increase. This trend will either require more funding of the public dental health services, or a change in the current system structure. Data from the present work contribute with

prevalence data, which may be of use for planning future health services.

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Oral health status among 65-year-olds in Oslo, Norway; periodontitis, chemosensory disorders, and oral health-related quality of life