A scoping review of anorexia of aging correlates and their relevance to population health interventions

Appetite 105 (2016) 688e699

Contents lists available at ScienceDirect

Appetite journal homepage: www.elsevier.com/locate/appet

A scoping review of anorexia of aging correlates and their relevance to population health interventions
le ne Payette a, e Mathieu Roy a, b, *, Pierrette Gaudreau c, d, He a Research Center on Aging, Eastern Townships Integrated University Center for Health & Social Services e Sherbrooke Hospital University Center, Sherbrooke, Qu
ebec, Canada b Department of Family Medicine and Emergency Medicine, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Qu
ebec, Canada c Laboratory of Neuroendocrinology of Aging, Centre Hospitalier de l’Universit
e de Montr
eal Research Center, Montreal, Qu
ebec, Canada d Department of Medicine, Faculty of Medicine, University of Montreal, Montreal, Qu
ebec, Canada e Department of Community Health Sciences, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Qu
ebec, Canada

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 February 2016 Received in revised form 27 June 2016 Accepted 28 June 2016 Available online 1 July 2016

Anorexia of aging (AA, i.e., loss of appetite and/or reduction of food intake with aging) is an important public health issue. It leads to unintentional weight loss, which is an independent risk factor for morbidity and mortality among seniors. AA has mainly been studied from a biological perspective and regarded as a normal physiological consequence of aging, rather than a negative health outcome with underlying determinants. Some potentially modifiable correlates have however been found to be associated with this geriatric condition. Here, we conducted a scoping review of the literature to: 1) identify AA correlates, and 2) discuss their relevance to population health interventions. Our results indicate two main categories of AA correlates, namely, physiopathological and non-physiopathological. The first category relates to physiological dysfunctions, pathologies involving (or culminating in) biomarker dysregulation, and polypharmacy. These correlates are difficult to modify, especially through population health interventions. The second category, which contains fewer correlates, includes potentially modifiable public health targets, such as food-related properties, psychological, sociocultural, and environmental issues. We conclude that there are several AA correlates. Some of them are modifiable and could be targeted for development and implementation as appropriate population health interventions to prevent appetite loss and promote maintenance of adequate food intake in aging. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Appetite Anorexia Weight loss Elderly Aged Review

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 689 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 689 2.1. Stage 1: formulation of research questions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 689 2.2. Stage 2: identification of relevant studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690 2.3. Stage 3: study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690 2.4. Stage 4: data charting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690 2.5. Stage 5: collating, summarizing and reporting results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690 2.6. Stage 6: relevance of identified correlates to population health interventions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692 3.1. Results of the selection procedure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692 3.2. Results of scoping review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692 3.3. Physiopathological correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692

* Corresponding author. Eastern Townships Integrated University Center for
bec Health & Social Services e CHUS, 375 rue Argyll (Office 3628), Sherbrooke, Que J1J 3H5, Canada. E-mail address: [email protected] (M. Roy). http://dx.doi.org/10.1016/j.appet.2016.06.037 0195-6663/© 2016 Elsevier Ltd. All rights reserved.

M. Roy et al. / Appetite 105 (2016) 688e699

4.

5.

689

3.3.1. Risk of infection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692 3.3.2. Biomarkers (proteins/hormones/peptides/neurotransmitters/minerals) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695 3.3.3. Gastrointestinal tract dysfunctions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695 3.3.4. Chemosensory changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695 3.3.5. Pathologies and dysfunctions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.3.6. Polypharmacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.4. Non-physiopathological correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.4.1. Food-related properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.4.2. Psychological correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.4.3. Sociocultural correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 3.4.4. Environmental correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 4.1. Summary of findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 4.2. Physiopathological correlates: a close relationship with aging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 4.3. Non-physiopathological correlates: a promising avenue for population health interventions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 696 4.4. Need for original and innovative research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 4.5. Correlates are causes or consequences? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 4.6. Strengths and limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697

1. Introduction Aging has been associated with loss of appetite and/or reduced food intake in both cross-sectional (Briefel et al., 1995; Callen & Wells, 2005; Silver, Guillen, Kahl, & Morley, 1993) and longitudinal studies (Hallfrisch, Muller, Drinkwater, Tobin, & Andres, 1990; Sjogren, Osterberg, & Steen, 1994; Sorbye et al., 2008). This decline in appetite and/or food intake is a condition termed Anorexia of aging (AA; Landi et al., 2013; Muscaritoli et al., 2010; Morley, 1997). Its prevalence ranges from 23% to 62% in hospitalized seniors (Ahari & Kimigiar, 1997; Elmstahl & Steen, 1987; Guigoz, Vellas, & Garry, 1996) and may reach 85% in elderly nursing home populations (Ahmed & Haboubi, 2010; Guigoz, Lauque, & Vellas, 2002). The prevalence of this geriatric condition in free-living seniors (Inouye, Studenski, Tinetti, & Kuchel, 2007) varies from 5% to 25% (Ahmed & Haboubi, 2010; Donini et al., 2011; Guigoz et al., 1996, 2002; Landi et al., 2012). AA usually leads to weight loss (Landi et al., 2000; Morley, 2007a), and losing weight, whether intentionally or not (Tayback, Kumanyika, & Chee, 1990), is an independent risk factor for institutionalization, morbidity, and all-cause mortality among freeliving frail elders (Payette, Coulombe, Boutier, & Gray-Donald, 1999; Payette, Coulombe, Boutier, & Gray-Donald, 2000), seniors in assisted living facilities (Cartwright, Hickman, Perrin, & Tilden, 2006), geriatric rehabilitation settings (Cornali, Franzoni, Frisoni, & Trabucchi, 2005; Sullivan & Walls, 1994; Sullivan, Patch, Walls, & Lipchitz, 1990) or at home but receiving assistance (Landi et al., 2012). Numerous other adverse outcomes have also been associated with AA, such as functional impairment, reduced cognitive capacities, psychological distress and depression (Boer, Horst, & Lorist, 2012; Landi, Laviano, & Cruz-Jentoft, 2010), diminished immunocompetence (Chapman & Nelson, 1994), cachexia (Morley, 2001a), and poor overall quality of life (Bostick, Rantz, Flesner, & Riggs, 2006; Landi et al., 2010). Loss of appetite and/or reduction of food intake after 65 years of age are not desirable, owing especially to increased vulnerability to nutritional deficiencies (Chandra, Imbach, Moore, Skelton, & Woolcott, 1991) and malnutrition (Allaz, Bernstein, Rouget, Archinard, & Morabia, 1998) among seniors. All these associations highlight why AA is so often linked with slower gait speed, poorer endurance, decreased

mobility and exercise capacity (Morley, 2001a), lower muscle mass (i.e., sarcopenia) and strength (i.e., dynapenia: Boer et al., 2012; Muscaritoli et al., 2010) and, ultimately, frailty (Martone et al., 2013). Based on current demographic transition, on deleterious consequences of AA and on its linkage with frailty (Martone et al., 2013), it is of public health relevance to identify modifiable correlates of this geriatric condition. Such information is needed to develop population health interventions aimed at preventing appetite loss and promoting the maintenance of adequate food intake during aging. An at-a-glance overview of the AA literature highlighted that many scientific efforts have been made to better understand the biological mechanisms involved in appetite loss with age, at the expense of identifying relevant and potentially modifiable correlates on which to build appropriate public health strategies. A scoping review of the literature was then performed to address this issue, with the objectives of: 1) identifying AA correlates, and 2) discussing their relevance to population health interventions.

2. Materials and methods This scoping review was conducted according to the Arskey & O’Malley procedure (2005). Five stages were completed in agreement with the procedure: 1) formulation of research questions, 2) identification of relevant studies, 3) study selection, 4) data charting, and 5) collating, summarizing, and reporting the results. Because the purpose of this scoping review was also to discuss the relevance of identified correlates with respect to population health interventions, we added a sixth stage to address the issue (Levac et al., 2010).

2.1. Stage 1: formulation of research questions We formulated two research questions: 1) What are AA correlates? and 2) Are these correlates modifiable and relevant to population health interventions?

690

M. Roy et al. / Appetite 105 (2016) 688e699

2.2. Stage 2: identification of relevant studies

2.4. Stage 4: data charting

We defined two lists of keywords. The first list (i.e., senior, elder, older, aging) collected literature on seniors, and the second list (i.e., anorexia, loss of appetite) found AA studies. All combinations of keywords (n ¼ 8) were entered in the following databases in August 2015: 1) MedLine (1948e2015), 2) Embase (1980e2015), 3) PsycINFO (1967e2015), and 4) AgeLine (1944e2015).

The data extracted from retained studies are chartered in Tables 2 and 3. Table 2 contains original research, and Table 3 refers to other types of publications.

2.5. Stage 5: collating, summarizing and reporting results

2.3. Stage 3: study selection Selection was two-step. First, all keyword combinations were entered in each database. The title and abstract of each resulting hit were examined. Articles with a title or an abstract containing keywords from both lists were retained. The remaining articles were selected according to five criteria: 1) sample/sub-sample of adults aged 65 years, 2) living in a Western industrialized society, 3) French or English, peer-reviewed, 4) AA (no other type of anorexia), and 5) information on any AA correlates. Articles not meeting these criteria were excluded (Table 1).

The results of this review are collated, summarized, and reported below. Identified correlates are summarized in Tables 4 and 5.

2.6. Stage 6: relevance of identified correlates to population health interventions In the discussion section, results were discussed with respect to their relevance to population health interventions aimed at preventing appetite loss and promoting adequate food intake in older adults.

Table 1 List of excluded articles (n ¼ 101) and rationale for exclusion. Excluded article 1-Ariyasu, Nakao, Hiroyuki, & Kazua (2006) 2-Inui (2004) 3-Bauer et al. (2007) 4-Kinner & Reuter (1986) 5-Starzomska (2008) 6-De la Montana Miguelez, Areal Salve, & Miguez (2009)
rez-Cruz, Melandez-Mier, & Caballero-Romo (2007) 7-Pe 8-Serra Prat, Fernandez, Ribo, Palomera, Papiol, & Serra (2008) 9-Hirschmann, Apter, Weizmann, & Radwan (1996) 10-Steinbach, Staudenmeier, Hummel, & Arnold (2008) 11-Gupta, Punetha, & Diwan (2006) 12-Majumder, Saha, & Chaudhuri (2014) 13-Lelovics (2009) 14-Petervari, Garami, Soos, Szekely, & Balasko (2010) 15-Foo (2009) 16-Huang, Wahlqvist, & Lee (2014) 17-Inagaki, Horiguchi, Tsubouchi, Miyaoka, Uegaki, & Seno (2002) 18-Suzana, Earland, Suriah, & Warnes (2002) 19-Vasquez-Valdez, Aguilar-Navarro, & Avila-Funes (2010) 20-Galloway et al. (2002)

Rationale Not written in French or English (n ¼ 10) Written in Japanese (n ¼ 2) Written in German (n ¼ 3)

Written in Spanish (n ¼ 3)

Written in Hebrew (n ¼ 1) Written in Polish (n ¼ 1) Not living in Western industrialized society (n ¼ 10) India (n ¼ 2) Hungary (n ¼ 2) China (n ¼ 1) Taiwan (n ¼ 1) Japan (n ¼ 1) Malaysia (n ¼ 1) Mexico (n ¼ 1) 8 developing countries (n ¼ 1) No seniors (n ¼ 10)

21-Boast, Coker, & Wakeling (1992) 22-Bowler (1992) 23-Cumella, Wall, & Kerr-Almeida (2000) 24-Fox & Leung (2009) 25-Gupta (1988) 26-Halmi, Casper, Eckert, Goldberg, & Davis (1979) 27-Joughin, Crisp, Gowers, & Bhat (1991) 28-Russell & Gilbert (1992) 29-Scholtz, Hill, & Lacey (2010) 30-Wolden-Hansson (2006) 31-Alfin-Slater & Friedman (1978) 32-Berg, Andersen, Yagger, Powers, 2007 33-Mitchell (1997) 34-Savina, Donini, Cannella, & Swain (2006) 35-Apolzan (2010)

Not article (n ¼ 5) Book chapter (n ¼ 4)

Dissertation abstract (n ¼ 1) Not peer-reviewed (n ¼ 2)

M. Roy et al. / Appetite 105 (2016) 688e699

691

Table 1 (continued ) Excluded article

Rationale

36-Lodge (2006) 37-Sandrick (1988) 38-Bloom (1996) 39-Cohen (2002) 40-Cosford & Arnold (1992) 41-Golden, Petropoulos, Silverman, Musson, & Hamdan (2003) 42-Hewitt, Coren & Steel (2001) 43-Keith & Midlarsky (2004) 44-Laws & Golding (1996) 45-Mangweth-Matzek, Hoek, & Pope (2014) 46-Manajias Parke, Yager, & Apfeldorf (2008) 47-Nicholson & Balance (1998) 48-Nottingham & Emerson (1991) 49-Pellerin, Mure-Petitjean, & Boiffin (2000) 50-Pobee & Lapalio (1996) 51-Preti et al. (2009) 52-Ronch (1985) 53-Wills & Olivieri (1998) 54-Battaglia et al. (2011) 55-Cartwright, Hickman, Perrin, & Tilden (2006) 56-Dorner (2005) 57-Elsner (2002) 58-Johns, Newton, Westley, & May (2006) 59-Kohrs (1981) 60-Lucas (1990) 61-McAlpine, Harper, McMurdo, Bolton-Smith, & Hetherington (2003) 62-Morley (1993) 63-Vincent, Lauque, Lanzmann, Vellas, & Albarede (1998) 64-Harpole & Williams (2004) 65-Kivela, Kingas-Saviaro, Kimmo, Kesti, & Laippala (1996) 66-Potter, Mcquoid, & Steffens (2015) 67-Baumann, Putz, Rohrig, Hoffken, & Wedding (2009) 68-Thekmedyian, Zahyna, Halpert, & Heber (1992) 69-Kerstetter, Holthausen, & Fitz (1992) 70-Nijs, de Graaf, van Staveren, & de Groot (2009) 71-Visvanathan & Chapman (2010) 72-McCarthey, Addington-Hall, & Altmann (1997) 73-Stahlmann & Lode (2010)

Topic other than AA (n ¼ 36) Anorexia nervosa (n ¼ 16)

Geriatric nutrition (n ¼ 10)

Depression (n ¼ 3)

Nutrition/quality of life among cancer patients (n ¼ 2) Malnutrition (n ¼ 2) Sarcopenia (n ¼ 1) Dementia (n ¼ 1) Medications (n ¼ 1) Incidental mention of AA (n ¼ 6)

74-Brymer & Winograd (1992)
ger et al. (2002) 75-Le 76-Paker-Eichelkraut et al. (2013) 77-Pilotto et al. (2006) 78-Pulska, Pahkala, Laippala, & Kivela (2000) 79-Rigler, Webb, Redford, Brown, Zhou, & Wallace (2001) No correlate of AA (n ¼ 22) 80-Bartlett (1990) 81-Blundell (1988) 82-Cuervo, Ansorena, Garcia, Astiasaran, & Martinez (2008) 83-Di Francesco et al. (2006) 84-Di Francesco et al. (2010) 85-Donini, Savina, & Cannella (2010) 86-Dorf (1998) 87-Giannini (1998) 88-Haren, Kim, & Kevorkian (2006) 89-Howden (1997) 90-Martinez, Arnalich, & Hernanz (1993) 91-Mermelstein & Basu (2000) 92-Miller, Morley, Rubenstein, & Pietruszka (1991) 93-Muscaritoli et al. (2010) 94-Pouyssegur & Lupi-Pegurier (2015) 95-Sarkisian, Gruenewald, Boscardin, & Seeman (2008) 96-Shock (1988) 97-Sturm, MacIntosh, Parker, Wishart, Horowitz, & Chapman (2003) 98-Sullivan et al. (2002) 99-Thomas (2005) 100-Wilson, Philpot, & Morley (2007) 101-Wurtman (1988)

692

M. Roy et al. / Appetite 105 (2016) 688e699

Table 2 Correlates of AA identified in articles including original results (n ¼ 15). Reference

Country

Design Descriptive characteristics

Martinez, Arnalich, Vasquez, & Hernanz et al. (1993) and Martinez, Hernanz, et al. (1993) Martinez, Arnalich, et al. (1993) and Martinez, Hernanz, et al. (1993) Clarkston et al. (1997)

Spain

EXP

Spain

EXP

USA

EXP

Portnoi (1997)

USA

CR

re, Dormenval, Budtz-Jorgensen, Mojon, Bruye and Rapin (1998) MacIntosh et al. (2001)

Switzerland CS Australia

EXP

Savina et al. (2003)

Italy

CS

Hughes, Bennett, and Hetherington (2004)

UK

CS

Cornali et al. (2005)

Italy

CS

Donini et al. (2008)

Italy

CS

Landi et al. (2010)

Italy

LG

Landi et al. (2012)

Italy

LG

Roy et al. (2015)

Canada

LG

Sarkisian et al. (2008)

USA

LG

van der Meij et al. (2015)

Netherland CS

n ¼ 14 (AA ¼ 100%, x age ¼ 78, \ ¼ 75%) n ¼ 14 (AA ¼ 100%, x age ¼ 78, \ ¼ 75%) n ¼ 14 (AA ¼ 100%, x age ¼ 76, \ ¼ 64%) n ¼ 3 (AA ¼ 100%, 2 \ aged 89 and 87, 1 _ aged 93) n ¼ 99 (AA ¼ 53.5%, x age ¼ 82, \ ¼ 76%) n ¼ 12 (AA ¼ 100%, x age ¼ 71.2, \ ¼ 50%) n ¼ 103 (AA ¼ 27.2%, x age ¼ 80.4, \ ¼ 66%) n ¼ 39 (AA ¼ 64.1%, x age ¼ 74.8, _ ¼ 100%) n ¼ 316 (AA ¼ 15.8%, x age ¼ 81, \ ¼ 82%) n ¼ 96 (AA ¼ 33.3%, \ ¼ 69%) n ¼ 364 (AA ¼ 21.5%). Among AA, (x age ¼ 86.8; \ ¼ 76%) n ¼ 2787 (AA ¼ 26.7%). Among AA (x age ¼ 81.0; \ ¼ 57%) n ¼ 1548 (AA ¼ 7.0%). Among AA (\ ¼ 74%) n ¼ 1189 (AA ¼ 18.7%) n ¼ 349 (AA ¼ 32.3%). Among AA (x age ¼ 80.8; \ ¼ 68%)

Setting

Correlates of AA

Freeliving Freeliving Freeliving SU

1) Y Glutamic acid levels, 2) [ Glutamine levels in plasma and CSF 1) Y b-endorphin levels, 2) [ NPY levels in plasma and CSF, 3) [ CCK8s levels in plasma, 4) Y Somatostatin levels in CSF 1) Y Postprandial desire to eat and hunger, 2) Slower gastric emptying, 3) Autonomic nerve dysfunction 1) Helicobacter pylori infection

HOSP

1) Oral dryness and Y salivary secretion, 2) Y Albumin concentration in plasma 1) [ Basal CCK8s levels in plasma, 2) [ Satiating effect of exogenous CCK 1) Poverty, 2) Social isolation, 3) Inability to cook, 4) Functional impairment, 5) AN, 6) Cognitive decline 1) Social isolation, 2) Inability to cook

Freeliving RU Freeliving RU

1) Y Serum albumin

AU þ RU 1) Chewing and swallowing problems, 2) Constipation, 3) Inability to cook Free1) Functional impairment, 2) CD living Freeliving

1) Functional impairment, 2) Cognitive decline, 3) Chewing problems, 4) CD

Freeliving Freeliving AHRC, HOSP, NCH,

1) Depression, 2) Body weight dissatisfaction 1) Y Mobility, 2) Functional impairment 1) Food preferences

Note. AHRC ¼ At-home receiving care; AA ¼ Anorexia of aging; AN ¼ Anorexia nervosa; AU ¼ Acute unit; CCK ¼ Cholecystokinin; CCK8s ¼ CCK8 sulfated; CD ¼ Chronic disease; CR ¼ Case report; CS ¼ Cross-sectional study; CSF ¼ Cerebrospinal fluid; EXP ¼ Experimental study; HOSP ¼ Hospitalized; LG ¼ Longitudinal study; NCH ¼ Nursing care home; NPY ¼ Neuropeptide Y; RU ¼ Rehabilitation unit; SU ¼ Subacute unit; UK ¼ United Kingdom; USA ¼ United States of America.

3. Results 3.1. Results of the selection procedure Fig. 1 is the flow chart of this review. Keyword combinations yielded 2158 hits. Analysis of titles/abstracts gave 161 articles with combination of both keyword lists. Of these articles, 101 were excluded (Table 1). Ten because they were written in a language other than French or English: Japanese (n ¼ 2), German (n ¼ 3), Hebrew, Polish, and Spanish (n ¼ 3). Ten because seniors were not living in Western industrialized countries: China, Japan, Taiwan, Hungary (n ¼ 2), Mexico, India (n ¼ 2), Malaysia, and one study focused on eight developing countries. Ten were excluded because they did not include adults aged 65 years, five because they were not articles (i.e., 4 book chapters, 1 abstract), and two because they were not peer-reviewed. Other exclusion reasons were AA not being the main topic (n ¼ 36), absence (or passing mention) of this type of anorexia (n ¼ 6), and no information on AA correlates (n ¼ 22), bringing the final number of papers in this review to 60.

3.2. Results of scoping review We synthesized the 60 studies in two Tables. Table 2 summarizes 15 original research articles whereas Table 3 presents other types of publications (n ¼ 45; 30 narrative reviews, six position papers, two proceedings, two editorials, and five commentaries). Reading of these papers identified 100 different AA correlates. From these correlates, 77% were classified as physiopathological (Table 4) whereas 23% were considered to be non-physiopathological

(Table 5). Physiopathological AA correlates refer to physiological dysfunctions, pathologies involving (or leading to) biomarker dysregulation, and polypharmacy. On the other hand, nonphysiopathological correlates include potentially modifiable factors, such as food-related properties, psychological, sociocultural, and environmental circumstances.

3.3. Physiopathological correlates Physiopathological AA correlates are divided into six subcategories: 1) risk of infection, 2) biomarkers (proteins/hormones/ peptides/neurotransmitters/minerals), 3) gastrointestinal tract dysfunctions, 4) chemosensory changes, 5) pathologies and dysfunctions, and 6) polypharmacy.

3.3.1. Risk of infection Two studies warn about the associations between AA and higher risk of infection. One of them is a commentary which raises the ^do, Garcia Moreira, Marina Moraes, Sanchez, & association (Cane Lourenço, 2015), whereas the other is a case study of three seniors living in nursing home facilities (i.e., one man and two women aged 93, 89, and 87 years old, respectively), highlighting an association with Helicobacter pylori infection. According to Portnoi (1997), Helicobacter pylori infection plays a role in AA prevalence through gastric diseases, such as duodenal and gastric ulcers, gastric lymphoma, adenocarcinoma, and gastritis. Treatment with antibiotics and hydrogen-ion proton inhibitor reverses AA in these cases.

M. Roy et al. / Appetite 105 (2016) 688e699

693

Table 3 Correlates of AA identified in other types of publications (n ¼ 45). Authors

Type of paper

Correlates of AAa

Basille-Filler (1997)

PP

Benelam (2009) Bhutto and Morley (2008)

R R

^do et al. (2015) Cane Chapman (2007)

C R

Chapman (2004)

R

Chapman et al. (2002) Chapman and Nelson (1994) Di Francesco et al. (2007)

R C PP

Donini et al. (2003)

R

Gorbien (1994)

C

Hamerman (2002) Hays and Roberts (2006)

R R

Horwitz, Blanton, and McDonald (2002) Kmiec (2010)

R R

Landi et al. (2010) MacIntosh et al. (2000)

PP R

Massler (1980) Morley (2012) Morley (2010)

PP PP E

Morley (2007b) Morley (2007c) Morley (2005)

R R C

Morley (2003)

E

Morley (2002)

R

Morley (2001a) Morley (2001b)

R C

Morley (2001c)

R

Morley (1997) Morley (1996)

R R

Morley (1990)

R

1) Slower gastric emptying, 2) Gastric atrophy, 3) [ CCK levels in plasma, 4) Y Opioid feeding drive (rodents), 5) Y Mobility, 6) CD, 7) Bereavement, 8) Depression, 9) Dementia, 10) Poverty, 11) Social isolation, 12) POL 1) Slower gastric emptying, 2) [ CCK levels in plasma, 3) Y GHR levels in plasma 1) Changes in gut physiology, 2) Y T and [ LEP levels in men’s plasma, 3) Y Opioïd feeding drive (rodents), 4) Y Taste and smell, 5) Y Fundal compliance, 6) [ Antral stretch, 7) Slower gastric emptying, 8) Y Saliva production, 9) Smaller excursion of hyoid and larynx during swallowing 1) Depression, 2) Social isolation, 3) Sarcopenia, 4) [ Infection risk 1) Y Taste and smell, 2) Y Sensory-specific satiety, 3) [ Pro-inflammatory CYT concentration, 4) Changes in gut physiology, 5) Y Opioïd feeding drive (rodents), 6) Y T and [ LEP levels in men’s plasma, 7) Y GHR levels in plasma, 8) Y NPY levels in plasma and CSF, 9) [ CART levels in CSF (rats), 10) [ CCK levels in plasma, 11) [ PYY levels in plasma, 12) Y GAL sensitivity, 13) Poverty, 14) Social isolation, 15) Inability to shop/prepare/cook meals, 16) Failure to cater to ethnic food preferences in institutionalized settings, 17) Cardiac failure, 18) COPD, 19) Cancer, 20) Dysphagia, 21) Rheumatoid arthritis, 22) Malabsorption syndromes, 23) Gastrointestinal syndromes, 24) Hypermetabolism, 25) POL, 26) Poor oral health, 27) Depression, 28) Bereavement, 29) Dementia, 30) Alcoholism 1) Y NPY levels in plasma and CSF, 2) Y GAL sensitivity, 3) Y Orexin levels in plasma, 4) Y GHR levels in plasma, 5) Y T and [ LEP levels in men’s plasma, 6) [ CART levels in CSF (rats), 7) [ CCK levels in plasma, 8) [ PYY levels in plasma, 9) [ Pro-inflammatory CYT level 1) Y Sensitivity to gastrointestinal tract distension, 2) [ CCK levels in plasma 1) Muscle wasting, 2) Weakness, 3) Depression, 4) Y Immunocompetence, 5) Dementia, 6) Alcoholism, 7) POL 1) Poverty, 2) Social isolation, 3) Changes in gut physiology, 4) Depression, 5) POL, 6) Y Taste and smell, 7) Y Sensoryspecific satiety 1) Poor oral health, 2) Poverty, 3) Social isolation, 4) [ CCK levels in plasma, 5) Y Opioid feeding drive (rodents), 6) Y Taste and smell, 7) Y Fundal compliance, 8) [ Antral stretch, 9) POL 1) No access to food, 2) Poverty, 3) Social isolation, 4) Inability to shop/prepare food, 5) Depression, 6) Dementia, 7) Poor oral health, 8) Edentulism, 9) Parkinson disease, 10) Cardiac diseases, 11) COPD, 12) Hyperthyroidism, 13) Cancer, 14) Constipation, 15) Pain, 16) POL 1) Y NO circulating levels (marsupials, mice, rats), 2) Y T and [ LEP levels in men’s plasma 1) Poverty, 2) Social isolation, 3) Inability to buy/prepare/cook food, 4) Failure to cater to ethnic food preferences in institutionalized settings, 5) Depression, 6) Dementia, 7) Bereavement, 8) Alcoholism, 9) Late-life paranoia/mania, 10) Edentulism, 11) Dysphagia, 12) CD, 13) Pain, 14) Malabsorption disorder, 15) Diets, 16) Physical limitation, 17) Hypermetabolism, 18) POL, 19) Y Taste and smell, 20) Slower gastric emptying 1) Y Taste and smell, 2) Y NPY levels in plasma and CSF, 3) Y Opioid feeding drive (in rodents), 4) [ CCK levels in plasma, 5) [ Pro-inflammatory CYT level 1) Y NPY levels in plasma and CSF (rats), 2) Y AgRP in hypothalamus (rats), 3) Y GHR levels in plasma (rats), 4) Y Orexin levels in plasma (rats), 5) [ POMC levels in plasma (rats), 6) [ a-MSH levels in plasma (rats), 7) [ CART levels in CSF (rats) 1) Functional impairment, 2) Social isolation, 3) Poor cooking skills, 4) Depression, 5) Money, 6) Weakness/fatigue 1) Y NPY levels in plasma and CSF, 2) Y MCH levels in plasma (rodents), 3) Y GAL sensitivity, 4) Y GHR levels in plasma, 5) Y Orexins levels in plasma, 6) Y Oxytocin levels in plasma, 7) [ Motilin levels in plasma, 8) [ PYY levels in plasma, 9) Y Norepinephrine synthesis, 10) [ Dopamine levels in plasma, 11) Y Histamine levels in plasma (rats), 12) [ Proinflammatory CYT concentration, 13) Activation of CRF in hypothalamus, 14) [ INS levels in plasma (primates and rodents), 15) [ CCK levels in plasma, 16) [ GLP-1 levels in plasma, 17) [ Neuromedin levels in plasma (mice and rats), 18) [ Neurotensin levels in plasma, 19) [ a-MSH levels in plasma (rats), 20) [ Serotonin levels in CSF, 21) Y Estrogen levels in plasma (rats), 22) [ Isatin in plasma (mice), 23) [ Amylin in plasma, 24) [ Bombesin in plasma, 25) Slower gastric emptying, 26) Poverty, 27) Inability to shop/prepare/cook meals, 28) Social isolation, 29) Failure to cater to ethnic food preferences in institutionalized settings, 30) Alcoholism, 31) Bereavement, 32) Depression, 33) Dementia, 34) Cancer, 35) Cardiac failure, 36) COPD, 37) Dysphagia, 38) CD, 39) Parkinson, 40) Hypermetabolism, 41) Malabsorption syndrome, 42) POL 1) Y Taste and smell, 2) Y Blood supply to the brain and cell degeneration 1) Y Taste and smell, 2) POL, 3) [ CCK levels in plasma, 4) Depression, 5) Diets, 6) Cancer 1) Y Taste and smell, 2) Y T and [ LEP levels in men’s plasma, 3) Depression, 4) Y Fundal compliance, 5) [ CCK levels in plasma, 6) [ Amylin in plasma 1) Y Taste and smell, 2) Y Fundal compliance, 3) Autonomic nerve dysfunction (rodents) 1) Y Taste and smell, 2) Y T and [ LEP levels in men’s plasma 1) Y Taste and smell, 2) Y Fundal compliance, 3) Depression, 4) [ CCK levels in plasma, 5) Y T and [ LEP levels in men’s plasma, 6) POL 1) Y Fundal compliance, 2) [ CCK levels in plasma, 3) Depression, 4) Enhancing environment in which meals are eaten, 5) Mealtime 1) Ethnicity, 2) Setting, 3) Poverty, 4) Social isolation, 5) Y Mobility, 6) Swallowing difficulty, 7) Food availability, 8) Gastrointestinal changes, 9) Y Taste and smell, 11) [ Pro-inflammatory CYT concentration, 12) Warnings about obesity are taken more seriously by seniors. 1) Gut changes, 2) Y T and [ LEP levels in men’s plasma, 3) [ Pro-inflammatory CYT concentration 1) Y Fundal compliance, 2) Y Taste and smell, 3) [ CCK levels in plasma, 4) Y Opioïd feeding drive (rodents), 5) Slower gastric emptying, 6) [ Pro-inflammatory CYT concentration, 7) Y T and [ LEP levels in men’s plasma 1) Slower gastric emptying, 2) [ Antral stretch, 3) [ CCK levels in plasma, 4) Y T and [ LEP levels in men plasma, 5) [ Pro-inflammatory CYT level, 6) Y Taste and smell 1) [ CCK levels in plasma, 2) Y Opioid feeding drive (rodents), 3) Y Taste and smell 1) Y Opioid feeding drive (rodents), 2) [ CCK levels in plasma, 3) Y NO circulating levels (marsupials, mice, rats), 4) Y Taste and smell, 5) Depression 1) Poverty, 2) Social isolation, 3) Inability to shop, 4) Failure to cater to ethnic food preferences in institutionalized setting, 5) Depression, 6) Bereavement, 7) Alcoholism, 8) Dementia, 9) Late-life paranoia/mania, 10) Sociopathy, 11) AN, (continued on next page)

694

M. Roy et al. / Appetite 105 (2016) 688e699

Table 3 (continued ) Authors

Type of paper

Morley, Anker, and Evans (2009)

P

Morley, Kim, Haren, Kevorkian, and Banks (2005) Morley et al. (1999)

R R

Morley, Mooradian, Silver, Heber, and P Alfin-Slater (1988) Morley and Silver (1988) R Morley and Thomas (1999)

R

Morley et al. (2006)

R

Moss, Dhillo, Frost, and Hickson (2011) R Moynihan (2007)

PP

Rolland et al. (2006)

R

Smith and Greenwood (2008)

R

Thomas (2011) Thomas (2009)

R R

Visvanathan and Chapman (2009)

R

Correlates of AAa 12) Malabsorption syndromes, 13) Swallowing difficulties, 14) Y Basal metabolic rate, 15) Y Taste and smell, 16) Food availability 1) Y Taste and smell, 2) Slower gastric emptying, 3) [ CCK levels in plasma, 4) Y T and [ LEP levels in men’s plasma, 5) [ Pro-inflammatory CYT level, 6) Depression, 7) Dementia, 8) Functional impairment 1) Y T and [ LEP levels in men’s plasma, 2) CRF activation in hypothalamus 1) Y Taste and smell, 2) [ Pro-inflammatory CYT concentration, 3) Activation of CRF in hypothalamus, 4) Y Fundal compliance, 5) Y Opioïd feeding drive (rodents) 1) Y Opioid feeding drive (rodents), 2) [ CCK levels in plasma, 3) Depression, 4) Zinc deficiency 1) [ CCK levels in plasma, 2) Y Opioïd feeding drive (rodents), 3) Y Taste and smell, 5) CRF activation in hypothalamus, 6) Depression, 7) Cancer 1) Gut changes, 2) [ CCK levels in plasma, 3) Y T and [ LEP levels in men’s plasma, 4) Y Opioïd feeding drive (rodents), 5) Y NPY levels in plasma and CSF, 6) Y Resting metabolic rate, 7) Y Taste and smell 1) [ Pro-inflammatory CYT concentration, 2) Gut changes, 3) [ CCK levels in plasma, 4) [ Amylin concentration, 5) Y NO circulating levels (marsupials, mice, rats), 6) Hyperleptinemia, 7) CD, 8) Pain, 9) Social isolation, 10) Depression 1) [ CCK levels in plasma, 2) [ PYY levels in plasma, 3) [ INS levels in plasma (primates and rodents), 4) Y GHR levels in plasma, 5) Gut changes, 6) Slower gastric emptying 1) Y Taste and smell, 2) POL, 3) Poor oral health, 4) Y Salivation, 5) Shopping difficulties, 6) Problems with food preparation, 7) Depression, 8) Poverty, 9) Dementia, 10) Acute illness, 11) Institutionalization 1) Depression, 2) Y Taste and smell, 3) Social isolation, 4) Y T and [ LEP levels in men plasma, 5) Diets, 6) POL, 7) Malabsorption syndromes, 8) Hypermetabolism 1) Y Opioïd feeding drive (rodents), 2) Y Norepinephrine synthesis, 3) Y NPY levels in plasma and CSF, 4) Y Orexin levels in plasma, 5) Y GAL sensitivity, 6) Y GHR levels in plasma, 7) [ Serotonin levels in CSF, 8) [ CCK levels in plasma, 9) [ INS levels in plasma (primates and rodents), 10) Y T and [ LEP levels in men’s plasma, 11) Y Taste and smell 1) CD, 2) POL 1) Y Taste and smell, 2) Depression, 3) Dementia, 4) POL, 5) Food preference, 6) Food consistency, 7) Food temperature, 8) Palatability, 9) CD, 10) Diets 1) Slower gastric emptying, 2) Y Taste and smell, 3) Y GAL sensitivity, 4) Y NPY levels in plasma and CSF, 5) [ CCK levels in plasma, 6) [ CART levels in CSF (rats), 7) Y Opioid feeding drive (rodents), 8) Y GHR levels in plasma, 9) [ GLP-1 levels in plasma, 10) Y Orexin levels in plasma, 11) Depression, 12) Dementia, 13) Poor oral health, 14) Social isolation, 15) Iatrogenesis, 16) Poverty

Note. AA ¼ Anorexia of aging; AD ¼ Alzheimer disease; AgRP ¼ Agouti-related protein; AN ¼ Anorexia nervosa; C ¼ Commentary; CART ¼ Cocaine and amphetamine regulated transcript; CCK ¼ Cholecystokinin; CD ¼ Chronic disease; COPD ¼ Chronic obstructive pulmonary disease; CRF ¼ Corticotrophin-releasing factor; CSF ¼ Cerebrospinal fluid; CYT ¼ Cytokines; E ¼ Editorial; GAL ¼ Galanin; GHR ¼ Ghrelin; GLP-1 ¼ Glucagon-like peptide 1; INS ¼ Insulin; LEP ¼ Leptin; MAL ¼ Malnutrition; MCH ¼ Melaninconcentrating hormone; MSH ¼ Melanocyte-stimulating hormone; NO ¼ Nitric oxide; NPY ¼ Neuropeptide Y; P ¼ Proceedings; PEM ¼ Protein energy malnutrition; POL ¼ Polypharmacy; POMC ¼ Pro-opiomelanocortin; PP ¼ Position paper; PYY ¼ Peptide YY; R ¼ Review of literature; T ¼ Testosterone. a When studies were performed in animal models, species are identified in parentheses in the table.

Table 4 Physiopathological AA correlates (n ¼ 77). Risk of infection (n ¼ 2)

Biomarkers (proteins/hormones/peptides/ neurotransmitters/minerals; n ¼ 37)

1) [ Risk of infection, Changes in level, synthesis and/or 2) Helicobacter pylori biological activity of: 1) CCK, 2) Opïod, 3) T, 4) GHR, 5) Pro-inflammatory infection CYT, 6) NO, 7) NPY, 8) CART, 9) PYY, 10) GAL, 11) Albumin, 12) Zinc, 13) Amylin, 14) Glutamic acid, 15) Glutamin, 16) b-endorphin, 17) AgRP, 18) Orexin, 19) POMC, 20) Oxytocin, 21) Motilin, 22) MCH, 23) Histamine, 24) Serotonin, 25) Dopamine, 26) Neuromedin, 27) Neurotensin, 28) Isatin, 29) Estrogens, 30) a-MSH, 31) Bombesin, 32) Norepinephrine, 33) Noradrenaline, 34) INS, 35) GLP, 36) CRF, 37) LEP

Gastrointestinal tract dysfunctions (n ¼ 6)

Chemosensory Pathologies and changes (n ¼ 2) dysfunctions (n ¼ 29)

1) Slower gastric emptying, 1) Y Smell, 2) Y Taste 2) Gastric atrophy, 3) Y Fundal compliance, 4) [ Antral stretch, 5) Gastrointestinal motility and function changes, 6) Y Sensitivity to gastrointestinal tract distension

Pharmacological (n ¼ 1)

1) POL 1) CD, 2) Pain, 3) Y Mobility, 4) Cardiac disease, 5) Dysphagia, 6) Gastrointestinal disorders, 7) Hypermetabolism, 8) Y Strength, 9) Y Muscle mass, 10) Weakness/fatigue, 11) Frailty, 12) Y Immunocompetence, 13) Poor oral health, 14) Constipation, 15) Diets, 16) Functional impairment, 17) Acute illness, 18) Institutionalization, 19) Cerebrovascular event, 20) Iatrogenesis, 21) Oral dryness, 22) Y Saliva production, 23) Chewing or swallowing problems, 24) Cognitive decline/ Alzheimer, 25) Y Brain blood supply, 26) Cell degeneration, 27) Y Basal metabolic rate, 28) Smaller excursion of hyoid and larynx during swallowing, 29) Autonomic nerve dysfunction

Note. AgRP ¼ Agouti-related protein; CART ¼ Cocaine amphetamine-regulated transcript; CCK ¼ Cholecystokinin; CD ¼ Chronic disease; CRF ¼ Corticotrophin-releasing factor; CYT ¼ Cytokines; GAL ¼ Galanin; GHR ¼ Ghrelin; GLP ¼ Glucagon-like peptide; INS ¼ Insulin; LEP ¼ Leptin; MCH ¼ Melanin-concentrating hormone; MSH ¼ Melanocytestimulating hormone; NO ¼ Nitric oxide; NPY ¼ Neuropeptide Y; POL ¼ Polypharmacy; POMC ¼ Pro-opiomelanocortin; PYY ¼ peptide YY; T ¼ Testosterone.

M. Roy et al. / Appetite 105 (2016) 688e699

695

Table 5 Non-physiopathological AA correlates (n ¼ 23). Food-related (n ¼ 3) Psychological (n ¼ 9)

Sociocultural (n ¼ 5)

Environmental (n ¼ 6)

1) Food consistency, 1) Psychological distress, 2) Anxiety, 3) Bereavement, 4) Depression, 5) Alcoholism, 6) Mania/paranoïa, 7) 2) Food temperature, 3) Sociopathy, 8) AN, 9) Body weight dissatisfaction Palatability

1) Social isolation, 2) Inability to cook, 3) Food preference, 4) Ethnicity 5) Poverty

1) Features of physical environment (e.g. air quality, presence of bugs) during the meal, 2) Characteristics of social environment (e.g., adequate cafeteria, music room) during the meal, 3) Mealtime, 4) Food availability, 5) Housing type (e.g. home, institution), 6) Misinterpretation of public health messages related to weight

Note. AA ¼ Anorexia of aging; AN ¼ Anorexia nervosa.

Fig. 1. Flow chart of scoping literature review.

3.3.2. Biomarkers (proteins/hormones/peptides/neurotransmitters/ minerals) We identified 37 biomarkers as AA correlates (Table 4). Among them, changes in synthesis, levels or biological activity of seven biomarkers were reported more often than others. They were: 1) elevated cholecystokinin (CCK) levels in human plasma, 2) weakly responsive food intake opioid system in rodents, 3) increased plasma leptin levels in men resulting from decreased testosterone levels, 4) decreased ghrelin levels in human plasma, 5) increased pro-inflammatory cytokines levels, 6) diminished circulating nitric oxide levels in marsupials, mice, and rats, and 7) decreased neuropeptide Y levels in human plasma and cerebrospinal fluid. These correlates are reported numerous times in commentaries, editorials, proceedings, position papers, and narrative reviews. They are listed in Table 3. Two original research articles (Table 2: MacIntosh et al., 2001; Martinez, Hernanz, Gomez-Cerezo, Pena, Vasquez, & Arnalich, 1993) also highlighted one of these correlates (i.e., increased CCK levels in human plasma) with experimental and cross-sectional designs, respectively. These biomarkers and the 30 others listed in Table 4 are hardly amenable to change in the context of preventive public health strategies.

3.3.3. Gastrointestinal tract dysfunctions Six conditions in the gastrointestinal tract were identified as AA correlates: 1) slower gastric emptying, 2) gastric atrophy, 3) decreased fundal compliance, 4) increased antral stretch, 5) altered gastrointestinal motility and function, and 6) reduced sensitivity to gastrointestinal tract distension (Table 4). These changes were mainly reported in narrative reviews by Morley (2001a, 2001c, 2007b, 2007c) or Morley and colleagues (Bhutto & Morley, 2008; Chapman, MacIntosh, Morley, & Horowitz, 2002; MacIntosh, Morley, & Chapman, 2000; Morley, Thomas, & Wilson, 2006, Table 3). Only one original research paper with an experimental design identified slower gastric emptying as an AA correlate (Clarkston et al., 1997). 3.3.4. Chemosensory changes Two chemosensory changes are identified as AA correlates (Table 4). Aging brings on a decline in olfactory and gustatory functions which begins in the 50 s. By age 80 years, most individuals have less smell and taste identification abilities than when they were young (Morley, 2007b). These changes are not reported in original research papers (Table 2) but in 26 of 45 studies (57.8%) in Table 3 (other types of publications).

696

M. Roy et al. / Appetite 105 (2016) 688e699

3.3.5. Pathologies and dysfunctions Many pathologies and dysfunctions (n ¼ 29) are identified as AA correlates (Table 4). Chronic diseases, such as cancer (Chapman, 2007; Gorbien, 1994; MacIntosh et al., 2000; Morley & Silver, 1988; Morley, 2012), chronic obstructive pulmonary disease (Chapman, 2007; Gorbien, 1994; MacIntosh et al., 2000), rheumatoid arthritis (Chapman, 2007), and Parkinson’s disease (Gorbien, 1994; MacIntosh et al., 2000), are cited most commonly. Other pathologies are acute diseases or conditions (e.g., cardiac failure, cerebrovascular events; Chapman, 2007; MacIntosh et al., 2000). Physical conditions also are responsible for AA (e.g., lower muscle mass and strength, fatigue, constipation, functional impairment, lower saliva production, chewing/swallowing problems, lower basal metabolic rate, cell degeneration, decreased brain blood supply, autonomic nerve dysfunction). All these correlates are mainly mentioned in narrative reviews of Morley (2001a, 2007a, 2007b) or Morley and colleagues (Bhutto & Morley, 2008; Morley, 1990; Morley et al., 1999; Morley & Thomas, 1999, Table 3) with the exception of constipation, functional impairment, reduced mobility, decreased saliva, and autonomic nerve dysfunction which are cited in both publication types. 3.3.6. Polypharmacy Polypharmacy use is covered in 14 studies (7 narrative reviews, 4 position papers, and 3 commentaries; Table 3). No original paper identifies this correlate, although most analyses are controlled for number and type of prescribed drugs. One paper (Donini, Savina, & Cannella, 2003) reports that more than 250 prescribed medications alter taste whereas many others affect smell. Several drugs taken by seniors are responsible for oral dryness and constipation which have both been linked to appetite reduction (DiFrancesco et al., 2007; Donini et al., 2003). 3.4. Non-physiopathological correlates Non-physiopathological AA correlates are divided into four subcategories: 1) food-related properties, 2) psychological, 3) sociocultural, and 4) environmental. 3.4.1. Food-related properties Three correlates are related to food characteristics (Table 5), namely, food consistency, food temperature (Thomas, 2009), and visual presentation of food (i.e., palatability; Morley, 2003; Thomas, 2009). The likelihood of AA is increased if these food-related properties are perceived negatively by seniors. These correlates are only reported in the narrative reviews of Morley (2003, 2007b) and Thomas (2009). No original research has focused on foodrelated properties. 3.4.2. Psychological correlates Nine psychological correlates of AA (Table 5) are cited in both types of publications. Being depressed and suffering from psychological distress or anxiety are the main psychological AA correlates. Again, these correlates are mainly addressed in reviews, commentaries or position papers (Table 3). However, three original articles (Landi et al., 2012; Roy, Shatenstein, Gaudreau, Morais, & Payette, 2015; Savina et al., 2003) highlight the role of depression, cognitive decline, body weight dissatisfaction, and anorexia nervosa as AA correlates. 3.4.3. Sociocultural correlates Five sociocultural AA correlates are identified (Table 5). Poverty, social isolation, and inability to buy, shop, prepare or cook meals are noted numerous times. Failure to cater to ethnic food preferences in long-term care institutions is also reported (Chapman,

2007; Hays & Roberts, 2006; MacIntosh et al., 2000; Morley, 1990). Ethnicity is the fifth correlate as food preferences are conditioned in part by cultural circumstances and socialization (Morley, 2002; Thomas, 2009; van der Meij, Wijnhoven, Finlayson, Oosten, & Visser, 2015). Sociocultural correlates are identified in both types of publications. 3.4.4. Environmental correlates Five environmental AA correlates are identified (Table 5). Food availability (Gorbien, 1994; Morley, 1990, 2002) and setting (institution vs. home; Morley, 2002) are noted in two narrative reviews and one commentary. Enhancing the environment in which meals are eaten (Morley, 2003) and eating in the morning (Morley, 2003; Thomas, 2009) are proposed as protective factors against AA. Finally, two narrative reviews (MacIntosh et al., 2000; Morley, 2002) warn public health actors about the potential negative impact of their messages related to nutrition. For example, advice on obesity aimed at younger age groups is often taken more seriously by seniors, although recommendations about healthy body weight are different for them. Similarly, a desire to limit cholesterol intake may lead to decreased intake of protein-rich food. No original research paper has identified these correlates. 4. Discussion 4.1. Summary of findings The results of this review raise many AA correlates. These correlates are further divided into two main categories and 10 subcategories (Tables 4 and 5). While physiopathological AA correlates appear to be less relevant to population health interventions, nonphysiopathological correlates are much more promising in the development and implementation of interventions aimed at preventing appetite loss and promoting adequate food intake during aging. 4.2. Physiopathological correlates: a close relationship with aging A total of 77 physiopathological AA correlates are identified. Among them, about half (i.e., 48.1%) are related to changes in biomarker levels, synthesis and/or activity previously associated with aging (Crimmins, Vasunilashorn, Kim, & Alley, 2008; MartinRuiz et al., 2011). The other half (i.e., 51.9%) is related to pathologies or dysfunctions usually observed in old people (and require medications). All these correlates are predominantly identified in “other types of publications” (Table 3) and are underrepresented in original papers (Table 2). Furthermore, these correlates appear to be mainly the result of commentaries, editorials, position papers, and narrative reviews from a single group of authors (i.e., Morley and colleagues) regrouping data from both animal and human studies. Because physiopathological AA correlates are closely linked to the aging process itself, they are less appropriate in the design of population health interventions. They are, however, relevant to other fields of knowledge that may elicit the development of new therapeutics, allowing the deleterious effects of aging to be delayed or diminished. 4.3. Non-physiopathological correlates: a promising avenue for population health interventions Non-physiopathological AA correlates are also identified (n ¼ 23). They are less numerous than physiopathological correlates, but they represent more relevant public health targets as they are potentially modifiable. These correlates are thus promising in the design of population health interventions aimed at preventing

M. Roy et al. / Appetite 105 (2016) 688e699

appetite loss and promoting adequate food intake. Such potentially modifiable AA correlates are, however, of recent interest in the scientific literature and advocate for more inclusive interventions. Strategies aimed at enhancing meal palatability in various care setting, such as efforts to improve food texture and flavor while providing assistance with eating (Martone et al., 2013), are examples of these interventions. Educating children and grandchildren to share meals with grandparents is a good way to promote maintenance of food intake (seniors’ adequate intake in part depends on eating with others; Paquet et al., 2008) while reducing psychological distress and fostering well-being. Sociocultural interventions should try to break isolation and promote social participation (Levasseur et al., 2015; Vaughan, LaValley, AlHeresh, & Keysor, 2015). Environmental correlates may also lead to innovative interventions, such as age-friendly global community networks (Menec et al., 2015; WHO, 2007). Finally, as two studies noted (MacIntosh et al., 2000; Morley, 2002), public health actors should be concerned about negative effects of their interventions targeting other age groups. Recommendations on obesity aimed at young adults are more often interiorized by seniors, although “healthy” body weight is shown to be higher after 65 years of age (Flegal, Kit, Orpana, & Graubard, 2013; Winter, MacInnis, Wattanapapenpaiboon, & Nowson, 2014). 4.4. Need for original and innovative research This review reveals the need for original and innovative research. It only identifies 15 original papers. Among them, 46.7% are cross-sectional studies or case reports, which are not providing as strong scientific evidence as experimental or longitudinal investigations. Therefore, on the basis of available literature, it is difficult to infer the direction of reported associations between AA and correlates, and generalization of the results is limited. There is a need for experimental designs to test the impact of different interventions on modifiable AA correlates. Likewise, longitudinal studies are needed to provide information about which modifiable correlates could evoke AA onset. Such evidence-based data are required to design appropriate population health interventions. 4.5. Correlates are causes or consequences? Further research would help to disentangle AA causes and consequences. This information would be a cornerstone in the development of appropriate population health interventions. It is difficult to answer the question on the basis of this review. Physiopathological AA correlates could be due to changes in peptide, neurotransmitter or cytokine levels and their receptors in various regions of the brain (e.g., hypothalamus). This, in turn could impact appetite, energy intake and expenditure. AA may also be the result of many physiopathological dysfunctions and biomarker changes that could be normalized with appropriate medication. This rationale could also apply to other physiopathological correlates (i.e., polypharmacy) as well as non-physiopathological correlates (i.e., food-related properties or psychological correlates). Sociocultural and environmental correlates are, however, more likely to be AA causes than consequences, emphasizing the relevance of developing population health interventions targeting these correlates (Martone et al., 2013). 4.6. Strengths and limitations This study has major strengths. To the best of our knowledge, it is the first scoping review to identify AA correlates and discuss their relevance to population health interventions. Our search included not only physiopathological correlates, as in most previous studies,

697

but also potentially modifiable non-physiopathological AA correlates. However, our study also has some limitations. Only English and French peer-reviewed articles are included. Valuable papers have likely been published in other languages or journals. Second, the scientific soundness of retained articles is not assessed. However, it is not the purpose of a scoping review to undertake any quality assessment procedures (Arskey & O’Malley, 2005). Third, there are few original papers compared to other types of publications. Finally, other types of publications (i.e., not reporting original research results) have largely derived from work by Morley and colleagues’ (28 out of 45 studies), limiting the generalizability of our results. 5. Conclusion One hundred AA correlates are identified in this scoping review. These correlates are classified in two broad categories (i.e., physiopathological and non-physiopathological). Physiopathological AA correlates have been found to be less relevant to population health interventions as they are closely related to (or are a consequence of) aging. However, non-physiopathological AA correlates are promising in the design of population health interventions as they are potentially modifiable factors. Further studies and interventions should test which of these correlates are most effective in preventing appetite loss and promoting adequate food intake during aging. Conflict of interest The authors have no competing interests associated with the publication of this review. Acknowledgments The first author of this paper holds a Postdoctoral Fellowship from the Fonds de Recherche du Qu
ebec - Sant
e (FRQ-S, # 22691). References Ahari, M., & Kimigiar, M. (1997). Food intake and body mass index in the privately institutionalized elderly in Teheran. International Journal of Vitamin and Nutrition Research, 67, 41e46. Ahmed, T., & Haboubi, N. (2010). Assessment and management of nutrition in older people and its importance to health. Clinical Interventions in Aging, 9, 207e216. Allaz, A. F., Bernstein, M., Rouget, P., Archinard, M., & Morabia, A. (1998). Body weight preoccupation in middle-age and ageing women: A general population survey. International Journal of Eating Disorders, 23, 287e294. Arskey, H., & O’Malley, L. (2005). Scoping studies: Towards a methodological framework. International Journal of Social Research Methodology, 8, 19e32. Basille-Filler, M. J. (1997). Anorexia and aging. Journal of Women & Aging, 9, 45e52. Benelam, B. (2009). Satiety and the anorexia of ageing. British Journal of Community Nursing, 14, 332e335. Bhutto, A., & Morley, J. E. (2008). The clinical significance of gastrointestinal changes with aging. Current Opinion in Clinical Nutrition and Metabolic Care, 11, 651e660. Boer, A., Horst, G. T., & Lorist, M. M. (2012). Physiological and psychosocial agerelated changes associated with reduced food intake in older persons. Ageing Research Reviews, 12, 316e328. Bostick, J. E., Rantz, M. J., Flesner, M. K., & Riggs, C. J. (2006). Systematic review of studies of staffing and quality in nursing homes. Journal of the American Directors Associations, 7, 366e376. Briefel, R. R., McDowell, M. A., Alaimo, K., Caughman, C. R., Bischof, A. L., Carroll, M. D., et al. (1995). Total energy intake of the US population: The third National Health and Nutrition Examination Survey, 1988e1991. American Journal of Clinical Nutrition, 62, S1072eS1080. Callen, B. L., & Wells, T. J. (2005). Screening for nutritional risk in communitydwelling old-old. Public Health Nursing, 22, 138e146. ^do, A. C., Garcia Moreira, V., Marina Moraes, J., Sanchez, M. A., & Lourenço, R. A. Cane (2015). High-calorie supplements for treatment of anorexia or cachexia in older adults. Journal of the American Geriatric Society, 63, 1041e1042. Cartwright, J. C., Hickman, S., Perrin, N., & Tilden, V. (2006). Symptom experiences of residents dying in assisted living. Journal of the American Directors Associations, 7, 219e223. Chandra, R. K., Imbach, A., Moore, C., Skelton, D., & Woolcott, D. (1991). Nutrition of

698

M. Roy et al. / Appetite 105 (2016) 688e699

the elderly. Canadian Medical Association Journal, 145, 1475e1487. Chapman, I. A. (2004). Endocrinology of anorexia of ageing. Best Practice & Research Clinical Endocrinology & Metabolism, 18, 437e452. Chapman, I. A. (2007). The anorexia of aging. Clinics in Geriatric Medicine, 23, 735e756. Chapman, I. A., MacIntosh, C. G., Morley, J. E., & Horowitz, M. (2002). The anorexia of ageing. Biogerontology, 3, 67e71. Chapman, I. A., & Nelson, R. A. (1994). Loss of appetite: Managing unwanted weight loss in the older patient. Geriatrics, 49, 54e59. Clarkston, W. K., Pantano, M. M., Morley, J. E., Horowitz, M., Littlefied, J. M., & Burton, F. R. (1997). Evidence for the anorexia of aging: Gastrointestinal transit and hunger in healthy elderly vs. young adults. American Journal of Physiology Regulatory Integrative and Comparative Physiology, 272, 243e248. Cornali, C., Franzoni, S., Frisoni, G. B., & Trabucchi, M. (2005). Anorexia as an independent predictor of mortality. Journal of the American Geriatrics Society, 53, 354e355. Crimmins, E., Vasunilashorn, S., Kim, J. K., & Alley, D. (2008). Biomarkers related to aging in human populations. Advances in Clinical Chemistry, 46, 161e217. DiFrancesco, V., Fantin, F., Omizzolo, F., Residori, L., Bissoli, L., Bosello, O., et al. (2007). The anorexia of aging. Digestive Diseases, 25, 129e137. Donini, L. M., Dominguez, L. J., Barbagallo, M., Savina, C., Castellaneta, E., Cuccinotta, D., et al. (2011). Senile anorexia in different geriatric settings in Italy. Journal of Nutrition, Health, and Aging, 15, 775e781. Donini, L. M., Savina, C., & Cannella, C. (2003). Eating habits and appetite control in the elderly: The anorexia of aging. International Psychogeriatrics, 15, 73e87. Donini, L. M., Savina, C., Piredda, D., Cucinotta, A., Fiorito, E. M., Inelmen, G., et al. (2008). Senile anorexia in acute e ward and rehabilitation settings. The Journal of Nutrition, Health, & Aging, 12, 511e517. re, A., & Rapin, C. H. (1998). Dormenval, V., Budtz-Jorgensen, E., Mojon, P., Bruye Associations between malnutrition, poor general health and oral dryness in hospitalized elderly patients. Age & Ageing, 27, 123e128. Elmstahl, S., & Steen, B. (1987). Hospital nutrition in a geriatric long-term care medicine. Age & Ageing, 16, 73. Flegal, K. M., Kit, B. K., Orpana, H., & Graubard, B. I. (2013). Associations of all-cause mortality with overweight and obesity using standard body mass index categories: A systematic review and meta-analysis. Journal of the American Medical Association, 309, 71e82. Gorbien, M. J. (1994). Anorexia of aging: A simple approach to management. Cleveland Clinic Journal of Medicine, 61, 253. Guigoz, Y., Lauque, S., & Vellas, B. J. (2002). Identifying the elderly at risk for malnutrition: The Mini Nutritional Assessment. Clinics in Geriatric Medicine, 18, 737e757. Guigoz, Y., Vellas, B., & Garry, P. J. (1996). Assessing the nutritional status of the elderly: The Mini Nutritional Assessment as part of the geriatric evaluation. Nutrition Reviews, 54, S59e65. Hallfrisch, J., Muller, D., Drinkwater, D., Tobin, J., & Andres, R. (1990). Continuing diet trends in men: The Baltimore Longitudinal Study of Aging (1961e1987). Journal of Gerontology, 45, M186eM191. Hamerman, D. (2002). Molecular-based therapeutic approaches in treatment of anorexia of aging and cancer cachexia. Journals of Gerontology Series A- Biological Sciences and Medical Sciences, 57A, M511eM518. Hays, N. P., & Roberts, S. B. (2006). The anorexia of aging in humans. Physiology & Behavior, 88, 257e266. Horwitz, B. A., Blanton, C. A., & McDonald, R. B. (2002). Physiologic determinants of the anorexia of aging: Insights from animal studies. Annual Review of Nutrition, 22, 417e438. Hughes, G., Bennett, K. M., & Hetherington, M. M. (2004). Old and alone: Barriers to healthy eating in older men living on their own. Appetite, 43, 269e276. Inouye, S. K., Studenski, S., Tinetti, M. E., & Kuchel, G. A. (2007). Geriatric syndromes: Clinical, research and policy implications of a core geriatric concept. Journal of the American Geriatrics Society, 55, 780e791. Kmiec, Z. (2010). Central control of food intake with aging. Interdisciplinary Topics in Gerontology, 37, 37e50. Landi, F., Laviano, A., & Cruz-Jentoft, A. J. (2010). The anorexia of aging: Is it a geriatric syndrome? Journal of the American Medical Directors Associations, 11, 153e156. Landi, F., Liperoti, R., Lattanzio, F., Russo, A., Tosato, M., Barillaro, C., et al. (2012). Effects of anorexia on mortality among older adults receiving home care: An observational study. The Journal of Nutrition, Health, & Aging, 16, 79e83. Landi, F., Liperoti, R., Russo, M., Giovannini, S., Tosato, C., Barillaro, R., et al. (2013). Association of anorexia with sarcopenia in a community-dwelling elderly population: Results from the ilSIRENTE study. European Journal of Nutrition, 52, 1261e1268. Landi, F., Onder, G., Gambassi, G., Pedone, C., Carbonin, P., & Bernabei, R. (2000). Body mass index and mortality among hospitalized patients. Archives of Internal Medicine, 160, 2641e2644. Landi, F., Russo, A., Liperoti, R., Tosato, M., Barillaro, C., Pahor, M., et al. (2010). Anorexia, physical function, and incident disability among the frail elderly population: Results from the ilSIRENTE Study. Journal of the American Medical Directors Associations, 11, 268e274. Levac, D., Colquhoun, H., & O’Brien, K. K. (2010). Scoping studies: Advancing the methodology. Implementation Science, 5, 69.
ne
reux, M., Richard, L., Therrien, F. H., Levasseur, M., Cohen, A. A., Dubois, M. F., Ge et al. (2015). Environmental factors associated with social participation of older adults living in metropolitan, urban, and rural areas: The NuAge study.

American Journal of Public Health, 105, 1718e1725. MacIntosh, C., Morley, J. E., & Chapman, I. M. (2000). The anorexia of aging. Nutrition, 16, 983e995. MacIntosh, C. G., Morley, J. E., Wishart, J., Morris, H., Jansen, J. B., Horowitz, M., et al. (2001). Effect of exogenous cholecystokinin (CCK)-8 on food intake and plasma CCK, leptin, and insulin concentrations in older and young adults: Evidence for increased CCK activity as a cause of the anorexia of aging. The Journal of Clinical Endocrinology & Metabolism, 86, 5830e5837. Martin-Ruiz, C., Jagger, C., Kingston, A., Collerton, J., Catt, M., Davies, K., et al. (2011). Assessment of a large panel of candidate biomarkers of ageing in the Newcastle 85þ study. Mechanisms of Ageing and Development, 132, 496e502. Martinez, M., Arnalich, F., Vasquez, J. J., & Hernanz, A. (1993). Altered cerebrospinal fluid amino acid pattern in the anorexia of aging: Relationship with biogenic amine metabolism. Life Sciences, 53, 1643e1650. Martinez, M., Hernanz, A., Gomez-Cerezo, J., Pena, J. M., Vasquez, J. J., & Arnalich, F. (1993). Alterations in plasma and cerebrospinal fluid levels of neuropeptides in idiopathic senile anorexia. Regulatory Peptides, 49, 109e117. Martone, A. M., Onder, G., Vetrano, D. L., Ortolanie, E., Tosato, M., Marzetti, E., et al. (2013). Anorexia of aging: A modifiable risk factor for frailty. Nutrients, 5, 4126e4133. Massler, M. (1980). Geriatric nutrition: The role of taste and smell in appetite. The Journal of Prosthetic Dentistry, 43, 247e250. van der Meij, B. S., Wijnhoven, H. A. H., Finlayson, G. S., Oosten, B. S. H., & Visser, M. (2015). Specific food preferences of older adults with a poor appetite. A forcedchoice test conducted in various care settings. Appetite, 90, 168e175. Menec, V., Bell, S., Novek, S., Minnigaleeva, G. A., Morales, E., & Ouma, T. (2015). Making rural and remote communities more age-friendly: Experts’ perspectives on issues, challenges, and priorities. Journal of Aging & Social Policy, 27, 173e191. Morley, J. E. (1990). Anorexia in older patients: Its meaning and management. Geriatrics, 45, 59e66. Morley, J. E. (1996). Anorexia in older persons: Epidemiology and optimal treatment. Drugs & Aging, 8, 134e155. Morley, J. E. (1997). Anorexia of aging: Physiologic and pathologic. The American Journal of Clinical Nutrition, 66, 760e773. Morley, J. E. (2001a). Anorexia, sarcopenia, and aging. Nutrition, 17, 660e663. Morley, J. E. (2001b). Anorexia, body composition, and ageing. Current Opinion in Clinical Nutrition and Metabolic Care, 4, 9e13. Morley, J. E. (2001c). Decreased food intake with aging. Journals of Gerontology Series A- Biological Sciences and Medical Sciences, 56A, 81e88. Morley, J. E. (2002). Pathophysiology of anorexia. Clinics in Geriatric Medicine, 18, 661e673. Morley, J. E. (2003). Anorexia and weight loss in older persons. Journals of Gerontology Series A- Biological Sciences and Medical Sciences, 58A, 131e137. Morley, J. E. (2005). Anorexia as an independent predictor of mortality. Journal of the American Geriatrics Association, 53, 354e355. Morley, J. E. (2007a). Weight loss in the nursing home. Journal of the American Medical Directors Associations, 8, 201e204. Morley, J. E. (2007b). Weight loss in older persons: New therapeutic approaches. Current Pharmaceutical Design, 35, 3637e3647. Morley, J. E. (2007c). The aging gut: Physiology. Clinics in Geriatric Medicine, 23, 757e767. Morley, J. E. (2010). Anorexia, weight loss, and frailty. Journal of the American Medical Directors Associations, 11, 225e228. Morley, J. E. (2012). Undernutrition in older adults. Family Practice-The International Journal for Research in Primary Care, 29, i89ei93. Morley, J. E., Anker, S. D., & Evans, W. J. (2009). Cachexia and aging: An update based on the fourth international cachexia meeting. The Journal of Nutrition, Health & Aging, 13, 47e55. Morley, J. E., Kim, M. J., Haren, T., Kevorkian, R., & Banks, W. A. (2005). Frailty and the aging male. The Aging Male, 8, 135e140. Morley, J. E., Miller, D. K., Perry, H. M., Patrick, P., Guigoz, Y., & Vellas, B. (1999). Anorexia of aging, leptin, and the mini nutritional assessment. Nestle Nutrition Workshop Series Clinical & Performance Program, 1, 67e76. Morley, J. E., Mooradian, A. D., Silver, A. J., Heber, D., & Alfin-Slater, R. B. (1988). Nutrition in the elderly. Annals of Internal Medicine, 109, 890e904. Morley, J. E., & Silver, A. J. (1988). Anorexia in the elderly. Neurobiology of Aging, 9, 9e16. Morley, J. E., & Thomas, D. R. (1999). Anorexia and aging: Pathophysiology. Nutrition, 15, 499e503. Morley, J. E., Thomas, D. R., & Wilson, M. M. (2006). Cachexia: Pathophysiology and clinical relevance. American Journal of Clinical Nutrition, 83, 735e743. Moss, C., Dhillo, W. S., Frost, G., & Hickson, M. (2011). Gastrointestinal hormones: The regulation of appetite and the anorexia of ageing. Journal of Human Nutrition & Dietetics, 25, 3e15. Moynihan, P. J. (2007). The relationship between nutrition and systemic and oral well-being in older people. The Journal of the American Dental Association, 138, 493e497. Muscaritoli, M., Anker, S. D., Argiles, J., Aversa, Z., Bauer, J. M., Biolo, G., et al. (2010). Consensus definition of sarcopenia, cachexia and pre-cachexia: Joint document elaborated by Special Interest Groups [SIG] ‘‘cachexia-anorexia in chronic wasting diseases’’ and ‘‘nutrition in geriatrics’’. Clinical Nutrition, 29, 154e159. Paquet, C., St-Arnaud-McKenzie, D., Ma, Z. F., Kergoat, M. J., Ferland, G., & Dube, L. (2008). More than just being alone: The number, nature, and complementarity of meal-time social interactions influence food intake in hospitalized elderly patients. Gerontologist, 48, 603e611.

M. Roy et al. / Appetite 105 (2016) 688e699 Payette, H., Coulombe, C., Boutier, V., & Gray-Donald, K. (1999). Weight loss and mortality among free-living frail elders: A prospective study. Journals of Gerontology Series A- Biological Sciences and Medical Sciences, 54, M440eM445. Payette, H., Coulombe, C., Boutier, V., & Gray-Donald, K. (2000). Nutrition risk factors for institutionalization in a free-living functionally dependent elderly population. Journal of Clinical Epidemiology, 53, 579e587. Portnoi, V. (1997). Helicobacter pylori infection and anorexia of aging. Archives of Internal Medicine, 157, 269e272. Rolland, Y., Kim, M. J., Gammack, J. K., Wilson, M. M., Thomas, D. R., & Morley, J. E. (2006). Office management of weight loss in older persons. American Journal of Medicine, 119, 1019e1026. Roy, M., Shatenstein, B., Gaudreau, P., Morais, J. A., & Payette, H. (2015). Seniors’ body weight dissatisfaction and longitudinal associations with weight changes, anorexia of aging, and obesity: Results from the NuAge Study. Journal of Aging and Health, 27, 220e238. Sarkisian, C. A., Gruenewald, T. L., Boscardin, W. J., & Seeman, T. E. (2008). Preliminary evidence for subdimensions of geriatric frailty: The MacArthur study of successful aging. Journal of the American Geriatrics Society, 56, 2292e2297. Savina, C., Donini, L. M., Anzivino, R., De Felice, M. R., Bernardini, L., & Cannella, C. (2003). Administering the “AHSP Questionnaire” (appetite, hunger, sensory perception) in a geriatric rehabilitation care. The Journal of Nutrition, Health & Aging, 7, 385e389. Silver, A. J., Guillen, C. P., Kahl, M. J., & Morley, J. E. (1993). Effect of aging on body fat. Journal of the American Geriatrics Society, 41, 211e213. Sjogren, A., Osterberg, T., & Steen, B. (1994). Intake of energy, nutrients and food items in a ten-year cohort comparison and in a six-year longitudinal perspective: A population study of 70- and 76-year-old Swedish people. Age and Ageing, 23, 108e112.

699

Smith, K. L., & Greenwood, C. E. (2008). Weight loss and nutritional considerations in Alzheimer disease. Journal of Nutrition for the Elderly, 27, 381e403. Sorbye, L. W., Schroll, M., Finne Soveri, H., Jonsson, P. V., Topinkova, E., Ljunggren, G., et al. (2008). Unintended weight loss in the elderly living at home: The aged in Home Care Project (AdHOC). Journal of Nutrition, Health, & Aging, 12, 10e16. Sullivan, D. H., Patch, G. A., Walls, R. C., & Lipchitz, D. A. (1990). Impact of nutritional status on morbidity and mortality in a select population of geriatric patients. American Journal of Clinical Nutrition, 51, 749e758. Sullivan, D. H., & Walls, R. C. (1994). Impact of nutritional status on morbidity in a population of geriatric rehabilitation patients. Journal of the American Geriatrics Society, 51, 1072e1076. Tayback, M., Kumanyika, S., & Chee, E. (1990). Body weight as a risk factor in the elderly. Archives of Internal Medicine, 150, 1065e1072. Thomas, D. R. (2009). Anorexia: Aetiology, epidemiology and management in older people. Drugs & Aging, 26, 557e570. Thomas, D. R. (2011). Use of orexigenic medications in geriatric patients. The American Journal of Geriatric Pharmacotherapy, 9, 97e108. Vaughan, M., LaValley, M. P., AlHeresh, R., & Keysor, J. J. (2015 Nov 17). Which feature of the environment impact community participation of older adults? A systematic review and meta-analysis. Journal of Aging and Health. pii: 0898264315614008. [Epub ahead of print]. Visvanathan, R., & Chapman, I. M. (2009). Undernutrition and anorexia in older person. Gastroenterology Clinics of North America, 38, 393e409. Winter, J. E., MacInnis, R. J., Wattanapapenpaiboon, N. A., & Nowson, C. A. (2014). BMI and all-cause mortality in older adults: A meta-analysis. American Journal of Clinical Nutrition, 99, 875e890. World Health Organization (WHO. (2007). Global age-friendly cities: A guide. Geneva: Switzerland.