Research in Gerontological Nursing

Translational Research/Implementation Science 

Thickened Drinks and Oral Nutritional Supplements as Potential Reservoirs of Oral Microorganisms: Microbial Assays In Vitro

Caroline Jung, PharmD; Nadine Molinari, RN; Aïmen Bouhlel, DDS; Raymond Ruimy, PhD, MD; Isabelle Prêcheur, PhD, DDS

Abstract

Oral hygiene is difficult to achieve for frail older adults. Aging, chronic diseases, polypharmacy, mouth-washes, and crushed drugs can contribute to uncontrolled proliferation and microbial deposits in the mouth. Looking for avoidable risk factors, in vitro microbial survival or proliferation in thickened drinks and oral nutritional supplements (ONS) was investigated. The safest thickened drinks were ready-to-use products containing preservatives. Escherichia coli, Staphylococcus aureus, and Candida albicans proliferated in dairy ONS at room temperature. C. albicans also proliferated in juices. Oral anerobic bacteria were recovered from part eaten ONS. Thickened drinks and ONS could contribute to microbial proliferation, especially with patients who have swallowing alterations or cognitive troubles, who may keep these solutions longer than necessary in their mouth. These products can also constitute microbial reservoirs in the environment of frail older adults. It is important for health care workers and family members to respect hand hygiene and refrigeration procedures. [Research in Gerontological Nursing, 13(4), 203–209.]

Abstract

Oral hygiene is difficult to achieve for frail older adults. Aging, chronic diseases, polypharmacy, mouth-washes, and crushed drugs can contribute to uncontrolled proliferation and microbial deposits in the mouth. Looking for avoidable risk factors, in vitro microbial survival or proliferation in thickened drinks and oral nutritional supplements (ONS) was investigated. The safest thickened drinks were ready-to-use products containing preservatives. Escherichia coli, Staphylococcus aureus, and Candida albicans proliferated in dairy ONS at room temperature. C. albicans also proliferated in juices. Oral anerobic bacteria were recovered from part eaten ONS. Thickened drinks and ONS could contribute to microbial proliferation, especially with patients who have swallowing alterations or cognitive troubles, who may keep these solutions longer than necessary in their mouth. These products can also constitute microbial reservoirs in the environment of frail older adults. It is important for health care workers and family members to respect hand hygiene and refrigeration procedures. [Research in Gerontological Nursing, 13(4), 203–209.]

Oral biofilm thickness and composition are controlled by healthy lifestyle and diet (i.e., avoiding sugars, acids, alcohol, tobacco and other addictive products), daily dental hygiene, and regular dental care provided by hygienists and dental surgeons. However, oral hygiene and oral health may become difficult to achieve for older adults, especially for frail older adults (Gil-Montoya et al., 2015; Johansson et al., 2016). But aging, chronic diseases, atropinic drugs, and multidrug prescriptions may not be the only factors responsible for uncontrolled growth of oral biofilm. Sometimes, inappropriate oral care can also contribute to microbial proliferation by inhibiting the protection given by saliva and endogenous microbial species. For instance, saliva is a key protective fluid and regular use of antiseptic mouthwashes can lead to oral dryness (Chevalier et al., 2015). Crushed drugs mixed in soft food or beverages are in direct contact with oral surfaces (Bourdenet et al., 2015; Clauson et al., 2016). Crushed drugs have antiseptic properties against endogenous oral bacteria and potentially unbalance the oral ecosystem (Lamure et al., 2018). All these reasons combined can lead to the development of thick microbial deposits on the teeth, tongue, and removable dentures, which are frequently observed in frail older adults (Chavez & Hendre, 2017).

In addition, older adults frequently experience difficulty in swallowing, called dysphagia. Dysphagia can provoke choking or aspiration pneumonia, which can in turn lead to death (Khan et al., 2014; Sura et al., 2012). To reduce the risk of aspiration, patients with dysphagia are given textured food and beverages (i.e., thickened drinks) eaten with a spoon (Chen et al., 2015; Cichero et al., 2017). Some thickened drinks can contain sugar, maltodextrin, vegetable oil, and other constituents, potentially allowing microbial survival or proliferation (Vallons et al., 2015). Older adults frequently also have malnutrition. They are often given protein- and energy-rich oral nutritional supplements (ONS), commonly in the form of dairy creams or beverage, and “juices.” Liquid ONS are generally sipped directly from small bottles.

ONS contain a variety of animal or vegetable proteins (e.g., bovine milk casein, soya proteins), sugar or diverse sweeteners, lipids, vitamins, and trace elements (Milne et al., 2009; Morilla-Herrera et al., 2016). The composition of thickened drinks and ONS may be similar to the one of culture media used in a laboratory, which contain proteins, sugars, lipids, vitamins, and trace elements. In vitro, these nutrients allow the growth of many endogenous bacteria and fungi, such as Candida albicans. Thus, according to manufacturers' recommendations, homemade thickened drinks and all categories of ONS must be cooled to 4°C before serving. After opening, sterile products are immediately contaminated by aerial microbes. Sterile and homemade products are also contaminated by oral microbes, by direct contact or via bottles, spoons, and straws. Partly consumed thickened drinks and ONS must be discarded or kept refrigerated after 1 hour at room temperature. Refrigeration must not exceed 24 hours (Réglier-Poupet et al., 2005). However, these recommendations are not always easy to enforce for busy nursing staff (Saeb et al., 2017). Finally, older adults with swallowing alterations or cognitive troubles may keep these solutions longer than necessary in their mouth (Khan et al., 2014; Sura et al., 2012). Thus, in recurrent conditions, such care products could contribute to the development of oral microbial deposits. The current authors hypothesized that bacteria and fungi colonizing the oral cavity could survive or proliferate in thickened drinks and ONS. The aim of the current work was to investigate in vitro microbial survival or proliferation in thickened drinks and ONS.

Method

Strains Tested

Eight reference strains of bacteria were tested: Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, Micrococcus luteus, Gemella haemolysans, Streptococcus salivarius, Rothia mucilaginosa, and Streptococcus mutans (Table 1). S. aureus, E. coli, P. aeruginosa, and M. luteus were grown in brain heart infusion (BHI) (Becton Dickinson, Le-Ponchaix, France) and onto Mueller-Hinton (bioMérieux, Marcy l'Etoile, France) for 24 hours in aerobic conditions. G. haemolysans, S. salivarius, and R. mucilaginosa were grown in liquid medium (Schaedler broth [bioMérieux]) and onto 5% sheep blood agar plates (bioMérieux) for 24 hours in aerobic conditions. S. mutans was grown in Schaedler broth and onto 5% sheep blood agar plates for 48 hours in microaerophilic conditions. One fungal reference strain was tested, C. albicans. It was grown into peptone-yeast extract broth (bioMérieux) and onto Sabouraud agar plates (bioMérieux) for 24 hours in aerobic conditions. E. coli, S. aureus, P. aeruginosa, and C. albicans are four reference strains recommended by United States, European, and Japanese Pharmacopeia for pharmaceutical microbiology (access https://www.atcc.org/pharmaceutical). The other bacterial strains are five cultivable strains representative of the oral ecosystem (Table 1).

Bacterial and Fungal Strains Tested

Table 1:

Bacterial and Fungal Strains Tested

Thickened Drinks

The current assay aimed at checking in vitro whether oral microorganisms can proliferate in thickened drinks. Four types of brand lemon-flavored thickened drinks were tested: dehydrated with sugar, dehydrated with artificial sweetener, ready-to-use with sugar, and ready-to-use with artificial sweetener. Ingredients and nutritional values are detailed in Table A and Table B (available in the online version of this article). The four thickened drinks were inoculated with C. albicans and the eight bacterial strains. At T0, thickened drinks were first diluted into sterile water (18% final concentration) and secondly inoculated 1/10 with C. albicans (106 colony forming units [CFU]) and bacterial strains (108 CFU). Cultures were grown at 37°C for 24 hours (T1), except for S. mutans, which was grown for 48 hours (T1). Microbial growth was measured by reading optical densities (OD 650 nm) in a spectrophotometer at T0 and T1.

Ingredients of the four thickened drinks tested

Table A:

Ingredients of the four thickened drinks tested

Nutritional values (theorical calculated values) of the four thickened drinks tested

Table B:

Nutritional values (theorical calculated values) of the four thickened drinks tested

Oral Nutritional Supplements

The current assay was designed to check whether some microbial strains can grow at room temperature in ONS. In a preliminary assay, E. coli, S. aureus, and C. albicans were tested. The products tested were: (a) a strawberry-flavored dairy drink containing sucrose and milk proteins; (b) a vanilla-flavored dairy cream containing sucrose and milk proteins; (c) a cherry-flavored juice containing sucrose, soya proteins, and pea proteins hydrolysate ; and (d) a sucrose-free dairy cream for diabetic patients containing fructose (carbohydrates: fructose, maltodextrin, and starch) and milk proteins. Ingredients are detailed and compared to BHI ingredients in Table C and Table D (available in the online version of this article). Dairy drink (Fortimel Compact Protein™) and dairy cream (Forticrème™) were obtained from Nutricia (Saint Ouen, France). Juice (ProvideXtra™) and sucrose-free dairy cream (Fresubin DB™) were obtained from Fresenius-Kabi (Bad Homburg vor der Höhe, Germany). At T0, E. coli, S. aureus, and C. albicans were pre-grown in liquid media. At T1, 5 mL of ONS were inoculated with 10 μL of pre-culture (E. coli and S. aureus 1.5 × 109 CFU/mL; C. albicans 5 × 107 fungal CFU/mL). Inoculated ONS were left for 48 hours at room temperature (T2). Microbial growth was controlled by spreading 1 mL of inoculated ONS on agar plates at T2, incubated for 24 hours at 30°C. Results were expressed as a qualitative evaluation of microbial growth (no colony [–], <10 colonies [+], 10 to 100 colonies [++], and >100 colonies [+++]), based on CFU numeration on Petri dishes.

Ingredients of the four oral nutritional supplements (ONSs) tested. Milk proteins: mainly casein from cow milk

Table C:

Ingredients of the four oral nutritional supplements (ONSs) tested. Milk proteins: mainly casein from cow milk

Properties and reagents of a general purpose medium suitable for the cultivation of a wide variety of bacteria, yeasts and filamentous fungi from clinical specimens (data sheet Brain Heart Infusion or BHI, Beckton Dickinson GmBH https://www.bd.com/resource.Aspx?IDX=9008)

Table D:

Properties and reagents of a general purpose medium suitable for the cultivation of a wide variety of bacteria, yeasts and filamentous fungi from clinical specimens (data sheet Brain Heart Infusion or BHI, Beckton Dickinson GmBH https://www.bd.com/resource.Aspx?IDX=9008)

In a second assay, ONS served to patients hospitalized in the geriatric ward of Nice University Hospital were collected to verify whether they were contaminated after opening and consumption. Collected ONS had been opened for <2 hours. Bottles were collected by nurse aides instead of being discarded, anonymously transported at 4°C to the laboratory, and immediately inoculated onto Petri dishes. Briefly, 100 μL of ONS were diluted into 900 μL of saline water (NaCl 0.9%) and this 1-mL inoculum was plated onto sheep blood agar plates. Plates were incubated for 5 days in microaerophilic conditions (5% CO2), adapted to oral microflora. Results were expressed as a qualitative evaluation of the rate of ONS contamination, ranging from — to +++, based on CFU numeration on Petri dishes.

Results

Thickened Drinks

The first assay aimed to investigate in vitro microbial survival or proliferation in unopened thickened drinks (ready-to-use) and dehydrated thickened drinks freshly reconstituted with mineral water. OD values were converted in CFU/mL from curves-standards realized by CFU numeration onto Petri dishes. These values were secondly converted to percentage of variation of concentration in microbial cells, which is the variation of biomass from T0 to T1, by assigning the 100% value to T0. It was hypothesized that compared to T0 (100% microbial mass), at T1, doubling of the microbial mass (200%), stability of the microbial mass (50% to 150%), or a reduction by 2/3 of the microbial mass (33%) corresponded respectively to proliferation, microbial survival, or diminution, respectively, in thickened drinks.

Eight measures of OD could not be achieved because of the residual viscosity of the thickened drink, despite 18% dilution. Results are shown in Figure 1. The four thickened drinks had specific profiles of proliferation-survival-diminution with the nine microbial strains tested. The nine microbial strains displayed their own profiles of proliferation-survival-diminution in the four thickened drinks tested. There was no microbial proliferation in ready-touse thickened drinks, which contained preservatives, either with sweetener or sugar.

Variation of the biomass from T0 to T1 in the four thickened drinks tested, expressed in percentage of initial biomass at T1. Dehydrated thickened drink with sugar: non-interpretable results for Pseudomonas aeruginosa, Streptococcus salivarius, and Rothia mucilaginosa cultures. Ready-to-use thickened drink sweetened: non-interpretable results for Staphylococcus aureus, Escherichia coli, Gemella haemolysans, S. salivarius, and R. mucilaginosa.

Figure 1.

Variation of the biomass from T0 to T1 in the four thickened drinks tested, expressed in percentage of initial biomass at T1. Dehydrated thickened drink with sugar: non-interpretable results for Pseudomonas aeruginosa, Streptococcus salivarius, and Rothia mucilaginosa cultures. Ready-to-use thickened drink sweetened: non-interpretable results for Staphylococcus aureus, Escherichia coli, Gemella haemolysans, S. salivarius, and R. mucilaginosa.

There were two main results. First, the absence of preservatives in dehydrated and reconstituted thickened drinks, containing either sweetener or sugar, can favor microbial growth, particularly C. albicans. Second, the presence of sugar in dehydrated and ready-to-use thickened drinks fosters microbial survival, rather than microbial growth. As a result, a dehydrated thickened drink with sugar was the most favorable medium for microbial growth (mostly C. albicans, E. coli, S. aureus, and M. luteus) and microbial survival (S. mutans and G. haemolysans). Conversely, ready-to-use and sweetened thickened drink was the most favorable medium to inhibit microbial proliferation and survival, for two reasons: the presence of preservatives (potassium sorbate and sodium benzoate) and low sugar content (0.5%). From this perspective, it was the safest thickened drink.

Oral Nutritional Supplements

The second assay aimed to investigate in vitro microbial survival or proliferation in part open ONS. E. coli, S. aureus, and C. albicans were able to grow at room temperature (20°C) in dairy drinks and creams. C. albicans was also able to grow in the juice, which was enriched in vegetal proteins but was milk protein–free and lipid-free (Table 2).

Qualitative Evaluationa of Microbial Growth in Oral Nutritional Supplements Inoculated With Escherichia coli, Staphylococcus aureus, and Candida albicans, Grown for 48 Hours at Room Temperature

Table 2:

Qualitative Evaluation of Microbial Growth in Oral Nutritional Supplements Inoculated With Escherichia coli, Staphylococcus aureus, and Candida albicans, Grown for 48 Hours at Room Temperature

In the second assay, seven samples of part open ONS were collected (Table 3). After 5 days of incubation in microaerophilic conditions at 37°C, samples B, D, E, and G displayed a dense microbial culture with a great number of colonies of different aspects, representative of the oral bacterial flora. The degree of contamination was not related to the type of ONS (dairy or non-dairy product, with or without sucrose). Instead, the degree of contamination could be related to the intensity of contamination of the product by the oral microflora of the patient. The samples of partly consumed ONS were grown in anaerobic conditions, because aerobic cultures of oral microbial samples yield only rare and tiny colonies. Anaerobic bacteria of the oral microflora had been exposed to oxygen before collection and they were not investigated. Partly consumed ONS helped preserve the viability of anaerobic or at least micro-aerophilic oral strains.

Details of the Seven Samples of Oral Nutritional Supplements Collected and Qualitative Evaluation of Colony Forming Units After 3 to 5 Days Incubation on Blood Agar Plates in Microaerophilic Conditions at 37°C

Table 3:

Details of the Seven Samples of Oral Nutritional Supplements Collected and Qualitative Evaluation of Colony Forming Units After 3 to 5 Days Incubation on Blood Agar Plates in Microaerophilic Conditions at 37°C

Discussion

The current study is the first to demonstrate that thickened drinks and ONS are similar to some bacterial and fungal culture media, with a risk of iatrogenic infection for malnourished older adults who consume these products.

First, some bacterial species can survive at room temperature in partly consumed servings of thickened drinks and ONS. Survival means low germ concentration and creation of microbial reservoirs in the environment (bed table) of frail older adults. In ONS, the degree of contamination was not bound to the type of ONS (dairy ONS vs. juice) but to the contamination of the product by the oral flora of the patient. Both types of ONS (with milk or vegetable proteins) contributed to preserving the viability of some microaerophilic oral strains. ONS and thickened drinks could be a source of contamination to other body sites. These reservoirs constitute a potential source of contamination to other residents via the hands of health care workers or family members. The risk increases with the necessity to assist frail older adults with eating and drinking (Saeb et al., 2017). Antibiotic resistance could also circulate via this route.

Second, certain germs can proliferate in some thickened drinks and ONS left at room temperature. Proliferation means high germ concentration, and the patient can ingest a contaminated product with a risk of diarrhea. There is also a risk of aspiration pneumonia for patients with dysphagia (Luk & Chan, 2014; Scannapieco & Cantos, 2016). The threat of bed table reservoirs is increased. For ONS, it must be noted that two bacterial strains, E. coli and S. aureus, were able to grow at room temperature in dairy drinks and creams containing lipids and milk protein (casein), but not in a juice that contained only vegetable proteins and no lipids. On the other hand, C. albicans could grow at room temperature in all tested ONS types, including juices. For thickened drinks, it is less expensive to use homemade drinks made with dehydrated products, but in the current study ready-to-use drinks seemed safer because they contained preservatives.

Finally, thickened drinks and ONS could contribute to microbial growth in the mouth. This situation may be heightened in patients with dysphagia and neurological and cognitive issues, who may keep these drinks in the mouth before swallowing. Healthy oral microbiota comprise many organisms, including bacteria, fungi, and protozoans (Zawadzki et al., 2017). The use of some thickened drinks and ONS at room temperature is analogous to turning the mouth into a Petri dish, encouraging the abnormal growth of specific species, which in turn shift the environment into a dysbiotic state. Oral environment combined with nutriments provided by these products can result in optimal conditions for microbial growth. Microbial proliferation could contribute to the formation of macroscopic microbial deposits, and halitosis (bad breath), which are frequently observed in the mouths of frail older adults. Such deposits worsen the risk of aspiration pneumonia. In addition, these products are often given several times daily, and consumption is not followed by tooth brushing. Thus, thickened drinks and ONS containing sugar could be assimilated to cariogenic diet and favor root caries in older adults (Gregory & Hyde, 2015; Hariyani et al., 2019). Candidiasis and proliferation on denture resin bases could be enhanced as well, resulting in denture stomatitis and angular cheilitis (Chevalier et al., 2018). Worsening of periodontal diseases cannot be excluded (Eke et al., 2016; Renvert & Persson, 2016).

Additional assays could detect oral bacteria, but also digestive and respiratory pathogens, C. albicans and other fungal species, and antibiotic/antifungal-resistant strains in partly consumed products collected in geriatric wards and nursing homes (Latour et al., 2019).

Conclusion

Institutions have infection control policies to prevent health care–associated infections. The current study confirmed that it is important to apply strict procedures to refrigerate or discard partly consumed ONS and thickened drinks. It is also important to remind family members of hand hygiene and the use of hydro-alcoholic solutions, because these individuals often help nursing home residents consume these products. The current work has other implications for practice, as it confirms that malnourished frail older adults need at least once daily mouth care with a toothbrush, and that nursing staff should favor “real food” instead of overly relying on easily administered ONS.

References

  • Bourdenet, G., Giraud, S., Artur, M., Dutertre, S., Dufour, M., Lefèbvre-Caussin, M., Proux, A., Philippe, S., Capet, C., Fontaine-Adam, M., Kadri, K., Landrin, I., Gréboval, E., Toublet, M., Nanfack, J., Tharasse, C., Varin, R., Rémy, E., Daouphars, M. & Doucet, J. (2015). Impact of recommendations on crushing medications in geriatrics: From prescription to administration. Fundamental & Clinical Pharmacology, 29(3), 316–320 doi:10.1111/fcp.12116 [CrossRef] PMID:25789404
  • Chávez, E. M. & Hendre, A. (2017). Clinical care for an aging population. The Compendium of Continuing Education in Dentistry, 38(9), 595–602 PMID:28972384
  • Chen, C. F., Chen, Y. F., Chan, C. H., Lan, T. H. & Loh, W. (2015). Common factors associated with choking in psychiatric patients. Journal of Research in Nursing, 23(2), 94–100 PMID:25967639
  • Chevalier, M., Ranque, S. & Prêcheur, I. (2018). Oral fungal-bacterial biofilm models in vitro: A review. Medical Mycology, 56(6), 653–667 doi:10.1093/mmy/myx111 [CrossRef] PMID:29228383
  • Chevalier, M., Sakarovitch, C., Prêcheur, I., Lamure, J. & Pouysségur-Rougier, V. (2015). Antiseptic mouthwashes could worsen xerostomia in patients taking polypharmacy. Acta Odontologica Scandinavica, 73(4), 267–273 doi:10.3109/00016357.2014.923108 [CrossRef] PMID:25601200
  • Cichero, J. A., Lam, P., Steele, C. M., Hanson, B., Chen, J., Dantas, R. O., Duivestein, J., Kayashita, J., Lecko, C., Murray, J., Pillay, M., Riquelme, L. & Stanschus, S. (2017). Development of international terminology and definitions of texture-modified foods and thickened fluids used in dysphagia management: The IDDSI framework. Dysphagia, 32(2), 293–314 doi:10.1007/s00455-016-9758-y [CrossRef] PMID:27913916
  • Clauson, H., Rull, F., Thibault, M., Ordekyan, A. & Tavernier, J. (2016). Crushing oral solid drugs: Assessment of nursing practices in health-care facilities in Auvergne, France. International Journal of Nursing Practice, 22(4), 384–390 doi:10.1111/ijn.12446 [CrossRef] PMID:27287304
  • Eke, P. I., Wei, L., Borgnakke, W. S., Thornton-Evans, G., Zhang, X., Lu, H., McGuire, L. C. & Genco, R. J. (2016). Periodontitis prevalence in adults ≥65 years of age, in the USA. Periodontology 2000, 72(1), 76–95. doi:10.1111/prd.12145 [CrossRef] PMID:27501492
  • Gil-Montoya, J. A., de Mello, A. L., Barrios, R., Gonzalez-Moles, M. A. & Bravo, M. (2015). Oral health in the elderly patient and its impact on general well-being: A nonsystematic review. Clinical Interventions in Aging, 10, 461–467 doi:10.2147/CIA.S54630 [CrossRef] PMID:25709420
  • Gregory, D. & Hyde, S. (2015). Root caries in older adults. Journal of the California Dental Association, 43(8), 439–445 PMID:26357814
  • Hariyani, N., Spencer, A. J., Luzzi, L., Harford, J., Tan, H., Mejia, G., Roberts-Thomson, K. & Do, L. G. (2019). The prevalence and severity of root surface caries across Australian generations. Community Dentistry and Oral Epidemiology, 47(5), 398–406 doi:10.1111/cdoe.12459 [CrossRef] PMID:31273824
  • Johansson, I., Jansson, H. & Lindmark, U. (2016). Oral health status of older adults in Sweden receiving elder care: Findings from nursing assessments. Nursing Research, 65(3), 215–223 doi:10.1097/NNR.0000000000000158 [CrossRef] PMID:27124257
  • Khan, A., Carmona, R. & Traube, M. (2014). Dysphagia in the elderly. Clinics in Geriatric Medicine, 30(1), 43–53 doi:10.1016/j.cger.2013.10.009 [CrossRef] PMID:24267601
  • Lamure, J., Chevalier, M., Rathelot, P., Mignolet, F. & Prêcheur, I. (2018). In vitro screening of the antibacterial and anti-Candida properties of crushed nonantimicrobial drugs frequently prescribed in nursing homes. Research in Gerontological Nursing, 11(2), 82–90 doi:10.3928/19404921-20180131-01 [CrossRef] PMID:29451932
  • Latour, K., Huang, T. D., Jans, B., Berhin, C., Bogaerts, P., Noel, A., Nonhoff, C., Dodemont, M., Denis, O., Ieven, M., Loens, K., Schoevaerdts, D., Catry, B. & Glupczynski, Y. (2019). Prevalence of multidrug-resistant organisms in nursing homes in Belgium in 2015. PLoS One, 14(3), e0214327. doi:10.1371/journal.pone.0214327 [CrossRef]
  • Luk, J. K. & Chan, D. K. (2014). Preventing aspiration pneumonia in older people: Do we have the ‘know-how’?Hong Kong Medical Journal, 20(5), 421–427 doi:10.12809/hkmj144251 [CrossRef] PMID:24993858
  • Milne, A. C., Potter, J., Vivanti, A. & Avenell, A. (2009). Protein and energy supplementation in elderly people at risk from malnutrition. The Cochrane Database of Systematic Reviews, 2, CD003288. doi:10.1002/14651858.CD003288.pub3 [CrossRef]
  • Morilla-Herrera, J. C., Martín-Santos, F. J., Caro-Bautista, J., Saucedo-Figueredo, C., García-Mayor, S. & Morales-Asencio, J. M. (2016). Effectiveness of food-based fortification in older people. A systematic review and meta-analysis. The Journal of Nutrition, Health & Aging, 20(2), 178–184 doi:10.1007/s12603-015-0591-z [CrossRef] PMID:26812514
  • Réglier-Poupet, H., Parain, C., Beauvais, R., Descamps, P., Gillet, H., Le Peron, J. Y., Berche, P. & Ferroni, A. (2005). Evaluation of the quality of hospital food from the kitchen to the patient. The Journal of Hospital Infection, 59(2), 131–137 doi:10.1016/j.jhin.2004.07.023 [CrossRef] PMID:15620447
  • Renvert, S. & Persson, G. R. (2016). Treatment of periodontal disease in older adults. Periodontology 2000, 72(1), 108–119. doi:10.1111/prd.12130 [CrossRef] PMID:27501494
  • Saeb, A., Mody, L. & Gibson, K. (2017). How are nursing homes cleaned? Results of a survey of 6 nursing homes in Southeast Michigan. American Journal of Infection Control, 45(11), e119–e122 doi:10.1016/j.ajic.2017.08.019 [CrossRef] PMID:28958448
  • Scannapieco, F. A. & Cantos, A. (2016). Oral inflammation and infection, and chronic medical diseases: Implications for the elderly. Periodontology 2000, 72(1), 153–175. doi:10.1111/prd.12129 [CrossRef] PMID:27501498
  • Sura, L., Madhavan, A., Carnaby, G. & Crary, M. A. (2012). Dysphagia in the elderly: Management and nutritional considerations. Clinical Interventions in Aging, 7, 287–298 PMID:22956864
  • Vallons, K. J., Helmens, H. J. & Oudhuis, A. A. (2015). Effect of human saliva on the consistency of thickened drinks for individuals with dysphagia. International Journal of Language & Communication Disorders, 50(2), 165–175 doi:10.1111/1460-6984.12120 [CrossRef] PMID:25298105
  • Zawadzki, P. J., Perkowski, K., Padzik, M., Mierzwińska-Nastalska, E., Szaflik, J. P., Conn, D. B. & Chomicz, L. (2017). Examination of oral microbiota diversity in adults and older adults as an approach to prevent spread of risk factors for human infections. BioMed Research International, 2017, 8106491 doi:10.1155/2017/8106491 [CrossRef] PMID:29082256

Bacterial and Fungal Strains Tested

Microbial Species and Reference NumberMain Reservoir and Most Often Linked Illnesses
Escherichia coliaATCC 10536Prominent member of digestive tract microbiome; can colonize the mouth. Diarrhea, urinary tract infection (UTI), meningitis, sepsis; possible member of oral biofilm in frail older adults.
Staphylococcus aureusaATCC 6538Frequently colonizing skin and mucosae, especially nasal mucosae; can colonize the mouth. Food poisoning (toxins), localized suppurative infections (skin, upper airway, pneumonia), infectious endocarditis, sepsis (immunocompromised persons); possible member of oral biofilm in frail older adults.
Pseudomonas aeruginosaaATCC15442Opportunistic pathogen: survival in aqueous environment (e.g., sanitary equipment, flower vase). Nosocomial infections (immunocompromised persons, diabetes, cystic fibrosis): eye infections, superinfection of wounds and burns, UTI, pneumonia, meningitis, and sepsis.
Micrococcus luteusaCIP A270TRegular member of oral biofilm: low pathogenicity except inhalation pneumonia (mixed flora).
Gemella haemolysansaCIP 101126TRegular member of oral biofilm: low pathogenicity except inhalation pneumonia (mixed flora).
Streptococcus salivariusaCIP 102505Regular member of oral biofilm: low pathogenicity except inhalation pneumonia (mixed flora).
Rothia mucilaginosaaCIP 71.14TRegular member of oral biofilm: low pathogenicity except inhalation pneumonia (mixed flora).
Streptococcus mutansaCIP 103220TRegular member of oral biofilm: the most virulent bacteria associated with dental caries; inhalation pneumonia; and infectious endocarditis.
Candida albicansbATCC 10231Yeast form: regular member of healthy mucosal microbiome. Hyphal form: oral, digestive, and gynecological infections; inhalation pneumonia; sepsis; and deep infections (immunocompromised persons).

Qualitative Evaluationa of Microbial Growth in Oral Nutritional Supplements Inoculated With Escherichia coli, Staphylococcus aureus, and Candida albicans, Grown for 48 Hours at Room Temperature

Oral Nutritional SupplementColony Forming Units
Negative ControlE. coliS. aureusC. albicans
Dairy drink strawberry flavor++++++++
Dairy cream vanilla flavor++++++++
Juice cherry flavor++
Sucrose-free dairy cream vanilla flavor++++++++

Details of the Seven Samples of Oral Nutritional Supplements Collected and Qualitative Evaluation of Colony Forming Units After 3 to 5 Days Incubation on Blood Agar Plates in Microaerophilic Conditions at 37°C

Oral Nutritional Supplement
SampleBrandTextureFlavorSpecific Con tent
AProvideXtra™JuiceCherryLactose free
BResource™Dairy creamMochaSaccharose free, lactose free
CProvideXtra™JuiceRed currantLactose free
DProvideXtra™JuiceCherryLactose free
EFortimel™Dairy drinkVanillaCholine
FFortimel™Dairy drinkVanillaLactose free
GProvideXtra™JuiceOrange-pineappleSaccharose free

Ingredients of the four thickened drinks tested

Thickened drinks testedIngredients
Dehydrated thickened drink - sweetenedCorn maltodextrin, thickening: guar gum, acidity regulator: citric acid, natural aroma (lemon), sweeteners: aspartame, acesulfame K, coloring: E102
Dehydrated thickened drink - with sugarSugar, thickening: guar gum, acidity regulator: citric acid, natural aroma (lemon), corn maltodextrin, sunflower oil, coloring: E102
Ready for use thickened drink - sweetened, with preservativesWater, gelling agents: carob flour, guar gum, carrageenan, acidity regulators: sodium citrate, gluconodeltalactanone, citric acid, potassium chloride, natural aroma (lemon), maltodextrin, preservatives: potassium sorbate, sodium benzoate, sweeteners: aspartame, acesulfame K, coloring: E102
Ready for use thickened drink - with sugar and preservativesWater, sugar, gelling agents: carob flour, guar gum, carrageenan, acidity regulators: sodium citrate, gluconodeltalactanone, citric acid, potassium chloride, corn maltodextrin, natural aroma (lemon), preservatives: potassium sorbate, sodium benzoate, coloring: E102

Nutritional values (theorical calculated values) of the four thickened drinks tested

Mean nutritional valuesDehydrated thickened drink sweetenedDehydrated thickened drink with sugarReady for use thickened drink sweetenedReady for use thickened drink with sugar 100 g
100 g powder100 g rehydrated mix1100 g powder100 g rehydrated mix 2100 gServing cup 125 g
Energy (kcal)26410346314543
Energy (kJ)11024214601331721183
Fat (g)<0.5<0.5<0.5<0.5<0.5<0.5<0.5
- of which saturates (g)<0.1<0.1<0.1<0.1<0.1<0.1<0.1
Carbohydrate (g)451.7777.00.70.810
- of which sugars (g)4.7<0.5766.9<0.5<0.510
Protein (g)2.2<0.51.0<0.5<0.5<0.5<0.5
Salt (g)0.02<0.01<0.01<0.010.250.310.25

Ingredients of the four oral nutritional supplements (ONSs) tested. Milk proteins: mainly casein from cow milk

Dairy drinkDrink strawberry flavor Fortimel Compact Protein™ NutriciaWater, milk proteins, dextrin-maltose, sucrose, plant oil (colza, sunflower), magnesium orthophosphate, emulsifier (soya lecithin), aroma (strawberry), choline chloride, sodium L-ascorbate, tri-potassium citrate, di-potassium orthophosphate, ferrous lactate, DL-a-tocopherol acetate, nicotinamide, coloring (curcumine), retinol acetate, copper gluconate, manganese sulphate, sodium selenite, calcium D-pantothenate, D-biotine, zinc sulphate, chromium chloride, cholecalciferol, pyridoxine chlorhydrate, pteroylmonoglutamic acid, thiamine chlorhydrate, potassium iodide, riboflavine, sodium molybdate, sodium fluoride, phytomenadione.
Dairy creamCream vanilla flavor Forticrème™ NutriciaWater, sucrose, milk proteins, corn syrup, plant oil (colza, sunflower), modified starch, aroma (vanilla), di-potassium orthophosphate, emulsifying (mono-and diglycerides of fatty acids), stabilizing carrageenan, sodium citrate, magnesium chloride, choline chloride, magnesium orthophosphate, sodium L-ascorbate, dextrin-maltose, potassium hydroxide, ferrous lactate, coloring (curcumine), DL-a-tocopherol acetate, retinol acetate, copper gluconate, zinc sulphate, sodium selenite, manganese sulphate, calcium D-pantothenate, chromium chloride, cholecalciferol, pyridoxine chlorhydrate, thiamine chlorhydrate, nicotinamide, sodium molybdate, riboflavine, sodium fluoride, phytomenadione, pteroylmonoglutamique acid, potassium iodide, D-biotine, cyanocobalamine.
JuiceJuice cherry flavor ProvideXtra™ Fresenius-KabiWater, maltodextrin, sucrose, pea protein hydrolysate, soya protein hydrolysate, cherry juice concentrate, acid regulator (E 330), calcium lactate, flavourings, magnesium citrate, magnesium glycerophposphate, stabilizer (E 440a), vitamin C, magnesium chloride, iron citrate, zinc sulphate, potassium chloride, vitamin E, niacin, vitamin A, pantothenic acid, manganese chloride, copper sulphate, vitamin B2, vitamin B6, sodium fluoride, vitamin B1, folic acid, chromium chloride, potassium iodide, sodium molybdate, sodium selenite, vitamin K1, biotin, vitamin D3, vitamin B12.
Sucrose-free dairy creamCream vanilla flavor Fresubin DB crème nutriment™ Fresenius-KabiWater, milk proteins, fructose, plant oil (sunflower, colza), maltodextrin, cocoa powder (1.4 %), aroma, emulsifiers (soya lecithin, E 471), potassium iodide, sodium chloride, vitamin C, stabilizers (E 460, E 466, E 407), acidity regulator (E 524), iron phosphate, zinc sulphate, niacine, pantothenic acid, manganese chlorinate, vitamin E, copper sulphate, vitamin B2, vitamin B6, sodium fluoride, vitamin B1, beta-carotene, vitamin A, folic acid, potassium iodide, sodium selenite, sodium molybdate, chromium chloride, vitamin K1, biotine, vitamin D3, vitamin B12.

Properties and reagents of a general purpose medium suitable for the cultivation of a wide variety of bacteria, yeasts and filamentous fungi from clinical specimens (data sheet Brain Heart Infusion or BHI, Beckton Dickinson GmBH https://www.bd.com/resource.Aspx?IDX=9008)

Brain Heart Infusion (BHI) liquid culture medium
PropertiesBrain-heart infusion, peptone and carbohydrate components bring nutriments.
Peptones and infusion are the sources of organic nitrogen, carbon, sulfur, vitamins and trace elements.
Sucrose is the source of carbohydrate which microorganisms use by fermentation.
The medium is buffered through the use of disodium phosphate.
Reagents1 L purified water: Brain-heart, infusion from (solids) 8.0 g Peptic digest of animal tissue 5.0 g Pancreatic digest of casein 16.0 g Sodium chloride 5.0 g Glucose 2.0 g Disodium hydrogen phosphate 2.5 g Agar 13.5 g pH 7.4 ± 0.2
Authors

Dr. Jung is Pharmacist, Dr. Bouhlel is Dental Surgeon, and Prof. Prêcheur is Senior Professor, Dental School, Ms. Molinari is Nursing Instructor, Service de Gérontologie, Hôpital de Cimiez, and Prof. Ruimy is Senior Professor, Laboratoire de Bactériologie, Hôpital l'Archet, Centre Hospitalier de Nice, Université Côte d'Azur, Nice, France.

The authors have disclosed no potential conflicts of interest, financial or otherwise.

The authors thank Marlène Chevalier, PhD, for laboratory protocol supervision and for providing curves standards.

Address correspondence to Isabelle Prêcheur, PhD, DDS, Senior Professor, Université Côte d'Azur, Dental School, Laboratoire Micoralis EA 7354, 24 avenue des Diables Bleus, 06300 Nice, France; e-mail: isabelle.precheur@univ-cotedazur.fr.

Received: July 15, 2019
Accepted: October 28, 2019
Posted Online: February 27, 2020

10.3928/19404921-20200220-01

Sign up to receive

Journal E-contents