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Dietary Trends and Management of Hyperphosphatemia Among Patients With Chronic Kidney Disease: An International Survey of Renal Care Professionals
ORIGINAL RESEARCH
Dietary Trends and Management of Hyperphosphatemia Among Patients With Chronic Kidney Disease: An International Survey of Renal Care Professionals Denis Fouque, MD, PhD,* Maria Cruz Casal, RN, DUE,† Elizabeth Lindley, PhD,‡ Susan Rogers, RN, BA,§ Jitka Pancır ova, RN,{ Jennifer Kernc, RD, CSR, LD,** and J. Brian Copley, MD†† Objective: The objective of this study was to review the opinions and experiences of renal care professionals to examine dietary trends among patients with chronic kidney disease (CKD) and problems associated with the clinical management of hyperphosphatemia. Design: This was an online survey comprising open and closed questions requesting information on patient dietary trends and the clinical management of hyperphosphatemia. The study was conducted in 4 European countries (the Netherlands, Spain, Sweden, and the United Kingdom). Subjects: Participants were 84 renal care professionals. Intervention: This was an online survey. Main Outcome Measure: Responder-reported experiences and perceptions of patient dietary trends and hyperphosphatemia management were assessed. Results: Most survey responders (56%) observed an increase in the consumption of processed convenience food, 48% noticed an increase in the consumption of foods rich in phosphorus-containing additives, and 60% believed that there has been a trend of increasing patient awareness of the phosphorus content of food. Patients undergoing hemodialysis (HD) were most likely to experience difficulties in following advice on dietary phosphorus restriction (38% of responders estimated that 25-50% of their patients experienced difficulties, and 29% estimated that 51-75% experienced difficulties). Maintaining protein intake and restricting dietary phosphorus were perceived as being equally important by at least half of responders for predialysis patients (56%) and for those undergoing peritoneal dialysis and HD (54% and 50%, respectively). There were international variations in dietary trends and hyperphosphatemia management. Conclusion: Although most responders have observed a trend of increasing awareness of the phosphorus content of food among patients with CKD, the survey results indicate that many patients continue to experience difficulties when attempting to restrict dietary phosphorus. The survey responses reflect the global trend of increasing consumption of processed convenience foods and phosphorus-containing additives, which has implications for the management of hyperphosphatemia in patients with CKD. Ó 2014 by the National Kidney Foundation, Inc. All rights reserved.
Introduction *
Department of Nephrology, Centre Hospitalier Lyon-Sud, CENS, CARMEN, Universite de Lyon, Lyon, France. † Department of Nephrology, Hospital Universitario 12 de Octubre, Madrid, Spain. ‡ Department of Renal Medicine, Leeds Teaching Hospitals NHS Trust, Leeds, United Kingdom. § Dialysis Department, Codia Waterland B.V., Purmerend, the Netherlands. { European Dialysis and Transplant Nurses Association/European Renal Care Association Secretariat and Conference Department, Prague, Czech Republic. ** Shire LLC, Internal Medicine BU, Wayne, Pennsylvania. †† Shire LLC, Clinical Development and Medical Affairs, Wayne, Pennsylvania. Financial Disclosure: See Acknowledgments on page 115. Address correspondence to Denis Fouque, MD, PhD, Centre Hospitalier Lyon-Sud, Department of Nephrology, Lyon, France. E-mail: denis.fouque@
chu-lyon.fr Ó
2014 by the National Kidney Foundation, Inc. All rights reserved. 1051-2276/$36.00 http://dx.doi.org/10.1053/j.jrn.2013.11.003
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YPERPHOSPHATEMIA, A COMMON disorder in patients with chronic kidney disease (CKD), is strongly associated with cardiovascular morbidity and mortality.1-3 Preventing and correcting hyperphosphatemia is integral to the management of patients with CKD. Achieving recommended levels of protein intake4 while maintaining guideline levels of serum phosphorus5 is associated with the best outcomes in these patients.6 The management of hyperphosphatemia typically consists of a combination of dietary modification, phosphate binder therapy, and dialysis (for patients with stage 5D CKD). Maintaining optimal serum phosphorus levels is often difficult. The Dialysis Outcomes and Practice Patterns Study found that serum phosphorus was maintained below the upper limit of the target range (5.5 mg/dL) in fewer than 50% of patients over a 5-year study period.7 Dietary
Journal of Renal Nutrition, Vol 24, No 2 (March), 2014: pp 110-115
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counseling is instrumental in achieving the required reduction in phosphorus burden for patients with CKD;8 however, it often poses a significant challenge for renal care professionals.9 One of the problems is that if protein intake is optimized, then there is a concomitant increase in dietary phosphorus that may exceed the recommended daily phosphorus intake in patients undergoing maintenance hemodialysis (HD).10 The implementation of dietary phosphorus restriction can also be complicated by the consumption of processed foods and drinks that are rich in phosphorus-containing additives. These additives can significantly increase the amount of phosphorus consumed in the daily diet.11 Furthermore, the phosphorus contained in additives (inorganic phosphorus) is more readily absorbed than the phosphorus in natural, protein-rich foods (organic phosphorus).12 Therefore, the rising consumption of low-cost convenience food in the global population has resulted in increasing dietary phosphorus burdens13 with implications for the management of hyperphosphatemia in patients with CKD. To explore trends in phosphorus consumption among patients with CKD and to examine the problems associated with the clinical management of hyperphosphatemia, we conducted a survey of renal care professionals in 4 European countries. Although there have been numerous surveys that have examined the attitudes and practices of renal care professionals,14-18 to our knowledge this survey is the first to investigate their experiences relating to dietary trends and restriction of dietary phosphorus intake in patients with CKD before and during dialysis.
Methods The survey was developed as part of a collaboration between the European Dialysis and Transplant Nurses Association/European Renal Care Association (EDTNA/ ERCA) and Shire Development LLC. It was designed to obtain information relating to responder demographics and their perceptions and experiences of patient dietary trends, clinical practices and recommendations, and problems associated with the management of hyperphosphatemia. The survey comprised open, free-text questions and closed, multiple-choice questions. For closed questions, ‘‘not applicable’’ or ‘‘other’’ were given as options if appropriate. The survey consisted of 26 questions in total. In this study, we analyzed the responses to a selection of closed, multiple-choice questions from the survey that related to patient dietary trends, the difficulties associated with dietary phosphorus restriction, and perceptions regarding the relative importance of maintaining protein intake versus dietary phosphorus restriction. Responders were required to state if they had observed, since entering clinical practice, an increase, decrease, or no change at all in patient consumption of fresh food, processed convenience food, and foods rich in phosphoruscontaining additives. In addition, they were asked to report
which trend best applied to patient awareness of the phosphorous content of food. They were also required to estimate the proportion of patients that experienced difficulties in following advice on restricting dietary phosphorus for a range of patient groups. Finally, responders were given the option to rank the importance of different hyperphosphatemia management approaches through selecting one of the following options: maintaining protein intake is more important, limiting dietary phosphorus is more important, or both strategies are equally important. Renal care professionals responsible for providing dietary advice to patients in renal units in the Netherlands, Spain, Sweden, and the United Kingdom were asked to complete the survey. These countries were selected to ensure that renal units in northern and southern Europe were represented in the survey. Invitations to participate in the survey were e-mailed to renal care professionals working in clinics that had been selected to ensure a reasonable geographical distribution within each country. Recruitment in each country was stopped when at least 20 responses had been received. Characteristics of nonresponders were not collected. The survey was completed online in September and October 2012. In each of the 4 countries, national coordinators from the EDTNA/ERCA oversaw the administration of the survey. The national coordinators were responsible for selecting and inviting renal care professionals in their region to participate in the survey. Individuals were invited from renal units that had been selected to ensure a reasonable geographical distribution within each country. With the exception of 1 year’s free membership to the EDTNA/ERCA, no responder incentives were provided for completing the survey. The survey was translated for Spanish responders and validated by a second translator. Translation was not required for responders in Sweden and the Netherlands. All responses from Spain were translated into English before analysis; if any other responses were received in a language other than English, then they were also translated. During the analysis, responders could be identified only by their renal unit. Responses were analyzed for each country separately to examine geographical variations in patterns and trends and were also analyzed after pooling the data from all 4 countries. Descriptive statistics were used to analyze all survey responses.
Results Responder Demographics and Patient Numbers Responses were received from 84 renal care professionals in total, comprising 48 renal dietitians, 35 renal nurses, and 1 renal physician from hospitals and outpatient clinics in the 4 countries (Spain, n 5 20; United Kingdom, n 5 22; Sweden, n 5 20; the Netherlands, n 5 22). These participants reported a total of 1,294 years of renal practice experience, with a mean of 15.4 years per individual (range,
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2-32 years). The proportions of renal nurse and renal dietitian responders varied among countries: In Sweden, 50% of responders were nurses and 50% were dietitians; in the United Kingdom, dietitians made up 100% of the responders; in Spain, 95% were nurses; and in the Netherlands, 73% were dietitians and 27% were nurses. Spain was the only country where a renal physician responded. Combined, the responders’ institutions were responsible for treating approximately 17,000 predialysis patients, more than 12,500 individuals undergoing HD, and nearly 3,000 undergoing peritoneal dialysis.
Dietary Trends The survey revealed several trends in dietary habits. Since entering clinical practice, 29 responders (35%) had noticed a decrease in the consumption of food prepared from fresh ingredients, 47 (56%) had noticed an increase in the consumption of processed convenience food (‘‘fast food’’), and 40 (48%) had noticed an increase in the consumption of foods rich in phosphorus-containing additives. Fifty responders (60%) believed that since entering clinical practice there has been a trend for patients with CKD to have a greater awareness of the phosphorus content of food. Dietary trends were found to vary among the 4 countries (Fig. 1). Most responders in the United Kingdom (59%, n 5 13) reported a decrease in the consumption of foods
prepared with fresh ingredients, whereas responders from the Netherlands, Spain, and Sweden predominantly reported no change. Most responders in the United Kingdom and Spain reported an increase in the consumption of fast food (77%, n 5 17; 65%, n 5 13, respectively); this was also the most common response in Sweden (50%, n 5 10). In the Netherlands, the most frequent observation (41%, n 5 9) was a decrease in fast food consumption. Most responders in the United Kingdom and Spain (59% and 55%, respectively) found that consumption of food containing phosphorus-based additives had increased; 40% of responders in Sweden also reported this trend. In the Netherlands, no change in the consumption of phosphatebased additives was most frequently reported (41%). Increasing patient awareness of the phosphorus content of food was the most common observation in Spain, Sweden, and the Netherlands (50%, 75%, and 77%, respectively), whereas most responders in the United Kingdom (59%) found that there had been no change in this respect.
Management of Hyperphosphatemia Patients undergoing HD were reported as being the most likely to experience difficulties in following advice on restricting daily phosphorus intake; 32 responders (38%) reported that 25% to 50% of their patients undergoing HD experienced difficulties, and 24 responders (29%) estimated this figure to be between 51% and 75% (Fig. 2). Predialysis Decrease No change Increase Consumption of fast food
Consumption of food made from fresh ingredients 100 Proportion of patients (%)
Proportion of patients (%)
100 80 60 40 20 0
80 60 40 20 0
Netherlands
Spain
Sweden
UK
Netherlands
Consumption of food containing phosphorus-based additives
Sweden
UK
Patient awareness of the phosphorus content of food 100 Proportion of patients (%)
100 Proportion of patients (%)
Spain
80 60 40 20 0
80 60 40 20 0
Netherlands
Spain
Sweden
UK
Netherlands
Spain
Sweden
UK
Figure 1. Dietary trends observed by renal care professionals in 4 European countries since entering clinical practice. Netherlands (n 5 22); Spain (n 5 20); Sweden (n 5 20); UK (n 5 22).
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Figure 2. Proportions of predialysis, peritoneal dialysis, and hemodialysis patients who renal care professionals believe experience difficulties restricting dietary phosphorus intake (n 5 84). N/A, not applicable.
patients were the least likely to experience difficulties restricting dietary phosphorus intake; 39 responders (46%) reported that fewer than 25% of their predialysis patients experienced difficulties, and only a small percentage (4%; n 5 3) estimated this figure to be 51% to 75% (Fig. 2). Compared with predialysis patients, a larger percentage of patients undergoing peritoneal dialysis were thought to find it difficult to restrict dietary phosphorus; 14 responders (17%) estimated that 51% and 75% of their patients undergoing peritoneal dialysis experienced difficulties (Fig. 2). There were differences in the percentages of patients believed to experience difficulties restricting dietary phosphorus among the 4 countries. In Spain, the most commonly reported percentage of predialysis patients who experienced difficulty was 25% to 50% (estimated by 50% of responders), compared with fewer than 25% of predialysis patients in the Netherlands, the United Kingdom, and Sweden (estimated by 50%, 64%, and 50% of responders, respectively). Most Spanish responders (60%) reported that 51% to 75% of their patients undergoing HD experienced difficulties restricting dietary phosphorus, which was higher than the figures in Sweden, the Netherlands, and the United Kingdom (30%, 18%, and 9%, respectively). The most frequently reported percentage of patients undergoing HD who experienced difficulties in the Netherlands and the United Kingdom was 25% to 50% (41% and 68% of responders, respectively). In the United Kingdom and Spain, 50% and 45% of responders, respectively, estimated that 25% to 50% of individuals undergoing peritoneal dialysis experienced difficulties restricting dietary phosphorus. In the Netherlands and the United Kingdom, the most commonly reported percentage of patients undergoing peritoneal dialysis to experience difficulties was less than 25% (41% and 40% of responders, respectively). Overall, 37 responders (44%) believed that younger patients (18-45 years) are more likely to find it difficult to restrict dietary phosphorus intake than any other age group. When asked if other groups of patients experienced diffi-
culties, individuals with low incomes, obese patients, malnourished individuals, and those with diabetes mellitus were the most commonly reported (64%, 58%, 54%, and 40% of responders, respectively). In comparison, only 12% of responders thought that patients suitable for transplant experienced difficulties restricting dietary phosphorus. In total, 42 responders (50%) perceived restricting dietary phosphorus and maintaining protein intake in patients undergoing HD as being equally important whereas 30 (36%) favored maintaining protein intake over restricting phosphorus (Fig. 3). There were similar findings for nutrition management in predialysis patients and in those undergoing peritoneal dialysis (Fig. 3). Most responders in all 4 countries rated restricting dietary phosphorus and maintaining protein intake as being equally important in the management of hyperphosphatemia in predialysis patients and in those undergoing peritoneal dialysis. However, for individuals undergoing HD, the most frequent response in Spain (45%) was to rate restricting dietary phosphorus as being more important than maintaining protein intake, whereas in Sweden, maintaining protein intake was rated as being more important than restricting dietary phosphorus by most responders (60%). In the United Kingdom, the most frequent response (82%) was that both approaches were perceived as being equally important. In the Netherlands, 45% of responders stated that both approaches
Maintaining protein intake is more important Limiting dietary phosphorus is more important Both strategies are equally important Predialysis
30% 56% 14%
Peritoneal dialysis
37% 54% 9%
Hemodialysis
36% 50% 14%
Figure 3. Relative importance of phosphorus restriction and adequate protein intake in predialysis patients and in those undergoing hemodialysis and peritoneal dialysis from the perspective of renal care professionals (n 5 84).
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were equally important and 45% reported that maintaining protein intake was more important. These responses were also analyzed according to the renal practice experience of the responders (0-9 years, n 5 19; 10-19 years, n 5 35; 20-29 years, n 5 23; and $30 years, n 5 6). Most responders in each practice experience group reported that both approaches were equally important (0-9 years 5 58% of responders, 10-19 years 5 54%, 20-29 years 5 52%, and $30 years 5 67%). Fewer responders in the most experienced renal practice groups regarded limiting dietary phosphorus intake as the most important approach compared with those with less practice experience (0-9 years 5 21% of responders, 10-19 5 17%, 20-29 5 9%, and $30 5 0%).
Discussion Hyperphosphatemia is a serious clinical consequence of renal failure that requires concerted management in patients with CKD. Assisting and encouraging individuals undergoing dialysis to maintain their serum phosphorus levels within guideline parameters5 is a considerable challenge for renal care professionals.9 Assessing the nutritional intake of individuals undergoing dialysis is a necessary part of the clinical approach to controlling serum phosphorus levels and improving patient outcomes.19 To our knowledge, this is the first survey to examine renal nurses’ and dietitians’ perceptions and experiences relating to dietary trends and the problems associated with the management of hyperphosphatemia in patients with CKD. In terms of dietary emphasis, the results of this survey indicate that most providers of dietary advice to patients with CKD perceive the maintenance of adequate protein intake to be equally or more important than dietary phosphorus restriction in the management of hyperphosphatemia in patients with CKD. The number of years of experience in renal care did not produce major variation in these responses. Given the importance of protein intake in these patients, and the fact that foods with a high protein content are major sources of organic phosphorus, a suitable dietary phosphorus metric for patients may be the ratio of phosphorus (milligrams) to protein (grams) for a given food item.12,20 Despite an increased awareness of the phosphorus content of food, the survey results indicate that many patients continue to experience problems restricting dietary phosphorus. The global trend of increasing consumption of processed foods,21 in which phosphorus-containing additives may be used to extend shelf life, to improve color or flavor, or to increase water retention, is reflected in the responses of the renal care professionals surveyed in this study. These food additives can account for more than 30% of dietary phosphorus intake.22 This type of dietary phosphorus burden has important implications for the management of hyperphosphatemia because the phosphorus is almost completely absorbed,12 undermining the effects of phosphate binding therapy8 and resulting in the need for
increased doses of phosphate binders to achieve the same effect on phosphorus balance. According to a review in 2010,13 an additional 1,000 mg of inorganic phosphate can be absorbed daily from processed food and drinks, which renders patients’ dietary efforts almost useless. Therefore, to achieve adequate protein intake while restricting dietary phosphorus, foods with low phosphorusto-protein ratios13,20 and minimal phosphorus-containing additives should be recommended to patients, together with appropriate regimens of phosphate binders when necessary. Although the European Community regulations require manufacturers to report the presence of phosphorus on the food label, disclosure of the amount is not required.8 In addition, there is no accurate method to distinguish between protein-based phosphorus and preservative-based phosphorus in food.23,24 Consequently, phosphorus from food additives may be unrecognized, which may create difficulties for patients undergoing dialysis who are attempting to restrict their phosphorus intake. Results of a survey among individuals with CKD revealed that they would find it useful to see nutrients of concern, particularly phosphorus, listed as absolute amounts on the Nutrition Facts label of food and drink products.25 Results from the present survey revealed international variations in patient dietary trends and renal care professionals’ experiences and perceptions of the management of hyperphosphatemia. Awareness of these differences may be useful for the development of guidance and educational materials for the management of hyperphosphatemia across this region. However, it is important to note that the proportions of renal nurses and dietitians who responded to the survey varied among countries. This may be considered to be a limitation of the study because the patient care roles and clinical duties of renal nurses and dietitians can differ. Therefore, the potential differences in the experiences and practices in each profession may have caused some variation in the responses across the 4 countries. However, in Spain, renal nurses have a dual role, performing the same duties as renal dietitians, and can therefore be considered to be representative of both professions. Furthermore, the inclusion of responders from both professions may be considered to be beneficial because it generates a wider representation of opinions and experiences. Another limitation of the study is that we did not examine potential cultural differences among the countries. Patients’ dietary phosphorus burdens can be influenced by factors such as common food preparation practices and food staples,8 which may vary among countries. It would be useful to include these factors in future surveys of this nature. In addition, repeating the survey in countries outside of Europe would enable examination of wider international trends, and repeating the survey in the same countries in the future would be useful for determining changes in the trends observed in the study presented here. It would also
DIETARY TRENDS AMONG PATIENTS WITH CKD
be interesting to conduct a survey of a similar nature to determine patients’ personal perceptions of dietary trends and the problems associated with the management of hyperphosphatemia. A further limitation is that the results from the survey cannot be analyzed statistically because of the small sample size (particularly in the responder subgroups). However, descriptive statistical analysis alone has revealed some interesting trends. One final limitation was that the survey was not validated; however, it was designed and developed by a team of renal care professionals and the executive committee of the EDTNA/ERCA. In conclusion, the results of this study indicate that there is increasing consumption of processed foods and that patients with CKD continue to experience difficulties when attempting to restrict dietary phosphorus. A key problem appears to be the extensive use of phosphorus-containing additives in food, alongside the lack of clear labeling of phosphorus content.
Practical Application The renal community must lobby for accurate labeling of food and drink to show the amount of phosphoruscontaining additives and, ideally, the phosphorus content per portion. This would enable patients to avoid or limit their intake of unnecessary phosphorus from additives and help them to maintain adequate protein intake within the limits set by dialysis and an acceptable phosphate binder regimen. In response to the widespread consumption of phosphorus-containing additives in modern diets, food regulation agencies need to re-evaluate the regulation of these additives in the food and drink industry.
Acknowledgments The survey was funded by Shire Development LLC. J.K. and J.B.C. are employees of Shire LLC. D.F. has received honoraria or lecture fees from Abbott, Amgen, Genzyme, and Shire LLC. The other authors have no conflicts of interest to declare. The authors thank Vivienne Johnson of PharmaGenesisÔ London for manuscript writing support, which was funded by Shire, LLC.
References 1. Achinger SA, Ayus JC. Left ventricular hypertrophy: is hyperphosphatemia a risk factor in dialysis patients? J Am Soc Nephrol. 2006;17:S255-S261. 2. Kestenbaum B, Sampson JN, Rudser KD, et al. Serum phosphate levels and mortality risk among people with chronic kidney disease. J Am Soc Nephrol. 2005;16:520-528. 3. Block GA, Klassen PS, Lazarus JM, et al. Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol. 2004;15:22082218. 4. Fouque D, Vennegoor M, Ter Wee P, et al. EBPG guideline on nutrition. Nephrol Dial Transplant. 2007;22(suppl 2):ii45-ii87.
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5. National Kidney Foundation. KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease–mineral and bone disorder (CKD–MBD). Kidney Int. 2009;76: S50-S69. 6. Shinaberger CS, Greenland S, Kopple JD, et al. Is controlling phosphorus by decreasing dietary protein intake beneficial or harmful in persons with chronic kidney disease? Am J Clin Nutr. 2008;88:1511-1518. 7. Young EW, Albert JM, Satayathum S, et al. Predictors and consequences of altered mineral metabolism: the Dialysis Outcomes and Practice Patterns Study. Kidney Int. 2005;67:1179-1187. 8. Cupisti A, Kalantar-Zadeh K. Management of natural and added dietary phosphorus burden in kidney disease. Semin Dial. 2013;33:180-190. 9. Shaw-Stuart N, Stuart A. The effect of an educational patient compliance program on serum phosphate levels in patients receiving hemodialysis. J Ren Nutr. 2000;10:80-84. 10. Fouque D, Pelletier S, Mafra D, Chauveau P. Nutrition and chronic kidney disease. Kidney Int. 2011;80:348-357. 11. Ritz E, Hahn K, Ketteler M, Kuhlmann MK, Mann J. Phosphate additives in food—a health risk. Dtsch Arztebl Int. 2012;109:49-55. 12. Noori N, Sims J, Kopple J, et al. Organic and inorganic dietary phosphorus and its management in chronic kidney disease. Iran J Kidney Dis. 2010;4:89-100. 13. Kalantar-Zadeh K, Gutekunst L, Mehrotra R, et al. Understanding sources of dietary phosphorus in the treatment of patients with chronic kidney disease. Clin J Am Soc Nephrol. 2010;5:519-530. 14. Thelen B, Byham-Gray L, Touger-Decker R, O’Sullivan Maillet J, Kahn H. Survey of current job functions of renal dietitians. J Ren Nutr. 2009;19:450-461. 15. Vergili J, Wolf R. Nutrition practices of renal dietitians in hemodialysis centres throughout the United States: a descriptive study. J Ren Nutr. 2010;20:e1-e8. 16. Hall-McMahon E, Campbell K. Have renal dietitians successfully implemented evidence-based guidelines into practice? A survey of dietitians across Australia and New Zealand. J Ren Nutr. 2012;22:584-591. 17. Zampieron A, Saraiva M, Corso M, Buja A. An international survey on attitudes of renal nurses towards older people. J Ren Care. 2012;38: 213-221. 18. Burrowes J, Russell G, Rocco M. Multiple factors affect renal dietitians’ use of the NKF-K/DOQI adult nutrition guidelines. J Ren Nutr. 2005;15:407-426. 19. Mathewson AM, Fouque D, Toft AJ. Dietary phosphate assessment in dialysis patients. J Ren Nutr. 2010;20:351-358. 20. National Kidney Foundation. K/DOQI clinical practice guidelines for bone metabolism and disease in chronic kidney disease. Am J Kidney Dis. 2003;42:S1-S201. 21. Stuckler D, McKee N, Ebrahim S, Basu S. Manufacturing epidemics: the role of global producers in increased consumption of unhealthy commodities including processed foods, alcohol, and tobacco. PLoS Med. 2012;9:e1001235. 22. Calvo MS, Park YK. Changing phosphorus content of the U.S. diet: potential for adverse effects on bone. J Nutr. 1996;126:1168S-1180S. 23. Murphy-Gutekunst L, Uribarri J. Hidden phosphorus-enhanced meats: part 3. J Ren Nutr. 2005;15:E1-E4. 24. Cupisti A, D’Alessandro C, Baldi D, Barsotti G. Dietary habits and counseling focused on phosphate intake in hemodialysis patients with hyperphosphatemia. J Ren Nutr. 2004;14:220-225. 25. Hager MH, Geiger C, Hill LJ, et al. Usefulness of nutrition facts label for persons with chronic kidney disease. J Ren Nutr. 2009;19:204-210.
Dietary Trends and Management of Hyperphosphatemia Among Patients With Chronic Kidney Disease: An International Survey of Renal Care Professionals Denis Fouque, MD, PhD,* Maria Cruz Casal, RN, DUE,† Elizabeth Lindley, PhD,‡ Susan Rogers, RN, BA,§ Jitka Pancır ova, RN,{ Jennifer Kernc, RD, CSR, LD,** and J. Brian Copley, MD†† Objective: The objective of this study was to review the opinions and experiences of renal care professionals to examine dietary trends among patients with chronic kidney disease (CKD) and problems associated with the clinical management of hyperphosphatemia. Design: This was an online survey comprising open and closed questions requesting information on patient dietary trends and the clinical management of hyperphosphatemia. The study was conducted in 4 European countries (the Netherlands, Spain, Sweden, and the United Kingdom). Subjects: Participants were 84 renal care professionals. Intervention: This was an online survey. Main Outcome Measure: Responder-reported experiences and perceptions of patient dietary trends and hyperphosphatemia management were assessed. Results: Most survey responders (56%) observed an increase in the consumption of processed convenience food, 48% noticed an increase in the consumption of foods rich in phosphorus-containing additives, and 60% believed that there has been a trend of increasing patient awareness of the phosphorus content of food. Patients undergoing hemodialysis (HD) were most likely to experience difficulties in following advice on dietary phosphorus restriction (38% of responders estimated that 25-50% of their patients experienced difficulties, and 29% estimated that 51-75% experienced difficulties). Maintaining protein intake and restricting dietary phosphorus were perceived as being equally important by at least half of responders for predialysis patients (56%) and for those undergoing peritoneal dialysis and HD (54% and 50%, respectively). There were international variations in dietary trends and hyperphosphatemia management. Conclusion: Although most responders have observed a trend of increasing awareness of the phosphorus content of food among patients with CKD, the survey results indicate that many patients continue to experience difficulties when attempting to restrict dietary phosphorus. The survey responses reflect the global trend of increasing consumption of processed convenience foods and phosphorus-containing additives, which has implications for the management of hyperphosphatemia in patients with CKD. Ó 2014 by the National Kidney Foundation, Inc. All rights reserved.
Introduction *
Department of Nephrology, Centre Hospitalier Lyon-Sud, CENS, CARMEN, Universite de Lyon, Lyon, France. † Department of Nephrology, Hospital Universitario 12 de Octubre, Madrid, Spain. ‡ Department of Renal Medicine, Leeds Teaching Hospitals NHS Trust, Leeds, United Kingdom. § Dialysis Department, Codia Waterland B.V., Purmerend, the Netherlands. { European Dialysis and Transplant Nurses Association/European Renal Care Association Secretariat and Conference Department, Prague, Czech Republic. ** Shire LLC, Internal Medicine BU, Wayne, Pennsylvania. †† Shire LLC, Clinical Development and Medical Affairs, Wayne, Pennsylvania. Financial Disclosure: See Acknowledgments on page 115. Address correspondence to Denis Fouque, MD, PhD, Centre Hospitalier Lyon-Sud, Department of Nephrology, Lyon, France. E-mail: denis.fouque@
chu-lyon.fr Ó
2014 by the National Kidney Foundation, Inc. All rights reserved. 1051-2276/$36.00 http://dx.doi.org/10.1053/j.jrn.2013.11.003
110
H
YPERPHOSPHATEMIA, A COMMON disorder in patients with chronic kidney disease (CKD), is strongly associated with cardiovascular morbidity and mortality.1-3 Preventing and correcting hyperphosphatemia is integral to the management of patients with CKD. Achieving recommended levels of protein intake4 while maintaining guideline levels of serum phosphorus5 is associated with the best outcomes in these patients.6 The management of hyperphosphatemia typically consists of a combination of dietary modification, phosphate binder therapy, and dialysis (for patients with stage 5D CKD). Maintaining optimal serum phosphorus levels is often difficult. The Dialysis Outcomes and Practice Patterns Study found that serum phosphorus was maintained below the upper limit of the target range (5.5 mg/dL) in fewer than 50% of patients over a 5-year study period.7 Dietary
Journal of Renal Nutrition, Vol 24, No 2 (March), 2014: pp 110-115
111
DIETARY TRENDS AMONG PATIENTS WITH CKD
counseling is instrumental in achieving the required reduction in phosphorus burden for patients with CKD;8 however, it often poses a significant challenge for renal care professionals.9 One of the problems is that if protein intake is optimized, then there is a concomitant increase in dietary phosphorus that may exceed the recommended daily phosphorus intake in patients undergoing maintenance hemodialysis (HD).10 The implementation of dietary phosphorus restriction can also be complicated by the consumption of processed foods and drinks that are rich in phosphorus-containing additives. These additives can significantly increase the amount of phosphorus consumed in the daily diet.11 Furthermore, the phosphorus contained in additives (inorganic phosphorus) is more readily absorbed than the phosphorus in natural, protein-rich foods (organic phosphorus).12 Therefore, the rising consumption of low-cost convenience food in the global population has resulted in increasing dietary phosphorus burdens13 with implications for the management of hyperphosphatemia in patients with CKD. To explore trends in phosphorus consumption among patients with CKD and to examine the problems associated with the clinical management of hyperphosphatemia, we conducted a survey of renal care professionals in 4 European countries. Although there have been numerous surveys that have examined the attitudes and practices of renal care professionals,14-18 to our knowledge this survey is the first to investigate their experiences relating to dietary trends and restriction of dietary phosphorus intake in patients with CKD before and during dialysis.
Methods The survey was developed as part of a collaboration between the European Dialysis and Transplant Nurses Association/European Renal Care Association (EDTNA/ ERCA) and Shire Development LLC. It was designed to obtain information relating to responder demographics and their perceptions and experiences of patient dietary trends, clinical practices and recommendations, and problems associated with the management of hyperphosphatemia. The survey comprised open, free-text questions and closed, multiple-choice questions. For closed questions, ‘‘not applicable’’ or ‘‘other’’ were given as options if appropriate. The survey consisted of 26 questions in total. In this study, we analyzed the responses to a selection of closed, multiple-choice questions from the survey that related to patient dietary trends, the difficulties associated with dietary phosphorus restriction, and perceptions regarding the relative importance of maintaining protein intake versus dietary phosphorus restriction. Responders were required to state if they had observed, since entering clinical practice, an increase, decrease, or no change at all in patient consumption of fresh food, processed convenience food, and foods rich in phosphoruscontaining additives. In addition, they were asked to report
which trend best applied to patient awareness of the phosphorous content of food. They were also required to estimate the proportion of patients that experienced difficulties in following advice on restricting dietary phosphorus for a range of patient groups. Finally, responders were given the option to rank the importance of different hyperphosphatemia management approaches through selecting one of the following options: maintaining protein intake is more important, limiting dietary phosphorus is more important, or both strategies are equally important. Renal care professionals responsible for providing dietary advice to patients in renal units in the Netherlands, Spain, Sweden, and the United Kingdom were asked to complete the survey. These countries were selected to ensure that renal units in northern and southern Europe were represented in the survey. Invitations to participate in the survey were e-mailed to renal care professionals working in clinics that had been selected to ensure a reasonable geographical distribution within each country. Recruitment in each country was stopped when at least 20 responses had been received. Characteristics of nonresponders were not collected. The survey was completed online in September and October 2012. In each of the 4 countries, national coordinators from the EDTNA/ERCA oversaw the administration of the survey. The national coordinators were responsible for selecting and inviting renal care professionals in their region to participate in the survey. Individuals were invited from renal units that had been selected to ensure a reasonable geographical distribution within each country. With the exception of 1 year’s free membership to the EDTNA/ERCA, no responder incentives were provided for completing the survey. The survey was translated for Spanish responders and validated by a second translator. Translation was not required for responders in Sweden and the Netherlands. All responses from Spain were translated into English before analysis; if any other responses were received in a language other than English, then they were also translated. During the analysis, responders could be identified only by their renal unit. Responses were analyzed for each country separately to examine geographical variations in patterns and trends and were also analyzed after pooling the data from all 4 countries. Descriptive statistics were used to analyze all survey responses.
Results Responder Demographics and Patient Numbers Responses were received from 84 renal care professionals in total, comprising 48 renal dietitians, 35 renal nurses, and 1 renal physician from hospitals and outpatient clinics in the 4 countries (Spain, n 5 20; United Kingdom, n 5 22; Sweden, n 5 20; the Netherlands, n 5 22). These participants reported a total of 1,294 years of renal practice experience, with a mean of 15.4 years per individual (range,
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2-32 years). The proportions of renal nurse and renal dietitian responders varied among countries: In Sweden, 50% of responders were nurses and 50% were dietitians; in the United Kingdom, dietitians made up 100% of the responders; in Spain, 95% were nurses; and in the Netherlands, 73% were dietitians and 27% were nurses. Spain was the only country where a renal physician responded. Combined, the responders’ institutions were responsible for treating approximately 17,000 predialysis patients, more than 12,500 individuals undergoing HD, and nearly 3,000 undergoing peritoneal dialysis.
Dietary Trends The survey revealed several trends in dietary habits. Since entering clinical practice, 29 responders (35%) had noticed a decrease in the consumption of food prepared from fresh ingredients, 47 (56%) had noticed an increase in the consumption of processed convenience food (‘‘fast food’’), and 40 (48%) had noticed an increase in the consumption of foods rich in phosphorus-containing additives. Fifty responders (60%) believed that since entering clinical practice there has been a trend for patients with CKD to have a greater awareness of the phosphorus content of food. Dietary trends were found to vary among the 4 countries (Fig. 1). Most responders in the United Kingdom (59%, n 5 13) reported a decrease in the consumption of foods
prepared with fresh ingredients, whereas responders from the Netherlands, Spain, and Sweden predominantly reported no change. Most responders in the United Kingdom and Spain reported an increase in the consumption of fast food (77%, n 5 17; 65%, n 5 13, respectively); this was also the most common response in Sweden (50%, n 5 10). In the Netherlands, the most frequent observation (41%, n 5 9) was a decrease in fast food consumption. Most responders in the United Kingdom and Spain (59% and 55%, respectively) found that consumption of food containing phosphorus-based additives had increased; 40% of responders in Sweden also reported this trend. In the Netherlands, no change in the consumption of phosphatebased additives was most frequently reported (41%). Increasing patient awareness of the phosphorus content of food was the most common observation in Spain, Sweden, and the Netherlands (50%, 75%, and 77%, respectively), whereas most responders in the United Kingdom (59%) found that there had been no change in this respect.
Management of Hyperphosphatemia Patients undergoing HD were reported as being the most likely to experience difficulties in following advice on restricting daily phosphorus intake; 32 responders (38%) reported that 25% to 50% of their patients undergoing HD experienced difficulties, and 24 responders (29%) estimated this figure to be between 51% and 75% (Fig. 2). Predialysis Decrease No change Increase Consumption of fast food
Consumption of food made from fresh ingredients 100 Proportion of patients (%)
Proportion of patients (%)
100 80 60 40 20 0
80 60 40 20 0
Netherlands
Spain
Sweden
UK
Netherlands
Consumption of food containing phosphorus-based additives
Sweden
UK
Patient awareness of the phosphorus content of food 100 Proportion of patients (%)
100 Proportion of patients (%)
Spain
80 60 40 20 0
80 60 40 20 0
Netherlands
Spain
Sweden
UK
Netherlands
Spain
Sweden
UK
Figure 1. Dietary trends observed by renal care professionals in 4 European countries since entering clinical practice. Netherlands (n 5 22); Spain (n 5 20); Sweden (n 5 20); UK (n 5 22).
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DIETARY TRENDS AMONG PATIENTS WITH CKD
Figure 2. Proportions of predialysis, peritoneal dialysis, and hemodialysis patients who renal care professionals believe experience difficulties restricting dietary phosphorus intake (n 5 84). N/A, not applicable.
patients were the least likely to experience difficulties restricting dietary phosphorus intake; 39 responders (46%) reported that fewer than 25% of their predialysis patients experienced difficulties, and only a small percentage (4%; n 5 3) estimated this figure to be 51% to 75% (Fig. 2). Compared with predialysis patients, a larger percentage of patients undergoing peritoneal dialysis were thought to find it difficult to restrict dietary phosphorus; 14 responders (17%) estimated that 51% and 75% of their patients undergoing peritoneal dialysis experienced difficulties (Fig. 2). There were differences in the percentages of patients believed to experience difficulties restricting dietary phosphorus among the 4 countries. In Spain, the most commonly reported percentage of predialysis patients who experienced difficulty was 25% to 50% (estimated by 50% of responders), compared with fewer than 25% of predialysis patients in the Netherlands, the United Kingdom, and Sweden (estimated by 50%, 64%, and 50% of responders, respectively). Most Spanish responders (60%) reported that 51% to 75% of their patients undergoing HD experienced difficulties restricting dietary phosphorus, which was higher than the figures in Sweden, the Netherlands, and the United Kingdom (30%, 18%, and 9%, respectively). The most frequently reported percentage of patients undergoing HD who experienced difficulties in the Netherlands and the United Kingdom was 25% to 50% (41% and 68% of responders, respectively). In the United Kingdom and Spain, 50% and 45% of responders, respectively, estimated that 25% to 50% of individuals undergoing peritoneal dialysis experienced difficulties restricting dietary phosphorus. In the Netherlands and the United Kingdom, the most commonly reported percentage of patients undergoing peritoneal dialysis to experience difficulties was less than 25% (41% and 40% of responders, respectively). Overall, 37 responders (44%) believed that younger patients (18-45 years) are more likely to find it difficult to restrict dietary phosphorus intake than any other age group. When asked if other groups of patients experienced diffi-
culties, individuals with low incomes, obese patients, malnourished individuals, and those with diabetes mellitus were the most commonly reported (64%, 58%, 54%, and 40% of responders, respectively). In comparison, only 12% of responders thought that patients suitable for transplant experienced difficulties restricting dietary phosphorus. In total, 42 responders (50%) perceived restricting dietary phosphorus and maintaining protein intake in patients undergoing HD as being equally important whereas 30 (36%) favored maintaining protein intake over restricting phosphorus (Fig. 3). There were similar findings for nutrition management in predialysis patients and in those undergoing peritoneal dialysis (Fig. 3). Most responders in all 4 countries rated restricting dietary phosphorus and maintaining protein intake as being equally important in the management of hyperphosphatemia in predialysis patients and in those undergoing peritoneal dialysis. However, for individuals undergoing HD, the most frequent response in Spain (45%) was to rate restricting dietary phosphorus as being more important than maintaining protein intake, whereas in Sweden, maintaining protein intake was rated as being more important than restricting dietary phosphorus by most responders (60%). In the United Kingdom, the most frequent response (82%) was that both approaches were perceived as being equally important. In the Netherlands, 45% of responders stated that both approaches
Maintaining protein intake is more important Limiting dietary phosphorus is more important Both strategies are equally important Predialysis
30% 56% 14%
Peritoneal dialysis
37% 54% 9%
Hemodialysis
36% 50% 14%
Figure 3. Relative importance of phosphorus restriction and adequate protein intake in predialysis patients and in those undergoing hemodialysis and peritoneal dialysis from the perspective of renal care professionals (n 5 84).
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were equally important and 45% reported that maintaining protein intake was more important. These responses were also analyzed according to the renal practice experience of the responders (0-9 years, n 5 19; 10-19 years, n 5 35; 20-29 years, n 5 23; and $30 years, n 5 6). Most responders in each practice experience group reported that both approaches were equally important (0-9 years 5 58% of responders, 10-19 years 5 54%, 20-29 years 5 52%, and $30 years 5 67%). Fewer responders in the most experienced renal practice groups regarded limiting dietary phosphorus intake as the most important approach compared with those with less practice experience (0-9 years 5 21% of responders, 10-19 5 17%, 20-29 5 9%, and $30 5 0%).
Discussion Hyperphosphatemia is a serious clinical consequence of renal failure that requires concerted management in patients with CKD. Assisting and encouraging individuals undergoing dialysis to maintain their serum phosphorus levels within guideline parameters5 is a considerable challenge for renal care professionals.9 Assessing the nutritional intake of individuals undergoing dialysis is a necessary part of the clinical approach to controlling serum phosphorus levels and improving patient outcomes.19 To our knowledge, this is the first survey to examine renal nurses’ and dietitians’ perceptions and experiences relating to dietary trends and the problems associated with the management of hyperphosphatemia in patients with CKD. In terms of dietary emphasis, the results of this survey indicate that most providers of dietary advice to patients with CKD perceive the maintenance of adequate protein intake to be equally or more important than dietary phosphorus restriction in the management of hyperphosphatemia in patients with CKD. The number of years of experience in renal care did not produce major variation in these responses. Given the importance of protein intake in these patients, and the fact that foods with a high protein content are major sources of organic phosphorus, a suitable dietary phosphorus metric for patients may be the ratio of phosphorus (milligrams) to protein (grams) for a given food item.12,20 Despite an increased awareness of the phosphorus content of food, the survey results indicate that many patients continue to experience problems restricting dietary phosphorus. The global trend of increasing consumption of processed foods,21 in which phosphorus-containing additives may be used to extend shelf life, to improve color or flavor, or to increase water retention, is reflected in the responses of the renal care professionals surveyed in this study. These food additives can account for more than 30% of dietary phosphorus intake.22 This type of dietary phosphorus burden has important implications for the management of hyperphosphatemia because the phosphorus is almost completely absorbed,12 undermining the effects of phosphate binding therapy8 and resulting in the need for
increased doses of phosphate binders to achieve the same effect on phosphorus balance. According to a review in 2010,13 an additional 1,000 mg of inorganic phosphate can be absorbed daily from processed food and drinks, which renders patients’ dietary efforts almost useless. Therefore, to achieve adequate protein intake while restricting dietary phosphorus, foods with low phosphorusto-protein ratios13,20 and minimal phosphorus-containing additives should be recommended to patients, together with appropriate regimens of phosphate binders when necessary. Although the European Community regulations require manufacturers to report the presence of phosphorus on the food label, disclosure of the amount is not required.8 In addition, there is no accurate method to distinguish between protein-based phosphorus and preservative-based phosphorus in food.23,24 Consequently, phosphorus from food additives may be unrecognized, which may create difficulties for patients undergoing dialysis who are attempting to restrict their phosphorus intake. Results of a survey among individuals with CKD revealed that they would find it useful to see nutrients of concern, particularly phosphorus, listed as absolute amounts on the Nutrition Facts label of food and drink products.25 Results from the present survey revealed international variations in patient dietary trends and renal care professionals’ experiences and perceptions of the management of hyperphosphatemia. Awareness of these differences may be useful for the development of guidance and educational materials for the management of hyperphosphatemia across this region. However, it is important to note that the proportions of renal nurses and dietitians who responded to the survey varied among countries. This may be considered to be a limitation of the study because the patient care roles and clinical duties of renal nurses and dietitians can differ. Therefore, the potential differences in the experiences and practices in each profession may have caused some variation in the responses across the 4 countries. However, in Spain, renal nurses have a dual role, performing the same duties as renal dietitians, and can therefore be considered to be representative of both professions. Furthermore, the inclusion of responders from both professions may be considered to be beneficial because it generates a wider representation of opinions and experiences. Another limitation of the study is that we did not examine potential cultural differences among the countries. Patients’ dietary phosphorus burdens can be influenced by factors such as common food preparation practices and food staples,8 which may vary among countries. It would be useful to include these factors in future surveys of this nature. In addition, repeating the survey in countries outside of Europe would enable examination of wider international trends, and repeating the survey in the same countries in the future would be useful for determining changes in the trends observed in the study presented here. It would also
DIETARY TRENDS AMONG PATIENTS WITH CKD
be interesting to conduct a survey of a similar nature to determine patients’ personal perceptions of dietary trends and the problems associated with the management of hyperphosphatemia. A further limitation is that the results from the survey cannot be analyzed statistically because of the small sample size (particularly in the responder subgroups). However, descriptive statistical analysis alone has revealed some interesting trends. One final limitation was that the survey was not validated; however, it was designed and developed by a team of renal care professionals and the executive committee of the EDTNA/ERCA. In conclusion, the results of this study indicate that there is increasing consumption of processed foods and that patients with CKD continue to experience difficulties when attempting to restrict dietary phosphorus. A key problem appears to be the extensive use of phosphorus-containing additives in food, alongside the lack of clear labeling of phosphorus content.
Practical Application The renal community must lobby for accurate labeling of food and drink to show the amount of phosphoruscontaining additives and, ideally, the phosphorus content per portion. This would enable patients to avoid or limit their intake of unnecessary phosphorus from additives and help them to maintain adequate protein intake within the limits set by dialysis and an acceptable phosphate binder regimen. In response to the widespread consumption of phosphorus-containing additives in modern diets, food regulation agencies need to re-evaluate the regulation of these additives in the food and drink industry.
Acknowledgments The survey was funded by Shire Development LLC. J.K. and J.B.C. are employees of Shire LLC. D.F. has received honoraria or lecture fees from Abbott, Amgen, Genzyme, and Shire LLC. The other authors have no conflicts of interest to declare. The authors thank Vivienne Johnson of PharmaGenesisÔ London for manuscript writing support, which was funded by Shire, LLC.
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