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Contents lists available at ScienceDirect

Patient Education and Counseling

journal homepage: www.elsevier.com/locate/pateducou

Patient education

Effect of behavioral stage-based nutrition education on management of

osteodystrophy among hemodialysis patients, Lebanon
Mirey Karavetiana,* , Nanne de Vriesa , Hafez Elzeinb , Rana Rizka , Fida Bechwatyc
a

Maastricht University, Maastricht, 6200 MD Maastricht, The Netherlands

Lebanese National Kidney Registry, Beirut, Lebanon
c
Universit Saint Joseph, Beirut, Lebanon
b

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 12 September 2014
Received in revised form 20 February 2015
Accepted 12 May 2015

Objective: Assess the effect of intensive nutrition education by trained dedicated dietitians on
osteodystrophy management among hemodialysis patients.
Methods: Randomized controlled trial in 12 hospital-based hemodialysis units equally distributed over
clusters 1 and 2. Cluster 1 patients were either assigned to usual care (n = 96) or to individualized
intensive staged-based nutrition education by a dedicated renal dietitian (n = 88). Cluster 2 patients
(n = 210) received nutrition education from general hospital dietitians, educating their patients at their
spare time from hospital duties. Main outcomes were: (1) dietary knowledge(%), (2) behavioral change,
(3) serum phosphorus (mmol/L), each measured at T0 (baseline), T1 (post 6 month intervention) and T2
(post 6 month follow up).
Results: Signicant improvement was found only among patients receiving intensive education from a
dedicated dietitian at T1; the change regressed at T2 without statistical signicance: knowledge (T0:
40.3; T1: 64; T2: 63) and serum phosphorus (T0: 1.79; T1: 1.65; T2: 1.70); behavioral stages changed
signicantly throughout the study (T0: Preparation, T1: Action, T2: Preparation).
Conclusion: The intensive protocol showed to be the most effective.
Practice implications: Integrating dedicated dietitians and stage-based education in hemodialysis units
may improve the nutritional management of patients in Lebanon and countries with similar health care
systems.
2015 Elsevier Ireland Ltd. All rights reserved.

Keywords:
Behavioral change
Hemodialysis
Osteodystrophy
Nutrition education

1. Introduction
Lack of adherence to dietary restrictions among hemodialysis
(HD) patients is common [1]; and globally, the prevalence of HD
patients is on the rise [2]. These patients often suffer from elevated
serum phosphorus (P); a leading cause of chronic kidney disease
mineral bone disorder (CKDMBD) and mortality [3]. The
management of this condition includes HD, dietary P restriction
to 8001000 mg/day, P density (P/protein) limited to 1012 mg/g/
day and P-binders [4,5]. Consequently, adherence to P-restricted
diet is the most difcult for HD patients [6].
Strong evidence support the use of behavioral change models to
facilitate dietary lifestyle changes [7]. The transtheoretical model
(TTM) or the stages of behavioral change model (referred to, in this

* Corresponding author. Present address: Zayed University, P.O. Box 19282 Dubai,
UAE. Tel.: +971562446865; fax: +31 97124434847.
E-mail addresses: mirey.karavetian@zu.ac.ae (M. Karavetian),
n.devries@maastrichtuniversity.nl (N. de Vries), hafezein@aol.com (H. Elzein),
r.rizk@maastrichtuniversity.edu (R. Rizk), da_b88@hotmail.com (F. Bechwaty).

article, as TTM stage) assesses the readiness to change in behavior

among individuals. Behavioral change is a dynamic process
whereby people move from one stage to another over time.
TTM includes 5 stages: (1) pre-contemplation, (2) contemplation,
(3) preparation, (4) action and (5) maintenance. To stimulate
transitions, an appropriate stage-based intervention needs to be
planned [8]. Recent literature illustrates the effectiveness of stagematched nutrition education (NE) [9,10], demonstrating its
superiority over non-stage-matched ones [11].
A recent review [12] on effective dietary counseling interventions for hyperphosphatemia management in HD patients
identied the following key tools to enhance behavioral change:
(1) multidisciplinary approach coupled with a decisional partnership with the patient, (2) behavioral theory-based individualized
education with frequent reinforcement, (3) easy-to-comprehend
educational material targeting simple skills using booklets, live
demonstrations, posters and recipes adapted to cultural preferences.
In Lebanon, HD units are exclusively hospital-based and
hospital dietitians are responsible for NE among other duties.

http://dx.doi.org/10.1016/j.pec.2015.05.005
0738-3991/ 2015 Elsevier Ireland Ltd. All rights reserved.

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

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Moreover, these dietitians are overloaded and do not have the

optimal competencies needed to manage HD patients [13].
The current study primarily aimed to assess the effect of trained
dedicated dietitians on HD patient clinical outcomes compared
with partially dedicated dietitians with or without specialized
training on hyperphosphatemia management. The secondary aim
was to study the effectiveness of an intensive, individualized,
stage-based psycho-educational nutrition intervention focused on
P compared with the non-stage-based model used in routine care.
2. Methods
2.1. Design
The protocol, data collection instruments, hospital and patient
selection criteria, randomization method and group baseline
characteristics have been published elsewhere [14]. For the scope
of this article, we will summarize the methodology and provide
additional details on the development of patient and dietitian
education materials and on data analysis addressing the aim of this
study.
In brief, the nutrition education for management of osteodystrophy (NEMO) is a randomized controlled trial in 12 hospitalbased HD units, equally and randomly allocated to clusters 1 and 2.
Half of the patients in cluster 1 were randomly chosen according to
their dialysis shift and assigned to the intensive protocol (dietitian
dedicatedDD), and the other half served as control (existing
practiceEP). All patients in HD units recruited to cluster 2 were
assigned to the partial intervention protocol (trained hospital
dietitianTHD). Sample size was calculated based on a previous
publication [15] to detect signicant changes in the primary
outcome (serum P). Accordingly, a minimum sample of 50
participants was identied for each study group. We doubled this
number for the THD group to account for the expected drop in the
effect size. Moreover, the sample size for all groups was multiplied
by 3 to account for the 3 different sizes of the HD units [14] and 20%
were added to compensate for refusals, loss to follow up, and dropouts. DD patients received individualized twice weekly stagedbased NE for 6 months by trained study dietitians. As for the EP
group, hospital dietitians who were blinded to study, provided
usual care. THD patients received NE by the trained hospital
dietitian, whenever the latter had spare time from their overloaded
schedule of other hospital duties. DD and THD dietitians were
trained by the studys principal investigator (PI) on renal dietetics.
The trial was conducted according to the guidelines of the
Declaration of Helsinki and all procedures involving human
subjects were approved by the institutional review board of each
participating institution. Patients were provided with consent
forms that explained the study procedure and timelines, pros and
cons and permission to review patients les. Only consenting
patients were included to the study. Condentiality and anonymity
of participants were maintained by the use of coding.

2.2. Patient education material and protocol

Semi-structured qualitative interviews were conducted with a
focus group of 15HD patients and 3 dietitians working with renal
patients in Lebanon. Our aim was to explore their perspectives on
facilitators and barriers toward optimal adherence to P-restricted
diet. Patients and dietitians answers are detailed in Tables 1 and 2,
respectively. According to the focus group results and the
principles of the TTM stages, patient educational material was
developed. Moreover, the structure of the lessons was adapted
from Fickenor and Byrd-Bredbenner [16], after the approval of the
main author; although the latter addressed a different topic in
chronically ill population. For practicality and following Fickenor
and Byrd-Bredbenner [16], the 5 TTM stages were grouped in 3
categories and accordingly, the educational material was prepared:
(1) pre-action (pre-contemplation, contemplation, and preparation), (2) action and (3) maintenance. In each stage, several topics
were discussed and repeated among stages (Table 3).
At the end of the study, all participants received a folder that
included the used material. The educational materials were
printed in low literacy level, in bold and in illustrative photos.
The Arabic language was used for all printed material. Fifth grade
level sentences were employed to facilitate comprehension as
recommended by Aldridge [17]. Along with the lessons, 4 other
educational tools were used: (1) a renal recipe book tailored to the
Lebanese cuisine, (2) an illustrated booklet of low P food options,
(3) a poster of low P foods hung in the units waiting room and (4)
an in-center patient adherence contest to serum P. Evidence
support the effectiveness of these types of the educational tools in
improving patient dietary adherence [18].
Throughout the intervention, these educational materials were
integrated in an individualized education protocol by the research
dietitians, only to the patients of the DD group.
All patients were assessed for TTM stage at baseline, but
irrelevant of their stage, they were rst educated with the preaction material. This was done for the fact that there are no full
time dietitians in Lebanese HD units, leading us to believe that
none of the patients had received a formal and complete dietary
counseling. After which educational material was provided
according to the readiness change of the patient. NE was given
twice per week for 15 min during 6 months, amounting to a total of
12 h of education per patient. The intervention duration was in
accordance with the 2-h per month of dietitian-to-renal patient
time recommendation by the Academy of Nutrition and Dietetics
(ADA-EAL) [19] and the minimum duration needed for behavioral
change to take place (6 months) as suggested by Sneed and Paul
[20]. During the 1st weekly session, the theme of the week was
explained. In the 2nd weekly session, the patient was asked to
recall the lesson of the previous session, to guarantee comprehension; whether the patient did or did not recall, the lesson was
explained again, but this time with individualized feedback.
Finally, at the beginning of each month, new monthly blood tests

Table 1
Patient focus group results (n = 15).
% of patient

Opinion

100
100
90
50
40
20
13
13
7

The need for more self-management skills and alternatives to forbidden foods, to have more freedom in choosing food items on a daily basis
Eating in group (with family or friends) makes it more difcult to comply with the restricted diet, when the others are eating forbidden foods
If the dietitian visited the HD unit daily, for sure I would comply more
Advice from health care professionals is not very realistic
Family bring forbidden foods to home, and make it available at all times. This makes it difcult to adhere to a restricted diet
Inability to buy or prepare foods for the uremic diet
Adherence becomes easier when symptoms appear
Bored of restrictions, want to live like everyone
Depression leading to indifference. No matter what I do, I will still be on HD, so why to comply?

HD, hemodialysis.

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

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Table 2
Dietitian focus group results (n = 3).
% of dietitians

Opinion

100

Insufcient time for the HD patients due to the overload by other duties in the hospital. Need for a full time dietitian in the HD unit.
Nurses and doctors should be educated about the diet
Able to visit the HD unit for a maximum of once a month
Need to simplify the diet by innovative techniques to help patients understand the important effect of diet on their clinical outcomes
Should involve family members in the dietary education
The dietitian should be the only health care professional responsible for the NE of HD patients
Need for more awareness in the community and among fellow health care professionals on the importance of diet and clinical outcomes among HD
patients
Difculty of cooking allowed food
Since depression is related to incompliance, depression needs to be tackled in the HD unit with a multidisciplinary team approach
Older age is a major barrier to dietary adherence
Need for food industry to develop renal food items available in supermarkets and restaurants (low K, low P, . . . )

100
100
66
66
66
66
66
66
33

HD, hemodialysis; NE, nutrition education; K, potassium; P, phosphorus.

related to the CKDMBD were evaluated and discussed with each

patient and an action plan was designed with the patient to achieve
better results.
As for the THD and EP groups, the study educational material
was provided at the end of the study.

from the analysis of 24-h recalls collected on 3 non-consecutive

days. The 24-h recall was analyzed through the renal exchange
systems and the USDA (version 25) [23] nutrient database for
daily P (mg) and protein (g) and P density of food calculated
through P (mg)/protein (g) ratio. Edible portion of the food was
analyzed, weather it was for cooked or raw items.

2.3. Dietitian oriented educational program

The dietitian education program covered all standards of renal
dietetics as per the KDOQI nutritional guidelines for HD patients
[5] in addition to behavioral counseling methods with a focus on
the TTM stages. It was provided to DD and THD dietitians. The
training included other topics and not only hyperphosphatemia
management, to assure that dietitians would be able to conduct a
holistic dietetic assessment and education of these patients. The
training was provided through 8 sessions (4 h each), and included
lectures, case studies and discussions with the PI. Moreover,
research dietitians took a post course knowledge test to assure the
adequacy of their information before the start of the study.
2.4. Instruments and measures
For all groups, all data were collected at 3 time points: T0
(baseline), T1 (post 6 month) and T2 (post 6 month follow up). This
was conducted by trained research dietitians under the supervision of the PI to minimize inter collector variability. Instruments
included:
a Knowledge questionnaire adapted from Ford et al. [21] and
included 18 questions about kidney disease, renal diet, Pbinders, vitamin D therapy and the perception of the importance
of diet in the treatment. All questions were closed-ended with
multiple answer choices. A correct and wrong answer were
scored as 1 and 0 respectively, leading to a total score ranging
from 0 to 18. The total score of each patient was then converted
into a percentage, where a cut-off score of 60% indicated
acceptable knowledge.
b Mean serum P of the 6 months prior to each study phase was
collected and the mean value represented each study phase.
c Stage of behavioral change in P-restricted diet was evaluated
among all patients; accordingly, they were assigned to their TTM
stage in P-restricted diet. Patients of the DD group were assessed
additionally on their TTM staging on the 1st day of each week all
throughout the 6-month intervention. The TTM stages were
evaluated using an algorithm (Fig. 1) inspired by Welch [22] who
assessed HD patients on TTM stages in uid-restricted diet. For
the current study, the dietary component was changed to
dietary and serum P. The constructed algorithm assigned each
patient to one of the TTM stages. Dietary intake was calculated

2.5. Data analysis

Collected data were entered into the statistical package for
social sciences (SPSS) version 16, IBM. Within group differences
were studied using general linear model (GLM). Repeated test
ANOVA with a GreenhouseGeisser correction was used for
repeated parametric measurement over the 3 study time points;
if signicant, analysis was followed by a post hoc test using the
Bonferroni correction to study the differences in means for all
possible pairs (T0 &T1, T0 & T2, T1 & T2) within the treatment
condition. A 0.05 signicance level was utilized.
Within group differences for the repeated non-parametric
measurements were explored through Friedman test. It was used
to detect statistical difference between the 3 time points
measurements (T0, T1, T2) within the same treatment condition;
If signicant, analysis was followed by a post hoc test (Wilcoxon
Signed Rank test, conducted with a Bonferroni coorection applied)
to study the differences in average ranks for all possible pairs (T0 &
T1, T0 & T1, T1 & T2) within the treatment condition. Corrected
signicance level was set at p  0.017 (0.05/ number of tests that
were run).
3. Results
Five hundred seventy patients were included to the study and
were randomly assigned to the study groups, as follows: DD
(n = 133), EP (n = 138) and THD (n = 299). Among these, 394
completed the study and provided sufcient data for analysis:
DD (n = 88), EP (n = 96), THD (n = 210). Attrition data are shown in
Fig. 2.
Baseline data are shown in detail in Karavetian et al. [14]; there
were no signicant baseline differences between any of the study
parameters.
Knowledge of patients in the DD group signicantly improved
to acceptable level at T1, and was maintained at T2. On the
contrary, the knowledge level dropped signicantly in the EP at T1,
and was elevated signicantly at T2 but did not reach acceptable
levels. As for patients in the THD group, knowledge scores had
signicantly improved at T2, but did not reach satisfactory levels
(Table 4).

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

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Table 3
Lesson plan according the TTM stages.
Stage

Pre-action

Action

Maintenance

Concepts

Raise
awareness
Identify
benets of
change
Encourage
support
networks
Provide
personalized
information
Resolve
ambivalence

Set action plan

Provide relapse
management
Identify skills to
implement the
new plan
Solve difculties
to adherence

Identify small
steps taken
before and
praise patient
for them

Lessons

(equivalent
topics in
each phase
are in the
same row)
Benets of life
changes on
health

Set short-term goals

Identify support needed

Solve barriers to adherence Identify local

resources and
support
Create consequences for
Empower with
failure to implement
self control
strength that is
not exhausted by
other problems
Encourage
Continue development
and rening skills needed continued
commitment as
to implement the plan
the path to
creating the new
behavioral norm
Small lifestyle changes to a Where is P found
better quality of life
in food

Holistic

4. Discussion and conclusion

4.1. Discussion

High P diet and How to live on a low P diet The harm on

health
health of high P
problems
diet, and benets
of the P
restricted diet
High P diet and Booklets on P rich foods
bone disease
and their low P
alternativesa
High P diet and Poster of foods rich in P
heart disease
and their P restricted
alternativesa
Normal ranges
of Ca, P, PTH

The progression of patients from one TTM stage to another in

the different study groups and phases are reported in Table 6.
Around 90% of the patients in the DD group who started at preaction stages of TTM advanced to post-action stages at T1, yet this
change was seen only in about 15% to 40% of the patients in the
other groups. At T2, almost all patients in all groups were back to
pre-action stage. A similar movement was achieved for the ones
that started the study at action in all groups. As for the ones who
started at maintenance stage, around 50% remained at maintenance at T1 in DD group yet a signicant regression of TTM stages
was seen in the other 2 groups.
Serum P signicantly dropped post-intervention (Table 7) only
in the DD group. There was a signicant elevation at T2, but the
value remained within the KDOQI optimal level. No signicant
improvement was seen in the other 2 groups.
P density in patients dietary intake (P/Protein ratio)
approached normal levels at T1 in the DD group, but the change
was not signicant. At T2, DD group had a signicantly elevated
ratio. There was no signicant change in the EP and THD groups;
the score remained unchanged at T1 yet signicantly increased at
T2 (Table 8).

P binders administration
methods

Importance and
benets of P
binders

Role of P
binders on
dietary P
Role of exercise Safety of exercise when on Importance of
on P clearance dialysis. How to do it?
the physical
in HD
activity on the
health of HD
patients
Role of vitamin Active vitamin D therapy
Importance of
D on bone
and serum P
Vitamin D on the
health
health of HD
patients
P restricted Lebanese
management
of
standardized recipes:
osteodystrophy breakfast + lunch + dinner;
7 menus of each

TTM, transtheoretical model; P, phosphorus; Ca, calcium; PTH, parathyroid

hormone; HD, hemodialysis.
a
Educational materials adapted from Karavetian et al. [13] (validated on adult HD
patients in Lebanon using local language (Arabic)).

Stages of behavioral change at post intervention in the DD

group (Table 5) progressed from Preparation to Action stage and
dropped back to Preparation at T2. No signicant change was noted
in the EP group. As for the THD group, there was no improvement
at T1, moreover the median dropped even lower (Contemplation)
at T2.

The education protocol assigned to the DD group was the most

effective in improving all study parameters. The main difference
between the DD protocol and the others was the intensive
individualized nutrition counseling for 6 months, tailored to the
readiness stage of each patient and provided by a renal dietitian
fully dedicated to the HD unit. The components of the DD protocol
were in line with the effective NE strategies highlighted in previous
reviews among HD patients [12].
Knowledge scores in the DD group improved post intervention
and did not drop at follow up, showing the effectiveness of
intensive education; this rhymes with published literature on NE
interventions [15,21,24]. Knowledge scores of the EP group
signicantly improved at follow up but did not reach acceptable
levels; this might be explained by the contamination of information through patients and nurses. As head nurses explained
afterwards; when the 6 month intervention ended, HD unit nurses,
who were blinded to the study, assumed that the study was over
and transferred the study educational material from the DD to the
EP group. This suggests that EP patients were receptive for new
dietary education but also highlights the crucial and unreplaceable
role of the dietitian in effectively improving patient nutrition
knowledge. As for the knowledge scores in the THD group,
improvement was seen only at follow up. A plausible explanation is
that the dietitians in this group, after receiving training from the PI,
upgraded their NE methods and increased the frequency of dietetic
consultations to HD patients; but the intensity of the education
stayed lower than that of the DD and thus achieved improvement
in a longer period of time. This explanation is supported by our
data (unpublished yet) which show that THD dietitians visited the
patients at best once monthly; this was an expected outcome
bearing in mind the schedule overload these dietitians had.
The individualized stage based nutrition education in the DD
group achieved better patient adherence and progression to the
action stage at post intervention. This was not seen in EP and THD
patients. Moreover, the lack of dietitian in the follow up phase in
the DD group, affected negatively on most outcomes. The results
highlight the detrimental effect of lack of continuous dietetic
monitoring. Long term dietary lifestyle change is difcult to
maintain; it often leads to depression [25] and relapse to the old
behavior. Patients constantly need to be reminded of the benets

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

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M. Karavetian et al. / Patient Education and Counseling xxx (2015) xxxxxx

Fig. 1. TTM staging algorithm.

HD, hemodialysis. P, phosphorus.
*Since serum P does not respond immediately to dietary change, it is expected that a patient following P restricted diet for 6 months should have a normalized serum P within
the past 3 months.

Fig. 2. Attrition rate throughout the study.

of the new behavior in order to maintain it. Literature emphasizes

on the importance of close patient follow up and effective behavior
change [1,12].
Behavior-based dietary education is strongly recommended for
increasing patient adherence to therapy [7]. Matteson and Russell
Table 4
Effect of NEMO trial on knowledge (n = 394).

T0
T1
T2
P

DD group (n = 88)

EP group (n = 96)

THD group (n = 210)

40.31a  13.00
63.97b  9.14
62.94ab  16.89
<0.001

38.73a  11.94
30.11b  20.79
51.22c  21.04
<0.001

39.43a  12.91
39.95a  19.15
55.26b  20.79
<0.001

Values are shown in mean  SD; P value in the table indicates signicance over time
as per GLM-repeated measure ANOVA with a GreenhouseGeisser correction;
different superscripts indicate statistical differences within columns between each
pair using post hoc Bonferroni correction with P < 0.05.
NEMO, nutrition education for management of osteodystrophy; DD, dedicated
dietitian; EP, existing practice; THD, trained hospital dietitian.

[1] went the extra mile and suggested integrating behavioral

theories in patient education in HD units. The signicant
improvement in serum P seen only in the DD group veried the
strong effect of nutritional psycho-education on patient adherence.
This improvement could also have been the result of better
adherence to P-binders We could not assess this, since dietitians in
Lebanon are not allowed to prescribe P-binders; it is solely
managed by the physician.
The drop of serum P in the DD group was not coupled with a low
protein intake; which usually is a common yet undesirable
consequence. Dietary P density was almost maintained within
the normal levels in the DD group throughout the study, despite
the ongoing dietary P restriction. We relate this protective effect to
the educational material used; it largely focused on P/protein
balance and helped patients identify low P food items with good
protein content. Other studies also noted that teaching patients
safe alternatives of restricted food items is a facilitator to dietary
adherence [24,26]. Moreover, the educational toolkit provided

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

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Table 5
Effect of NEMO trial on TTM stages* on diet restricted in P (n = 394).
DD group (n = 88)

To
T1
T2
P

EP group (n = 96)

THD group (n = 210)

25th

50th

75th

Mean rank

25th

50th

75th

Mean rank

25th

50th

75th

Mean rank

2
3
2
0.001

3
4
3

4
5
3

1.95a
2.47b
1.59a

1
2
2
0.467

2
3
3

4
4
3

2.08a
2.01a
1.92a

1
1
1
<0.001

1
1
1

2
2
1

2.19a
2.09a
1.73b

NEMO, nutrition education for management of osteodystrophy; TTM, transtheoretical model; DD, dedicated dietitian; EP, existing practice; THD, trained hospital dietitian.
*
TTM Stages are shown in their numbers; values are shown in quartiles, where 50th percentile indicated the median; P value in the table indicates Friedman test group
statistics; ranks with different superscripts are statistically different from each other as post hoc Wilcoxon Signed Rank test with a Bonferroni correction applied. Corrected
signicance level set at P  0.017.

Table 6
Effect of NEMO trial on transition of patients from One TTM stage to another (n = 394).
DD group (n = 88)

Pre action

T0

T1

T2

T0

T1

T2

T0

T1

T2

5
(9%)
23
(41%)
28
(50%)

37
(66%)

57
(100%)

48
(84%)
7
(12%)
2
(4%)

49
(86%)

124
(100%)

71
(57%)
33
(27%)
20
(16%)

105
(85%)
2
(2%)
9
(7%)

3
(12%)
19
(73%)
4
(15%)

24
(92%)

24
(77%)

30
(97%)

2
(8 %)

7
(23%)

1
(3%)

31
(62%)
13
(26%)
6
(12%)

37
(74%)
5
(10%)
5
(10%)

3
(23%)
4
(31%)
6
(46%)

12
(92%)

9
(69%)
3
(23%)

11 (85%)

32
(62%)
9
(17%)
13
(25%)

43
(83%)
1
(2%)
7
(14%)

Maintenance

Pre action
26
(100%)

Maintenance

Pre action
Action
Maintenance

THD group (n = 210)

56
(100%)

Action

Action

EP group (n = 96)

13
(100%)

5
(9%)

31
(100%)

1
(8%)

13 (100%)

50
(100%)

54 (100%)

All percentages are rounded up; at T2, numbers do not add up to 100% due to drop out rates by the end of the study.
NEMO, nutrition education for management of osteodystrophy; TTM, transtheoretical model; DD, dedicated dietitian; EP, existing practice; THD, trained hospital dietitian.

Table 7
Effect of NEMO trial on serum P (n = 394).

T0
T1
T2
P

DD group (n = 88)

EP group (n = 96)

THD group (n = 210)

1.79  0.50 mmol/La

1.65  0.46 mmol/Lb
1.70  0.53 mmol/Lab
0.012

1.72  0.47 mmol/La

1.71  0.50 mmol/La
1.82  0.65 mmol/La
0.087

1.67  0.48 mmol/La

1.63  0.48 mmol/La
1.65  0.48 mmol/La
0.176

Values are shown in mean  SD; P value in the table indicates signicance over time
as per GLM-repeated measure ANOVA with a GreenhouseGeisser correction;
different superscripts indicate statistical difference between each pair as per post
hoc Bonferroni correction P < 0.05.
NEMO, nutrition education for management of osteodystrophy; P, phosphorus; DD,
dedicated dietitian; EP, existing practice; THD, trained hospital dietitian.
Table 8
Effect of NEMO trial on dietary P (mg)/protein (g) ratio (n = 394).

T0
T1
T2
P

DD group (n = 88)

EP group (n = 96)

THD group (n = 210)

15.51  5.3ab
14.71  3.93a
16.11  2.1b
0.006

15.74  4.41
15.55  4
15.67  1.41
0.91

14.62  4.49a
14.93  3.42a
16.04  2.34b
0.001

Values are shown in mean  SD; P value in the table indicates signicance over time
as per GLM-repeated measure ANOVA with a GreenhouseGeisser correction;
different superscripts indicate statistical difference between each pair as per post
hoc Bonferroni correction P < 0.05.
NEMO, nutrition education for management of osteodystrophy; P, phosphorus; DD,
dedicated dietitian; EP, existing practice; THD, trained hospital dietitian.

recipe book of modied traditional dishes, so patients would not

feel deprived from their customary and traditional meals. Patients
often complain that the dietary restrictions are too complicated to
understand and leave them with diet that is not appealing [27].
Chan et al. [28] conrmed that easy-to-follow patient information
leads to behavioral change. At follow up, dietary P density
increased in all 3 groups. We related this to the seasonal change
that happened at the end of the12-month study; it was winter and
people tend to eat more than usual due to the cold weather [29].
Since in Lebanon a highly consumed food item is dairy, which is
also high in P, we assume that the increase in P/protein ratio was
due to the increased consumption of food, especially dairy
products.
The research team prepared a patient educational tool kit,
culturally t to the specic patient population needs and used it in
the DD group. The team needed excellent knowledge of the topic,
time, effort and access to literature; all of which are difcult to nd
among dietitians who are not specialized in renal care and are
overwhelmed with various duties in the hospital; as is in Lebanon
[13].
Overall, the lack of improvement in the EP group shed light on
the insufciency of the current dietetic practice in HD units in
Lebanon. As well as the poor results in the THD group pointed out
the negative effect of schedule overload and lack of resources. THD
dietitians did receive the same training as that of DD but were not
provided with sufcient resources; accordingly, they were not able
to provide optimal and effective NE to HD patients.

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005

G Model
PEC 5047 No. of Pages 7

M. Karavetian et al. / Patient Education and Counseling xxx (2015) xxxxxx

While at rst look the intervention might seem costly and

difcult to integrate in routine practice, such interventions in other
countries have proven to be cost-effective on the long run [30] and
are linked to decreased patient hospitalization and better patient
clinical outcomes [31]. Country specic economic evaluation
would help clarify the exact resources and thus be a cornerstone
for health-care reform.
There are several limitations to our study: signicantly
decreased serum P in the DD group might be also subsequent to
increased adherence to P-binders, since some of the educational
sessions focused on them; this remains to be explored in future
studies. Potential differences in the medical teams between HD
units might play a potential role of uncontrolled confounding
variable.
4.2. Conclusion
Providing HD patients with a specialized, stage-based, culturally-adapted intensive NE by a competent DD resulted in a
signicantly higher patient knowledge about kidney disease and
its management, enhanced readiness to change toward adherence
to medical nutrition therapy and subsequently improved clinical
outcomes.
4.3. Practice implications
The results of the study indicate that a 6-month intensive
individualized stage-based NE through a 2-h per month of
dietitian-to-HD patient time leads to signicant improvement in
P among HD patients. This method can serve as a model to follow in
HD units in Lebanon and other countries with similar health care
systems. Its adoption may be the pillar of change toward better
nutritional management in the HD unit.
Funding sources
None.
Conict of interest statement
None.
Acknowledgments
The study was under the patronage of the Lebanese Ministry of
Public Health. The Nutrition Department of the Faculty of Sciences
in the Lebanese University provided graduate students who helped
in data collection. Ahmad Abdallah developed a software to
facilitate data entry. Special thanks to the staff and patients in each
of the participating units for facilitating the process.
References
[1] Matteson M, Russel C. Interventions to improve hemodialysis adherence: a
systematic review of randomized-controlled trials. Hemodial Int 2010;4:370
82.
[2] Anand S, Bitton A, Gaziano T. The gap between estimated incidence of endstage renal disease and use of therapy. PloS One 2013;8:e72860.
[3] Sun C, Chang K, Chen S, Chang C, Wu M. Patient education: an efcient
adjuvant therapy for hyperphosphatemia in hemodialysis patients. Ren Fail
2008;30:5762.
[4] Caldeira D, Amaral T, David C, Sampaio C. Educational strategies to reduce
serum phosphorus in hyperphosphatemic patients with chronic kidney
disease: systematic review with meta-analysis. J Ren Nutr 2011;21:28594.

[5] McCann L. Pocket Guide to Nutrition assessment of the Patient with Chronic
Kidney Disease. 4th ed. New York: National Kidney Foundation Council on
Renal Nutrition; 2009.
[6] Durose CL, Holdsworth M. Knowledge of dietary restrictions and the medical
consequences of noncompliance by patients on hemodialysis are not
predictive of dietary compliance. J Am Diet Assoc 2004;104:3541.
[7] Spahn J, Reeves R, Keim K, Laquatra I, Kellogg M, Jortberg B, et al. State of the
evidence regarding behavior change theories and strategies in nutrition
counseling to facilitate health and food behavior change. J Am Diet Assoc
2010;110:87991.
[8] Prochaska J. Decision making in the transtheoretical model of behavior
change. Med Decis Making 2008;28:8459.
[9] Molaison E, Yadrick K. Stages of change and uid intake in dialysis patients.
Patient Educ Couns 2003;49:512.
[10] Mochari-Greenberger H, Terry M, Mosca L. Does stage of change modify the
effectiveness of an educational intervention to improve diet among family
members of hospitalized cardiovascular disease patients. J Am Diet Assoc
2010;110:102735.
[11] Whitelaw S, Baldwin S, Bunton R, Flynn D. The status of evidence and
outcomes in stages of change research. Health Educ Res 2000;15:70718.
[12] Karavetian M, De Vries N, Rizk R, Elzein H. Dietary educational interventions
for management of hyperphosphatemia in hemodialysis patients: a systematic
review and meta-analysis. Nutr Rev 2014;72:47182.
[13] Karavetian M, El Zein H, Hwalla N, De Vries N. Dietetic practices in
hemodialysis units in lebanon and their conformity with KDOQI nutrition
guidelines. Int J Health Nutr 2013;4:18.
[14] Karavetian M, De Vries N, El Zein H. Nutritional education for management of
osteodystrophy in hemodialysis patients (NEMO) trial program, Lebanon:
design and patient characteristics. Nutr Res Pract 2014;8:10311.
[15] Karavetian M, Ghaddar S. Nutritional education for the management of
osteodystrophy (NEMO) in patients on haemodialysis: a randomised
controlled trial. J Ren Care 2012;39:1930.
[16] Fickenor M, Byrd-Bredbenner C. Nutrition intervention group program based
on preaction-stage-oriented change processes of the transtheoretical model
promotes long-term reduction in dietary fat intake. J Am Diet Assoc
2000;100:33542.
[17] Aldridge M. Writing and designing readable patient education material.
Nephrol Nurs J 2004;31:3737.
[18] 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;10:804.
[19] American Dietetic AssociationEvidence Analysis Library (ADAEAL). Is MNT
provided by a Registered Dietitian for chronic kidney disease (CKD) in adults
effective? ADA Evidence Analysis Library [Internet] 2010 [cited 2012 Oct
10];16. Available from: http://www.adaevidencelibrary.com/evidence.cfm?
format_tables=0&evidence_summary_id=251091.
[20] Sneed NV, Paul SC. Readiness for behavioral changes in patients with heart
failure. Am J Crit Care 2003;12:44453.
[21] Ford JC, Pope JF, Hunt AE, Gerald B. The effect of diet education on the
laboratory values and knowledge of hemodialysis patients with
hyperphosphatemia. J Ren Nutr 2004;14:3644.
[22] Welch J. Hemodialysis patient beliefs by stage of uid adherence. Res Nurs
Health 2000;24:10512.
[23] USDA National Nutrient Database for Standard Reference, Release 25
[application]. MS-DOS version. Agricultural Research Service, Department
of Agriculture, 2012.
[24] Nisio JM, Bazanelli AP, Kamimura MA, Lopes MGG, Ribeiro FSDM, Vasselai P,
et al. The impact of a nutrition educational program on the control of the
hyperphosphatemia in hemodialysis patients. J Bras Nefrol 2007;29:1527.
[25] Morey B, Walker R, Davenport A. More dietetic time, better outcome? A
randomized prospective study investigating the effect of more dietetic time on
phosphate control in end-stage kidney failure haemodialysis patients.
Nephron Clin Pract 2008;109:c17380.
[26] Lou LM, Caverni A, Gimeno JA, Moreno R, Perez J, Alvarez R, et al. Dietary
intervention focused on phosphate intake in hemodialysis patients with
hyperphosphoremia. Clin Nephrol 2012;77:47683.
[27] Breiterman WR. Adherence to the dialysis prescription: partnering with
patients for improved outcomes. Nephrol Nurs J 2004;31:4326.
[28] Chan YM, Zalilah MS, Hii SZ. Determinants of compliance behaviours among
patients undergoing hemodialysis in Malaysia. PloS One 20127: 41362.
[29] Lloyd L, Miller B. The impact of seasonality on changes in body weight and
physical activity in Mexican-American women. Women Health 2013;53:262
81.
[30] Sabariego C, Grill E, Brach M, Fritschka E, Mahlmeister J, Stucki G. Incremental
cost-effectiveness analysis of a multidisciplinary renal education program for
patients with chronic renal disease. Disabil Rehabil 2010;32:392401.
[31] Wingard RL, Pupim LB, Krishnan M, Shintani A, Ikizler TA, Hakim RM. Early
intervention improves mortality and hospitalization rates in incident
hemodialysis patients: RightStart program. Clin J Am Soc Nephrol
2007;2:11705.

Please cite this article in press as: M. Karavetian, et al., Effect of behavioral stage-based nutrition education on management of osteodystrophy
among hemodialysis patients, Lebanon, Patient Educ Couns (2015), http://dx.doi.org/10.1016/j.pec.2015.05.005