Document 11212799

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Journal Of Musculoskeletal Pain, Vol. 21(4): 365–370, 2013
! 2013 Informa Healthcare USA, Inc.
ISSN: 1058-2452 print / 1540-7012 online
DOI: 10.3109/10582452.2013.852649
RESEARCH IDEA
Allen Ernst,
MS
and John Shelley-Tremblay,
PhD
Department of Psychology, University of South Alabama, Mobile, AL, USA
ABSTRACT
Objectives: This study was conducted to assess the association between a non-ketogenic, low-carbohydrate diet
[NKLCD] and symptoms of fibromyalgia syndrome [FMS], mood and energy levels, and confusion, as compared to
controls reporting adherence to the Western Pattern Diet [WPD].
Methods: Participants were 33 middle-aged females with FMS who reported adherence to a NKLCD or the WPD.
Respondents completed a questionnaire packet measuring state and trait mood and energy level as well as a measure of
FMS symptoms and daily functioning.
Results: The NKLCD sample reported less affective distress, less Confusion, less Fatigue and more Vigor than the WPD
sample on the Profile of Mood States. Group scores for the Hospital Anxiety and Depression Scales showed lower
Anxiety and Depression scores for the NKLCD sample. The NKLCD sample showed lowered symptom scores on the
Fibromyalgia Impact Questionnaire. Morbidity was significantly reduced for all measures in the NKLCD sample.
Conclusions: Results support hypotheses of less dysphoria, more energy, decreased FMS symptomatology in a NKLCD
sample versus the WPD group. Results suggest the potential for development of a dietary intervention for managing
affective and functional symptoms of this syndrome.
KEYWORDS: Depression, diet, fibromyalgia, FIQ, HAD Scales, low-carbohydrate, POMS
INTRODUCTION
For three decades, the per capita and caloric
proportional measures of the macronutrient carbohydrate [CHO] has increased in the American diet
(1). At the same time an association between CHO
intake and depressive affect has been empirically
demonstrated in individuals presumed to be particularly sensitive to carbohydrate intake (2), as well
as healthy females [Ernst and Shelley-Tremblay,
unpublished observation].
Among the many laboratory abnormalities found
in the fibromyalgia syndrome [FMS], an impairment
of glycolysis, an oxidative stage in glucose metabolism within the Krebs metabolic cycle, has been
observed. In one study, glycolysis was impaired such
that the reaction products of this process, particularly
adenosine triphosphate [ATP], the energy source for
cell metabolism, was reduced in all FMS participants
(3,4). Similar ATP energy deficits have also been
observed in muscle biopsies of FMS patients (5).
Both findings have been frequently cited to explain
the profound anergy experienced in FMS. This
metabolic dysfunction is pervasive and chronic, as
digestible starches and most sugars are eventually
rendered into glucose, which then goes on to partial
conversion to ATP during the Krebs cycle (6).
It has been suggested that the carbohydrate
cravings observed in FMS (7) may arise out of a
drive to self-medicate this anergic state. However,
carbohydrate cravings have also been associated with
20
13
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Non-Ketogenic, Low Carbohydrate Diet Predicts Lower Affective
Distress, Higher Energy Levels and Decreased Fibromyalgia
Symptoms in Middle-Aged Females with Fibromyalgia Syndrome as
Compared to the Western Pattern Diet
Correspondence: Allen Ernst, Department of Psychology, University of South Alabama, Mobile, AL 36688, USA. E-mail:
ernsta@sanjuancollege.edu
Submitted: 6 March 2013; Revisions Accepted 30 September 2013; published online 11 November 2013
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366
A. Ernst & J. Shelley-Tremblay
depression (8,9), as well as other dysphoric mood
and energy states (10) – both found in FMS in
greater frequency than the American adult
population.
In an attempt to establish a direction of causality
for this association, Christensen et al. (11) reported
three case studies that showed improvement in
depressive symptoms when participants restricted
their carbohydrate intake, specifically sucrose.
Following up these results, Christensen and Somers
(8) reported greater CHO intake for depressed
individuals. Some additional support for these
findings comes from comparative animal studies
that have shown antidepressant effects of an isoenergetic ketogenic diet on rats during the Porsolt test, an
animal model of depression used in pharmaceutical
research. Treated rats showed less ‘‘behavioral despair’’ than chow-fed subjects in response to this
hopeless water tank escape dilemma (12).
A ketogenic diet study with human subjects using
the Profile of Mood States [POMS] assessments
found no subscale score differences save for
Confusion-Bewilderment, found to be higher in
the American Dietetic Association diet group
increasing over time, while the ketogenic, lowcarbohydrate diet [KLCD] group actually logged a
decrease in Confusion scores over time (13). They
also found group differences in cognitive performance tasks, with mixed results.
A naturalistic study by Ernst and Shelley-Tremblay
[2012, unpublished observations] has shown less
affective distress in a sample of middle-aged females
reporting adherence to a low-carbohydrate diet
versus a second group that reported no diet or
rather the Western pattern diet [WPD]. The WPD is
characterized by a high consumption of red meat,
refined grains, processed meat, high-fat dairy products, desserts, high-sugar drinks and eggs, as well as
French fries and potatoes (14). In 1999, Hu et al. (15)
reported on a study to test the validity of the construct
WPD versus the Prudent Diet and found that from
a factorial standpoint both constructs were stable
over time and valid.
In the laboratory Shelley-Tremblay et al. (16)
reported a significant group interaction between
FMS patients and healthy females in the high-alpha
electroencephalogram [Alpha EEG] band, which the
authors interpreted as associated with the
‘‘approach’’ emotion of anger, and correlated with
the POMS Anger-Hostility subscale. These effects
were in response to the intake of a 75-g sucrose
challenge measured at five epochs over 3 h.
In contrast to the aforementioned study, the
present study was conducted in the same laboratory
but sought to measure the association for females
with FMS between KLCD and self-reported affect
and symptoms. Numerous subjective reports indicate that low-CHO diets afford FMS patients more
energy. Not only have these claims not been assessed
systematically, but an empirically-based model of
carbohydrate-mediated serotonin neurotransmitter
production sometimes called the Wurtman Effect
actually predicts a drop in tryptophan absorption
across the blood–brain barrier and as a necessary
precursor to serotonin production in the period
following CHO consumption with subsequent
depressive affect [for a review see (17)]. The present
study was conducted to test the hypothesis that a
low-carbohydrate diet is associated with a lower
physiological and affective symptom profile in
subjects diagnosed with FMS.
MATERIALS AND METHODS
Oversight
The study was reviewed and approved by the
Institutional Review Board of the University of
South Alabama, which endorses the Helsinki
Protocols of 1964. All subjects participated voluntarily in this study.
Recruitment of subjects
In this correlational study, 33 [4 non-ketogenic, lowcarbohydrate diet [NKLCD] and 29 Western Pattern
Diet [WPD] adherents] age-equivalent groups with
FMS were recruited from the student subject pool of
a large southeastern university and the local community via newspaper. University subject pool
participants received class credit, while locally
recruited subjects were thanked for their
participation.
Group assignment
Participants endorsed an informed consent form
where potential respondents were informed, ‘‘The
purposes of the study is to evaluate the difference(s),
if any, in mood states. . .between two different meal
types, on a population of women who have been
diagnosed with FMS. You have been invited to this
study because you are a woman with a history of
FMS. You will be asked to fill out some questionnaires. One questionnaire will ask you some general
questions about age and medical history. Another
form will measure personality traits, while a third
will inquire about how you have been feeling. . .’’
Respondents then completed the demographic questionnaire and self-report battery. All included
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Diet and Fibromyalgia Symptoms
subjects reported treatment under the care of a
physician and diagnosis of FMS according to the
American College of Rheumatology criteria (18).
Respondents were eliminated if they reported an
eating disorder, other diet type, diabetes mellitus or
severe clinical depression, as evidenced by reported
history during telephone screening or Hospital
Anxiety and Depression Scale [HADS] Depression
score exceeding a clinical cutoff of 14.
Those respondents reporting adherence to either a
NKLCD or WPD were assigned to separate sample
groups. Respondents were asked about their overall
adherence to the low-carbohydrate diet to determine
if their particular stage or level of adherence would be
likely to produce ketosis. In addition, they were asked
if they had recently been experiencing any of the
recognized signs and symptoms of ketosis including
headaches and distinctive breath odor. No participants were given instructions to modify their diet.
Measurements
Profile of Mood States
Mood and energy levels were measured by the POMS
(19). The POMS contains 65, five-response Likertscale adjective items [including 15 fillers] with scoring
to yield six subscales to immediate or long-term
somatic and affective states and one composite score,
the Total Mood Disturbance Score. The subscales
were factor-analytically derived to load on the
constructs Tension-Anxiety, Depression-Dejection,
Anger-Hostility, Vigor, Fatigue and ConfusionBewilderment. The Total Mood Disturbance Score
was derived by the summation of the five ‘‘negative’’
subscales, then subtracting from this total the ‘‘positive’’ Vigor score. The POMS was administered with
validated instructions to report subjective states
‘‘right now’’, within the last 3 min.
Hospital Anxiety and Depression Scales
The HAD Scales (20) were validated on a sample of
hospital patients. Patients endorsed one of four
statements for each of 16 items. In its development,
all items were factor-derived such that any items
loading strongly on somatization were eliminated,
thus eliminating confounds from medical disorders.
Another departure from the usual depression inventory is the factorization of depression-scale items to
load on the anhedonic component of depressive
states.
Fibromyalgia Impact Questionnaire
The Fibromyalgia Impact Questionnaire [FIQ] (21)
is a self-report measure of physical functioning,
367
work status, depression, anxiety, sleep, pain, stiffness, fatigue and well-being. In its construction,
some items were used from both the Health
Assessment Questionnaire and the Arthritis Impact
Measurement Scales.
RESULTS
Study subjects
Recruitment efforts were successful in identifying a
total of 87 females with FMS who were willing to
participate in the study [see Figure 1]. Of those, 75
individuals had responded to a local newspaper
advertisements and 12 individuals came from a
University Subject Pool. Unfortunately, 45 of those
recruited had to be excluded because they did not
meet inclusion criteria, declined to participate or for
other reasons. That left 42 subjects as study participants to be allocated to a study group, with five selfselecting to the NKLCD group and 37 self-selecting
to the WPD group.
Characteristics of groups
The observed demographic characteristics of the two
groups are shown in Table 1. Independent-samples
t-tests were conducted to determine if a possible
confound of age was different between the two
groups. Group age difference was not significant.
Independent samples non-parametric tests were
conducted to determine if sample groups differed
in their use of antidepressants, sleep meds, pain
meds or guaifenisin, and no significant differences
were found [Table 1] Further independent-samples
t-tests were conducted with SPSS 20 to test the
hypothesis that subjects reporting adherence to a
NKLCD would report lower scores on measures of
affective distress, fatigue and FMS symptoms.
Table 2 shows significant group differences were
evident for both HAD Scales Depression and Anxiety
subscales and the HAD Scales Total Score such that
subjects on NKLCD showed lower affective distress.
In addition, mean score differences in seven of seven
POMS scales did reach significance with the NKLCD
sample showing less affective distress, confusion and
fatigue. Finally, the NKLCD sample showed significantly lower FMS-related symptom scores than the
WPD sample as reported on the FIQ. All measures
showed large effect sizes as measured by Cohen’s d as
calculated by G*Power 3.
DISCUSSION
This study has shown that individuals with FMS
eating carbohydrate-restricted diets differed
A. Ernst & J. Shelley-Tremblay
368
Assessed for eligibility (n=87)
Recruited from local newspaper
(n=75) From University Subject
Pool (n=12)
Enrollment
Excluded (n=45)
♦ Not meeng inclusion criteria (n=16 )
♦ Refused to parcipate (n=2)
♦ Other reasons (n=27 no packet)
Assigned (n= 42)
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Allocaon
Western Paern Diet
Allocated to intervenon (n= 37)
♦Received allocated intervenon (n=37)
♦Did not receive allocated intervenon
diabetes (n=3); depression (n=6)
Non-Ketogenic Low-Carbohydrate Diet
Allocated to intervenon (n=5)
♦Received allocated intervenon (n=5)
Follow-Up
Lost to follow-up
Lost to follow-up
Disconnued intervenon (incomplete packet)
(n= 1)
Disconnued intervenon (incomplete packet)
n=3)
Analysis
Analysed (n= 4 )
Analysed (n= 29)
FIGURE 1. Sampling and flow of participants for survey study.
significantly from those on WPD with respect to all
measures of affective state, energy levels and FMS
symptoms. These findings support the hypothesis
that the low carbohydrate diet sample would report
less affective distress, fatigue and lower FMS symptom scores. Greater Vigor and lower Fatigue scores
for the NKLCD group may be explained by a finding
for healthy subjects by Piatti (22) that CHO intake
actually reduced glucose oxidation or glycolysis, with
the result that the system would have greater energy
at its disposal at the cellular level.
These results are of note in that the carbohydraterestricted diet appears to be associated with lessened
affective distress and fatigue in a clinical population,
supporting the results of Galletly et al. (23) who
found that their low-CHO group showed a statistically-significant reduction in depression over time,
as measured by the HAD Scales. It should be noted,
however, that their subject group was comprised of
female subjects diagnosed with a rare disorder.
Interestingly, the prediction of greater affective
distress as inferred from the model of brain
serotonin augmentation by CHO intake (9) was
not supported these or our results.
The scope of this study and its conclusions were
constrained by several limitations. Although the
demographic variables seemed to support comparability between the study groups, there was a
substantial disparity between study group sample
sizes. In addition, the subject sample was restricted
to females as this population may be more responsive to the modulation of CHO as a macronutrient
in the diet (24). Therefore, the results from this
study may not be applicable to males, even to males
of a similar demographic.
In the literature, non-ketogenic diets are often
confounded with ketogenic diets. In general, it
appears that most studies report potentially ketogenic diet samples, and that this type of diet should
yield different metabolic effects than the nonketogenic type. To complicate matters, the descriptions of dietary manipulations in some studies have
Diet and Fibromyalgia Symptoms
369
TABLE 1. Group sample characteristics.
Group
NKLCD
Measure
Age
Education
FMS Duration
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Binomial data
Antidepressants
Sleep meds.
Pain meds.
Compensation
Hypoglyemia
Counseling
Guaifenisin
WPD
Statistic
M
SD
N
M
SD
N
t
p
53.75
13.25
13.00
8.62
1.50
8.72
4
4
4
45.97
14.00
10.29
7.98
1.54
7.32
29
29
29
1.814
.932
.679
0.079
0.404
0.502
%
M rank
N
%
M rank
N
U
p
17.38
23.00
14.25
13.50
0.50
14.50
19.13
4
4
4
4
4
4
4
72
59
69
24
24
0.17
10
16.95
16.17
17.38
17.48
0.44
17.34
16.71
29
29
29
29
29
29
29
56.50
34.00
47.00
44.00
86.00
48.00
49.50
0.936
0.203
0.576
0.472
0.580
0.613
0.651
75
100
50
00
25
00
25
NKLCD, non-ketogenic, low-carbohydrate diet; WPD, Western pattern diet; FMS, fibromyalgia syndrome.
TABLE 2. Sample group comparisons on measures of HAD Scales, POMS and FIQ.
NKLCD
Measure
WPD
Statistic
M
SD
N
M
SD
N
t
p
d
HADS
HADSdep
HADSanx
HADStot
5.50
5.25
10.75
1.00
0.96
0.957
4
4
4
9.76
11.55
21.31
3.27
3.59
5.52
29
29
29
5.42
7.68
9.33
0.000
0.000
0.000
1.76
2.40
2.66
POMS
TMDS
Depression
Tension
Anger
Vigor
Fatigue
Confusion
2.00
4.25
5.25
0.75
20.25
8.25
3.75
10.23
5.32
1.708
0.96
5.19
1.89
2.75
N
4
4
4
4
4
4
51.86
14.59
12.03
6.24
8.21
16.31
10.90
35.52
14.44
7.39
6.63
6.16
7.49
5.14
N
29
29
29
29
29
29
5.97
2.74
4.20
4.16
4.25
4.79
4.27
0.000
0.019
0.000
0.000
0.012
0.000
0.005
1.91
0.95
1.26
1.16
2.12
1.48
1.74
FIQ
52.58
8.26
4
66.86
15.41
29
2.84
0.027
1.91
HADS ¼ Hospital Anxiety and Depression Scale, POMS ¼ Profile of Mood States, TMDS ¼ Total Mood Disturbance Score, FIQ ¼ Fibromyaliga Impact
Questionnaire, NKLCD ¼ non-ketogenic, low-carbohydrate diet, WPD ¼ Western Pattern Diet, FMS ¼ fibromyalgia syndrome
not specified nor verified ketogenesis. Some studies
that are unequivocally ketogenic have been reviewed
here to fill in gaps in the literature that might have
been filled by non-ketogenic studies, if they existed.
The NKLC diets in general see greater adherence in
the general public due to less dietary rigor coupled
with a lack of signs and symptoms arising out of
ketosis. Results of the study suggest that an efficacious dietary treatment may be developed through
further applied studies.
DIRECTIONS FOR FURTHER STUDY
The ideal follow-up study would test the putative
analgesic properties of a low-carbohydrate nonketogenic or ketogenic diet (25) through
FMS-specific and general-research developed dolormetric and nociceptive measures throughout the life
of the study using both objective and subjective
measures. The use of tender points as a marker
that is sensitive to change has come under question
in recent years (26); therefore more responsive
measures should be considered. The FIQR would
be a good choice here, as well as the Modified
Visual Analog Scale of the FIQ and measures of
restorative sleep.
Both NKLCD and KLCD groups should be
studied with subjects randomly assigned to tease
apart any discrete effects observed in each group.
The ideal study would incorporate the use of
diabetic reagent sticks for the in-stream assay of
any ketone bodies in a mid-stream urine sample at
A. Ernst & J. Shelley-Tremblay
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370
regular intervals over the life of the study. This pilot
study was able to attain to statistical significance and
large effects sizes with small sample groups. However
the population with FMS may contain a subgroup of
dietary responders and therefore a larger sample
group would enable the post hoc identification of any
subject traits or patterns in the data that might be
markers for responders or individuals refractory to
response. A design employing repeated-measures
ANOVA to follow before and after measures and
Student’s t-test for group differences would capture
time and group differences, along with measures of
effect size.
Despite an increase in acceptance of the construct
of FMS within the rheumatology community there
remains variance in the application of the American
College of Rheumatology criteria and sparse use of
algometry in the examination room. More progress
needs to be realized in the area of differential
diagnosis. Ideally subjects would be recruited directly from a rheumatology practice with physicians
that are known to follow the most current ACR
criteria. Any study lifetime should well exceed the
standard 2-week period for carbohydrate washout
and its commonly encountered malaise, fatigue and
carbohydrate cravings.
Therapeutic effects were shown in this present
study with subjects despite no washout of prescribed
antidepressants, pain meds, sleep medications or
guaifenisin. As this pilot study showed significant
group differences on all measures, it suggests that the
observed effects were robust in the face of these
concomitant treatments.
DECLARATION OF INTEREST
This study was funded entirely by the researchers using
university facilities.
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