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Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6 7
INTRODUCTION
The red seaweed Chondrus crispus (Rhodophyta) is widely
distributed in the northern Atlantic.1 As an economically
important seaweed species in the Atlantic Canada
region, Chondrus crispus is also cultivated on land in Nova
Scotia, Canada.1
In addition to high content of total proteins, oligopeptides
and pigments, this alga is rich in the water-soluble
Clinical effects of overwintered-stressed Chondrus
Crisupus and non-overwintered-stressed
Chondrus crispus dietary supplementations
Beniamino Palmieri1, Maria Vadalà2, Carmen Laurino3
1Professor, Department of General Surgery and Surgical Specialities, University of Modena and Reggio Emilia.
Largo del Pozzo 71, 41124 Modena (MO). Second Opinion Medical Network, Modena (MO), Italy, 2,3Medical Doctor,
Department of General Surgery and Surgical Specialities, University of Modena and Reggio Emilia. Largo del Pozzo
71, 41124 Modena (MO). Second Opinion Medical Network, Modena (MO), Italy
ABSTRACT
ORIGINAL ARTICLE ASIAN JOURNAL OF MEDICAL SCIENCES
Background: Chondrus crispus is red seaweed widespread in the northern Atlantic coasts
due to the high proteins, burden it is quite helpful supplement for some symptoms such
as fatigue, asthenia, and weakness and for supporting skeletal muscles in sports athletes.
Aims and Objectives: This retrospective observational “not inferiority” study investigates and
compares the clinical effects of overwintered-stressed Chondrus Crisupus and non-overwintered-
stressed Chondrus crispus dietary supplementations for the treatment of musculoskeletal
and articular symptomatology related diseases. Materials and Methods: Eighty patients were
retrospectively reviewed through the Second Opinion Medical Network. Patients were prescribed
3 capsules/day after the main meals for 3 weeks of overwintered-stressed Chondrus Crisupus
or non-overwintered stressed Chondrus crispus dietary supplementations. Quality of life (QOL)
assessment was evaluated by the Short Form-36 (SF-36) health survey questionnaire before
starting the treatment and after the third week. Benets declared by patients were also reported
after the treatment in addition to some subjective observations related to the symptomatology
and to the health status. Results: Fifty patients were treated with overwintered-stressed
Chondrus Crisupus and 30 patients were treated with the non-overwintered-stressed Chondrus
crispus dietary supplementation. The general benet of treatment with overwintered-stressed
Chondrus Crisupus was 76%, while that obtained with non-overwintered-stressed Chondrus
crispus was 33.3% (P <0.01). Results of SF-36 general health status after the treatment
demonstrated that 37 patients (74%) and 11 patients (36.7%) felt better than before in the
overwintered-stressed Chondrus Crisupus group and non-overwintered-stressed Chondrus
crispus group, respectively (P < 0.01). A great improvement of subjective exhaustion, fatigue,
pain, digestive, and peristalsis disturbances symptoms, in addition to mood and concentration
amelioration that would be a consequence of symptomatology regression, was also observed.
Conclusions: This retrospective observational comparative study evidences that overwintered-
stressed Chondrus Crisupusimproved musculoskeletal and articular symptomatology related
diseases better than non-overwintered-stressed Chondrus crispus.
Key words: Chondrus crispus; Energy; fatigue; Musculoskeletal symptoms; Articular
symptoms; Overwintered; Cold; L-citrullynin-L-arginine
Access this article online
Website:
http://nepjol.info/index.php/AJMS
DOI: 10.3126/ajms.v9i6.20978
E-ISSN: 2091-0576
P-ISSN: 2467-9100
Address for correspondence:
Carmen Laurino, Department of General Surgery and Surgical Specialities, University of Modena and Reggio Emilia. Largo del Pozzo 71,
41124 Modena (MO). Second Opinion Medical Network, Modena (MO), Italy. Phone: +390594222483. E-mail: carmen.laurino@hotmail.it.
© Copyright AJMS
Submitted:03-09-2018 Revised: 19-09-2018 Published: 01-11-2018
Palmieri, et al: Chondrus crispus dietary supplementations
8 Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6
polysaccharide carrageenan (approximately 50-65 % on a
basis of dry weight).2,3 Carrageenan is widely used in the
food industry as a thickener, stabilizer and emulsier.
Thanks to the high content of total proteins among these
seaweeds, Chondrus crispus is in the folk medicine, reputed as
effective supplement for some symptoms such as fatigue,
asthenia, and weakness and for supporting skeletal muscles
in sports athletes.4
Physiologically, the food content in amino acids is the
substrate of biosynthesis of structural and functional
proteins in the body. These digested amino acids can be used
for oxidative phosphorylation and gluconeogenesis5, 6 as
well as the facilitation of numerous physiological functions
including acting as precursors for the biosynthesis
of neurotransmitters, hormones, phosphoglycerols,
glycolipids and nucleic acids.7, 8
It has been estimated that the skeletal muscles in the human
body are 40–60% of body mass and thus represent the
major bulk of the body’s protein.9 The body does not has
specic protein stores, but when it is not possible to obtain
sufcient protein via ingestion during exercise, illness or
trauma, it breaks down proteins to amino acids via the
process of proteolysis where the non-myobrillar proteins
display a high turnover rate to meet demands.10 The amino
acids released from this turnover of protein can enter the
blood circulation for metabolism as required and can be
lost in sweat and urine.5, 6
An increased amino acids recruitment would be seen during
illness and recovery from trauma11 as also in sarcopenia12
an in patients with critical illness or other muscle wasting
illness.13 Increased losses of amino acids were observed in
cancer patients affecting by fatigue during and following
radiation therapy and chemotherapy, involving amino acid
homeostasis.11 Signicantly, depleted amino acid levels have
also been associated with long-term fatigue leading often
to a frank nitrogen imbalance.14
This retrospective observational comparative study
investigates and compares the clinical effects of overwintered-
stressed Chondrus Crisupus* and non-overwintered-stressed
Chondrus crispus dietary supplementations for the treatment
of musculoskeletal and articular symptomatology related
diseases.
MATERIALS AND METHODS
Patients. We reviewed medical records (electronic or paper-
based) of 80 patients that had appealed to our “Second
Opinion Medical Network”, (Modena, Italy), between
January and April 2018, because of musculoskeletal and
articular symptomatology (asthenia, fatigue, articular,
musculoskeletal, rheumatic and post-traumatic pain, digestive
and peristalsis disturbances and migraine). Patients were
aged over 40 years and were affected at least 6 months by
different clinical conditions (cancer, infections, sarcopenia,
colitis, rheumatologic, traumatic, musculoskeletal, articular,
autoimmune and genetic diseases) with an attested related
symptomatology and diagnosis. The Second Opinion
Medical Network is a consultation referral web and Medical
Ofce System recruiting a wide panel of real-time available
specialists, to whom any patient affected by any disease or
syndrome and not satised with the diagnosis or therapy, can
apply for an individual clinical audit.15 Due to the doctor-
patient communication gap, most of the patients usually
wander around the medical websites looking for proper
answers to their health problems. However, this search
often becomes compulsive and obsessive and is frequently
ambiguous and frustrating. Palmieri et al, 16 describe this
borderline or even pathological behaviour as the “Web Babel
Syndrome” – a psychological imbalance affecting young and
elderly patients, especially those with multiple synchronous
diseases who receive from their caregivers heterogeneous
and misleading information or advice, including confused,
contradictory statements and prescriptions.17 To deal with
this problem, the Second Opinion Network aims to be a
useful “problem-solving” support revisiting each diagnostic
and therapeutic step and properly re-addressing tailored
treatments and prognoses, as well as preventing unnecessary
investigational procedures and unhelpful and expensive
medical and surgical interventions.15
All patients used pharmacological treatments, dietary
supplementation, surgery, manual and electro - medical
physiotherapy especially for the management of pain and
strain with only partial benet from them. However, these
strategies produces light, moderate or severe side effects
(e.g., hypersensitivity reactions, sensation of pressure or
constriction, ushing to face and in the thoracic region,
asthenia, myalgia, drowsiness, insomnia, restlessness,
vertigo, gastrointestinal symptoms, skin rashes, nausea,
vomiting, etc.), and frequent drug interactions and
contraindications. Dietary supplementation included
herbal products and nutraceutical supplementations, while
electro-medical physiotherapy was based on laser therapy,
iontophoresis, magneto therapy, electrostimulation, etc.
In our clinical practice, we washed out previous
treatments for a period of 2 weeks, and then the dietary
supplementations were administered.
The selected patients were informed, via individual
interview, and informed consent previously approved by
the Local Institutional Review Board under the Helsinki
Declaration.
Palmieri, et al: Chondrus crispus dietary supplementations
Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6 9
Study design and dietary supplementations. We run a retrospective
observational “not inferiority” study for 3 weeks duration. At
the start up the patients were prescribed 3 capsules/day after
the main meals of overwintered-stressed Chondrus Crisupus
of either non-overwintered stressed Chondrus crispus dietary
supplementations. Each capsule contains 500 mg of 100%
powder of the overwintered-stressed red seaweed or 500 mg of
100% powder of the non-overwintered-stressed red seaweed.
overwintered-stressed Chondrus Crisupus is naturally enriched
in a dipeptide, the L-citrullynin-L-arginine (2.8% - 4%), with
antioxidant and energizing properties, compared to the non-
overwintered-stressed Chondrus crispus (0.2%). The cultivation
method of overwintered-stressed Chondrus Crisupus consists
to expose to overwintered conditions the Chondrus crispus with
increased production of amino acids and others peptides
(European Patent 1652435B1). Energizing and antioxidant
peptides contained in both the dietary supplementations are
summarized in Table 1.
The rst clinical examination consisted in the evaluation
of the physical status of the patient. Tolerability and
adverse effects were assessed weekly during the treatment
period through direct contact (email or telephone) with
the patients or their parents.
Quality of life (QOL) assessment was performed using
the Short Form-36 (SF-36) health survey questionnaire
before starting the treatment and after the fourth week. The
questionnaire measures (A) symptomatology; (B) health
status before starting the treatment dened as (i) excellent;
(ii) good; (iii) liable; (iv) shoddy; (C) general health status
after the treatment dened as (i) better than before; (ii) more
or less the same as before; (iii) worse than before. The
percentage scores range from 0% (lowest or worst response)
to 100% (highest or best possible response) 18. Benets
declared by patients were also reported after the treatment
in addition to some subjective observations related to the
symptomatology and to the health status. Adverse reactions
presented during the treatment were also declared.
Statistical analysis. The statistical analysis was performed
using the Mann-Whitney test (continuous variables not
normally distributed) and the chi-squared test (categorical
variables). Statistical signicance was set at a P value <
0.05, and all data were analysed using the R software,
version 3.1.2.
RESULTS
Patients. Fifty patients [28 women (56%) and 22 men (44%),
aged between 40 and 85 years old (mean age 64 years old)]
were treated with overwintered-stressed Chondrus Crisupus
dietary supplementation and 30 patients [15 women (50%)
and 15 men (50%), aged between 40 and 83 years old (mean
age 65 years old)] were treated with the non-overwintered-
stressed Chondrus crispus dietary supplementation formula.
(A) Results of SF-36 symptomatology of both the treated
group are summarized in Table 2.
(B) Results of SF-36 health status before starting the
treatment with overwintered-stressed Chondrus Crisupus
demonstrated that 38 patients (76%) had a liable health
and 12 patients (24%) had a shoddy health. Results of
SF-36 health status before starting the treatment of
the non-overwintered-stressed Chondrus crispus group
demonstrated that 21 patients (70%) had a liable health
and 9 patients (30%) had a shoddy health. Anyone
declared to have excellent or good health.
(C) Results of SF-36 general health status after the
treatment with overwintered-stressed Chondrus Crisupus
demonstrated that 37 patients (74%) felt better than
before and 31 patients (26%) felt unchanged. Results
of SF-36 general health status after the treatment of
the non-overwintered-stressed Chondrus crispus group
demonstrated that 11 patients (36.7%) felt better than
before and 19 patients (63.3%) felt more or less the
same as before. Anyone declared to felt a worse health
than before (P < 0.01).
Thirty eight patients (76%) treated with overwintered-
stressed Chondrus Crisupus declared to have benets to the
treatment and 12 patients (24%) did not report any relief.
Of the non-overewintered-stressed Chondrus crispus group,
10 patients (33.3%) declared to have benets to the treatment
and 20 patients (66.7%) did not report any relief (P < 0.01).
Subjective observations related to the symptomatology
declared by patients after the treatment are summarized
in Table 3.
Subjective observations about health status declared by
patients after the treatment are summarized in Table 4.
Five patients (10%) treated with overwintered-stressed
Chondrus Crisupus referred adverse reactions to the
treatment (3 patients had diarrhoea and 2 patients had
constipation), so the dosage was reduced to 2 capsules/
day. The treatment was well tolerated at the dosage of 3
capsules/day in 90% of patients. Of the non-overwintered-
stressed Chondrus crispus group, any patients referred adverse
reactions to the treatment that was well tolerated at the
dosage of 3 capsules/day in 100% of patients. Any other
adverse reaction was observed in both the groups.
Muscle energy recovery of subjects treated with
overwintered-stressed Chondrus Crisupus was higher
(84%, 42/50 patients; Table 4) than in the group treated
with non-overwintered-stressed Chondrus crispus (33.3%,
10/30 patients; Table 4), as shown the request of the
Palmieri, et al: Chondrus crispus dietary supplementations
10 Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6
same patients to follow-up with the dietary supplement
administration at the end of the rst bottle due to the
observed and subjective clinical benets, while patients
treated with non-overwintered-stressed Chondrus crispus did
not require to repeat the treatment.
The best treatment responders were people complaining
of musculoskeletal and articular pain, due to articular and
cartilaginous causes (with arthrosis, arthritis, lumbar pain
on a slipped disc basis). They declared satisfactory tness
recovery and joint mobility at the end of the treatment.
The energetic benefit was also observed in patients
with cancer undergoing chemotherapy and radiotherapy
with overwintered-stressed Chondrus Crisupus dietary
supplementation.
A further benet observed in at least 30% of patients
taking overwintered-stressed Chondrus Crisupus said they
Table 1: Comparative table of non-overwintered-stressed chondrus crispus and overwintered-stressed
chondrus crisupus dietary supplementations nutritional values. Note that nutritional values of
overwintered-stressed chondrus crisupus are referred to different cultivations in the related years after
overwintered exposition
Parameter Unit Non-overwintered-stressed
chondrus crispus
Overwintered-stressed
chondrus
crispus (2014)
Overwintered-stressed
chondrus
crispus (2015)
Overwintered-stressed
chondrus crispus
(2017)
Citrulline g/kg 2.81 5.16 4.69 3.33
Tryptophan g/100 0.174 0.203 0.195 0.196
Hydroxyproline g/100 < 0.05 < 0.05 < 0.05 < 0.05
Ornithine g/100 0.178 0.889 0.532 0.526
Threonine g/100 0.684 0.802 0.706 0.744
Aspartic acid g/100 1.47 1.81 1.52 1.63
Serine g/100 0.802 0.908 0.756 0.814
Lysine g/100 0.787 1.05 0.882 0.896
Valine g/100 0.795 0.996 0.872 0.881
Proline g/100 0.669 1.2 0.961 1.00
Alanine g/100 0.957 1.15 1.02 1.07
Phenylalanine g/100 0.658 0.877 0.813 0.820
Isoleucine g/100 0.652 0.778 0.692 0.696
Glycine g/100 0.789 0.99 0.845 0.900
Thirosine g/100 0.466 0.561 0.475 0.564
Arginine g/100 1.02 3.83 2.48 2.52
Leucine g/100 1.05 1.27 1.12 1.20
Histidine g/100 0.200 0.263 0.234 0.253
Glutamic acid g/100 1.85 3.06 2.21 2.24
Methionine g/100 0.290 0.342 0.321 0.324
Cysteine g/100 0.249 0.341 0.271 0.274
Taurine mg/100 333 319 452 468
L-citrullynin-L-arginine g/100 0.2 4.1 2.8 3.0
Azote g/100 2.96 5.27 3.81 3.92
Proteins g/100 18.5 32.9 23.8 24.5
Sugars g/100 2.9 < 0.1 < 0.1 < 0.1
Fats g/100 0.6 0.6 1.0 1.2
Minerals g/100 25.47 21.91 24.07 23.58
Sodium g/100 4.4 3.3 4.1 3.982
Table 2: Symptomatology declared by patients before starting the treatment assessed by the SF-36
questionnaire. Results are expressed in terms of symptoms’ frequency
Symptoms Frequency
Overwintered-stressed chondrus
crisupus group (N=50)
Non-overwintered-stressed chondrus
crispus group (N=30)
Asthenia 25 16
Fatigue 19 6
Articular pain 5 5
Musculoskeletal pain 8 4
Post-traumatic pain 1 1
Rheumatic pain 6 2
digestive and peristalsis disturbances 8 0
Migraine 5 3
Palmieri, et al: Chondrus crispus dietary supplementations
Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6 11
had benets on the normalization of intestinal peristalsis
and on digestive functions (patients suffering from colitis,
3/8 patients (Table 3-4).
In conclusion, as assessed before, the general benet
improvement of overwintered-stressed Chondrus Crisupus
administration was 76%, while that obtained with non-
overwintered-stressed Chondrus crispus was 33.3% (P <0.01)
DISCUSSION
This retrospective observational “not inferiority” study
evidences that overwintered-stressed Chondrus Crisupus dietary
supplementation improved musculoskeletal and articular
symptoms with underlying inammatory and degenerative
background better than non-overwintered-stressed Chondrus
crispus, with very mild side effects. Specically, it has been
observed a great improvement of exhaustion, fatigue, pain,
digestive, and peristalsis disturbances symptoms, in addition
to mood and mental concentration amelioration probably
as surrogate endpoints of symptoms. Comparatively, the
general benet of treatment with the overwintered-stressed
red seaweed was 76%, while with the one non-overwintered-
stressed was 33.3% (P <0.01).
A possible explanation of this different performance is
that overwintered exposition of Chondrus crispus naturally
enriched the seaweed in a dipeptide, the L- citrullynin-L-
arginine, compared to other sources of regular Chondrus
crispus (Table 1). In addition, this one has a major content
in total proteins that makes the dietary supplementation
more energizing than the normal seaweed demonstrating
the best therapeutic results obtained in patients treated
with the overwintered-stressed Chondrus crispus. Seasonal
variations in nutritional values of Chondrus crispus are
notable, as described in Table 1. Furthermore, previous
studies demonstrated seasonal different concentrations in
amino acids and in the dipeptide L- citrullynin-L-arginine
in Chondrus crispus and in others red seaweeds.19 This one
has been demonstrated to have in vitro antioxidant activity19.
Laycock et al. (1980) demonstrated that cold exposure (8°)
of Chondrus crispus improved this dipeptide production and
it accumulates at this temperature.20 This could be due
to a direct effect of temperature on the enzyme systems
involved in dipeptide metabolism or simply by a result of
slower growth.20 In fact, the experiments demonstrated that
when Chondrus crispus was kept in nitrogen decient culture
at higher temperatures (15°), L- citrullynin-L-arginine was
consumed rapidly, by arginase enzyme that catalyse the
hydrolysis of the dipeptide bond between citrulline and
arginine. This condition is not veried at lower temperature.
In fact, it would be advantageous for the plant to invest
the energy needed for uptake and reduction of nitrate and
the biosynthesis of nitrogen storage compounds during a
time of low temperatures when growth is restricted and
there is a surplus of available nitrate.20 Generally speaking,
dipeptides, has a high nutritional values in terms of
energetic contribution because of the break of chemical
Table 3: Subjective observations related to the symptomatology declared by patients after the
treatment. Results are expressed in terms of frequency
Subjective observations about symptoms Frequency
Overwintered-stressed chondrus
crisupus group (N=50)
Non-overwintered-stressed chondrus
crispus group (N=30)
Less exhaustion 19 5
Less fatigue 17 6
Mood improvement 13 1
Less pain 5 0
Mild improvement of the symptoms 5 3
Concentration improvement 2 0
Digestive and peristalsis disturbances improvement 3 0
No effects 9 21
Table 4: Subjective observations related to the health status declared by patients after the treatment.
Results are expressed in terms of frequency
Subjective observations about health
status
Frequency
Overwintered-stressed chondrus
crisupus (N=50)
Non-overwintered-stressed chondrus
crispus group (N=30)
More strength and energy 42 10
Persistent asthenia and/or fatigue 10 15
Symptoms persistence but the patients felt
better before starting the treatment
10 4
Improvement of serenity 10 1
Absence of symptoms 3 1
Palmieri, et al: Chondrus crispus dietary supplementations
12 Asian Journal of Medical Sciences | Nov-Dec 2018 | Vol 9 | Issue 6
bonds between the two amino acids, releases a stronger
energetic power compared to single amino acid content.
In fact, commercially available dietary supplementation
with the claim to improve strength and energy has a high
content of others dipeptide, such as L-carnosine (β-alanyl-
L-histidine) to achieve the ne sporting art results due
to the buffering activities of carnosine and its related
imidazole-containing compounds which contribute to
the maintenance of the acid-base balance in the acting
muscles.21
A recent study demonstrated that a further red seaweed
that coexisted with Chondrus crispus, e.g., Mostocarpus stellatus,
has a greater freezing tolerance when compared with
Chondrus crispus due to its denite proline content storage
after cold exposure.22 In this study, a range of molecular
mechanism have been proposed for cryprotectants,
including detoxifying radical oxygen species (ROS),
scavenger with the function of compatible osmolytes,
and replacing water in the stabilization of membrane and
protein conformation.22 With regard to membrane integrity,
cryoprotectants such as proline interact with membrane
surfaces to limit damaging phospholipid phase changes or
membrane fusion during freezing-induced cell collapse.23, 24
Clinical conditions with significantly depleted amino
acid levels have, such as cancer, infections, sarcopenia,
colitis, rheumatologic, trauma, musculoskeletal, articular,
autoimmune and genetic diseases have been associated
with long-term fatigue due to negative nitrogen balance in
the energetic metabolism.14 This can be due to inadequate
amino acids availability because of insufcient protein
intake or impaired digestion. The amino acids requirement
is balanced by proteolysis of non-myobrillar muscle
proteins. A prolonged state of negative nitrogen balance
could result in further proteolysis of myobrillar proteins,
with subsequent muscle wasting and damage. Increased
metabolic activities to support exercise, mount host
defences against infection, or support recovery from illness
and injury, place additional demands on protein turnover
within the body. 9, 10, 25 If a net negative nitrogen balance
is associated with fatigue then it would follow that amino
acid supplementation would have the potential to assist in
restoring nitrogen balance.26
The benets of overwintered-stressed Chondrus Crisupus
might also depends on the higher total proteins
concentrations compared to the non-stressed red seaweed
(from 23.8 g/100 to 32.9 g/100 and 18.5 g/100 respectively
and amino acids content as especially arginine and citrulline
(Table 1).
In conclusion, overwintered-stressed Chondrus Crisupus
supplementation displayed most energizing properties
than the non-stressed red seaweed dietary supplementation
because of a huge content in amino acids and total proteins
supplying deciency.
* BIO-ARCT® (Iontec, Monaco)
Conflict of interest statement
The authors certify that there is no conict of interest with
any nancial organization regarding the material discussed
in the manuscript.
The authors hereby certify that all work contained in this
article is original. The authors claim full responsibility for
the contents of the article. The article has been neither
published elsewhere nor submitted for publication
simultaneously. If accepted, the paper will not be published
elsewhere in the same or similar form, in English or in any
other language
All the authors contributed equally to this work.
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Authors Contribution:
BP- Concept and design of the study, reviewed the literature, manuscript preparation and critical revision of the manuscript; CL- Concept, collected data and
review of literature and helped in preparing rst draft of manuscript, critical revision of the manuscript; MV- Concept of study, collected data and review of study.
Work attributed to:
Department of General Surgery and Surgical Specialities, University of Modena and Reggio Emilia, Second Opinion Medical Network, Modena (MO), Italy.
Orcid ID:
Prof. Beniamino Palmieri- http://orcid.org/0000-0002-0871-138X
Dr Maria Vadalà- http://orcid.org/0000-0001-7873-5072
Dr Carmen Laurino- http://orcid.org/0000-0002-3020-2338
Source of Support: Not Applicable., Acknowledgement: None., Conict of Interest: None declared.
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