Literature Review

An Evidence-Based Systematic Review of Bee Pollen by the Natural Standard Research Collaboration

Article· Literature Review (PDF Available)inJournal of Dietary Supplements 6(3):290-312 · January 2009with 12,147 Reads 
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DOI: 10.1080/19390210903081381 · Source: PubMed
Cite this publication
Abstract
An evidence-based systematic review including written and statistical analysis of scientific literature, expert opinion, folkloric precedent, history, pharmacology, kinetics/dynamics, interactions, adverse effects, toxicology, and dosing.
An Evidence-Based Systematic Review
of Bee Pollen by the Natural Standard
Research Collaboration
Catherine Ulbricht, PharmD
Julie Conquer, PhD
Nicole Giese, MS
Karta Purkh Singh Khalsa, CDN, RH (AHG)
Joshua Sklar, PharmD
Wendy Weissner, BA
Jen Woods, BS
ABSTRACT. An evidence-based systematic review including written
and statistical analysis of scientific literature, expert opinion, folkloric
precedent, history, pharmacology, kinetics/dynamics, interactions, ad-
verse effects, toxicology, and dosing.
KEYWORDS. adverse effects, bee pollen, dosing, evidence-based, in-
teractions, pharmacodynamics, pharmacology, pharmacokinetics, sys-
tematic review
Catherine Ulbricht is affiliated with the Massachusetts General Hospital.
Julie Conquer, Nicole Giese, and Wendy Weissner are affiliated with the Natural
Standard Research Collaboration.
Karta Purkh Singh Khalsa is affiliated with the Bastyr University.
Joshua Sklar is affiliated with the University of Rhode Island.
Jen Woods is affiliated with the Northeastern University.
Address correspondence to: Catherine Ulbricht, PharmD, Massachusetts General
Hospital, c/o Natural Standard, 1 Davis Square, Somerville, MA 02144 (E-mail:
ulbricht@naturalstandard.com).
290
Journal of Dietary Supplements, Vol. 6(3), 2009
Available online at www.informaworld.com/WJDS
C
2009 by Informa Healthcare USA, Inc. All rights reserved.
doi: 10.1080/19390210903081381
Ulbricht et al. 291
SYSTEMATIC AGGREGATION, ANALYSIS, AND REVIEW OF THE
LITERATURE
Search Strategy
To prepare each Natural Standard review, electronic searches are con-
ducted in nine databases, including AMED, CANCERLIT, CINAHL, CIS-
COM, the Cochrane Library, EMBASE, HerbMed, International Pharma-
ceutical Abstracts, Medline, and NAPRALERT. Search terms include the
common name(s), scientific name(s), and all listed synonyms for each
topic. Hand searches are conducted of 20 additional journals (not indexed
in common databases), and of bibliographies from 50 selected secondary
references. No restrictions are placed on language or quality of publica-
tions. Researchers in the field of complementary and alternative medicine
(CAM) are consulted for access to additional references or ongoing re-
search.
Selection Criteria
All literature is collected pertaining to efficacy in humans (regardless
of study design, quality, or language), dosing, precautions, adverse effects,
use in pregnancy/lactation, interactions, alteration of laboratory assays, and
mechanism of action (in vitro, animal research, human data). Standardized
inclusion/exclusion criteria are utilized for selection.
Data Analysis
Data extraction and analysis are performed by healthcare profession-
als conducting clinical work and/or research at academic centers, using
standardized instruments that pertain to each review section (defining
inclusion/exclusion criteria and analytic techniques, including validated
measures of study quality). Data are verified by a second reviewer.
Review Process
A blinded review is conducted by multidisciplinary research-clinical
faculty at major academic centers with expertise in epidemiology and bio-
statistics, pharmacology, toxicology, CAM research, and clinical practice.
In cases of editorial disagreement, a three-member panel of the Editorial
292 JOURNAL OF DIETARY SUPPLEMENTS
Board addresses conflicts, and consults experts when applicable. Authors
of studies are contacted when clarification is required.
Synonyms/Common Names/Related Substances
rAnemophilous pollen, apiary products, Asteraceae, bee bread, bee
pollen extract, Boraginaceae, Brassia campestres L., buckwheat pollen,
Bursera simaruba,Cecropia peltata, cernilton, cernitin pollen extract,
Compositae, Convolvulaceae, dandelion pollen (Compositae), dark blue
bee pollen, Echium vulgare (Boraginaceae), Entomophilous pollen, Er-
agrostis, Eugenia, Eupatorium albicaule, Euphorbiaceae, Fabaceae, flo-
ral honey, floral pollen honey, honeybee pollen, Lonchocarpus, maize
pollen, mesquite pollen, Metopium brownei,Mimosa bahamensis,Myr-
taceae, pine pollen, Poaceae, pollen, pollen d’abeille, pouteria, propolis,
pyrrolizidine alkaloid, rape pollen, Sapindaceae, Sapotaceae, songhu-
uafen, Spanish bee pollen, Thouinia canesceras, Tiliaceae, Trema mi-
crantha,Viguiera dentata.
rCombination product examples: NaO Li Su (bee pollen, radix poly-
goni multiflore, semen ziziphi spinosae, radix salviae multiorhizae, fruc-
tus schisandrae, and fructus ligustris lucidae).
CLINICAL BOTTOM LINE/EFFECTIVENESS
Brief Background
Bee pollen is considered a highly nutritious food because it contains
a balance of vitamins, minerals, proteins, carbohydrates, fats, enzymes,
and essential amino acids. Pollen comes from various plants, including
buckwheat, maize, pine (songhaufen), rape, and typha (puhuang) (Leung
& Foster, 1996). Avoid confusion with bee venom, honey, and royal jelly.
Bees use propolis, a resinous substance, to construct their hives, while
royal jelly is secreted from the salivary glands of bees.
Ulbricht et al. 293
The lay public probably uses it more often than is prescribed in clinical
practice. Typically, bee pollen is used as a rejuvenator or a tonic. It is also
used to enhance athletic stamina and strength and to assist in recovery
from illness. Bee pollen is often used as a pollen and spore antidote during
allergy season. It may aid in respiratory complaints such as bronchitis, sinus
congestion, and common rhinitis. In the support of hormonal disorders, bee
pollen is thought to balance the endocrine system with specific benefits in
menstrual and prostate disorders. In Chinese medicine bee pollen is used for
blood formation, reducing cravings for sweets and alcohol, as a radiation
protectant, and a cancer inhibitor. Available research does not adequately
support its use for these indications.
Scientific Evidence for Common/Studied Uses
Indication Evidence Grade
Athletic performance enhancement C
Cancer treatment side-effects C
Natural Standard evidence-based validated grading rationaleTM
rGrades reflect the level of available scientific evidence in support of the
efficacy of a given therapy for a specific indication.
rExpert opinion and folkloric precedent are not included in this assess-
ment, and are reflected in a separate section of each review (“Strength
of Expert Opinion and Historic/Folkloric Precedent”).
rEvidence of harm is considered separately; the below grades apply only
to evidence of benefit.
Level of Evidence Grade Criteria
A (Strong scientific evidence) Statistically significant evidence of benefit from >2
properly randomized trials (RCTs), OR evidence
from one properly conducted RCT AND one
properly conducted meta-analysis, OR evidence
from multiple RCTs with a clear majority of the
properly conducted trials showing statistically
significant evidence of benefit AND with supporting
evidence in basic science, animal studies, or theory.
(Continued on next page)
294 JOURNAL OF DIETARY SUPPLEMENTS
Level of Evidence Grade Criteria
B (Good scientific evidence) Statistically significant evidence of benefit from 1–2
properly randomized trials, OR evidence of benefit from
>1 properly conducted meta-analysis, OR evidence of
benefit from >1 cohort/case-control/nonrandomized
trials AND with supporting evidence in basic science,
animal studies, or theory.
C (Unclear or conflicting
scientific evidence)
Evidence of benefit from >1 small RCT(s) without
adequate size, power, statistical significance, or quality
of design by objective criteria,aOR conflicting evidence
from multiple RCTs without a clear majority of the
properly conducted trials showing evidence of benefit
or ineffectiveness, OR evidence of benefit from >1
cohort/case-control/nonrandomized trials AND without
supporting evidence in basic science, animal studies,
or theory, OR evidence of efficacy only from basic
science, animal studies, or theory.
D (Fair negative scientific
evidence)
Statistically significant negative evidence (i.e., lack of
evidence of benefit) from
cohort/case-control/nonrandomized trials, AND
evidence in basic science, animal studies, or theory
suggesting a lack of benefit.
F (Strong negative scientific
evidence)
Statistically significant negative evidence (i.e., lack of
evidence of benefit) from >1 properly randomized
adequately powered trial(s) of high-quality design by
objective criteria.a
Lack of evidencebUnable to evaluate efficacy due to lack of adequate
available human data.
aObjective criteria are derived from validated instruments for evaluating study quality, including the 5-
point scale developed by Jadad et al., in which a score below 4 is considered to indicate lesser quality
methodologically (Jadad et al., 1996).
bListed separately in reviews in the “Historical or Theoretical Uses Which Lack Sufficient Evidence” section.
Historical or Theoretical Uses Which Lack Sufficient Evidence
rAging (Liu & Li, 1990), allergies, amenorrhea, antibacterial, antifungal
(Ozcan et al., 2004), antioxidant (Anan’eva & Dvoretskii, 1999;
Campos et al., 2003), appetite stimulant, arthritis, benign prostatic
hypertrophy (BPH), bleeding, bronchitis, chronic renal insufficiency
(Koslik, 1987), colitis, constipation, cough (bloody), diarrhea, diuretic,
dysentery (bloody diarrhea), dysmenorrhea, eczema, enteritis, growth,
hay fever, hemorrhage (cerebral), hemorrhoids, high cholesterol,
immunomodulator (Iarosh et al., 1990; Qian, Zang, & Liu, 1990),
infertility, liver dysfunction (Bevzo & Grygor’eva, 1997), memory,
menstrual problems, mouth sores, multiple sclerosis (Iarosh et al., 1990;
Ulbricht et al. 295
Krivopalov-Moscvin, 1997), nosebleed, nutrition, pregnancy nutritional
supplement (Xie, Wan, & Li, 1994), prostatitis, radioprotection, rash, re-
nal impairment, rheumatism, sexual performance, Sjogren’s Syndrome,
skin care, skin eruptions, tonic, vomiting (blood), weight loss.
Expert Opinion and Historic Precedent
rIn Chinese medicine, bee pollen is used orally as a diuretic and for
alcohol intoxication; topically it is used for eczema, pustular eruptions,
and diaper rash.
rUse of bee pollen is mentioned in the Bible, other religious texts, and
ancient Egyptian texts.
Brief Safety Summary
rPossibly safe: When used orally and appropriately (Maughan & Evans,
1982; Steben & Boudreaux, 1978).
rLikely unsafe: When used orally by individuals with pollen allergies.
It can cause allergic reactions, including anaphylaxis in any given indi-
vidual, depending on the type of pollen.
rNote: Greyman et al. have suggested that although bee pollen allergy
is relatively rare, warnings to include information regarding potential
adverse reactions in sensitive individuals are urgently needed to caution
the public (Geyman, 1994).
DOSING/TOXICOLOGY
General
rRecommended doses are based on those most commonly used in avail-
able trials or in historical practice. However, with natural products it is
often not clear what the optimal doses are to balance efficacy and safety.
Preparation of products may vary from manufacturer to manufacturer,
and from batch to batch within one manufacturer. Because it often is not
clear what the active components of a product are, standardization may
not be possible, and the clinical effects of different brands may not be
comparable.
Standardization
rBee pollen is collected by bees from a variety of flowers, plants, and
weeds near the hive. While pausing in various other places, the bee
296 JOURNAL OF DIETARY SUPPLEMENTS
contaminates this pollen mixture with molds, spores, and bacteria.
Therefore, it is impossible to produce a stable, consistent, and clean
product from this contaminated source. It should be emphasized that
the major problem with bee pollen is not the pollen itself, but the col-
lection, storage, and processing methods used by the bee.
rNote: There is currently insufficient available dosing from well-designed
clinical trials. Dosing below is based on folkloric, traditional, or anec-
dotal use.
Dosing
Adult (age 18):
Oral:
rGeneral: An initial theoretical dose is 1/8 to 1/4 teaspoon, once per day.
The dosage may be gradually increased to 1–2 teaspoons one to three
times per day (anecdotal).
Pediatric (age <18):
rInsufficient available evidence.
Toxicology
rAnalysis of ready-to-eat bee pollen samples has revealed contamina-
tion with potential mycotoxin producing species, including Penicillium
verrucosum,Aspergillus niger aggregate, Aspergillus carbonarius,As-
pergillus ochraceus,Aspergillus flavus,Aspergillus parasiticus, and Al-
ternaria spp. (Gonzalez et al., 2005). Five mycotoxins were not found
in 20 samples of bee pollen (Garcia-Villanova et al., 2004). However,
there is still concern that bee pollen may constitute an important risk
factor concerning the presence of ochratoxin A in the diet of consumers
(Medina et al., 2004).
PRECAUTIONS/CONTRAINDICATIONS
Allergy
rKnown allergy/hypersensitivity to the pollen, especially those included
in commercial preparations. Allergic reactions can include itching,
swelling, shortness of breath, light-headedness, and anaphylaxis. In
atopic individuals, ingestion of bee pollen has resulted in numerous
Ulbricht et al. 297
cases of anaphylaxis (Cohen et al., 1979; Geyman, 1994; Greenberger
& Flais, 2001; Mansfield & Goldstein, 1981).
Adverse Effects/Post-Market Surveillance
rGeneral: Hypersensitivity to pollens included in commercial prepara-
tions has been observed. Symptoms include allergic reactions such as
gastrointestinal upset, rash, erythema, asthma, hay fever, nausea, ab-
dominal cramps, diarrhea, and vomiting.
rDermatologic: Ingestion of a product containing bee pollen ingestion
precipitated a wheal or erythema reaction in one subject. Microscopic
analysis revealed the bee pollen product contained ragweed, Alternaria,
Cladosporium, honeysuckle (Lonicera sp), privet shrub (Ligustrum sp),
and vetch (Vicia sativa) (Greenberger & Flais, 2001).
rA case report of photosensitivity was reported when a 32-year-old
woman suffered a phototoxic reaction after taking a dietary supple-
ment containing ginseng, goldenseal, bee pollen, and other ingredients.
On presentation, she had a pruritic, erythematous rash, localized to the
sun-exposed surfaces of her neck and extremities. She had no significant
past medical history and was not taking any other medications. The skin
rash slowly resolved after discontinuation of the supplement and with
treatment, including subcutaneous and topical corticosteroids. It is not
clear if this was due to the bee pollen specifically (Palanisamy, Haller,
& Olson, 2003).
rA patient developed hypereosinophilia six weeks after beginning the in-
gestion of bee pollen. Dermatological symptoms included generalized
pruritus. Evaluation revealed no other known cause for the patient’s hy-
pereosinophilia, which resolved after bee pollen ingestion was stopped
(Lin et al., 1989).
rGastrointestinal: A 34-year-old Spanish woman with a lifelong his-
tory of seasonal rhinoconjunctivitis and honey intolerance (pyrosis
and abdominal pain) developed astenia, anorexia, abdominal pain, and
diarrhoea, three weeks after starting ingestion of bee pollen. Repeated
parasitological stool studies, as well as a duodenal aspirate showed neg-
ative results. Symptoms resolved after bee pollen ingestion was stopped
(Puente et al., 1997).
rA patient developed hypereosinophilia six weeks after beginning the
ingestion of bee pollen. Gastrointestinal symptoms included nausea, ab-
dominal pain, and diarrhea. Evaluation revealed no other known cause
for the patient’s hypereosinophilia, which resolved after bee pollen in-
gestion was stopped (Lin et al., 1989).
298 JOURNAL OF DIETARY SUPPLEMENTS
rHematologic: A 34-year-old Spanish woman with a lifelong history of
seasonal rhinoconjunctivitis and honey intolerance (pyrosis and abdom-
inal pain) developed peripheral blood hypereosinophilia and elevated
serum total IgE levels three weeks after starting ingestion of bee pollen.
A duodenal biopsy showed eosinophilic infiltration of the mucosal layer.
Other causes of hypereosinophilia were not found (Puente et al., 1997).
rA patient developed hypereosinophilia (13,440 cells/mm3) six weeks
after beginning the ingestion of bee pollen. Symptoms included gener-
alized malaise, headache, nausea, abdominal pain diarrhea, generalized
pruritus, and decreased memory. Evaluation revealed no other known
cause for the patient’s hypereosinophilia, which resolved after bee pollen
ingestion was stopped (Lin et al., 1989).
rHepatic: There have been multiple cases of acute hepatitis associated
with bee pollen use. One case involved ingestion of two Tbsp of pure
bee pollen daily for several months. Another case involved the ingestion
of 14 tablets per day of a combination herbal product containing bee
pollen, chaparral, and 19 other herbs for six weeks (Shad, Chinn, &
Brann, 1999). Two additional cases of acute hepatitis have been reported.
One patient took a mixture including chaparral and bee pollen, while the
other patient took pure bee pollen (Shad et al., 1999). Chaparral has been
associated with development of acute hepatitis. In these cases, it is not
known if bee pollen or another herb might have caused the adverse event.
rNeurologic/CNS: A patient developed hypereosinophilia six weeks
after beginning the ingestion of bee pollen. Neurological symptoms
included generalized malaise, headache, and decreased memory. Evalu-
ation revealed no other known cause for the patient’s hypereosinophilia,
which resolved after bee pollen ingestion was stopped. The product
contained a mixture of entomophilous and anemophilous pollens to
which the patient was skin test positive. An open challenge with the bee
pollen later reproduced the presenting symptoms with a concomitant
rise of the eosinophil count from 207–890 cells/mm3(Lin et al., 1989).
rPulmonary/Respiratory: Three patients presented who had ingested bee
pollen and who experienced an immediate allergic reaction. Exami-
nation revealed that the bee pollen contained dandelion pollen, which
belongs to the Compositae family. In vivo and in vitro studies demon-
strated that the patients were sensitive to several Compositae family
members, rather than to insect-derived antigens. In addition, radioal-
lergosorbent inhibition studies confirmed the suspected cross-reactivity
between the health food and Compositae pollens (Cohen et al., 1979).
rAn atopic patient experienced a non-life-threatening anaphylactic reac-
tion upon initial ingestion of bee pollen (Greenberger & Flais, 2001).
Ulbricht et al. 299
Microscopic examination revealed ragweed, Alternaria, Cladosporium,
honeysuckle (Lonicera sp), privet shrub (Ligustrum sp), and vetch
(Vicia sativa) in the sample.
rA patient presented with respiratory reactions to mesquite pollen, a
major component of the bee pollen he ingested. Four other allergic
patients were known to have systemic reactions after taking bee pollen
(Mansfield & Goldstein, 1981).
Precautions/Warnings/Contraindications
rAvoid in patients with existing liver disease due to possible cases of
hepatitis.
rAvoid bee pollen in patients allergic or hypersensitive to bee pollen and
other bee products due to potential for allergic reactions and other side
effects.
rAvoid in patients with hematological disorders due to possible develop-
ment of hypereosinophilia.
rUse cautiously due to potential for containing mycotoxins, such as
ochratoxin A.
rHoney intolerance and/or bee pollen administration should be consid-
ered a cause of eosinophilic gastroenteritis.
Pregnancy & Lactation
rNot recommended due to lack of sufficient data.
INTERACTIONS
Bee Pollen/Drug Interactions
rInsufficient available evidence.
Bee Pollen/Herb/Supplement Interactions
rInsufficient available evidence.
Bee Pollen/Food Interactions
rInsufficient available evidence.
300 JOURNAL OF DIETARY SUPPLEMENTS
Bee Pollen/Lab Interactions
rLiver function tests: Bee pollen might increase alkaline phosphatase
(Alk Phos), alanine aminotransferase (ALT), aspartate aminotransferase
(AST), lactate dehydrogenase (LDH), total bilirubin, and prothrombin
time (PT) (Shad et al., 1999). Bee pollen has been associated with two
cases of acute hepatitis (Shad et al., 1999).
rWBC count: In two case reports, patients developed hypereosinophilia
three to six weeks after beginning the ingestion of bee pollen. Evaluation
revealed no other known causes for the patients’ hypereosinophilia (Lin
et al., 1989; Puente et al., 1997).
MECHANISM OF ACTION
Pharmacology
rConstituents: Bee pollen contains more amino acids and vitamins than
many other amino acid containing products like beef, eggs, or cheese.
A tablespoonful of bee pollen contains about 45 calories and is 15%
lecithin (required for normal fat metabolism) by weight (Kamen, 1991).
Bee pollen refers to the flower pollen that collects on the legs and
bodies of worker bees. It can also include amounts of nectar and bee
saliva. Bee pollen composition varies depending on plant source and
geographic region. Up to 50% of bee pollen can be made of polysaccha-
rides. The other constituents include lipids (oleic, palmitic, and linoic
acids as well as pentacosane and octacosane) (Lei et al., 2004), protein,
simple sugars, vitamin C, and carotenoids (Foster & Tyler, 1993), an-
thocyanins, phytochemicals (Paola-Naranjo et al., 2004), pyrrolizidine
alkaloids (Boppre, Colegate, & Edgar, 2005), and flavonoids such as
rutin, quercetin, myricetin, and trans-cinnamic acid as free aglycons
(Serra, Soliva, & Centelles, 2001). Furthermore, total phenols, in the
form of non-tannins have been isolated (Serra et al., 2001).
rIn blue pollen, eight different pigments were identified, the principal
anthocyanin being petunidin-3-O-rutinoside. The other pigments found
were delphinidin, cyanidin and petunidin-3-O-glucoside; delphinidin,
cyanidin, peonidin and malvidin-3-O-rutinoside and cyanidin-3-(6-
malonylglucoside) (Paola-Naranjo et al., 2004).
rAntifungal: The antifungal properties of methanol extracts of pollen
(2% and 5% concentrations) were determined on Alternaria alternata
and Fusarium oxysporium. Neither concentration completely inhibited
Ulbricht et al. 301
mycelial growth of fungi used in the experiment. Percent inhibition of
both pollen concentrations against A. alternata and F. oxysporium was
lower than 50% (Ozcan et al., 2004).
rAntiproliferative: Pollen extracts inhibit respiratory burst within cancer
cell lines probably by their antioxidant potentials (Aliyazicioglu et al.,
2005).
rImmune stimulation: In animal models, the weight and relative weight
of thymuses, cloacal bursa, and spleens of bee pollen treated animals
were higher than nontreated animals (Wang et al., 2005).
Pharmacodynamics/Kinetics
rAbsorption: Before contents of bee pollen can be digested the cell wall
must be destroyed. Theoretically, human and animal digestive systems
have difficulty destroying cell walls (Chen, 1992).
rPollen pellets taken into the gastrointestinal tract first absorb water,
swell, and then the cell walls of the individual pollens break. After the
cell walls are destroyed, the usual absorption of proteins, vitamins, and
minerals occurs. The cell walls of the pollen are not digested and pass
into the excreta (Linskens & Jorde, 1997). Experiments in dogs, rabbits,
and humans demonstrated that pollen in the 5–200 µm size range
can be absorbed directly into the blood stream. Electron microscopy
determined that 6–10 thousand pollen grains are absorbed into the
bloodstream after consumption of 100–150 g of pollen (Linskens &
Jorde, 1997).
HISTORY
rPollen has been traditionally used in Chinese medicine as a nutritive,
diuretic, and hemostatic agent. It has been recommended for treatment of
abdominal pain, amenorrhea, bloody diarrhea, dysmenorrhea, dysuria,
hematemesis, and oral sores (Leung & Foster, 1996).
rThe use of bee products for medicinal purposes is as old as beekeeping.
There are many mentions of it in Chinese texts that are 2,000 years
old, and Hippocrates also wrote about it. Honey was so valued during
Roman times that it was often used instead of gold to pay taxes.
rOf all the bee products, propolis was the most valued as a medicinal
agent. Hippocrates prescribed propolis to help heal both internal and
external sores and ulcers, and the ancient Egyptians looked upon the
bees and their propolis as the source of eternal health and life.
EVIDENCE TABLE
Condition
Study
Design
Author,
Year
N
Statistically
Significant?
Quality of
Study: 0–2
=Poor; 3–4
=Good; 5
=Excellent
Magnitude
of
Benefit ARR NNT Comments
Athletic per-
formance
enhance-
ment
Randomized
controlled
trial
Chandler &
Hawkins,
1985
46 No NA NA NA NA Randomization not
discussed in
abstract. Published in
abstract form only.
Athletic per-
formance
enhance-
ment
Case series Maughan &
Evans,
1982
20 No NA NA NA NA No effect on athletic
enhancement.
However, training
days missed due to
upper respiratory
infections were less
in the pollen group (4
days) than in the
placebo group (27
days)
Cancer
treatment
side-
effects
Randomized
controlled
trial
Murray, 1991 25 Yes 1 NA NA NA Adverse effects of
radiation were less in
the bee pollen group.
Leukocyte
concentrations were
also higher.
302
EVIDENCE DISCUSSION
Explanation of Columns in Natural Standard Evidence Table
1 2345678910
Condition Study
Design
Author,
Year
N Statistically
Signifi-
cant?
Quality of
Study: 0–2
=Poor;
3–4 =
Good; 5 =
Excellent
Magnitude of
Benefit
Absolute
Risk
Reduction
Number
Needed to
Treat
Comments
303
304 JOURNAL OF DIETARY SUPPLEMENTS
Condition:
Refers to the medical condition or disease targeted by a therapy.
Study Design:
Common types include:
rRandomized controlled trial (RCT): An experimental trial in which par-
ticipants are assigned randomly to receive either an intervention being
tested or placebo. Note that Natural Standard defines RCTs as being
placebo-controlled, while studies using active controls are classified as
equivalence trials (see below). In RCTs, participants and researchers are
often blinded (i.e., unaware of group assignments), although unblinded
and quasi-blinded RCTs are also often performed. True random allo-
cation to trial arms, proper blinding, and sufficient sample size are the
basis for an adequate RCT.
rEquivalence trial: An RCT which compares two active agents. Equiva-
lence trials often compare new treatments to usual (standard) care, and
may not include a placebo arm.
rBefore and after comparison: A study that reports only the change in
outcome in each group of a study, and does not report between-group
comparisons. This is a common error in studies that claim to be RCTs.
rCase series: A description of a group of patients with a condition, treat-
ment, or outcome (e.g., 20 patients with migraine headache underwent
acupuncture and 17 reported feeling better afterwards). Case series are
considered weak evidence of efficacy.
rCase-control study: A study in which patients with a certain outcome
are selected and compared to similar patients (without the outcome) to
see if certain risk factors/predictors are more common in patients with
that outcome. This study design is not common in the complementary
and alternative medicine literature.
rCohort study: A study which assembles a group of patients with certain
baseline characteristics (e.g., use of a drug), and follows them forward
in time for outcomes. This study design is not common in the comple-
mentary and alternative medicine literature.
rMeta-analysis: A pooling of multiple trials to increase statistical power
(often used to pool data from a number of RCTs with small sample
sizes, none of which demonstrates significance alone, but in aggregate
can achieve significance). Multiple difficulties are encountered when
Ulbricht et al. 305
designing/reviewing these analyses; in particular, outcomes measures or
therapies may differ from study to study, hindering direct comparison.
rReview: An author’s description of his or her opinion based on personal,
nonsystematic review of the evidence.
rSystematic review: A review conducted according to prespecified crite-
ria in an attempt to limit bias from the investigators. Systematic reviews
often include a meta-analysis of data from the included studies.
rP: Pending verification.
Author, Year:
Identifies the study being described in a row of the table.
N:
The total number of subjects included in a study (treatment group plus
placebo group). Some studies recruit a larger number of subjects initially,
but do not use them all because they do not meet the study’s entry criteria.
In this case, it is the second, smaller number that qualifies as N.Nincludes
all subjects that are part of a study at the start date, even if they drop out,
are lost to follow-up, or are deemed unsuitable for analysis by the authors.
Trials with a large number of dropouts that are not included in the analysis
are considered to be weaker evidence for efficacy. (For systematic reviews
the number of studies included is reported. For meta-analyses, the number
of total subjects included in the analysis or the number of studies may be
reported.) P =pending verification.
Statistically Significant?:
Results are noted as being statistically significant if a study’s authors
report statistical significance, or if quantitative evidence of significance is
present (such as pvalues). P =pending verification.
Quality of Study:
A numerical score between 0–5 is assigned as a rough measure of study
design/reporting quality (0 being weakest and 5 being strongest). This
number is based on a well-established, validated scale developed by Jadad
et al. (1996). This calculation does not account for all study elements that
306 JOURNAL OF DIETARY SUPPLEMENTS
may be used to assess quality (other aspects of study design/reporting are
addressed in the “Evidence Discussion” sections of reviews).
rA Jadad score is calculated using the seven items in the table below.
The first five items are indications of good quality, and each counts as
one point toward an overall quality score. The final two items indicate
poor quality, and a point is subtracted for each if its criteria are met. The
range of possible scores is 0 to 5.
Jadad Score Calculation
Item Score
Was the study described as randomized (this includes words such as
randomly, random, and randomization)?
0/1
Was the method used to generate the sequence of randomization described
and appropriate (table of random numbers, computer-generated, etc.)?
0/1
Was the study described as double blind? 0/1
Was the method of double blinding described and appropriate (identical
placebo, active placebo, dummy, etc.)?
0/1
Was there a description of withdrawals and dropouts? 0/1
Deduct one point if the method used to generate the sequence of
randomization was described and it was inappropriate (patients were
allocated alternately, or according to date of birth, hospital number, etc.).
0/1
Deduct one point if the study was described as double blind but the method of
blinding was inappropriate (e.g., comparison of tablet vs. injection with no
double dummy).
0/1
Magnitude of Benefit
This summarizes how strong a benefit is: small, medium, large, or
none. If results are not statistically significant “NA” for “not applicable”
is entered. In order to be consistent in defining small, medium, and large
benefits across different studies and reviews, Natural Standard defines the
magnitude of benefit in terms of the standard deviation (SD) of the outcome
measure. Specifically, the benefit is considered:
rLarge: if >1SD
rMedium: if 0.5 to 0.9 SD
rSmall: if 0.2 to 0.4 SD
Ulbricht et al. 307
P=Pending verification
In many cases, studies do not report the standard deviation of change
of the outcome measure. However, the change in the standard deviation of
the outcome measure (also known as effect size) can be calculated, and is
derived by subtracting the mean (or mean difference) in the placebo/control
group from the mean (or mean difference) in the treatment group, and
dividing that quantity by the pooled standard deviation (Effect size =
[Mean Treatment – Mean Placebo]/SDp).
Absolute Risk Reduction
This describes the difference between the percentage of people in the
control/placebo group experiencing a specific outcome (control event rate),
and the percentage of people in the experimental/therapy group experienc-
ing that same outcome (experimental event rate). Mathematically, Absolute
risk reduction (ARR) equals experimental event rate minus control event
rate. ARR is better able to discriminate between large and small treatment
effects than relative risk reduction (RRR), a calculation thatis often cited in
studies ([control event rate – experimental event rate]/control event rate).
Many studies do not include adequate data to calculate the ARR, in which
cases “NA” is entered into this column. P =pending verification.
Number Needed to Treat
This is the number of patients who would need to use the therapy under
investigation, for the period of time described in the study, in order for one
person to experience the specified benefit. It is calculated by dividing the
Absolute Risk Reduction into 1 (1/ARR). P =pending verification.
Comments
When appropriate, this brief section may comment on design flaws (in-
adequately described subjects, lack of blinding, brief follow-up, no inten-
tion to treat, etc.), notable study design elements (crossover, etc.), dosing,
and/or specifics of study group/subgroups (age, gender, etc.). More detailed
description of studies is found in the “Evidence Discussion” section that
follows the “Evidence Table” in Natural Standard reviews.
308 JOURNAL OF DIETARY SUPPLEMENTS
EVIDENCE DISCUSSION
Athletic Performance Enhancement
rSummary: Preliminary studies suggest that the use of bee pollen does
not significantly enhance athletic performance. However, well-designed
clinical trials are required before recommendations can be made in this
field.
rEvidence: No changes in objective measures of athletic performance
were reported in a group of athletes taking bee pollen for 75 days. Ath-
letic performance was evaluated in this double-blind, placebo controlled
study of 46 normal healthy adults (ages 20–42 years). All subjects in-
gested similar capsules, one of which contained granulated brown sugar,
the other 400 mg bee pollen. Six tests were administered before and af-
ter the 75-day administration period. These tests were VO2max, forced
vital capacity, forced expiratory volume in 1 s (FEV1), grip strength, per-
cent body fat, and body weight. No statistically significant differences
were noted in scores (Chandler & Hawkins, 1985).
rThe effects of a six-week course of pollen extract administration were
investigated on a variety of physiological parameters in a group (N=
20) of adolescent swimmers. At the time of the study, all subjects were
training on a daily basis. During the course of the study, maximum
oxygen uptake increased in both the treatment group and the placebo
group. There were no differences between the responses of the two
groups. Vital capacity showed a significant increase in the treatment
group, but not in the placebo group. The number of training days missed
due to upper respiratory tract infections was less in the pollen treatment
group (4 days) than in the placebo group (27 days). It was suggested
that if the study had been of longer duration, this may have resulted in
an improved performance by the pollen treatment group due to fewer
interruptions to training (Maughan & Evans, 1982).
Cancer Treatment Side-Effects
rSummary: In a preliminary study, bee pollen was found to reduce some
adverse effects of cancer treatment. Well-designed clinical trials are
required before recommendations can be made in this field.
rEvidence: Bee pollen was effective in reducing adverse effects of cancer
treatment in a double-blind, placebo controlled study of 25 women with
inoperable uterine cancer. The stresses and adverse effects of radiation,
Ulbricht et al. 309
such as anorexia, nausea, alopecia, inflammation, and sleeplessness were
less in the bee pollen group. Leukocyte concentrations were also higher
(Murray, 1991).
Memory
rSummary: In a preliminary study, bee pollen, as part of multiplant ther-
apy, was not found to increase memory in an elderly group of subjects.
Well-designed clinical trials are required before recommendations can
be made in this field.
rEvidence (combination study): No significant effects on memory, as
determined by Wechsler Memory Scale scores, were noted in a three
month, double-blind, placebo controlled, cross-over study of 100 elderly
Danish volunteers taking NaO Li Su (a Chinese remedy which contains
bee pollen as well as radix polygoni multiflore, semem ziziphi spinosae,
radix salviae multiorhizae, fructus schisandrae, and fructus ligustris
lucidae) (Iversen et al., 1997).
Multiple Sclerosis
rSummary: In a preliminary study, bee pollen, as part of multi-bee
product therapy, was found to decrease symptoms of multiple sclerosis.
Well-designed clinical trials are required before recommendations can
be made in this field.
rEvidence (combination study): Apitherapy (including bee venom, bee
pollen, and honey) improved symptoms in 92 patients with multiple
sclerosis (MS). Three 20-day courses of bee venom 4.5 mg daily was
administered over one year. Honey 30 g twice daily (orally) was admin-
istered with bee pollen 10 g daily for six months. No other therapy was
given. The forms of MS in this group were cerebrospinal (70 patients)
and cerebellar (22 patients). Stage I to II patients represented 72.8%
and stage III to IV patients were 27.2%. Clinical improvement was seen
in 100% of patients and 72.8% of disabled patients were able to return
to work (Krivopalov-Moscvin, 1997). In this study the criteria used to
determine clinical improvement and improvement type were not cited
and no control group was mentioned.
Brands Used in Human Studies
rNot applicable.
310 JOURNAL OF DIETARY SUPPLEMENTS
Brands Shown to Contain Claimed Ingredients Through Third-Party
Testing
rNot applicable.
U.S. Equivalents of Most Commonly Recommended European Brands
rNot applicable.
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  • ... The uses of bee pollen in the management of OA have been less explored but are not less important. Three mechanisms may explain the usefulness of this product in the management of the disease: its antioxidant effect, nutritional value provided by pollen, and its immunoregulatory effect [70]. ...
    Article
    Osteoarthritis is one of the most common rheumatic disease in the world and one of the leading causes of disability in the elderly. There is still no curative management for the disease, so the search for new therapeutic alternatives continues. -Apitherapy is a therapeutic tool based on the use of beehive products used since ancient times and, at present, their mechanism of action begins to be known. Many of the mechanisms of action of the beehive products are useful for chronic articular pathophysiological processes such as those described in osteoarthritis. This article presents a review of the current state of understanding of the mechanisms through which bee venom, propolis, honey, pollen, and royal jelly may act on osteoarthritis. © 2020 S. Karger AG, Basel.
  • ... Pollen, a powdery compound produced by the male part of a flower, has been considered a tonic and rejuvenator since ancient times, and evidence of its uses are reported in the Bible and in ancient Egyptian texts (Campos, Frigerio, Lopes, & Bogdanov, 2010;Ulbricht et al., 2009). In Traditional Chinese Medicine, pollen is mainly prescribed as a remedy for malnutrition, alcohol intoxication, skin diseases, and other disorders (Ulbricht et al., 2009). ...
    Article
    Pollen has been used for centuries as a tonic and a multipurpose remedy in traditional medicine. The present umbrella review aims to qualitatively assess the therapeutic efficacy of orally administered pollen in the management of nonallergic diseases. MEDLINE via PubMed, Embase, Scopus, Web of Science, CINAHL, Cochrane Library, and Google Scholar were systematically searched for relevant systematic reviews and meta‐analyses. Articles were independently screened and selected, then quality of evidence of included studies was evaluated with a dedicated NIH tool. Retrieved evidence was critically appraised and discussed. Two hundred four articles were found and, after selection process, five systematic reviews were included in the present work, including one with a meta‐analysis. Evidence from these reviews supports the use of grass pollen extracts for symptomatic benign prostatic hyperplasia (BPH) and chronic prostatitis (CP). Additional preliminary evidence on the topic indicates the potential use of grass pollen extracts for vasomotor symptoms in women. Overall, results of the present review suggest that flower pollen extracts may be useful as a complementary remedy for the management of BPH, CP, and vasomotor symptoms. Evidence regarding bee pollen is too limited to draw any conclusion on its clinical efficacy. Further studies are needed.
  • ... [31] In contrast, there have also been studies that did not support the effects of bee-pollen on exercise. [32] We therefore hypothesized that feeding of multiple transportable carbohydrate source 30 min before exercise would result in delayed fatigue and improved 1500 meters running capacity compared with placebo. In this study, it was aimed at whether there is a beneficial outcome of honey supplementation formula on runners' performance and fatigue parameters. ...
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    Full-text available
    Background: Honey, royal jelly, and bee-pollen are promoted as nutraceuticals that have numerous nutritional and therapeutic properties with a capability of endurance athletic performance enhancement. Objective: The study aimed to evaluate the effect of honey supplementation formula on runners' performance and fatigue parameters. Subjects: Fifty male runners, members of the Egyptian Athletic Federation (EAF), were recruited to perform two study groups; one with intervention with the honey drink for one week before and after running and the second group was running without using the honey drink (placebo). Systolic and diastolic blood pressures, pulse rate, blood glucose, blood lactic acid concentration, creatine kinase-muscle/brain (CK-MB), and Lactate dehydrogenase (LDH) were measured before and after running. Results: No significant baseline intergroup differences were observed while there were significant changes were detected in both groups in all parameters investigated according to the pre-and post-exercise intragroup comparison. Blood lactic acid concentration was higher among the honey group than the placebo (19.50 ± 3.78 vs 11.0 ± 3.83 mmol/L, respectively) as well as LDH (311.30 ± 55.40 vs 242.0 ± 20.98 U/L, respectively). However, it can be explained by the insignificant faster race finishing time of the honey group than the placebo group (5.01 ± 0.24 vs 5.16 ± 0.11 minutes, respectively, (p = 0.221). The blood glucose was enormously higher among the athletes who ingested honey than who took placebo only (139.68 ± 37.76 vs 81.40 ± 7.43 mg/dl, respectively). While, there was no statistical difference in the blood pressure, either systolic or diastolic, and CK-MB between both groups. Conclusions: Acute ingestion of honey drink mixed with royal jelly and bee-pollen before running is ergogenic and plays a beneficial role in enhancing running performance.
  • ... Bal; bitki nektarlarının, bitkilerin canlı kısımlarının salgılarının veya bitkilerin canlı kısımları üzerinde yaşayan bitki emici böceklerin salgılarının bal arısı Apis mellifera tarafından toplandıktan sonra kendine özgü maddelerle birleştirerek değişikliğe uğrattığı, su içeriğini düşürdüğü ve petekte depolayarak olgunlaştırdığı doğal bir üründür (61). Bal tarihte uzun zamandır bir besin olma yanında şifalı özelliğiyle de ilaç gibi kullanılmaktadır. ...
  • ... The health benefits associated with bee pollen are related to the presence of compounds with the biological potential to inhibit the growth of microorganisms and aid in the prevention of oxidative stress, identified as one of the causes of the development of chronic degenerative diseases such as cancer, cardiovascular diseases, and neuronal degeneration (Uttara et al. 2009). Commonly, this food is consumed as a rejuvenator or tonic, to increase physical resistance, and to help in the treatment of respiratory infirmities, hormonal disturbances, and in the prevention of cancer, though current research is insufficient to validate all of these indications (Ulbricht et al. 2009). ...
    Chapter
    Bee pollen is an apiculture product that contains bioactive compounds with antioxidant, antibacterial and antitumor potential. Many studies suggest that phenolic compounds are the main active agents of this product, but not the only ones. In this chapter, both the compounds and their biological potential are presented, considering the influence of the botanical origin and other factors, such as beekeeping practices, on these parameters. Most of the researchers carried out in vitro studies, mainly regarding the antibacterial and antioxidant activity of bee pollen; however, in vivo studies were also carried out and these will also be approached.
  • ... In pediatric (age < 18) available evidence for determining of bee pollen dosage is insufficient. 77 Therefore, it seems very difficult to determine the effective dose of bee pollen intake and bee pollen combination for each disorder so further in vivo experiments and clinical trials are needed to determine the doses and compositions of bee pollen for consumption in each disease. ...
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    Bee pollen grains, as the male reproductive part of seed-bearing plants contain considerable concentrations of various phytochemicals and nutrients. Since antiquity, people throughout the world used pollens to cure colds, flu, ulcers, premature aging, anemia and colitis. It is now well-documented that some bee pollen secondary metabolites (e.g. flavonoid) may have positive health effects. In recent years, the flavonoids have attracted much interest because of their wide range of biological properties and their beneficial effects on human health. The current review, points out potential therapeutic effects of bee pollen flavonoids as one of the main bee pollen bioactive compounds in allergic and immunological diseases. Due to the fact that some types of flavonoid components in bee pollen have anti-allergic, anti-oxidant and anti-inflammatory properties, bee pollen flavonoids can be excellent candidates for future studies including phytotherapy, molecular pharmacology and substitutes for chemicals used in treating allergic and immunological disorders.
  • ... According to a recent report, the average proportions of the main ingredients in air-dried pollen are 32.8% proteins (including 11.5% essential amino acids), 40.7% reducing sugars, 12.8% lipids, 0.19% vitamin C, 0.07% β-carotene, and 4.0% bioelements [10]. Bee pollen is considered a highly balanced nutrient and has been used for allergies, antibacterial and antifungal effects, appetite stimulation, arthritis, benign prostatic hypertrophy, colitis, diuretic dysentery, eczema, immunomodulation, memory, skin care, and weight loss [22]. ...
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    Bee pollen is produced by honeybees and is considered one of the most balanced and nourishing nutritional supplements available. Historically, bee pollen has been prescribed for its healing properties and consumed for its high-energy supply. Recent research has provided evidence that bee pollen has diverse biological activities, such as anti-oxidant, anti-inflammatory, anti-bacterial, and even anti-cancer effects. However, the outer membrane of the pollen grain, exine, is highly resistant to most acidic solutions, high pressure, and even digestive enzymes, and the resulting low bioavailability limits its nutritional and clinical applications. This study applied a wet-grinding method to destroy the exine effectively, and it then examined the pollen`s enhanced biological activity. First, microscopic observations provided strong evidence that wet grinding destroyed the exine time-dependently. In addition, the content of polyphenols, well-known ingredients of bee pollen and used as internal standards for the quality control of commercial pollen preparations, increased up to 11-fold with wet grinding. Further, the anti-oxidant activity demonstrated on the ABTS anti-oxidant assay, as well as the DPPH radical scavenging assay, was also dramatically increased. Together, the results presented here support a new technology by which bee pollen can be used as a resource for medical, nutritional, and cosmetic applications.
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    Contamination with sanitary microorganisms from Enterobacteriaceae, Pseudomonadaceae, Staphylococcaceae, Micrococcaceae and Bacillaceae families in flower bee pollen from Bulgaria after one-year vacuum-packed cold storage has been found. Dried flower bee pollens intended for human consumption were with high incidence rate of contamination with Pantoea sp. (P. agglomerans and P. agglomerans bgp6) (100%), Citrobacter freundii (47%), Proteus mirabilis (31.6%), Serratia odorifera (15.8%) and Proteus vulgaris (5.3%). Bee pollens were also positive for the culture of microorganisms from Staphylococcaceae, Micrococcaceae and Bacillaceae families: Staphylococcus hominis subsp hominis, Staphylococcus epidermidis, Arthrobacter globiformis, Bacillus pumilis, Bacillus subtilis and Bacillus amyloliquefaciens. It was concluded that, if consumed directly, the vacuum-packed cold stored dried bee pollen, harvested according hygienic requirements from bee hives in industrial pollution-free areas without intensive crop production, is not problem for healthy human. © 2016, Chonnam National University Medical School. All rights reserved.
Literature Review