|
.
PEER REVIEWED
The Moringa tree ( Moringa oleifera) has been praised for its nutritional and medicinal properties, and many claims have been made regarding its benefits. This first in a series of brief reviews looks at the published scientific evidence on this tree.
PEER REVIEWED
Moringa
appears to be a nutritional and medicinal cornucopia. The author, a
Western-trained nutritional biochemist who has studied some of Moringa’s
phytochemicals for almost a decade, gives a brief commentary and extensive
references, and presents a table introducing some of the tree’s most intriguing
features. This is the first article in a series, and will be followed by more
detailed analysis of some of the strongest claims made regarding this edible
plant.
Abstract
Moringa oleifera, or the horseradish
tree, is a pan-tropical species that is known by such regional names as
benzolive, drumstick tree, kelor, marango, mlonge, mulangay, nébéday, saijhan,
and sajna. Over the past two decades, many reports have appeared in mainstream
scientific journals describing its nutritional and medicinal properties. Its
utility as a non-food product has also been extensively described, but will not
be discussed herein, (e.g. lumber, charcoal, fencing, water clarification, lubricating
oil). As with many reports of the nutritional or medicinal value of a natural
product, there are an alarming number of purveyors of “healthful” food who are
now promoting M. oleifera as a panacea. While much of this recent
enthusiasm indeed appears to be justified, it is critical to separate rigorous
scientific evidence from anecdote. Those who charge a premium for products
containing Moringa spp. must be held to a high standard. Those who
promote the cultivation and use of Moringa spp. in regions where hope is
in short supply must be provided with the best available evidence, so as not to
raise false hopes and to encourage the most fruitful use of scarce research
capital. It is the purpose of this series of brief reviews to: (a) critically evaluate
the published scientific evidence on M. oleifera, (b) highlight claims
from the traditional and tribal medicinal lore and from non-peer reviewed
sources that would benefit from further, rigorous scientific evaluation, and
(c) suggest directions for future clinical research that could be carried out
by local investigators in developing regions.
This is the first of four planned papers on
the nutritional, therapeutic, and prophylactic properties of Moringa oleifera.
In this introductory paper, the scientific evidence for health effects are
summarized in tabular format, and the strength of evidence is discussed in very
general terms. A second paper will address a select few uses of Moringa in
greater detail than they can be dealt with in the context of this paper. A
third paper will probe the phytochemical components of Moringa in more
depth. A fourth paper will lay out a number of suggested research projects
that can be initiated at a very small scale and with very limited resources, in
geographic regions which are suitable for Moringa cultivation and
utilization. In advance of this fourth paper in the series, the author
solicits suggestions and will gladly acknowledge contributions that are
incorporated into the final manuscript. It is the intent and hope of the
journal’s editors that such a network of small-scale, locally executed
investigations might be successfully woven into a greater fabric which will
have enhanced scientific power over similar small studies conducted and
reported in isolation. Such an approach will have the added benefit that
statistically sound planning, peer review, and multi-center coordination brings
to a scientific investigation.
The following paper is intended to be useful
for both scientific and lay audiences. Since various terms used herein are
likely not familiar to the lay reader, nor are many of the references readily
available to either scientific or lay audiences, we encourage active on-line
dialog between readers and both the author and the journal staff. Both will
attempt to answer questions and to direct readers to the experts in an open and
public manner.
Introduction
Moringa oleifera is the most widely cultivated species of a
monogeneric family, the Moringaceae, that is native to the sub-Himalayan tracts
of India, Pakistan, Bangladesh and Afghanistan. This rapidly-growing
tree (also known as the horseradish tree, drumstick tree, benzolive tree,
kelor, marango, mlonge, moonga, mulangay, nébéday, saijhan, sajna or Ben oil
tree), was utilized by the ancient Romans, Greeks and Egyptians; it is now
widely cultivated and has become naturalized in many locations in the tropics.
It is a perennial softwood tree with timber of low quality, but which for
centuries has been advocated for traditional medicinal and industrial uses. It
is already an important crop in India, Ethiopia, the Philippines and the Sudan, and is being grown in West, East and South Africa, tropical Asia, Latin America, the Caribbean, Florida and the Pacific Islands. All parts of the
Moringa tree are edible and have long been consumed by humans. According to
Fuglie (47) the many uses for Moringa include: alley cropping (biomass production), animal forage (leaves and treated seed-cake), biogas (from leaves), domestic cleaning agent (crushed leaves), blue dye (wood), fencing (living
trees), fertilizer (seed-cake), foliar nutrient (juice expressed from the
leaves), green manure (from leaves), gum (from tree trunks), honey- and sugar
cane juice-clarifier (powdered seeds), honey (flower nectar), medicine (all
plant parts), ornamental plantings, biopesticide (soil incorporation of leaves
to prevent seedling damping off), pulp (wood), rope (bark), tannin for tanning
hides (bark and gum), water purification (powdered seeds). Moringa seed oil
(yield 30-40% by weight), also known as Ben oil, is a sweet non-sticking,
non-drying oil that resists rancidity. It has been used in salads, for fine
machine lubrication, and in the manufacture of perfume and hair care products (158). In the West, one of the best known uses for Moringa is the use of powdered seeds to flocculate contaminants and purify drinking water (11,50,113), but the seeds are also eaten green, roasted, powdered and steeped for tea or used in curries (50). This tree has in recent times been advocated as an outstanding indigenous source of highly digestible protein, Ca, Fe, Vitamin C, and carotenoids suitable for utilization in many of the so-called “developing” regions
of the world where undernourishment is a major concern.
Nutrition
Moringa trees have been used to combat
malnutrition, especially among infants and nursing mothers. Three
non-governmental organizations in particular—Trees for Life, Church World
Service and Educational Concerns for Hunger Organization—have advocated Moringa
as “natural nutrition for the tropics.” Leaves can be eaten fresh,
cooked, or stored as dried powder for many months without refrigeration, and
reportedly without loss of nutritional value. Moringa is especially promising
as a food source in the tropics because the tree is in full leaf at the end of
the dry season when other foods are typically scarce.
A large number of reports on the nutritional
qualities of Moringa now exist in both the scientific and the popular
literature. Any readers who are familiar with Moringa will recognize the
oft-reproduced characterization made many years ago by the Trees for Life
organization, that “ounce-for-ounce, Moringa leaves contain more Vitamin A than
carrots, more calcium than milk, more iron than spinach, more Vitamin C than
oranges, and more potassium than bananas,” and that the protein quality of
Moringa leaves rivals that of milk and eggs. These readers will also recognize
the oral histories recorded by Lowell Fuglie in Senegal and throughout West Africa, who reports (and has
extensively documented on video) countless instances of lifesaving nutritional
rescue that are attributed to Moringa (47,48). In fact, the nutritional properties of Moringa are now so well known that there seems to be little doubt of the substantial health benefit to be realized by consumption of Moringa leaf powder in situations where
starvation is imminent. Nonetheless, the outcomes of well controlled and well
documented clinical studies are still clearly of great value.
In many cultures throughout the tropics,
differentiation between food and medicinal uses of plants (e.g. bark, fruit,
leaves, nuts, seeds, tubers, roots, flowers), is very difficult since plant
uses span both categories and this is deeply ingrained in the traditions and
the fabric of the community (85). Thus, Table 1 in this review captures both nutritional and medicinal references as they relate to Moringa, whilst avoiding most of the better known agro-forestry and water purification applications of this plant.
The interested reader is also directed to the very comprehensive reviews of the
nutritional attributes of Moringa prepared by the NGOs mentioned earlier (in
particular, see references 47,123,157).
Phytochemistry
Phytochemicals are, in the strictest sense of
the word, chemicals produced by plants. Commonly, though, the word refers to
only those chemicals which may have an impact on health, or on flavor, texture,
smell, or color of the plants, but are not required by humans as essential
nutrients. An examination of the phytochemicals of Moringa species affords the
opportunity to examine a range of fairly unique compounds. In particular, this
plant family is rich in compounds containing the simple sugar, rhamnose, and it
is rich in a fairly unique group of compounds called glucosinolates and
isothiocyanates (10,38). For example, specific components of Moringa preparations that have been reported to have hypotensive, anticancer, and antibacterial activity include 4-(4'-O-acetyl-a-L-rhamnopyranosyloxy)benzyl isothiocyanate [1],
4-(a-L-rhamnopyranosyloxy)benzyl isothiocyanate [2], niazimicin [3],
pterygospermin [4], benzyl isothiocyanate [5], and 4-(a-L-rhamnopyranosyloxy)benzyl
glucosinolate [6]. While these compounds are relatively unique to the
Moringa family, it is also rich in a number of vitamins and minerals as well as
other more commonly recognized phytochemicals such as the carotenoids
(including b-carotene or
pro-vitamin A). These attributes are all discussed extensively by Lowell Fuglie (47) and others, and will be the subject of a future review in this series.
(Click to enlarge)
Figure 1. Structures
of selected phytochemicals from Moringa spp.: 4-(4'-O-acetyl-a-L-rhamnopyranosyloxy)benzyl
isothiocyanate [1], 4-(-L-rhamnopyranosyloxy)benzyl isothiocyanate [2],
niazimicin [3], pterygospermin [4], benzyl isothiocyanate [5],
and 4-(a-L-rhamnopyranosyloxy)benzyl glucosinolate [6].
Disease Treatment and Prevention
The benefits for the treatment or prevention
of disease or infection that may accrue from either dietary or topical
administration of Moringa preparations (e.g. extracts, decoctions, poultices,
creams, oils, emollients, salves, powders, porridges) are not quite so well
known (116). Although the oral history here is also voluminous, it has been subject to much less intense scientific scrutiny, and it is useful to review the claims that have been made and to assess the quality of evidence
available for the more well-documented claims. The readers of this review are
encouraged to examine two recent papers that do an excellent job of contrasting
the dilemma of balancing evidence from complementary and alternative medicine
(e.g. traditional medicine, tribal lore, oral histories and anecdotes) with the
burden of proof required in order to make sound scientific judgments on the
efficacy of these traditional cures (138,154). Clearly much more research is justified, but just as clearly this will be a very fruitful field of endeavor for both basic and applied researchers over the next decade.
Widespread claims of the medicinal effectiveness
of various Moringa tree preparations have encouraged the author and his
colleagues at The Johns Hopkins University to further investigate some of these
possibilities. A plethora of traditional medicine references attest to its
curative power, and scientific validation of these popular uses is developing
to support at least some of the claims. Moringa preparations have been cited in
the scientific literature as having antibiotic, antitrypanosomal, hypotensive,
antispasmodic, antiulcer, anti-inflammatory, hypocholesterolemic, and
hypoglycemic activities, as well as having considerable efficacy in water
purification by flocculation, sedimentation, antibiosis and even reduction of
Schistosome cercariae titer (see Table 1).
Unfortunately, many of these reports of
efficacy in human beings are not supported by placebo controlled, randomized
clinical trials, nor have they been published in high visibility journals. For
example, on the surface a report published almost 25 years ago (141) appears to
establish Moringa as a powerful cure for urinary tract infection, but it provides
the reader with no source of comparison (no control subjects).
Thus, to the extent to which this is antithetical to Western medicine, Moringa
has not yet been and will not be embraced by Western-trained medical practitioners
for either its medicinal or nutritional properties.
In many cases, published in-vitro
(cultured cells) and in-vivo (animal) trials do provide a degree of
mechanistic support for some of the claims that have sprung from the
traditional medicine lore. For example, numerous studies now point to the
elevation of a variety of detoxication and antioxidant enzymes and biomarkers
as a result of treatment with Moringa or with phytochemicals isolated from
Moringa (39,40,76,131). I shall briefly introduce antibiosis and cancer prevention as just two examples of areas of Moringa research for which the existing scientific evidence appears to be particularly strong.
Antibiotic Activity. This is clearly the
area in which the preponderance of evidence—both classical scientific and
extensive anecdotal evidence—is overwhelming. The scientific evidence has now
been available for over 50 years, although much of it is completely unknown to
western scientists. In the late 1940’s and early 1950’s a team from the
University of Bombay (BR Das), Travancore University (PA Kurup), and the
Department of Biochemistry at the Indian Institute of Science in Bangalore (PLN
Rao), identified a compound they called pterygospermin [4] a compound
which they reported
readily dissociated into two molecules of benzyl
isothiocyanate [5] (23,24,25,26,77,78,79,80,81,108). Benzyl isothiocyanate was already understood at that time to have antimicrobial properties. This group not only identified pterygospermin, but performed extensive and elegant characterization of its mode of
antimicrobial action in the mid 1950’s. (They identified the tree from which
they isolated this substance as “Moringa pterygosperma,” now regarded as
an archaic designation for “M. oleifera.”) Although others were to
show that pterygospermin and extracts of the Moringa plants from which it was
isolated were antibacterial against a variety of microbes, the identity of
pterygospermin has since been challenged (34) as an artifact of isolation or structural determination.
Subsequent elegant and very thorough work,
published in 1964 as a PhD thesis by Bennie Badgett (a student of the well
known chemist Martin Ettlinger), identified a number of glyosylated derivatives
of benzyl isothiocyanate [5] (e.g. compounds containing the 6-carbon
simple sugar, rhamnose) (8). The identity of these compounds was not available in the refereed scientific literature until “re-discovered” 15 years later by Kjaer and co-workers (73). Seminal reports on the antibiotic activity of the primary rhamnosylated compound then followed, from U Eilert and colleagues in Braunschweig, Germany (33,34). They re-isolated and confirmed the identity of 4-(a-L-rhamnopyranosyloxy)benzyl
glucosinolate [6] and its cognate isothiocyanate [2] and verified
the activity of the latter compound against a wide range of bacteria and
fungi.
Extensive field reports and ecological studies
(see Table 1) forming part of a rich traditional medicine history, claim
efficacy of leaf, seed, root, bark, and flowers against a variety of dermal and
internal infections. Unfortunately, many of the reports of antibiotic efficacy
in humans are not supported by placebo controlled, randomized clinical trials.
Again, in keeping with Western medical prejudices, practitioners may not be
expected to embrace Moringa for its antibiotic properties. In this case,
however, the in-vitro (bacterial cultures) and observational studies
provide a very plausible mechanistic underpinning for the plethora of efficacy
claims that have accumulated over the years (see Table 1).
Aware of the reported antibiotic activity of [2],
[5], and other isothiocyanates and plants containing them, we undertook
to determine whether some of them were also active as antibiotics against Helicobacter
pylori. This bacterium was not discovered until the mid-1980’s, a
discovery for which the 2005 Nobel Prize in Medicine was just awarded. H. pylori
is an omnipresent pathogen of human beings in medically underserved areas of
the world, and amongst the poorest of poor populations worldwide. It is a
major cause of gastritis, and of gastric and duodenal ulcers, and it is a major
risk factor for gastric cancer (having been classified as a carcinogen by the
W.H.O. in 1993). Cultures of H. pylori, it turned out, were
extraordinarily susceptible to [2], and to a number of other
isothiocyanates (37,60). These compounds had antibiotic activity against H. pylori at concentrations up to 1000-fold lower than those which had been used in earlier studies against a wide range of bacteria and fungi. The extension of
this finding to human H. pylori infection is now being pursued in the
clinic, and the prototypical isothiocyanate has already demonstrated some
efficacy in pilot studies (49,168).
Cancer Prevention. Since Moringa species have long been
recognized by folk medicine practitioners as having value in tumor therapy (61), we examined compounds [1] and [2] for their cancer preventive potential (39). Recently, [1] and the related compound [3] were shown to be potent inhibitors of phorbol ester (TPA)-induced Epstein-Barr virus early antigen
activation in lymphoblastoid (Burkitt’s lymphoma)
cells (57,104). In one of these studies, [3] also inhibited tumor promotion in a mouse two-stage DMBA-TPA tumor model (104). In an even more recent study, Bharali and colleagues have examined skin tumor prevention following ingestion of drumstick (Moringa seedpod) extracts (12). In this mouse model, which included appropriate positive and negative controls, a dramatic reduction in skin papillomas was demonstrated.
Thus, traditional practice has long suggested that cancer
prevention and therapy may be achievable with native plants. Modern
practitioners have used crude extracts and isolated bioactive compounds. The
proof required by modern medicine has not been realized because neither the
prevention of cancer nor the modification of relevant biomarkers of the
protected state has been adequately demonstrated in human subjects. Does this
mean that it doesn’t work? No. It may well work, but more rigorous study is
required in order to achieve a level of proof required for full biomedical
endorsement of Moringa as, in this case, a cancer preventative plant.
Acknowledgements
I thank Dr. Mark Olson for his encouragement and collaboration early in
my research involvement with Moringa (joint publications are still
pending). I gratefully acknowledge the Lewis B. and Dorothy Cullman
Foundation for providing unrestricted research funds that facilitated
preparation of this review and work on Moringa in my laboratory; funding
was also provided by the American Institute for Cancer Research and the
NCI (Grant # R01 CA93780).
Table 1. Reported
nutritional, therapeutic & prophylactic uses of Moringa oleifera
Traditional Use
Condition/Effecta
|
Plant Partb
|
Referencesc
|
ANT Antimicrobial / Biocidal
|
LFSPRBGO
|
8, 13,
19, 24, 27, 31, 34, 64, 68, 100, 104, 114, 115, 126, 140, 151, 160, 161, 162
|
|
|
|
Bacterial
|
LFS
|
25, 26,
55, 63, 77-81, 149
|
Urinary Tract Infection
|
L
|
141
|
Typhoid
|
G
|
47
|
Infection
|
LF
|
47
|
Syphilis
|
G
|
47
|
Dental Caries/Toothache
|
RBG
|
47
|
|
|
|
Fungal/
Mycoses
|
O
|
111
|
Thrush
|
|
88, 111
|
|
|
|
Viral
|
|
|
Common cold
|
FRB
|
47
|
Epstein-Barr Virus (EBV)
|
L
|
104
|
Herpes Simplex Virus (HSV-1)
|
L
|
84
|
HIV-AIDS
|
L
|
1, 124
|
Warts
|
S
|
47
|
|
|
|
Parasites
|
|
|
Dranunculiasis (guinea-worm)
|
|
36
|
Helminths
|
LFP
|
47
|
Schistosomes
|
S
|
113
|
Trypanosomes
|
LR
|
95
|
|
|
|
Other /
Not Attributed to a Specific Pathogen
|
|
|
Skin
(Dermal)
|
O S
|
15
|
Hepatic
|
L
|
6
|
Fever
|
LRGS
|
47
|
Earache
|
G
|
47
|
External Sores/Ulcers
|
LFRB
|
15
|
Bronchitis
|
L
|
47
|
Throat Infection
|
F
|
47
|
Water treatment (general)
|
S
|
11, 50,
75, 86, 169
|
|
|
|
AST Asthma
|
RG
|
47
|
|
|
|
CAN Cancer Therapy / Protection
|
LFPBS
|
12, 17,
28, 39, 45, 59, 61, 64, 104, 115
|
Anti-tumor
|
LFSB
|
45, 48,
57, 61, 87
|
Prostate
|
L
|
47, 48
|
Radioprotective
|
L
|
132
|
Skin
|
P
|
12
|
|
|
|
CIR Circulatory/Endocrine Disorders
|
LFSPR
|
56, 93
|
Anti-anemic
|
L
|
47, 125
|
Anti-hypertensive
|
LP
|
40, 41,
42, 43, 44, 53, 83, 137
|
Cardiotonic
|
R
|
47
|
Diabetes/hypoglycemia
|
LP
|
6, 45,
71, 87, 101, 167
|
Diuretic
|
LFRG
|
6, 14,
62
|
Hypocholestemia
|
L
|
52, 94
|
Thyroid
|
L
|
153
|
Tonic
|
F
|
47
|
Hepatorenal
|
LR
|
93, 120
|
|
|
|
DET Detoxification
|
BO
|
76, 135,
166
|
Antipyretic
|
|
148
|
Purgative
|
O
|
47
|
Snakebite
|
B
|
47
|
Scorpion-bite
|
B
|
47
|
|
|
|
DIG Digestive Disorders
|
LSRBG
|
53
|
For
TRTMNT of:
|
|
|
Colitis
|
LB
|
47
|
Diarrhea
|
LR
|
47, 62,
64
|
Digestif
|
B
|
47
|
Dysentery
|
LG
|
47
|
Flatulence
|
R
|
47
|
Ulcer / Gastritis
|
LS
|
3, 115,
136
|
|
|
|
INF Inflammation
|
LFSPRG
|
14, 28,
35, 45, 62, 64, 68, 110, 131, 160, 161
|
Rheumatism
|
LFSPRG
|
28
|
Joint Pain
|
P
|
47
|
Edema
|
R
|
47
|
Arthritis
|
S
|
47
|
|
|
|
IMM Immunity
|
SO
|
69
|
Immune-stimulant
|
S
|
69
|
Lupus
|
O
|
28
|
|
|
|
NER Nervous Disorders
|
LFRBGO
|
58, 59,
62, 96
|
Anti-spasmodic
|
SR
|
14, 53
|
Epilepsy
|
RB
|
47
|
Hysteria
|
FRBO
|
47
|
Headache
|
LRBG
|
47
|
|
|
|
NUT Nuritional
|
LSBO
|
6, 7,
18, 22, 28, 30, 31, 32, 46, 47, 48, 51, 65, 66, 67, 70, 92, 102, 112, 116, 133,
163
|
|
|
|
Antinutritional
factors
|
B
|
88, 89,
90, 110, 127, 128, 139, 156, 164, 165
|
Antioxidant
|
LO
|
110, 147
|
Carotenoids
|
L
|
29, 105,
152
|
Energy
|
LSO
|
85
|
Goitrogen
|
S
|
2
|
Iron
deficiency
|
LS
|
16
|
Oil
quality
|
O
|
5, 98,
110, 158, 159
|
Protein
|
LS
|
47
|
Vitamin/Mineral deficiency
|
LS
|
7, 9,
54, 56, 85, 119
|
|
|
|
REP Reproductive Health
|
LFPRBGO
|
44, 53,
64, 121, 122
|
Abortifacient
|
FRBG
|
106, 107,
155
|
Aphrodisiac
|
RB
|
47
|
Birth Control
|
B
|
45, 53,
142-146
|
Lactation Enhancer
|
L
|
47
|
Prostate function
|
O
|
47
|
|
|
|
SKI Skin Disorders
|
LRSG
|
160, 161
|
Antiseptic
|
L
|
47
|
Astringent
|
R
|
47
|
Pyodermia
|
S
|
15
|
Rubefacient
|
RG
|
47
|
Vesicant
|
R
|
47
|
|
|
|
GEN General Disorders/Conditions
|
LFSPRBO
|
4, 6,
8, 20, 21, 45, 48, 64, 66, 67, 68, 73, 74, 82, 91, 92, 99, 102, 103, 109, 116,
117, 118, 123, 125, 128, 129, 130, 134, 150, 163
|
Bladder
|
OS
|
47
|
Catarrh
|
LF
|
47
|
Gout
|
RO
|
47
|
Hepatamegaly
|
R
|
47
|
Lactation
|
L
|
47
|
Low.Back/Kidney Pain
|
R
|
47
|
Scurvy
|
LSRBO
|
47
|
Splenomegaly
|
R
|
47
|
“Tonic”
|
LFPSO
|
47
|
a |
It is very difficult in some cases to separate the effects of
severe nutritional deficiencies (e.g. Vitamin C) from sequelae (e.g. scurvy)
which transcend categorization by organ systems or classification into single
disease states. |
b |
Plant parts are designated by their first letters (in
bold): |
|
Leaves
Flowers
Seeds
Pods (drumsticks)
Roots
Bark
Gum
Oil (from seeds)
|
c |
Many of the original citations have been collected by
Lowell J. Fuglie, [and can be found in his excellent treatise entitled The
Miracle Tree, (47)] and by Manuel Palada (116), Julia Morton (102), and Trees For Life (157). Most other
compendiums in recent publications or on commercial websites appear to be highly derivative of these seminal works. |
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(3-letter
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