J. Soc. CosmeticChemists,19, 173-185 (Mar. 4, 1968)
Baldness
in Nonhuman
WILLIAM
MONTAGNA,
Primates*
Ph.D., and HIDEO
UNO, M.D.t
PresentedMay 2, 1967, New York City
Synopsis--Long believed to be a disorder peculiar to the scalp of man, alopecia occurs in
some of the other pritnates. Even discounting the oddities of hair growth patterns in the
head of some marmosets, sakis and sakiwinkis from South America, all adult species of
uacaris are completely bald. A close look at the head of these animals shows that the bald
scalp is covered with short hairs of small diameter. An identical situation occurs in the
stump-tailed macaque (Macaca speciosa); the scalp of young stump-tails is covered with
hair down to the eyebrows. Beginning in adolescence, the forehead becomes gradually
"naked" and adult animals have a high, apparently glabrous forehead. Actually, the number
of very small hairs on these bald areas is the same as in the haired comparableareas of young
animals. The population of hair follicles, then, is not reduced in nu•nbers but the follicles
are much smaller and produce very small hairs.
With the diminution in size of the hair follicles, there is a substantial increase in the size
of the accompanyingsebaceousglands. Such a pattern of developmentof alopeciais identical
with what takes place in some young adult men.
Additional evidences of baldnessoccur in the orangutan, which, like the stump-tailed
macaque, attains a naked forehead as it matures. Inspections of many chimpanzees of all
ages also reveal varying degreesof alopecia in a triangle of forehead just above the brows;
this appears in adolescent animals and becomesprominent only in some adult animals.
These observations point out that human alopecia has some phylogenetic significance
and is not to be considered a disorder or disease.
INTRODUCTION
Despite the heroicmethodsusedby somedermatologistsin their
study of alopeciain human subjects,many factors still limit their re* Publication No. 257 from the OregonRegional Primate ResearchCenter supportedin
part by Grant FR 00163 of the National Institutes of Health and by funds from Grant AM
08445, Biologyof the Skin of Man and Other Primates. Alsosupportedin part by fundsfrom
Carter-Wallace, Inc., Cranbury, N.J.
t OregonRegional Primate ResearchCenter, 505 N. W. 185th Ave., Beaverton, Ore.
97005
173
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search. The investigator of human subjectsmust be constantly aware
of the moral and legal restrictionsthat curtail his experiments. Furthermore,man's longevity, the vagariesof his nature and temperament
and the near-impossibility of controlling the experimental design and
heterogeneityof his genetic makeup render him an unsuitable and often
unpleasantsubjectfor experiment.
Investigators have long searched for animal substitutes, but these
half-hearted efforts have failed. Hamilton (1), for lack of a better
model, studied the wattled starling (Creatophoracarunculata),the male
of whichacquiresa glabrous,coloredtumescentskin duringthe breeding
seasonin areasof the head that had been leathered during the off season.
Female birds, which have a fully feathered head at all times, can be
inducedto undergothe samechangesas thoseof the maleswhen they are
treated with testosteronepropionate. These are most interesting observations but their pertinence to the phenomenonof baldness in man is
somewhat oblique. Allusions have been made to the South American
uacari, the adults of which are all bald, but no one outsideour grouphas
observed the histology of their scalp. The contention that these animals are difficult to obtain is simply not true. Actually, the• are numerous,but being slow-movingand slow-witted, with a melancholynature,
they rarely survive captivity for very long and henceare poor experimental animals. Most male chimpanzees,after reaching maturity,
attain a triangular "bald" area on the forehead, but these formidable
animals are expensiveand difficult to handle in captivity.
There is now little doubt that the most desirableanimal for the study
of baldnessis the stump-tailed macaque (J/Iacacaspeciosa). The mature
adult animals all have a furrowed forehead covered by small
vellus hairs. The "naked" forehead of large adult males may
extend to the middle of the calvarium or beyond, but that of females
rarely does. Since this bald condition developsin a manner similar to
that in man, we have adopted theseanimals exclusivelyfor the study of
alopecia. The lack of greater progressthan we now claim can be explained by severalfactors. First, a great deal of exploratory work still
has to be done on normal animals before experimental work can begin in
earnest. Also, primates are costly animals, which are used sparingly,
thoughtfully and with great deliberateness. Finally, most simian primatesare long-lived. For example,stump-tailed macaquesdo not reach
adolescenceuntil 5 years and becomebald only after the sixth year.
Since the condition of baldness is best exemplified in the human
scalp, we use this as the point of reference. What happens in other
BALDNESS
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175
mammalsmust be comparableto what happensin man. In discussing
baldnessone must rememberthat man's scalpis one of the most highly
specializedareas of his skin. In most other mammalsthe scalpshows
little differencefrom the rest of the skin. This is true even in many of
the primates.
THE SCALP OF MAN
In the adult human scalpapproximately600 hairs emergeper square
centimeter of surface;in the newborn there are about 1000. This means
that sinceno new follicles are formed, the initial onesgrow farther apart
asthe headgrows. The numberof follicleson the foreheadis only somewhat lower than that in the scalp. Also, in youngmen, the number of
folliclesin the bald areas of the scalp doesnot differ appreciablyfrom
the number in those areas where no clinical evidence of baldness exists.
The microscopicanatomy of the scalpand of the foreheadis similar, if
not identical, and, exceptfor differencesin the hair folliclesand sebaceous
glands,thereis no line of demarcationbetweenthe two. In four-month
old fetuses there is no hairline and hence no distinctive
feature between
the two areas; hair follicles extend from above the eyebrows over the
cranial vault and back. After the fifth month of fetal life, the follicles
on the foreheadremain approximately the samesizewhile the sebaceous
glandsattached to them becomelarger.
In contrast, the follicles of the scalp proper become progressively
larger while their sebaceous
glandsremain approximatelythe same size
and thus relatively smaller. Also, the few wispsof smoothmusclefiber
formerly attached to the follicleson the presumptiveforeheadpractically disappearwhereasthe arrector pili musclesattached to the terminal follicles of the scalp become stouter. Scalp and forehead, then,
become distinct at about the fifth fetal month.
After birth, the hair
folliclesat the margin of the "scalp" continueto becomeinvoluted for
two or threeyearsuntil the recedinghair line assumes
whateverfamilial
pattern the child has inherited. This phenomenonis the exact mechanism adapted by the follicles later when alopecia develops. In the
"precocious"alopeciaof men, the hair folliclesbecomeinvoluted,but the
total populationof hairsin bald areasremainsrelatively unaltered. All
human beings, then, are to some degreebald. The balding scalp of
adult men repeatsthe processin the foreheadof infants.
What happenslater in old men and womenis a different phenomenon.
In senescence
not only doesthe number of involuted follicles increase
but many follicles disappear outright. Even in those old men and
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women who showno clinical signsof baldnessthere is a mosaicpattern of
senile alopecia, that is, a "thinning" of the hair does occur. Kligman
(2) has pointed out that as many as 70% of the hairs from the scalpmay
be lost before clinical signs of alopecia become apparent. In discussing
baldness,then, one must distinguishbetween the "precocious"type that
developsin mature men and the "senile" type that developsin men and
women of advanced years.
In comparing human baldness with that in subhuman primates,
only the "precocious"type is of interest. Being a degenerativephenomenon,senilealopeciais lesssignificant.
THE STUMP-TAILED MACAQUE
Since only few readers may be acquainted with these animals, a
brief descriptionis in order.
They are muscular, heavy-bodiedand short-limbed. Their hair is
variably dark gray-brown, turning almost black on the mid-back, with
a contrastingwhite on the underparts. The eyebrowsconsistof sparse,
relatively coarsehairs,someof which are vibrissae,crowdingtoward the
midline. They have a naked,furrowedforehead(Figs. 1, 2, 3, 4) which,
in'fullygrownadultmales,is3 or4 inches
across
andanywhere
from2•
to',5inchesin height. Thisnakedareaismuchsmallerin adultfemales.
The nakedforeheadand scalp are usually reddish,actually hemangiomatous,and spatteredwith black and brownpigmentedspots. Aroundthe
bald scalpgrowlong straighthairsthat form a distinctcrown,giving the
animal an appearanceof dignity. This hair may be 4 to 6 incheslongin
the males and 3 to 5 inches long in the females. Three to 4 incheslong
•'mutton chops"grow from the jaws, and on the chinis a goateeabout3
inches. On the face, muzzle, and other apparently naked areas grow
short sparsehairs (Fig. 3). The longhairsof the crown,the nape, the
extensor surface of the arms, dorsal thoracic and lumbar regions form a
handsomemane, 5 or more incheslong. The hairs on the ventral surface
are white and finer and sparserthan those on the back. In the axilla,
verylongreddishhairsgrowin distinctrows. Justmedialto the cavum
axillae is a narrow strip of naked pink skin, similar to that foundon the
inguinal fold.
The clippedskin is pinkish white with blue or brown maculaescat
tered at random.
In male animals the skin of the mons, scrotum and
medial sidesof the thighs is usually red.
Both male and female animals, but particularly male, have greasy
hair and dandruff on the hairy scalpbut seldomelsewhere.
BALDNESS
IN
NONHUMAN
PRIMATES
177
ßi i'*•'•
..,
'' '-• '
..
'•,.
•: •.
:..
. ': .• .-
::*::....
;.:?5.:.:
'::?' '2•'• 1
..... ,•'?
-.•.2
•,2?"
. :•
.....
o
F•gure 1. Immature female animal with fully haired forehead
Figure 2. Young nmle stump-tail with "sparsely haired" forehead
F, gure 3. Forehead and scalp of a young adult male showing nearly "naked" forehead
Figure 4. Adult male stump-tail with a "naked" forehead and muzzle
Despite their name (speciosa,beautiful, comely), they are rather
filthy animals with a strongbody odor compoundedof fecal encrustation
and the secretion of skin glands. A curious characteristic of infant
stump-tails is the appalling musky odor, strongly reminiscent of that of
the unwashed human axilla. Young animals gradually lose this aura
and acquirethe different,but equally offensiveodor of the adult animals.
The sparsepc!age of infant and juvenile animals is generally a pale
russet color or creamy white with pink skin showing through it. This
178
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Figure 5.
OF THE
SOCIETY
OF COSMETIC
CHEMISTS
Docile young male enjoying an embrace from his handler
fur is gradually replacedby a darker, coarser,and longer one as the
animalsgrow and attain maturity. The foreheadand face, definitely
haired in young animals (Figs. 1, 2), becomegradually naked after
adolescence
(Figs. 3, 4).
All animalsshowsomesexualdimorphismin their hair. The hairsof
males are everywhere coarser and longer than those of the females.
Baldnessin the malesmay advanceto the middleof the calvariumand
beyondbut in the femalesit doesnot reach the fronto-parietalsuture.
The malesalwayshave more dandruff and a greasierscalp. The males
have longerhairs on the tragusof the pinna and a much longertuft of
hairs from a fleshy eminenceoppositethe scaphoidfossaof the ear.
Only the goateeof the malesgrowsfrom a carunculareminenceat the
baseof the chin. The bare areasin the inguinalfold are larger in the
female.
Thosewho may plan to use stump-tailedmacaquesin their laboratory but who are inexperienced
in handlingmonkeysshouldbe forewarned. When young, these animals are relatively docile and even
affectionate(Fig. 5). In adulthood, however, their temperamentis
unpredictableand mercurial. When annoyed, adult males become
treacherous,
displayfits of temper,and evenbite their ownhandsor feet.
An adult stump-taled macaquecan be formidable and shouldbe managedonly by skillful handlers.
BALDNESS
IN
THE
NONHUMAN
HAIR
PRIMATES
179
FOLLICLES
Hair follicles generally grow in groups of two or three, with one
apocrinesweat gland associatedwith each group; on the face the follicles
usually grow singly. In thosescalpareasthat are still coveredwith long
hairs, the groups consistof one or two large terminal and one or two
vellus hairs. The bald forehead and scalp are covered with a sparse
population of vellus hairs with an occasional terminal hair scattered
among them. Although the follicles in the bald areas are notably reduced in size, most still have arrectores pilorum muscles attached to
them; true veilus follicles have no muscle. Terminal hair follicles have a
small bulge for the attachment of stout muscles. In quiescent"veilus"
folliclesthe muscle,when present, is attached to the epithelial capsule
around the club hair, below which is the small hair germ. Quiescent
terminal follicles are about one-half the length of the growing ones,the
small, eccentrichair germ extendingonly a shortdistancebelowthe bulge.
Sinushair folliclesare found in the median aspectof the eyebrows,on
the mystacialareas,on the lower lip, and on the chin scatteredamongthe
folliclesof the goatee.
Although grosslythe transitional area between the bald and nonbald
portions of the scalp appearsto be abrupt, in histologicalsectionsit is
surprisingly gradual. The normal-sized terminal hair follicles grow
sparsely,having among them numerousveilus types or intermediate
follicles. Farther back, on the temporal and occipital areas, where the
terminal hairs grow longest, there is an appreciablepopulation of small
follicles. Even on the back of the trunk and nape, where the hairs form
the mane, and elsewherenearly every hair group containssmall ones.
In the scalp and face every follicle, large or small, has a complex of
sensorynervesthat composethe follicle nerve end-organ(Fig. 6). This
is found around the pilary canal between the bulge and duct of the sebaceous glands. These nerves, reactive for both butyryl- and acetylcholinesterase,are arranged in both a perpendicular and a horizontal
direction. Elsewhere, not all of the follicles have such an abundant
nerve supply. The sinushair folliclesare envelopedby very fine nerves
that swirl aroundthe upper portion, just belowthe sebaceous
glands.
In the foreheadand eyebrows,the bald areasof the scalp and in some
parts of the naked face, cholinesterase-containing
nerve fibersare found
in the papillary layer of the dermisthat accompanies
the undersideof the
epidermisfor somedistance. These terminate at the baseof someof the
epidermal ridges in small bulbous endings or in small bodies that re-
semblemucocutaneous
end-organs(Figs.7, 8).
180
JOURNAL OF THE SOCIETY OF COSMETIC CHEMISTS
Figure
G. Butyrylcholinesterase
activityinthehairfollicle
end-organ
fromthescalp
Ftgure7. Butyrylcholinesterase
activityin smallbulbous
endingsthat resemble
mucocutancousendorgansfrom the bald scalp
Figure
8. Moreextensive
mucocutaneous-like
end-organs
fromthebaldscalp
Unoetal. (3)havemadea detailed
quantitative
studyofthepopulations
andsizes
ofhairfollicles
in youngandadultstump-tailed
macaques. They have alsodissectedout intact hair folliclesfrom the sur-
rounding
connecting
tissue
tomeasure
accurately
theirsizeandtostudy
(to be reported
later)theirenzyme
content,
eliminating
the contam-
inationof surrounding
tissues.
Their resultsare shownin Figs. 9 to 12. Here are recordedthe
actualrepresentative
populationsand sizesof hair follicleson the lower
BALDNESS
IN
NONHUMAN
Table
NUMBER
Aboveeyebrow
AND LENGTH
OF HAIR
Forehead(bold)
181
PRIMATES
I
FOLLICI-E
Trans•honal
Ha*ry pormtal
19
O5 •
0
__
Above eyebrow
Forehead (Nonbald)
Hairy parielal
(Fig. 9) and upperforehead(Fig. 10), the transitionalarea (Fig. 11), and
the hairy scalpin the parietal area (Fig. 12). The summationof these
resultsis presentedin Table I. The first and third sets of trichograms
in the table show the number of hair follicles per 1.6 mm 2 of surface
found in different areasof the scalp of adult and young animals, respectively. The foreheadsof young and adult animalshave a scantier population of follicles than the other areas.
Most
of the follicles in the alo-
pecic forehead of adult animals are very short and quiescent;in the
"hairy" foreheadof young animals, the folliclesvary widely in size, but
their number
is about the same as in the adult
animals.
These tricho-
gramsalsoshowthe actuallengthsof the folliclesin telogen,anagenand
catagen.
The proportion of anagento telogenhair folliclesin the various scalp
areas in young and adult animals is significant. In the bald forehead
telogen hair folliclespredominate, whereasin the area about half the
folliclesare in anagenand half in telogen. These folliclesare distributed
almost identically in both young and adult animals. In both casesthe
foreheadhas more telogen than anagen folliclesthan the other two areas.
Figure 13 showsthe different types and sizesof hair folliclesin the
different areas of the scalp. In the parietal area most of the follicles in
anagenare about 2 mm long. Some of the anagenfolliclesin the transitional area, in the area above the eyebrow, and in most of the bald area
are about
1 ram.
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JOURNALOF THE SOCIETYOF COSMETIC
CHEMISTS
.-•X%•
•'.•%-5'•E,:'
'&½•
•:•-&•r;
'"'
%.......
Fifure9. •orehead
justabove
theeyebrow
sho•ing
oneeachofanagen
andtelogen
type
of terminal hair follide &nd so•e yellus fMlides
Figure
10. Baldareaofforehead
showing
3 telogen
and2 &nagen
typeofvdlusfollicles
Fifure
11. Tr•sitional
•eabetween
bald&nd
haiwareas
show•g
2each
ofguard
andvellus
hair
follicles
Fi½ure
12. Parietal
haiwareashowing
manytermi.al hairfollicles
in
The shortfollicles,
calledveilusfollicles,
arenotlimitedto thebald
areabut are foundin the transitionalareasand elsewhere.However,
whereas
truevdlushairfollicles
arenonerectile,
havingno arrectorpill
muscleattachedto them(4), manyof the vellusfollicles
in the bald
scalp
ofstump-tails
stillhavemuscle
fiberattached,
thefollicles
having
arisenfrom an involutionof terminal hair follicles.
THE SEBACEOUSGLANDS
A description
ofsebaceous
glands
isincluded
herebecause
theyshow
some
sexual
dimorphism,
beinglargerinmaleanimals,
andbecause
they
change
character
in thebaldingscalp.
Rdatively
smallin theskinofthetrunk,theycanattainthesizeof
sebaceous
lollideson the face,lips,chinandbaldforehead,
andscalp
BALDNESS
IN
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PRIMATES
183
Figure13. Microdissected
hairfollicles:ontheleftisananagen,
terminalfollicle,2.2 mm
in length;in the middlean anagen,
yellusfollicle,1.2 ram; andon the right a telogen,ter•ninal follicle, 0.8 mm
Figure 14.
Large sebaceous
gland "follicle" from the bald forehead
(Fig.14).Theglandsareeverywhere
largerin themalethanin thefemale.
Melanocytes
oftensurroundthe ductsof the glands,whichin some
areasmayberemarkably
pigmented.In theglands
of theforehead
and
scalpandthoseon the chinandlips,smalldendriticmelanocytes
are
ofteninsinuatedbetweenthe peripheralcellsof the acini,impartingsome
melaningranules
to the sebaceous
cells. Distinctmelaningranules
may
be found even in some mature cells and in the sebum.
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184
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DISCUSSION
Since there is no structural
demarcation
between
the forehead and the
scalp, even in man, except for the presenceof terminal hairs, a "naked"
forehead indicates that alopecia has occurred. When the hairline recedes,as it doesin most human beings, there is no way of differentiating
between what was originally forehead and what was scalp. Thus, every
human beingand every adult stump-tail is partially bald.
Stump-tails, even in those scalp areas with an apparently dense
pelage, have an appreciable number of vellus hair follicles. Furthermore, in some males, probably older animals, baldnessadvances to the
occiput and beyond. The presenceof naked expansesof skin on the
anterior axillary border and the inguinal folds, the sparsepelage of the
ventral areas and the presenceeverywhere of vellus type follicles, coupled with the development of true alopecia, suggestthat the stumptailed macaquesmay be undergoinga general loss of hair cover. The
luxuriant growth of hairs on the occiput, nape, back and shoulders,and
the goatee are no doubt protective devices,but they are also definitely
ornamental. These phenomena may be comparable to those that
might have taken place in man as he evolved from a heavily furred creature.
Aside from theoretical implications, the gradual diminution of the
size of the folliclesof the foreheadand scalpin stump-tailed macaquesis
similar to what takes place in human infants at the "hair line" and later
when pattern alopeciadevelops.
Another similarity between the bald human scalp and the bald scalp
of the stump-tails is the presenceof specialnerve end-organsunderneath
the epidermis. These are identical with those describedby Montagna
and Giacometti in man (5) and may arise from the follicle end-organs
releasedwhen the follicles became atrophied. These structures are not
present in young animals.
It is significant that the distribution of hair folliclesin the scalpis
almost identical in young nonbald animals and in adult ones. In both
groups,hair folliclesare normally least numerousin the forehead.
Since baldness
is the result
of a transformation
of terminal
hair fol-
licles to vellus ones, somethingmust be said about these follicles. Noback (6) identifiedvellus hairs as thosethat grow from follicleshaving no
erectile tissue. Danforth (7) believed that the vellus hair folliclesfrom
the foreheadundergono changesfrom childhoodto old age. During the
development of baldness and with the onset of old age, however, vellus
hair folliclesvary greatly in size, dependingon their location (8, 9, 10).
BALDNESS
IN
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PRIMATES
185
Hence, a sharp distinction between veilus and terminal hair follicles
cannot be made on the basis of length alone. Also, the vellus follicles
that developfrom terminal onesduring the processof baldnessmay still
have wispsof arrectorespilorum musclesattached to them.
Although the aging processin man causesa progressivedegeneration
of the follicles as well as of the bodily organs in general, baldnessin
young men (as in the stump-tailed macaques)can be attributed only to
the transformation
described here.
Now that we have an experimentalanimal model for the study of
alopecia,we may look forward to someprogressin our understandingof
this interestingbiologicalphenomenon.
(ReceivedMay 19, 1967)
REFERENCES
(1) Hamilton, J. B., Age, sex, and genetic factors in the regulation of hair growth in man:
a comparison of Caucasian and Japanese populations, The Biology of ]]air Growth
(Montagna, W., and Ellis, R., eds.), Academic Press, New York and London, 1958,
pp. 400-432.
(2) Kligman, A.M., Pathologicdynamicsof human hair loss. I. Telogen effluvium, Arch.
Dermatol., 83, 175-198 (1961).
(3) Uno, H., Allegra, F., Adachi, K., and Montagna, W., Studies of common baldness of the
stump-tailed macaque. I. Distribution of the hair follicles. J. Invest. Dermatol., (In
press).
(4) Montagna, W., Machida, H., and Perkins, E., The skin of primates. XXVIII.
The
stump-tailed macaque (Macaca speciosa),Am. J. Phys. Anthrop., 24, 71-86 (1966).
(5) Montagna, W., Giacometti, L., and Machida, H., Histology and cytochemistryof
human skin. XXXI.
Aging changes in the cholinesterase-containing nerves of the
scalp, J. Geron., 20, 401-404 (1965).
(6) Noback, C. R., Morphologyand phylogenyof hair, Ann. N.Y. Acad. Sci., 53,476-492
(1951).
(7) Danforth, C. H., Physiology of human hair, Physiol. Rev., 19, 94-111 (1939).
(8) Montagna, W., and Ellis, R. A., eds., The Biologyof Hair Growth,AcademicPress,Inc.,
New York, 1958.
(9) Ellis, R. A., Aging of the human male scalp, The Biologyof Hair Growth,(Montagna
W., and Ellis, R., eds), Academic Press, New York, 1958, pp 469-485.
(10) Giaeometti, L., The anatomy of the human scalp, Advancesin the Biologyof Skin, VI.
.4ging (Montagna, W., ed.), Pergamon Press, Oxford, England, 1965, pp. 97-120.