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Home , Apocrine sweat gland, Eccrine sweat gland, Epidermis, Sebaceous gland

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HISTOLOGY AND CYTOCHEMISTRY OF . XIV. THE SUPPLY OF THE CUTANEOUS * RICHARD A. ELLIS, PH.D., WILLIAM MONTAGNA, Pn.D. AND HERBERT FANGER, M.D.

Although the general blood supply to the skinout clearly against a nearly colorless background. has been mapped out in some detail (1), the exactIn thick frozen sections the entire plexus vascular patterns of the human cutaneous ap-surrounding the cutaneous glands can frequently pendages need clarification. Other authors havebe seen as they emerge from their parent used injection methods, silver impregnation, and(Figs. 3, 6, 8). The of the benzidine to demonstrate the blood vessels of thehas practically no alkaline phosphatase activity, skin. None of these methods is completely satis-but activity becomes increasingly strong factory or practical in all cases. We have found,near the emergence of the and is in- however, that the capillaries supplying the skintense in the final capillary loops (9). Although it and the cutaneous appendages can be easilyis difficult to positively identify the arterioles and visualized in frozen sections with the azo-dyevenules in these preparations, recent observations technic for alkaline phosphatase (Fig. 1). Thisin our on the localization of phos- method is superior to the others used. It is simple,phorylase activity in make the identi- quasi-specific, and demonstrates clearly even col-fication of arterioles easy, since the smooth mus- lapsed or blocked capillaries. Using this techniccle cells around them are rich in this enzyme (Fig. Montagna and Ellis (9) have studied the vascular2). The arterioles demonstrated with the phos- patterns surrounding active and quiescent humanphorylase technic are identical with the larger follicles, and are now studying the effects ofvessels visualized with the alkaline phosphatase aging on the vascularity of the skin. The currenttechnic (Figs. 2, 8). report presents only our observations on the The vascular bed around each of the three blood vessels of the sweat glands and sebaceoustypes of cutaneous glands will be described glands. separately. These descriptions are a general sum- mation of all the material studied, but a few MATERIALS AND METHODS vascular changes that occur during aging are This investigation is based on 77 specimens ofalso briefly reported. These will be dealt with in skin removed during surgery and from cadaversdetail in another paper. dead not longer than four hours. Specimens taken The patterns of the blood vessels of the skin from all the representative regions of the bodyhave been reviewed in general terms by Horst- were obtained from 34 subjects, aged 9 months tomann (5). He states that the vascular nets around 78 years. All of the tissues were presumablythe hair follicles and sebaceous glands originate as normal. side branches from any level of the candelabra The technic for the demonstration of alkalinearterias. These arteries spring from the deeper phosphatase activity in frozen sections is thatdermal plexuses and go straight to the surface, outlined by Gomori (4). The particular way inwhere they branch out at once, giving the ap- which the method is handled has been describedpearance of an inverted candelabrum. The eccrine by Montagna and Ellis (9) and is used in thissweat glands are vascularized by branches from study without modification. both the candelabra arteries and the cutaneous plexus. Horstmann (5) gives no information on OBSERVATIONS the blood vessels of the sweat glands, or Human skin has so little alkaline phosphataseon the relationships between the cutaneous glands activity that the endothelium of capillaries standsand their capillaries. *Fromthe Department of , Brown THE SEBACEOUS GLANDS University and Department of Pathology, Rhode Island Hospital, Providence, Rhode Island. The small sebaceous glands, such as those This work was supported in part by a grant fromfound in the of young people, are invested the United States Public Service, RG 2125 C7 with a network of capillaries that generally arises Received for publication October 9, 1957. from one of the arterioles associated with vascular 137 138 THEJOURNAL OF INVESTIGATIVE DERMATOLOGY

nets of the hair follicles (Fig. 3). The nets aroundis accompanied by one or more capillaries or ar- each glandular is formed by the bifurcationterioles that wind loosely about it as it courses of capillary twigs and by cross-shunts betweentoward the (Fig. 1). These vessels are the capillaries. The capillaries assunìe more intri-all connected by cross-shunts that form a loose cate patterns around the larger and more complexplexus or lattice along the . The straight sebaccous glands. More or less evenly spacedvessels branch at the level of the subpapillary vessels follow the contours of the ; theyplexus and send capillary loops underneath the penetrate the delicate septa of connective tissueepidermis. These vessels outline a cone around that separate the lobes and lobules of the glandthe epidermis that surrounds the eccrine sweat (Fig. 4); in some sections the vessels seemgland unit. Near the surface of the skin the eecrine to be penetrating the sebaceous acini or lyingduct may also be supplied with capillary branches within the . In specimens of skinfrom the arcades of vessels that lie under the from aged subjects, the capillaries supplying aepidermis. single sebaceous gland may be derived from a Although obvious changes occur in the sweat number of arterioles. In bald scalp, together withducts during ageing, the vascular beds around the retrograde metamorphosis of the hair folliclesthem remain almost unaltered. to vellus types, the schaceous glands undergo a prodigious increase in size. The follicles of vellus APOCRINE 5WEAT GLANn5 are supplied by a vestige of capillary nets, As examples of apoerine sweat glands we have while the sebaceous glands seem to usurp theexamined the axillary organ and the external capillaries that were once around the largerauditory meatus. In the secretory coils of these parent follicle (Fig. 5). With ageing there is anglands a considerable amount of alkaline phos- increasing disorganization of the blood vascularphatase activity is concentrated mostly in the system of the skin and these changes are reflectedmyoepithelial cells. The ducts of these glands in the vascularization of the sebaceous glands. have no enzyme activity. The capillaries supplying apocrine sweat glands ECCEINE SWEAT GLANn5 emerge from arterioles that are often seen in these Human eccrine sweat glands consist of threepreparations. The capillaries form elaborate sys- segments: (1) a glomerate deep portion consistingtems of loops and interconnecting branches, hi- of the secretory coil and the coiled duct; (2) afurcations and cross-shunts around the tubules straight dermal sweat duct; and (3) a spiral(Fig. 8). These vessels adhere to the surfaces of within the epidermis called the epidermal sweatthe tubules but they are never seen penetrating duct unit. The deeper coils of the glomerate parttheir surface. There is no apparent difference in of the glands are the secretory portions, rich inthe blood supply to the dilated or the constricted alkaline phosphatase activity; the superficial coilssegments of the tubules; each is supplied with an are a part of the duct and are lacking in phospha-equal number of capillaries. A few capillaries tase (Figs. 1, 6). Myoepithelial cells, which con-follow the duct of the apocrine gland to its junc- tain small amounts of alkaline phosphatase, in-tion with the pilary canal. vest only the secretory coil. The capillaries that surround the secretory and CIRCULATORY RELATIONSHIPS the coiled portion of the dermal duct Although they are seldom observed in skin frequently originate from the same vessel (Fig.specimens of young subjects, capillaries that con- 6); in large eecrine glands, however, the capil-nect the vascular beds of the various structures of laries may arise from several arterioles. In thethe skin are frequently seen in adults, and are , where the ecerine sweat glands arecommon in the aged. Capillaries joining the loosely coiled, the capillaries can be seen followingvascular system of eecrine sweat glands with the different loops of the tubule, and giving offthose around follicles are often seen branches and shunts connecting the vessels(Fig. 9). Interconnecting capillaries are always around adjacent loops (Fig. 7). In tightly coiledpresent between the sebaeeous gland and the tubules, as for example in the arm (Fig. 1), orhair follicle, or between the sebaceous gland and , this pattern is compressed and multiplied.the apocrine sweat glands. Vessels that are pri- The straight portion of the dermal sweat ductmarily associated with the epidermis often invest AND CYTOCHEMISTRY OF HUMAN SKIN. XIV 139

the terminal portion of the duets of eeerine sweatalso been studied by Eichner (3), using a silver glands or hair follicles. The exception is found inimpregnation method and iron hematoxylin, but the axilla, where regardless of the fact that thehis results were less satisfactory than ours. Re nests of eccrine and apocrine sweat glands arefound in the upper part of the knot of the gland crowded together, their individual capillary bedsan arteriole that runs parallel to the straight are rarely seen to be interconnected. These twodcrmal part of the gland up to the epidermis, types of glands, then, are not only profoundlywhere it branches in brush-like fashion, sending a different in other respects, but even their vascularplexus of capillaries in the subpapillary plexus. beds remain separate. Actually, several arterioles and capillaries may run along the duct; these are all connected by DIscussIoN cross-shunts of capillaries and at the level of the The relationships of capillaries to the threesubpapillary plexus send capillary loops under- types of cutaneous glands are simple and direct.neath the epidermis. The capillaries are evenly distributed over the The capillary plexus around the various dermal surface of the glands and no gland appears to beglands often has connecting branches. The capil- more richly vascularized than any other. When,lary plexus around the hair follicles is always with ageing, the sebaceous glands become largercontinuous with those around the scbaceous and more complex, the extent of the capillaryglands, and these often send branches that form plexuses around them increases proportionately,loops underneath the epidermis. It is remarkable and no part of a gland has a greater vascularityto find connecting shunts between the capillary than any other. nets around eccrine sweat glands and those sur- This point attains particular importance inrounding hair follicles (Fig. 9). The numerous respect to the ducts of eccrine sweat glands. Theinterconnecting vessels between the capillaries coiled dermal duct and the straight dermal ductsurrounding different cutaneous appendages may are equally richly vascularized. Several bits ofexpedite the integration of function of these evidence suggest that these ducts are active partsorgans. of the gland, perhaps in the reabsorption of water. For example, urea secreted in the secretory seg- SUMMARY ment becomes more concentrated in the duct The blood vessels supplying sebaceous and (10, 11). The total extent of the duct is greatersweat glands were visualized by the azo-dyc than that of the secretory segment; if the ducttechnique of Gomori for alkaline phosphatnse had no function this would seem to be a wastefuland examined in skin specimens from 34 subjects, mechanism in such metabolically active organs.9 months to 78 years old. Lobitz ct a!. (6) have succinctly reviewed the 1. The sebaccous glands arc invested by a histology and histochemistry of the duct in thenetwork of capillaries which generally spring from gland under controlled physiological conditions.a single parent arteriole that comes from the hair They have shown that moderate sweating resultsfollicle. With ageing, the complexity of the blood in the depletion of the glycogen only from thesupply increases in proportion to the degree of luminal cells of the ducts, but severe sweatingthe lobulation and the size of thc glands. depletes it from all of the cells. This observation 2. There is no difference in the vascularity of may not constitute proof of functional activity,the secretory and the duct portions of the coiled but it nonetheless indicates that changes takeeccrine sweat gland. The straight eccrine sweat place during functional stress. The presence ofduct is accompanied by two or three intercon- basophil granules in some of the cells of the duct,nected vessels as it courses toward the epidermis. as well as an abundance of succinic dehydrogenase Where the duct reaches the epidermis, these vessels (8) and phosphorylase (2) in the entire duct leadsbranch into the subpapillary plexus. one to conclude that this is not a passive struc- 3. Apocrinc sweat glands arc supplied by a rich ture as is generally assumed The rich capillaryplexus of capillaries that surround all portions plexus which we have observed around the ductof the tubules. The dilated segments of the strongly supports the conclusion that the ducttubules are as richly vnscularized as the con- may function as a reabsorption mechanism (7).stricted ones. The vascularization of eccrine sweat glands has 4. Some capillaries directly interconnect the 140 THEJOURNAL OF INVESTIGATIVE DERMATOLOGY plexus of the different cutaneous glands with each Brtopny, Doms: Histochemical evidence for human eccrine sweat duct activity. Arch. other and with those supplying hair follicles and Dermat. & Syph., 72: 229—236, 1955. the epidermis. These interconnections become par- 7. LOBITZ, W. C., JR. AND MAsoN, H. L.: Chemis- ticularly abundant in the skin of aged people. try of palmar sweat. VII. Discussion of studies on chloride, urea, glucose, uric acid, ammonia nitrogen and creatinine. Arch. REFERENCES Dermat. & Syph., 57: 907—915, 1948. 1. BAZETT, H. C.: Temperature, its Measure- 8. MONTAGNA, W.: Structure and Function of ment and Control in Science and Industry. Skin. Academic Press, Inc. 1956. New York, 1941. 9. MONTAGNA, W. AND ELLIS, H. A.: Histology 2. BRATJN-FALCO, 0.: Uber die Fkhigkeit der and eytoehemistry of human skin. XIII. menschlichen Haut zur Po]ysaceharid- The blood supply of the . J. Nat. synthese, emBeitrag zur Histotopochemie Cancer Inst., 19: 451—463, 1957. der Phosphorylase. Arch. fur kim. u. exp.10. NITTA, H.: On the possibility of a reabsorption Dermatol., 202: 163—170, 1955. in the excretory duct of the sweat gland: 3.EJCHNHR,F.: Zur Frage der Motivbildung in experiments on the chaoges in sweat consti- der menschliehen Haut. Anat. Anz., 100: tuents resulting from application of collo- 303—310, 1954. dion membrane on the skin. Nagoya M. J., 4. Gouom, C.: Microscopic Histochemistry. I: 59, 1953. Principles and Practice. Chicago, University 11.SCHWARTZ, I. L., TrsAY5EN, J.H.AND DOLE, of Chicago Press, 1952. V. P.: Urea excretion in human sweat as a 5. HORSTMANN, E.: Die Haut. Handbueh mikr. tracer for movement of water within the Anatomie, 3: 488, 1957. secreting gland. J. Exper. Med., 97: 429—437, 6. LOBTTZ, W.C.,JR., HOLYOKE, J0ITN B. AND 1953.

PLATEI Explanation of Figures FIG. 1. A montage of the blood vessels surrounding two large eccrine sweat glands in the skin of the upper arm of a man 75 years old. An arteriole which sends branches to both glands is indicated by the arrow. A capillary plexus surrounds the coiled portions of both the secretory and the duct of the sweat glands. Two or three vessels follow the straight duet to the surface. Just beneath the epidermis these vessels branch and join the subpapillary plexus. Gomori azo-dye method for alkaline phosphatase (X60). HISTOLOGY AND CYTOCHEMISTRY OF HUMAN SKIN. XIV 141 A 1 r 'I, '44 P - -e - - 61 J .a. 1

PLATEI 142 THEJOURNAL OF INVESTIGATIVE DERMATOLOGY

PLATE II Explanation of Figures FIG. 2. Phosphorylase activity in an unfixed frozen section through the axillary organ of a woman 47 years old. The coiled tubules of the eecrine sweat glands in the upper part of the figure are rlch in phosphorylase hut the tubules of apocrine sweat glands in the lower half of the figure have none. The arteriole indicated by the arrow is identified by the phosphorylase activity in the smooth muscle cells of its wall. This vessel, seen branching among the coiled tubules of an apoerine sweat gland, is com- parable to the arteriole in Fig. 8. Takeuchi-Kuriaki technique (X60). FIG. 3. Alkaline phosphatase activity in the skin from the pubic region of a woman 41 years old. The capillaries surrounding the simple sebaceous gland arise from a single vessel by a series of bifurcations. Gomori azo-dye technique (X120). FIG. 4. A section through two sebaceous glands in the axillary skin of a woman 67 years old. The capillaries that seem to penetrate the gland are actually compressed between its lobules. The close as- sociation between the capillaries of the glands and those surrounding the neck of the pilary canal is also demonstrated. Gomori azo-dye method for alkaline phosphatase (X60). FIG. 5. Circulatory patterns in the scalp of a man 68 years old. This figure shows capillaries around a coiled in the lower left, a large sebaceous gland in the upper right, and part of the follicle of a vellus hair in the upper right. The disorganized patterns seen in the capillary plexus of these organs are typical of the observable aging changes. Gomori azo-dye method for alkaline phosphatase 0<60). HISTOLOGY AND CYTOCHEMISTRY OF HUMAN SKIN. XIV 143 ,'Je p .j' I - P.' — -t 'fl-fl? I. —'S

PLATE II 144 THEJOURNAL OF INVESTIGATIVE DERMATOLOGY

PLATE III Explanation of Figures FIG. 6. Alkaline phosphatase activity around an eccrine sweat gland in the scalp of a man 75 years old. The capillaries surrounding the tubules arise from the large parent arteriole in the center. The coiled secretory tubules exhibit moderate phosphatase activity while four sections through the coiled duct (arrow) are devoid of activity. There is no difference in the phosphatase activity in the vessels around these two segments, however. Gomori azo-dye technique (X60). FIG. 7. This shows the capillaries surrounding the loosely coiled eccrine sweat gland from the scrotum of a man 36 years old. This circulatory pattern is probably compressed and augmented in tightly coiled glands. Compare with Figs. 1 and 6. Gomori azo-dye technique (X60). FIG. 8. Vessels supply the coiled tubules of an in the axillary organ of a woman 43 years old. A parent arteriole (arrow) is seen dividing into a plexus of capillaries that surrounds the tubules. Alkaline phosphatase is also present in the myoepithelial cells in the secretory tubules. Gomori- azo-dye technique (X60). FIG. 9. Alkaline phosphatase activity in the skin of the upper arm of a man 75 years old. The capil- laries surrounding the bulb of a lanugo hair are directly connected with the plexus around two coiled eccrine sweat glands. The parent arteriole supplying one of the eccrine glands is indicated by the arrow. Gomori azo-dye technique (X60). HISTOLOGY AND CYTOCHEMISTRY OF HUMAN SKIN. XIV 145 A -5 A I :.\4 -. I N 'C!, I —S I V. —— 4— /

PLATE III