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Anatomy and Normal Microbiota of the Skin and Eyes

Learning Objectives

Part 1

Sam, a college freshman with a bad habit of oversleeping, nicked himself shaving in a rush to get to class on time. At the time, he didn’t think twice about it. But two days later, he noticed the cut was surrounded by a reddish area of skin that was warm to the touch. When the wound started oozing pus, he decided he had better stop by the university’s clinic. The doctor took a sample from the lesion and then cleaned the area.

Jump to the next Clinical Focus box.

Human skin is an important part of the innate immune system. In addition to serving a wide range of other functions, the skin serves as an important barrier to microbial invasion. Not only is it a physical barrier to penetration of deeper tissues by potential pathogens, but it also provides an inhospitable environment for the growth of many pathogens. In this section, we will provide a brief overview of the anatomy and normal microbiota of the skin and eyes, along with general symptoms associated with skin and eye infections.

Layers of the Skin

Human skin is made up of several layers and sublayers. The two main layers are the epidermis and the dermis. These layers cover a third layer of tissue called the hypodermis, which consists of fibrous and adipose connective tissue ([link]).

The epidermis is the outermost layer of the skin, and it is relatively thin. The exterior surface of the epidermis, called the stratum corneum, primarily consists of dead skin cells. This layer of dead cells limits direct contact between the outside world and live cells. The stratum corneum is rich in keratin, a tough, fibrous protein that is also found in hair and nails. Keratin helps make the outer surface of the skin relatively tough and waterproof. It also helps to keep the surface of the skin dry, which reduces microbial growth. However, some microbes are still able to live on the surface of the skin, and some of these can be shed with dead skin cells in the process of desquamation, which is the shedding and peeling of skin that occurs as a normal process but that may be accelerated when infection is present.

Beneath the epidermis lies a thicker skin layer called the dermis. The dermis contains connective tissue and embedded structures such as blood vessels, nerves, and muscles. Structures called hair follicles (from which hair grows) are located within the dermis, even though much of their structure consists of epidermal tissue. The dermis also contains the two major types of glands found in human skin: sweat glands (tubular glands that produce sweat) and sebaceous glands (which are associated with hair follicles and produce sebum, a lipid-rich substance containing proteins and minerals).

Perspiration (sweat) provides some moisture to the epidermis, which can increase the potential for microbial growth. For this reason, more microbes are found on the regions of the skin that produce the most sweat, such as the skin of the underarms and groin. However, in addition to water, sweat also contains substances that inhibit microbial growth, such as salts, lysozyme, and antimicrobial peptides. Sebum also serves to protect the skin and reduce water loss. Although some of the lipids and fatty acids in sebum inhibit microbial growth, sebum contains compounds that provide nutrition for certain microbes.

(a) A micrograph of a section through human skin shows the epidermis and dermis. (b) The major layers of human skin are the epidermis, dermis, and hypodermis. (credit b: modification of work by National Cancer Institute)
a) A micrograph of a large light pink region labeled dermis, a thinner dark pink region on top of that labeled epidermis, and a thin region of clear cells. The division between the dermis and epidermis is wavy; with areas where one projects into the other. B) A diagram of skin. The top layer is dark and is labeled epidermis. The next layer is lighter and much thicker; this is the dermis. Inside the dermis are vase-shaped hair follicles with hairs projecting out of the skin. Next to the hair follicle is a smaller vase-shape labeled sebaceous gland; this empties into the space of the hair follicle. There are also coiled shapes labeled receptor and a variety of long tubes labeled: nerve, lymph vessel and blood vessels. A coiled blob is labeled sweat gland; this leads to a tube that opens at the surface called a sweat pore. Below the dermis is a yellow bubbly-looking layer labeled fatty tissue; this is the hypodermis.

Normal Microbiota of the Skin

The skin is home to a wide variety of normal microbiota, consisting of commensal organisms that derive nutrition from skin cells and secretions such as sweat and sebum. The normal microbiota of skin tends to inhibit transient-microbe colonization by producing antimicrobial substances and outcompeting other microbes that land on the surface of the skin. This helps to protect the skin from pathogenic infection.

The skin’s properties differ from one region of the body to another, as does the composition of the skin’s microbiota. The availability of nutrients and moisture partly dictates which microorganisms will thrive in a particular region of the skin. Relatively moist skin, such as that of the nares (nostrils) and underarms, has a much different microbiota than the dryer skin on the arms, legs, hands, and top of the feet. Some areas of the skin have higher densities of sebaceous glands. These sebum-rich areas, which include the back, the folds at the side of the nose, and the back of the neck, harbor distinct microbial communities that are less diverse than those found on other parts of the body.

Different types of bacteria dominate the dry, moist, and sebum-rich regions of the skin. The most abundant microbes typically found in the dry and sebaceous regions are Betaproteobacteria and Propionibacteria, respectively. In the moist regions, Corynebacterium and Staphylococcus are most commonly found ([link]). Viruses and fungi are also found on the skin, with Malassezia being the most common type of fungus found as part of the normal microbiota. The role and populations of viruses in the microbiota, known as viromes, are still not well understood, and there are limitations to the techniques used to identify them. However, Circoviridae, Papillomaviridae, and Polyomaviridae appear to be the most common residents in the healthy skin virome.123

The normal microbiota varies on different regions of the skin, especially in dry versus moist areas. The figure shows the major organisms commonly found in different locations of a healthy individual’s skin and external mucosa. Note that there is significant variation among individuals. (credit: modification of work by National Human Genome Research Institute)
A diagram showing different regions of the body. Each region has a pie chart that shows which bacteria are most prevalent. The most common bacterium in each region: Glabella (corynebacterineae), Alar Crease (propionibacterineae), External auditory canal (propionibacterineae), Nare (other actinobacteria), manubrioum (propionibacterineae), Axillary vault (proteobacteria), antecubital fossa (proteobacteria), Volar forearm (proteobacteria), interdigital web space (proteobacteria), hypothenar palm (proteobacteria), inguinal crease (corynebacterineae), umbilicus (corynebacterineae), toe web space (corynebacterineae, , propionibacterineae, and staphylococcaceae), reticular crease (propionibacterineae), occiput (staphylococcaceae, back (propionibacterineae), buttock (proteobacteria), gluteal crease (corynebacterineae), popliteal fossa (staphylococcaceae), plantar heel (staphylococcaceae).  Second part of the image shows that different subjects have different bacterial percentages and that these percentages change over time.

Infections of the Skin

While the microbiota of the skin can play a protective role, it can also cause harm in certain cases. Often, an opportunistic pathogen residing in the skin microbiota of one individual may be transmitted to another individual more susceptible to an infection. For example, methicillin-resistant Staphylococcus aureus (MRSA) can often take up residence in the nares of health care workers and hospital patients; though harmless on intact, healthy skin, MRSA can cause infections if introduced into other parts of the body, as might occur during surgery or via a post-surgical incision or wound. This is one reason why clean surgical sites are so important.

Injury or damage to the skin can allow microbes to enter deeper tissues, where nutrients are more abundant and the environment is more conducive to bacterial growth. Wound infections are common after a puncture or laceration that damages the physical barrier of the skin. Microbes may infect structures in the dermis, such as hair follicles and glands, causing a localized infection, or they may reach the bloodstream, which can lead to a systemic infection.

In some cases, infectious microbes can cause a variety of rashes or lesions that differ in their physical characteristics. These rashes can be the result of inflammation reactions or direct responses to toxins produced by the microbes. [link] lists some of the medical terminology used to describe skin lesions and rashes based on their characteristics; [link] and [link] illustrate some of the various types of skin lesions. It is important to note that many different diseases can lead to skin conditions of very similar appearance; thus the terms used in the table are generally not exclusive to a particular type of infection or disease.

Some Medical Terms Associated with Skin Lesions and Rashes
Term Definition
abscess localized collection of pus
bulla (pl., bullae) fluid-filled blister no more than 5 mm in diameter
carbuncle deep, pus-filled abscess generally formed from multiple furuncles
crust dried fluids from a lesion on the surface of the skin
cyst encapsulated sac filled with fluid, semi-solid matter, or gas, typically located just below the upper layers of skin
folliculitis a localized rash due to inflammation of hair follicles
furuncle (boil) pus-filled abscess due to infection of a hair follicle
macules smooth spots of discoloration on the skin
papules small raised bumps on the skin
pseudocyst lesion that resembles a cyst but with a less defined boundary
purulent pus-producing; suppurative
pustules fluid- or pus-filled bumps on the skin
pyoderma any suppurative (pus-producing) infection of the skin
suppurative producing pus; purulent
ulcer break in the skin; open sore
vesicle small, fluid-filled lesion
wheal swollen, inflamed skin that itches or burns, such as from an insect bite
(a) Acne is a bacterial infection of the skin that manifests as a rash of inflamed hair follicles (folliculitis). The large whitehead near the center of the cheek is an infected hair follicle that has become purulent (or suppurative), leading to the formation of a furuncle. (b) An abscess is a pus-filled lesion. (credit b: modification of work by Bruce Blaus)
a) Acne (labeled whitehead) on a person’s cheek. B) A drawing of skin with a yellow bubble labeled pus. This is below a raised region on the skin.
Numerous causes can lead to skin lesions of various types, some of which are very similar in appearance. (credit: modification of work by Bruce Blaus)
A table labeled types of skin lesions. Crust is shown as a raised region on the surface of the skin. Cyst is shown as a large white sphere in the upper layers of the skin. Macule is shown as a dark mark on the surface. Papule is shown as a raised bubble on the surface. Pusture is shown as a large yellow sphere in the upper layers of the skin. Ulcer is a large cavity in the skin. Vesicle is a small blue bubble in the upper regions of the skin. Wheal is a small blue bubble on the surface of the skin.

Anatomy and Microbiota of the Eye

Although the eye and skin have distinct anatomy, they are both in direct contact with the external environment. An important component of the eye is the nasolacrimal drainage system, which serves as a conduit for the fluid of the eye, called tears. Tears flow from the external eye to the nasal cavity by the lacrimal apparatus, which is composed of the structures involved in tear production ([link]). The lacrimal gland, above the eye, secretes tears to keep the eye moist. There are two small openings, one on the inside edge of the upper eyelid and one on the inside edge of the lower eyelid, near the nose. Each of these openings is called a lacrimal punctum. Together, these lacrimal puncta collect tears from the eye that are then conveyed through lacrimal ducts to a reservoir for tears called the lacrimal sac, also known as the dacrocyst or tear sac.

From the sac, tear fluid flows via a nasolacrimal duct to the inner nose. Each nasolacrimal duct is located underneath the skin and passes through the bones of the face into the nose. Chemicals in tears, such as defensins, lactoferrin, and lysozyme, help to prevent colonization by pathogens. In addition, mucins facilitate removal of microbes from the surface of the eye.

The lacrimal apparatus includes the structures of the eye associated with tear production and drainage. (credit: modification of work by “Evidence Based Medical Educator Inc.”/YouTube)
Diagram of an eye. Above the eye is the lacrimal gland. At the point nearest the nose is the punctums and tubes leading to the lacrimal sac and nasolacrimal duct.

The surfaces of the eyeball and inner eyelid are mucous membranes called conjunctiva. The normal conjunctival microbiota has not been well characterized, but does exist. One small study (part of the Ocular Microbiome project) found twelve genera that were consistently present in the conjunctiva.4 These microbes are thought to help defend the membranes against pathogens. However, it is still unclear which microbes may be transient and which may form a stable microbiota.5

Use of contact lenses can cause changes in the normal microbiota of the conjunctiva by introducing another surface into the natural anatomy of the eye. Research is currently underway to better understand how contact lenses may impact the normal microbiota and contribute to eye disease.

The watery material inside of the eyeball is called the vitreous humor. Unlike the conjunctiva, it is protected from contact with the environment and is almost always sterile, with no normal microbiota ([link]).

Some microbes live on the conjunctiva of the human eye, but the vitreous humor is sterile.
A cross section of the eye. The large spherical center is the vitreous humor. The layer surrounding this is the retina. A projection out of the back of the eye is the optic nerve. A region on the retina just above the optic nerve is the fovea. At the front of the eye is the lens. In front of this is a space labeled pupil. The colored region around the pupil is the iris. The cornea is the covering in front of the iris and pupil. The conjunctiva is a mucous membrane on the eye.

Infections of the Eye

The conjunctiva is a frequent site of infection of the eye; like other mucous membranes, it is also a common portal of entry for pathogens. Inflammation of the conjunctiva is called conjunctivitis, although it is commonly known as pinkeye because of the pink appearance in the eye. Infections of deeper structures, beneath the cornea, are less common ([link]). Conjunctivitis occurs in multiple forms. It may be acute or chronic. Acute purulent conjunctivitis is associated with pus formation, while acute hemorrhagic conjunctivitis is associated with bleeding in the conjunctiva. The term blepharitis refers to an inflammation of the eyelids, while keratitis refers to an inflammation of the cornea ([link]); keratoconjunctivitis is an inflammation of both the cornea and the conjunctiva, and dacryocystitis is an inflammation of the lacrimal sac that can often occur when a nasolacrimal duct is blocked.

(a) Conjunctivitis is inflammation of the conjunctiva. (b) Blepharitis is inflammation of the eyelids. (c) Keratitis is inflammation of the cornea. (credit a: modification of work by Lopez-Prats MJ, Sanz Marco E, Hidalgo-Mora JJ, Garcia-Delpech S, Diaz-Llopis M; credit b, c: modification of work by Centers for Disease Control and Prevention)
a) photo of an eyelid being pulled back to show a red are. B) A photo of inflamed eyelids. C)A photo of an eye with a cloudy cornea.

Infections leading to conjunctivitis, blepharitis, keratoconjunctivitis, or dacryocystitis may be caused by bacteria or viruses, but allergens, pollutants, or chemicals can also irritate the eye and cause inflammation of various structures. Viral infection is a more likely cause of conjunctivitis in cases with symptoms such as fever and watery discharge that occurs with upper respiratory infection and itchy eyes. [link] summarizes some common forms of conjunctivitis and blepharitis.

Types of Conjunctivities and Blepharitis
Condition Description Causative Agent(s)
Acute purulent conjunctivitis Conjunctivitis with purulent discharge Bacterial (Haemophilus, Staphylococcus)
Acute hemorrhagic conjunctivitis Involves subconjunctival hemorrhages Viral (Picornaviradae)
Acute ulcerative blepharitis Infection involving eyelids; pustules and ulcers may develop Bacterial (Staphylococcal) or viral (herpes simplex, varicella-zoster, etc.)
Follicular conjunctivitis Inflammation of the conjunctiva with nodules (dome-shaped structures that are red at the base and pale on top) Viral (adenovirus and others); environmental irritants
Dacryocystitis Inflammation of the lacrimal sac often associated with a plugged nasolacrimal duct Bacterial (Haemophilus, Staphylococcus, Streptococcus)
Keratitis Inflammation of cornea Bacterial, viral, or protozoal; environmental irritants
Keratoconjunctivitis Inflammation of cornea and conjunctiva Bacterial, viral (adenoviruses), or other causes (including dryness of the eye)
Nonulcerative blepharitis Inflammation, irritation, redness of the eyelids without ulceration Environmental irritants; allergens
Papillary conjunctivitis Inflammation of the conjunctiva; nodules and papillae with red tops develop Environmental irritants; allergens

Key Concepts and Summary

Multiple Choice

_____________ glands produce a lipid-rich substance that contains proteins and minerals and protects the skin.

  1. Sweat
  2. Mammary
  3. Sebaceous
  4. endocrine

C

Which layer of skin contains living cells, is vascularized, and lies directly above the hypodermis?

  1. the stratum corneum
  2. the dermis
  3. the epidermis
  4. the conjunctiva

B

Fill in the Blank

The ________ is the outermost layer of the epidermis.

stratum corneum

The mucous membrane that covers the surface of the eyeball and inner eyelid is called the ________.

conjunctiva

Short Answer

What is the role of keratin in the skin?

What are two ways in which tears help to prevent microbial colonization?

Which label indicates a sweat gland?

(credit: modification of work by National Cancer Institute)
A diagram of skin. i – a vase shape in the center of skin with a long projection out the top. iv – the long projection from i. iii – a small vase shape attached to i. ii – a coiled structure in the center with a tube leading out.

Critical Thinking

Explain why it is important to understand the normal microbiota of the skin.

Besides the presence or absence of ulceration, how do acute ulcerative and nonulcerative blepharitis differ?

Footnotes

  1. 1 Belkaid, Y., and J.A. Segre. “Dialogue Between Skin Microbiota and Immunity,” Science 346 (2014) 6212:954–959.
  2. 2 Foulongne, Vincent, et al. “Human Skin Microbiota: High Diversity of DNA Viruses Identified on the Human Skin by High Throughput Sequencing.” PLoS ONE (2012) 7(6): e38499. doi: 10.1371/journal.pone.0038499.
  3. 3 Robinson, C.M., and J.K. Pfeiffer. “Viruses and the Microbiota.” Annual Review of Virology (2014) 1:55–59. doi: 10.1146/annurev-virology-031413-085550.
  4. 4 Abelson, M.B., Lane, K., and Slocum, C.. “The Secrets of Ocular Microbiomes.” Review of Ophthalmology June 8, 2015. http://www.reviewofophthalmology.com/content/t/ocular_disease/c/55178. Accessed Sept 14, 2016.
  5. 5 Shaikh-Lesko, R. “Visualizing the Ocular Microbiome.” The Scientist May 12, 2014. http://www.the-scientist.com/?articles.view/articleNo/39945/title/Visualizing-the-Ocular-Microbiome. Accessed Sept 14, 2016.

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