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ANTIMICROBICS

AND INFECTIOUS

DISEASES

NEWSLETTER

Editor-in-Chief

W. Stratton, MD

Vanderbilt University

School of Medicine

Nashville, Tennessee

Full editorial board

appears on back cover

Volume 18, Number 7

July 2000

W. Stratton, MD

Vanderbilt University School of Medicine

Nashville, TN 37232

Introduction

Chlamydia pneumoniae was initially

recognized as a cause of acute lower

respiratory tract infections such as pneu-

monia and bronchitis in both adults and

children (1-7), hence the species name

“pneumoniae.” Moreover, C. pneu-

moniaewas noted in some individuals

to cause a persistent respiratory tract

infection following an acute infection

(8), which is entirely consistent with the

known chronic nature of chlamydial

infections (9,10). In addition, C. pneu-

moniaehas been shown to establish a

subclinical asymptomatic respiratory

tract infection (11).

Pathogenesis of Chronic

Chlamydial Infections

Establishment of persistent low-grade

infections in the lung by C. pneumoniae

creates an important factor for the

pathogenesis of this microorganism.

The ability of C. pneumoniaeto infect

a wide variety of human cells, including

epithelial, endothelial, and smooth mus-

cle cells as well as macrophages and

monocytes, is well documented (12-

20). The infection of macrophages, in

particular, allows C. pneumoniaeto

enter the circulation from pulmonary

tissues and cause systemic dissemina-

tion. The tendency for C. pneumoniae

to disseminate from the initial site of

infection in the lung has been described

in the murine model of infection (21,22).

Similar dissemination is presumed to

occur in humans. Indeed, the presence

of C.pneumoniaeDNAin peripheral

blood mononuclear cells (PBMCs) has

been well documented (23-29). More-

over, the viability of C. pneumoniaein

circulating PBMCs has recently been

established (30). The ability of C. pneu-

moniaeto cause persistent infections

combined with its ability to disseminate

via the vascular system has raised ques-

tions as to the role of this pathogen in a

number of chronic human diseases (31-

33). Viable C. pneumoniaecirculating

in PBMCs may reach various human

tissues after an inflammatory trigger

event occurs in the tissue and then

cause chronic infection in the tissue.

This might create or worsen a chronic

disease process. The purpose of this

article is to review the association of

C. pneumoniaewith chronic human

diseases.

Chronic Lung Diseases

The predilection of C. pneumoniaeto

cause acute respiratory tract infections

combined with its persistent nature

suggests that it might play a role in

chronic lung diseases (34). Chronic

obstructive pulmonary disease (COPD)

is a slowly developing irreversible and

generally progressive chronic lung dis-

ease in which three disorders are com-

monly included: chronic bronchitis,

peripheral airway disease, and emphy-

sema. Indeed, C. pneumoniaehas been

found to be a frequent cause of acute

exacerbations of COPD (35). Accord-

ingly, it has been suggested that C.

pneumoniaemay have a role in the

pathogenesis of COPD (36). Immuno-

histochemical staining for C. pneumo-

niaeis increased in lung tissue from

subjects with COPD, suggesting that

persistent infection with this organism

is common (37). In addition, morpho-

logical findings by electron microscopy

in pulmonary emphysema reveal aberrant

chlamydiaethat are identical to those

seen in atherosclerosis (38). Persistent

low-grade infection of the lung by C.

pneumoniaeis thus likely to contribute

to chronic lung disease and, in some

instances, may even be causal.

Chronic Otolaryngeal Diseases

Otolaryngeal infections include sinusitis,

otitis media, pharyngitis, tonsillitis, and

laryngitis. These infections may be acute,

recurrent, or chronic. The seroprevalence

of antibodies to C.pneumoniaesuggests

that this microorganism is an important

and common pathogen of otolaryngeal

disease (39). C. pneumoniaehas been

isolated from both acute and chronic

otitis media (40,41), and polymerase

chain reaction (PCR) studies have

confirmed and extended these early

observations (42,43). Isolation of C.

pneumoniaefrom the maxillary sinus

has been described in one case report

(44), but additional studies evaluating

the role of C. pneumoniaein sinusitis

have not been done. C. pneumoniaehas

been isolated from pharyngeal tissue

biopsies as well as demonstrated by

Association of Chlamydia pneumoniaewith Chronic Human

Diseases

ANTIMICROBICS

AND INFECTIOUS

DISEASES

NEWSLETTER

In This Issue

Association of Chlamydia

pneumoniaewith Chronic

Human Diseases. . . . . . . . . . . . . . . 49

W. Stratton, MD

Editor-in-Chief

W. Stratton, MD

Vanderbilt University

School of Medicine

Nashville, Tennessee

Full editorial board

appears on back cover

Volume 18, Number 7

July 2000

AIDIEX 18(7)49-56,2000 ©2001 Elsevier Science Inc.

1069-417X/00 (see frontmatter) 49

50 1069-417X/00 (see frontmatter) ©2001 Elsevier

Science Inc. Antimicrobics and Infectious Diseases

Newsletter 18(7) 2000

immunohistochemical methods in

patients with chronic pharyngitis (45).

Similarly, immunohistochemical anal-

ysis and PCR have demonstrated C.

pneumoniaein adenoid tissue from

children undergoing adenoidectomy for

hyperplastic adenoids (46,47). Clearly

C. pneumoniaeis present in otolaryn-

geal tissues and plays a role in both

acute and chronic infections as well as a

possible role in a hyperplastic response.

Asthma

Infection has long been thought to play

a role in asthma (48). For example, res-

piratory tract infections are thought to

precipitate wheezing in many asthmatic

patients. The recent use of PCR to diag-

nose viral infections of the respiratory

tract has documented the role of rhino-

virus and respiratory syncytial virus in

acute exacerbations of asthma (49). As

C. pneumoniaeis a pathogen causing

acute and chronic respiratory tract

infections, it may play a similar role

in asthma. One of the first studies to

investigate this possibility found that

there is an association of C. pneumoni-

aeinfection with wheezing, asthmatic

bronchitis, and adult-onset asthma (50).

Not only did C.pneumoniaeappear to

exacerbate asthma, it seemed in some

patients to initiate asthma. The authors

concluded that repeated or prolonged

exposure to C. pneumoniaemay have a

causal association with wheezing, asth-

matic bronchitis, and asthma. Other

investigators have confirmed the asso-

ciation of C. pneumoniaewith acute

exacerbations of asthma in both adults

and children (51-58). Several studies

suggest that antimicrobial therapy

against C. pneumoniaeis beneficial in

the course of reactive airway disease

(59-61). Whether or not C. pneumoniae

plays a causal role in addition to its role

in exacerbations of asthma remains to

be determined.

Atherosclerosis

Despite significant advances in our

understanding of the various risk fac-

tors involved in atherosclerosis, there

are significant gaps in the elucidation

of the etiology of vascular injury and

atherogenesis. Chronic infection of vas-

cular tissue has received considerable

attention recently as an inducer of vas-

cular injury and subsequent develop-

ment of atherosclerosis. Although

infection with a variety of infectious

agents such as cytomegalovirus has

been implicated in atherogenesis, the

best evidence to date links the presence

of C. pneumoniaewith the pathogenesis

of atherosclerosis. Saikku et al. (62,63)

first reported an association between

anti-C. pneumoniaeantibody titers and

coronary artery disease. In a 1999

review, Wong, Gallagher, and Ward (64)

reported that 21 of 27 studies showed

“some sort of positive serological

association between positive anti-C.

pneumoniaetiters and atherosclerosis.”

Similar results have been reported in

cerebrovascular accidents with a num-

ber of studies showing a positive

correlation with anti-C. pneumoniae

antibodies (65-67). Direct evidence

of C. pneumoniaeinfection of blood

vessels is provided by studies using

electron microscopy (68,69,74), PCR

(69,71-78,82), immunohistochemistry

(68,70-75,80,82), reverse transcriptase

PCR (79), and cultures (75,77,80,81).

Finally, animal models support a role

for C. pneumoniaein the pathogenesis

of atherosclerosis (83-85).

Neurological Diseases

The serologic association of C. pneu-

moniaeinfections with neurological

diseases began with several individual

case reports that linked this micro-

organism with Guillain-Barre syndrome

(86) and lumbosacral meningoradiculi-

tis (87). These observations were

followed by additional reports asso-

ciating C. pneumoniaewith meningitis

(88,89). The association of chlamydial

infections with neurological syndromes

has been strengthened by a large sero-

logical survey of patients with neuro-

logical disease (90). These observations

suggest that C.pneumoniaemay be

more prevalent as an associated agent

in central nervous system (CNS) dis-

eases than appreciated (90) and that

chlamydial infections should be includ-

ed in the differential diagnosis of neuro-

logical syndromes (91). The first direct

evidence that C. pneumoniaeinfection

may be risk factor for a chronic neuro-

logical disease was a study that demon-

strated that C. pneumoniaeis present,

viable, and transcriptionally active in

areas of neuropathy in the Alzheimer’s

disease brain (92). This was followed

by a report of a case in which C. pneu-

moniaewas isolated from the cerebro-

spinal fluid (CSF) of a patient with

multiple sclerosis (MS) (93). Anti-

chlamydial therapy markedly improved

the course of MS in this patient. Amore

extensive study by the same investiga-

tors demonstrated that infection of the

CNS is a frequent occurrence in MS

patients (94).Other investigators have

confirmed the presence of C. pneumo-

niaein CSF from MS patients (95,96)

as well as in CSF from patients with

other types of neurological disease (97).

Additional case reports for meningo-

encephalitis and encephalomyelitis

(98,99) suggest that C.pneumoniaeis

a neurotrophic pathogen and thus may

play a role in a variety of chronic

neurological diseases.

Chronic Rheumatological

Diseases

Rheumatological diseases include those

diseases that involve the connective

tissues. Joints and related structures of

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frontmatter) 51

the skeleton are considered the principal

connective tissues and vary widely in

structure and function as well as in pre-

disposition to disease. Many connective

tissue diseases in humans are chronic

and involve inflammation. The most

common is rheumatoid arthritis (RA).

RAis a chronic connective tissue dis-

ease of unknown etiology which has

been considered by some to be the

result of a chronic inflammatory syn-

ovial response to an unrecognized

antigen, such as that from infectious

agent(s). Vasculitis is a recognized

component of many chronic rheuma-

tological diseases (100) including RA

(101). Vasculitis has been associated

with a number of infectious agents

(102). The recognition that C. pneumo-

niaemay induce isolated and systemic

vasculitis in small and large blood

vessels (103) has therefore raised ques-

tions as to its role in chronic rheuma-

tological diseases. Moreover, Chlamydia

species are known to cause polyarthritis

in calves and sheep (104-107). Thus, it

is not surprising to find that C. tracho-

matisis now recognized as a cause of

reactive arthritis (108-112). Similarly,

C. pneumoniaealso has been associated

with reactive arthritis (113-118). It is

possible that C. pneumoniaecould also

play a role in RA. Such a role may be

secondary infection of inflamed joints,

or it may be causal. The observations

that antimicrobial therapy with tetracy-

clines, agents active against Chlamydia

species,is beneficial for some patients

with rheumatoid arthritis (119-122)

suggests that chlamydial infection may

be a factor.

In addition, C. pneumoniaehas been

associated with other chronic rheumato-

logical diseases. One case report has

found an association of C. pneumoniae

with systemic lupus erythematosus in

which the patient was cured by a com-

bination of clarithromycin, predniso-

lone, and cyclophosphamide (123).

More intriguing is the association of

C. pneumoniaewith temporal arteritis.

Temporal arteritis is a clinical manifes-

tation of giant-cell arteritis. Giant-cell

arteritis is a vasculitis of unknown etiol-

ogy that predominantly affects medium-

and large-sized arteries (124). Giant-

cell arteritis and a closely related clini-

cal syndrome, polymyalgia rheumatica,

affect the elderly and often involve an

acute onset with flu-like upper respira-

tory tract symptoms. For this reason, an

infectious process has been proposed as

a trigger mechanism (125). An initial

case in which C. pneumoniaeDNAwas

detected in an artery specimen has been

reported (126). Amore extensive inves-

tigation found that C. pneumoniaewas

present in temporal artery specimens

from most patients with giant cell arter-

itis (127). This study detected C. pneu-

moniaeby both immunohistochemistry

and PCR and noted that the dendritic

cells in the adventitial layer of the arter-

ies may represent the antigen-present-

ing cells. This work further supports

the association of C. pneumoniaewith

chronic rheumatological diseases.

Cancer

Chronic infections are known to predis-

pose to malignant growth. As C. pneu-

moniaemay cause chronic infections,

it may predispose to cancer. There is

serological evidence of an association

between C. pneumoniaeinfection and

lung cancer. In on study, chronic C.

pneumoniaeinfection was positively

associated with the incidence of lung

cancer and was especially increased in

men younger than 60 years (128). This

has been corroborated by a second

study showing that chronic C. pneumo-

niaeinfection is common in patients

with lung cancer (129). Another sero-

logical study found evidence of an asso-

ciation between chronic C. pneumoniae

infections and malignant lymphoma

(130). In cutaneous T-cell lymphoma,

there is a protein that has been identi-

fied and found to be stimulatory for

malignant Sezary Tcells. This protein

has been termed Sezary T-cell activat-

ing factor and is often present in the

skin of patients with mycosis fungoides,

the predominant form of cutaneous T-

cell lymphoma. This Sezary T-cell acti-

vating factor has been found to be a C.

pneumoniae-associated protein (131).

Therefore, it is possible that C. pneumo-

niaemay play a role in the pathogenesis

of cutaneous T-cell lymphoma.

Miscellaneous Chronic Diseases

C. pneumoniaehas been associated

with a number of other chronic dis-

eases. It is not surprising that C. pneu-

moniaehas been reported as a treatable

cause of chronic fatigue syndrome (132).

It is likely that many chronic infections

would result in patients experiencing

chronic fatigue; thus, a chronic chlamy-

dial infection would be expected to

do the same. Fibromyalgia and other

myalgia of unknown cause have been

described in patients with chronic

fatigue syndrome; C. pneumoniaeanti-

bodies have been linked with myalgia

of unknown cause, including fibromyal-

gia (133). An interesting association of

C. pneumoniaeinfections with diabetic

nephropathy has been noted (134). This

is interesting because of the possible

relationship between glucose metabo-

lism and chlamydial infection. For years,

it has been speculated that chlamydiae

are energy parasites that are totally

dependent on their host cells for ATP

and other high-energy intermediates

(135), although this concept has been

questioned recently due to the complete

sequencing of genes from C. tracho-

matisand C. pneumoniae. Analysis of

these chlamydial genes suggests that

chlamydiae have some functional

capacity to produce their own ATPand

reducing power (136). Nonetheless, it is

clear that infection of eukaryotic cells

with chlamydiae results in an increase

in the rate of glycolysis and that this

increase is not caused by chlamydial

metabolic activity but instead is a host

cell response to the infection (137,138).

This might offer an advantage for chla-

mydial replication in a host with diabetes

and increased levels of glucose. If this

were the case, chlamydial infection

might be the source of the accelerated

atherosclerosis known to occur in dia-

betics. An association of C. pneumoniae

infection with pyoderma gangrenosum/

skin ulcers in diabetic patients has been

described (139,140). C.pneumoniae

therefore might be an important patho-

gen in diabetic patients. Finally, an

association of C. pneumoniaeand

interstitial cystitis has recently been

described (141). Interstitial cystitis

(IC) is a chronic inflammatory disease

occurring primarily in females. IC is

considered a sterile bladder condition

characterized by symptoms of urgency,

frequency, and pain. The etiology of IC

is unknown, but autoimmune mecha-

nisms have been thought to play a role.

Analysis of urine samples of IC patients

by PCR revealed that 71% of patients

with IC were positive for C. pneumoni-

ae(141). Therefore, bladder biopsies

were done for culture of this pathogen.

Of those patients with IC, 82% (14/17)

52 1069-417X/00 (see frontmatter) ©2001 Elsevier

Science Inc. Antimicrobics and Infectious Diseases

Newsletter 18(7) 2000

had tissue cultures positive for C.

pneumoniae(141). Control patients

were limited to those patients without a

history of irritative voiding symptoms,

transitional cell carcinoma, or recurrent

urinary tract infection. In these control

patients, 16% (1/6) had tissue cultures

positive for C. pneumoniae. This differ-

ence was statistically significant (P=

0.004). Thus, C. pneumoniaemay

have a role in the pathogenesis of IC.

Summary

It is apparent from this review that

C. pneumoniaehas been implicated

in many chronic diseases of humans.

Whether the role is that of innocent

bystander, cause, or perhaps something

in between remains to be determined.

Regardless of the role of C. pneumoni-

aein these or other chronic diseases,

this microorganism is becoming a major

health concern. Considerable resources

will be needed to determine its role in

human disease. If C. pneumoniaeproves

to play an important role in any or all

of these chronic diseases, its eventual

control or eradication may do much to

improve the health of countless persons.

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