Periodontology 2000, Vol. 23, 2000, 13–18 Copyright C Munksgaard 2000Printed in Denmark ¡ All rights reserved

PERIODONTOLOGY 2000ISSN 0906-6713

A history of oral sepsisas a cause of diseasePAUL G. O’REILLY & NOEL M. CLAFFEY

The twentieth century had four main pathogenicconcepts: autointoxification, focal infection, psycho-somatic disease and autoimmunity (3). Psychosom-atic disease and autoimmunity are not dealt withhere as they are topics in their own right. However,autointoxification will be dealt with in some detail,as it was popular and coincidental with the conceptof oral sepsis and focal infection, and treatment ofpatients was often based on the elimination of focalinfection and intestinal bacteria.

Autointoxification concerns the belief that the co-lon, with its large mass of living bacteria, can act byeither absorbing bacterial toxins or by transportingliving organisms from the bowel to other parts of thebody. Ancient Egyptians would wash out their lowerbowels. Louis XIV was the recipient of several thou-sand colonic irrigations in his lifetime. In the firstquarter of this century, bowel washing was a stan-dard part of practice in medicine (20). It was be-lieved that the accumulation of fecal material mightshorten the life span because it ‘‘becomes a nidusfor microbes which produce fermentations and putr-ification harmful to the organism’’. Metchnikoff et al.advocated the administration of lactic acid–produc-ing bacteria in an attempt to change the relative pro-portion of bacteria in the gut (26). One of the greatproponents of this concept was the English surgeonWilliam Arbuthnot Lane. He attributed a whole lit-any of human ailments to intestinal stasis: Gastriculcer, gastric cancer, gall stones, cholecystitis, gallbladder cancer, loss of fat, wasting of voluntarymuscles, degenerative changes in the skin, subnor-mal body temperature, Raynaud’s disease, mentalapathy, stupidity, misery, insomnia, raised or de-pressed blood pressure, breast cancer, cardiac de-generation, Bright disease, pancreatitis, diabetes, eyedegeneration, rheumatoid arthritis, cystitis, pyleitis,endometritis, salpingitis, Still’s disease and bacterialendocarditis (22).

To eliminate this intestinal stasis, he advised that

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the colon be evacuated three times a day. He devisedsurgical procedures to speed the elimination of in-testinal contents and described them fully in hisbook The operative treatment of chronic constipation(23). These methods included tacking up a saggingcolon, releasing constricting mesenteric bands,short-circuiting by means of ileocolostomy and totalcolectomy.

Novel studies were carried out to try to ascertainwhether colonic stasis could be causative in manydisorders. In one, a group of human volunteers hadrectal plugs inserted for several days. The only symp-toms encountered were headache and discomfort,quickly relieved by the release of the plug (1). As lateas 1930, a routine part of urinalysis was the indicantest for the presence of indol, presumed to reflectbacterial overgrowth in the intestinal tract. It is stillfelt that an overgrowth of intestinal bacteria in cer-tain diseases can cause steatorrhea and vitamin B12

deficiency (3), and in complementary medicine co-lonic lavage has again become popular as both treat-ment for some diseases and also as a method ofachieving weight loss.

Oral sepsis

Oral sepsis was first introduced into the medicalliterature in a report entitled ‘‘Oral sepsis as a causeof disease’’ (18) by William Hunter in 1900. This wasthen superseded by focal infection, introduced byFrank Billings in 1911 (4). However, a careful reviewof the medical literature indicates that the belief thatconditions affecting the mouth could have impli-cations on peripheral tissues and organs has beenheld from the very earliest medical recordings.

In ancient Egypt the importance of oral hygieneappears not to have been appreciated, with discov-ered human remains exhibiting large accretions ofcalculus with consequent periodontal bone loss even

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though oral hygiene devices have been discovered inthe burial crypts of royal princesses of the 12th Dyn-asty (2130–1930 BC), and one of the oldest medicalpapyri of the Middle Dynasty (2100 BC) mentionstooth pain associated with disease of women’s repro-ductive system (15).

Ancient civilizations

Sound, healthy teeth were highly valued by the earlyHebrews. The physical requirements for the role ofHigh Priest as stated in Leviticus prevent anyonefrom serving who is not a whole person, and theRabbis have interpreted this to include one who haseven a single tooth missing. One reference in the Ba-bylonian Talmud (AD 352–427) suggests a connec-tion between the oral cavity and the eyes, for it saysto avoid the extraction of the eye tooth ‘‘becauseyour eyes must suffer instead’’ (31). The Hebrewbook Sefer haolsmot o maaseh tovia compared thehuman body to a house. The mouth was seen as thedoorway and must be kept scrupulously clean toprotect the body from contamination.

In Niniveh, the capital of ancient Assyria on theeastern bank of the river Tigris, a Cuneiform tablewas found whose text deals with a King Ashurbani-pal (669–626 BC) whose physician said ‘‘The pains inhis head, arms and feet are caused by his teeth andmust be removed’’ (12, 16).

The Greeks considered strong teeth indicative ofgood health. Diocles of Carystus, an Athenian physi-cian of Aristotle’s time, stated ‘‘Every morning youshould rub your gums and teeth with your bare fin-gers and with finely pulverized mint, inside and out-side, and remove thus the adherent particles’’ (31).Hippocrates (400 BC) described a patient with‘‘rheumatism’’ whose arthritis was cured by the ex-traction of a tooth (24).

The Roman physician Galen (166–201 AD) be-lieved that the head was the source of all ills. An ex-tract from his book On hygiene emphasizes this in-ter-relationship between the oral cavity and other ill-nesses although he sees oral sepsis as being theresult rather than the cause of a variety of ailments.

When the head becomes disordered in nature it pro-duces many excrements from which lesions of the lowerorgans occur because excrement passes to them. Nowmost readily their passage is to the mouth ... It is obvi-ous also that uvulitis, tonsillitis and gingivitis and cervi-cal adenitis and dental caries and ulcers and pyorrheain the mouth are due to the catarrhal ichors descendingto them from the head (31).

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The middle ages

The next notable occurrence in dentistry probablyoccurred in the Middle Ages. In 1548, Walter Herm-ann Ryff wrote a monograph that dealt exclusivelywith dental afflictions. In this pamphlet entitled‘‘Useful instructions on the way to keep healthy, tostrengthen and re-invigorate the eyes and the sight.With further instructions of the way of keeping themouth fresh, the teeth clean and the gums firm’’ hemakes the following statement (33):

The eyes and teeth have an extraordinary affinity or re-ciprocal relation to one another, by which they easilycommunicate to each other their defects and diseases,so that one cannot be perfectly healthy without theother being so too.

Giovanni d’Arcoli stated that, in cases of violent den-tal pains, early intervention was advisable as ‘’suchviolent pains are followed by syncope or epilepsy,through injury communicated to the heart or brain’’(2).

The importance of oral hygiene in relation tobacteriology was first detailed by the Dutch scientistAntonie von Leeuwenhoek in 1683. Using a primitivehomemade microscope, he described ‘‘animicules’’found in scrapings from between the teeth. He re-lated lack of oral hygiene to an increase in the quan-tity of these organisms (8).

In 1768, Thomas Berdmore in A treatise on the dis-orders and deformities of the teeth and gums de-scribed the relationship between the teeth and theentire body as one leading to the most ‘‘excruciatingpains and dangerous inflammations and sometimesdeep seated abscesses which destroy neighboringparts and affect the whole system by sympathy, orby infecting the blood with corrupted matter’’ (32).

Modern times

In 1818, one of the most famous physicians in Amer-ica, Benjamin Rush (a signatory to the Declarationof Independence) reported the course of a disease inwhich a woman who was suffering from rheumatismof long standing had an aching tooth extracted and‘‘she recovered in just a few days’’ (32).

The evolution of the study of microbiology tookmajor strides in the nineteenth century thanks to thework of Pasteur, Lister and Koch. In 1884, Koch pre-sented a paper on the causation of tuberculosis thatincluded recovery of the organism from the infectedpatients, identifying it microscopically, obtaining

A history of oral sepsis as a cause of disease

pure cultures and producing the infection by inocu-lation of the pure culture (31). These later becameknown as Koch’s postulates. Working in Koch’s lab-oratory at this time was an American dentist W.D.Miller. In 1891 Miller published a classic article en-titled ‘‘The human mouth as a focus of infection’’(28). In this article he endeavors

to call attention to the various diseases both local andgeneral, which have been found to result from the ac-tions of micro-organisms which have collected in themouth, and to the various channels through whichthese micro-organisms or their waste products may ob-tain entrance to parts of the body adjacent to or remotefrom the mouth.

He also tried ‘‘to establish the great importance of athorough understanding on the part of the physi-cian, no less than of the dentist, of mouth germs asa factor in the production of disease’’. Diseases hefelt were able to be traced ‘‘to the action of mouthbacteria’’ included: ostitis, osteomyelitis, septicemia,pyemia, meningitis, disturbance of alimentary tract,pneumonia, gangrene of the lungs, angina Ludovici,diseases of the maxillary sinus, actinomycosis,noma, diphtheria, tuberculosis, syphilis and thrush(28).

Miller also reported fistulae of dental origin thatopened on the neck, shoulder, arm or breast andcites a case report of a 33-year-old woman where

the connection of a chronic fistula on the breast justabove the nipple was discovered by the discharge, onthe day following a visit to a dentist, smelling like themedicament used by the dentist in treating a badly dis-eased root. A solution of cochineal injected into the rootalso made an appearance at the opening of the fistulaa few hours later.

The fistula resolved upon extraction of the tooth.Miller stressed that, wherever such germ organ-

isms existed, there was a risk that they could pro-duce ‘‘a metastic abscess wherever a point ofdiminished resistance existed’’. Therefore not onlyteeth may be suspected as a focus he said butother organs as well such as the tonsils and uterus.Miller presented this paper at the InternationalCongress of Hygiene, in the Bacteriology sectionpresided over by Lord Lister. In the audience thatday was William Hunter, at that time the seniorassistant physician at the London Fever Hospital.This topic particularly interested Dr. Hunter, as hisearlier work on pernicious anemia had drawn hisattention to the mouth as a possible source of in-fection. In 1900, he wrote an article entitled ‘‘Oral

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sepsis as a cause of disease’’ (18), in which hestates because of oral sepsis

... that not only is the constant swallowing of pus a mostpotent and prevalent cause of gastric trouble, but thatthe catarrh set up is not simply irritant but actually in-fective, and may lead in time to other more permanenteffects – namely atrophy of glands and chronic gastritisand in certain cases even to suppurative gastritis.

However, he did not believe that the effects of oralsepsis were confined to gastritis but also diseasessuch as tonsillitis, glandular swellings, middle-earsuppurations, ulcerative endocarditis, empyemata,meningitis, nephritis and osteomyelitis. He advo-cated oral antisepsis measures including the appli-cation of carbolic acid (a 1 to 20 solution) to diseasedteeth or inflamed gums, the removal of ‘‘toothstumps’’, the boiling of every ‘‘tooth plate’’ worn andthe avoidance of too much conservative dentistryand ‘‘the use of contrivances like bridges which can-not be kept aseptic’’.

In 1900, Godlee (14) described how the signs andsymptoms of other conditions (such as pleurisy andsuspected carcinoma of the stomach) could be attri-buted to pyorrhea alveolaris and how all the signsand symptoms disappeared after careful removal ofall calculus and regular syringing of the pockets witha hydrogen peroxide solution. In 1902, Colyer de-scribed the resolution of irregular heartbeat, gastriceffects and ‘‘general debility’’ after the treatment ofany oral sepsis present. He also suggested a goodmaxim for the dentist to work was ‘‘better no teeththan septic ones’’ (7).

Antral disease was put forward as an importantsequela of oral sepsis. It was believed that prolongedantral suppuration could lead to extreme mental de-pression, often ending in a suicidal tendency (38).Also special reference was made to oral asepsis be-fore surgical procedures involving the pelvic viscerawith several cases of parotitis and fatal cases of an-gina ludovica following pelvic operations being attri-buted to buccal sepsis.

Other relationships that were put forward werethose between oral sepsis and migraine headaches,laryngeal pain and spasm (which could inducecough, loss of voice and wasting), blindness anddeafness all which may be cured on treatment of theoral sepsis (21).

As the theory of oral sepsis became more popular,theories were put forward as to which organs weremost susceptible to different types of oral sepsis andhow the treatment of oral sepsis could lead to recov-ery from tonsillitis, tuberculosis and diabetes. It was

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also believed that oral sepsis could be transmittedby the licking of envelopes, use of contaminatedtelephone receivers and men with beards (35). Inmany cases of malnutrition the sole cause was feltto be a ‘‘filthy mouth’’ and that ‘‘no greater goodcould come to humanity than the full recognition ofthe dangers from this insidious, prolific, and virulentinfection in the human mouth ‘‘ and that the adop-tion of proper oral hygiene practices would result inimmediate and marked improvement to generalhealth, and in notable increase in the average dur-ation of human life’’ (25).

Oral sepsis and septic dentistry

On October 3rd, 1910, William Hunter delivered anaddress at the opening of McGill University in Mon-treal. The title of his address was ‘‘The role of sepsisand antisepsis in medicine’’, and because he wasconsidered the pre-eminent physician in this field,his address was reprinted fully in the leading Britishmedical journal of the time, The Lancet. In his ad-dress he formally warned his medical colleagues ofthe danger of ignoring sepsis, particularly oral sepsis.What made the address particularly remarkable wasthe surprising attack he made on conservative den-tistry, or as he called it, ‘‘septic dentistry’’:

No one has probably had more reason than I have hadto admire the sheer ingenuity and mechanical skill con-stantly displayed by the dental surgeon. And no one hashad more reason to appreciate the ghastly tragedies oforal sepsis which misplaced ingenuity so often carriesin its train. Gold fillings, gold caps, gold bridges, fixeddentures, built in, on, and around diseased teeth whichform a veritable mausoleum of gold over a mass of sep-sis to which there is no parallel in the whole realm ofmedicine.

Hunter was particularly fierce in his criticism ofAmerican dentistry. He blamed the ‘‘dirty grey, sal-low, pale, wax-like complexions, and chronic dys-pepsias, intestinal disorders, ill health, anaemias andnervous complaints’’ on ‘‘high class American’’ workand the inability of the dentist to recognize the sep-tic effects he produces (19).

Unfortunately for American dentistry, the highstandard of its work and the strong reputation it hadgarnered in Europe had led to a number of un-scrupulous European dentists adding DDS to theirtitle, and indeed, Edward Cameron Kirk, the re-spected editor of The Dental Cosmos, in reply toHunter’s attack suggested that the work Hunter hadseen was by an ‘‘advertising quack’’ and ‘‘... a so

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called American dentist, who had never seen Amer-ica and of whose cult London is full’’ (12). Kirk, how-ever, recognized the potential systemic effects of oralsepsis, for in that year’s description of dentistry inthe Encyclopaedia Britannica, he characterized theincreasingly apparent relationship between diseasesof the teeth and general pathology as laying the basisfor a scientific foundation in dentistry (11).

In 1911 Frank Billings, Professor of Medicine andhead of the focal infection research team at RushMedical College and Presbyterian Hospital in Chi-cago, replaced the term oral sepsis with ‘‘focal infec-tion’’. In the Lane medical lecture delivered in SanFrancisco in 1915, he defined a focus of infection asa ‘‘circumscribed area of tissue infected with patho-genic organisms’’ and said that the term focal infec-tion implied 1) that such a focus or lesion of infec-tion existed, 2) that the infection was bacterial in na-ture and 3) that as such it was capable ofdissemination, resulting in systemic infection ofother contiguous or noncontiguous parts. Theseareas were most commonly located in the head inthe form of an alveolar abscess, an infected tonsil,or a chronic sinusitis, although other areas such asa cholecystitis could equally be a cause of focal in-fection (5). Billings advocated the removal of all fociof infection and the improvement in patient immun-ity by absolute rest and improvement of the generaland individual hygiene. It was his opinion ‘‘thatthese measures alone will stop the further progressof the disease, and usually entire recovery will takeplace’’ (4). A measurement of the clinical benefit ofremoving focal infection was conducted as a retro-spective postal survey in 1917. Twenty-three percentof cases reported a cure for their arthritis followingremoval of infective foci, while another 46% experi-enced some improvement in symptoms (17).

One of Billings’ research associates in Chicago wasDr. E.C. Rosenow, who later went on to work at theMayo Clinic in Minnesota. He utilized specialmethods for culturing material from various foci ofinfection. He obtained a number of pathogenic bac-teria, including streptococci and gonococci, whichwere injected in animals. He found that strains ofthese organisms obtained from patients with chronicarthritis, rheumatic fever, or chronic infectious en-docarditis, when injected into animals, tended toproduce lesions similar to the secondary manifes-tations noted in the patients from whom the foci hadbeen removed. On the basis of these experimentalresults, Rosenow introduced the term ‘‘elective local-ization’’ for certain strains of pathogenic organisms,with special reference to streptococci, meaning that

A history of oral sepsis as a cause of disease

these bacteria had special predilection for joints,cardiac valves, uvea of the eyes etc. (34).

Focal infection was also implicated as being acausative factor in miscarriage, pyelitis, mastitis,phlebitis, anemia and toxemia in pregnancy (13), aswell as predisposing to ‘‘gastric cancer’’ (36). Leadingmembers of the medical community such as CharlesMayo of the Mayo Clinic advocated the focal infec-tion theory. He stated that ‘‘in children the tonsilsand mouth probably carry eighty percent of the in-fective diseases that cause so much trouble in laterlife’’ (24). Rosenow advocated that

... the prevention of oral sepsis in the future, with a viewto lessening the incidence of systemic diseases, shouldhenceforth take precedence in dental practice over thepreservation of the teeth almost wholly for mechanicalor cosmetic purposes, as has largely been the case inthe past (6).

What followed in dentistry was the avoidance of con-servative dentistry in favor of extractions. There de-veloped a philosophy by which many dentists prac-ticed that came to be known as the ‘‘hundred per-center’’, whereby all teeth that were endodontically(symptomatic, asymptomatic or successfully treated)or periodontally involved were extracted to avoid apossible focus of infection. The leading spokesper-son for this radical approach was the physiologistMartin H. Fisher from Cincinnati. He regarded atooth with a root filling as a dead organ. To Fisher,extraction was the only possible way out of what hetermed ‘‘the dentists’ dilemma’’.

The turning of the tide in dentistry

An editorial in The Dental Cosmos in 1930 stated that

the policy of indiscriminate extraction of all teeth inwhich the pulps are involved has been practiced suffi-ciently long to convince even the most rabid ‘‘hundredpercenter’’ that it is irrational and does not meet thedemands of either medical or dental requirements, andmuch less those of the patient.

The editorial called for a return to ‘‘constructiverather than destructive treatment’’. The medicalcommunity also started to re-evaluate its approachto focal infection. R.C. Cecil, who had been a greatproponent of the focal infection theory, published anarticle in 1938 in which he reported a follow-upstudy of 156 patients with rheumatoid arthritis whohad teeth and/or tonsils removed because of foci ofinfection. Of the 52 patients that had teeth extracted,

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47 did not get any better and 3 became more ill (6).Williams & Burket (39) reviewed a series of paperson focal infection and found that

there is no good scientific evidence to support thetheory that removal of these infected teeth would re-lieve or cure arthritis, rheumatic heart disease, and kid-ney, eye, sin, or other disorders ... On the other hand, itis well to keep in mind that if a focus of infection hasbeen found in the mouth, every effort should be madeto remove the infection as a general hygiene measure.

Edmund Kells (a pioneer in the field of dental radi-ology) asserted that conservative treatment might bejustifiable but that the danger of focal infection hadto be kept in mind (12).

In 1951, the 2nd annual Workshop of the New Jer-sey section of the American Academy of DentalMedicine considered ‘‘Focal infection with relationto dental medicine’’. Submissions were made bymany study groups including periodontology, endo-dontics, oral surgery, internal medicine and pathol-ogy. The reports from this group were inconclusive;the periodontal group stated that ‘‘there is a directrelationship between a periodontal condition and anassociated systemic problem, particularly in opthal-mology and cardiology’’, whereas the endodonticgroup said there was no systemic contraindicationfor endodontic treatment of teeth, while later statingthat endodontics may act as a ‘‘trigger area’’ wherethere is a base of lowered resistance (29).

An editorial in the Journal of the American MedicalAssociation in 1952 (10) stated that the focal infec-tion theory had fallen out of favor because

many patients with diseases presumably caused by fociof infection have not been relieved of their symptomsby removal of the foci. Many patients with these samesystemic diseases have no evident focus of infection,and also foci of infection are, according to statisticalstudies, as common in apparently healthy persons asthose with disease.

Focal infection has continued to be explored as apossible cause or exacerbating factor of some sys-temic conditions, but this time it is being evaluatedon a scientific basis (9, 27, 30, 37). The concept offocal infection, while shifting in and out of favor asa pathogenic mechanism, has always been recog-nized as being potentially causal in bacterial endo-carditis. Most recently, intense attention has focusedon ‘‘oral sepsis’’ and its relation to the causology ofconditions such as osteopenia, diabetes, cardio-vascular disease, and pre-term low-birth-weight in-fants. Apparently, an old concept is seeing new light

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as biomedical research begins to unravel the mysteryof oral infection and systemic health.

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