Periodontology 2000, Vol.

23, 2000, 1318 Printed in Denmark All rights reserved

Copyright C Munksgaard 2000

PERIODONTOLOGY 2000
ISSN 0906-6713

A history of oral sepsis as a cause of disease

PAUL G . OR EILLY & N OEL M . C LAFFEY

The twentieth century had four main pathogenic concepts: autointoxication, focal infection, psychosomatic disease and autoimmunity (3). Psychosomatic disease and autoimmunity are not dealt with here as they are topics in their own right. However, autointoxication will be dealt with in some detail, as it was popular and coincidental with the concept of oral sepsis and focal infection, and treatment of patients was often based on the elimination of focal infection and intestinal bacteria. Autointoxication concerns the belief that the colon, with its large mass of living bacteria, can act by either absorbing bacterial toxins or by transporting living organisms from the bowel to other parts of the body. Ancient Egyptians would wash out their lower bowels. Louis XIV was the recipient of several thousand colonic irrigations in his lifetime. In the rst quarter of this century, bowel washing was a standard part of practice in medicine (20). It was believed that the accumulation of fecal material might shorten the life span because it becomes a nidus for microbes which produce fermentations and putrication harmful to the organism. Metchnikoff et al. advocated the administration of lactic acidproducing bacteria in an attempt to change the relative proportion of bacteria in the gut (26). One of the great proponents of this concept was the English surgeon William Arbuthnot Lane. He attributed a whole litany of human ailments to intestinal stasis: Gastric ulcer, gastric cancer, gall stones, cholecystitis, gall bladder cancer, loss of fat, wasting of voluntary muscles, degenerative changes in the skin, subnormal body temperature, Raynauds disease, mental apathy, stupidity, misery, insomnia, raised or depressed blood pressure, breast cancer, cardiac degeneration, Bright disease, pancreatitis, diabetes, eye degeneration, rheumatoid arthritis, cystitis, pyleitis, endometritis, salpingitis, Stills disease and bacterial endocarditis (22). To eliminate this intestinal stasis, he advised that

the colon be evacuated three times a day. He devised surgical procedures to speed the elimination of intestinal contents and described them fully in his book The operative treatment of chronic constipation (23). These methods included tacking up a sagging colon, releasing constricting mesenteric bands, short-circuiting by means of ileocolostomy and total colectomy. Novel studies were carried out to try to ascertain whether colonic stasis could be causative in many disorders. In one, a group of human volunteers had rectal plugs inserted for several days. The only symptoms encountered were headache and discomfort, quickly relieved by the release of the plug (1). As late as 1930, a routine part of urinalysis was the indican test for the presence of indol, presumed to reect bacterial overgrowth in the intestinal tract. It is still felt that an overgrowth of intestinal bacteria in certain diseases can cause steatorrhea and vitamin B12 deciency (3), and in complementary medicine colonic lavage has again become popular as both treatment for some diseases and also as a method of achieving weight loss.

Oral sepsis
Oral sepsis was rst introduced into the medical literature in a report entitled Oral sepsis as a cause of disease (18) by William Hunter in 1900. This was then superseded by focal infection, introduced by Frank Billings in 1911 (4). However, a careful review of the medical literature indicates that the belief that conditions affecting the mouth could have implications on peripheral tissues and organs has been held from the very earliest medical recordings. In ancient Egypt the importance of oral hygiene appears not to have been appreciated, with discovered human remains exhibiting large accretions of calculus with consequent periodontal bone loss even

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though oral hygiene devices have been discovered in the burial crypts of royal princesses of the 12th Dynasty (21301930 BC), and one of the oldest medical papyri of the Middle Dynasty (2100 BC) mentions tooth pain associated with disease of womens reproductive system (15).

The middle ages

The next notable occurrence in dentistry probably occurred in the Middle Ages. In 1548, Walter Hermann Ryff wrote a monograph that dealt exclusively with dental afictions. In this pamphlet entitled Useful instructions on the way to keep healthy, to strengthen and re-invigorate the eyes and the sight. With further instructions of the way of keeping the mouth fresh, the teeth clean and the gums rm he makes the following statement (33):
The eyes and teeth have an extraordinary afnity or reciprocal relation to one another, by which they easily communicate to each other their defects and diseases, so that one cannot be perfectly healthy without the other being so too.

Ancient civilizations
Sound, healthy teeth were highly valued by the early Hebrews. The physical requirements for the role of High Priest as stated in Leviticus prevent anyone from serving who is not a whole person, and the Rabbis have interpreted this to include one who has even a single tooth missing. One reference in the Babylonian Talmud (AD 352427) suggests a connection between the oral cavity and the eyes, for it says to avoid the extraction of the eye tooth because your eyes must suffer instead (31). The Hebrew book Sefer haolsmot o maaseh tovia compared the human body to a house. The mouth was seen as the doorway and must be kept scrupulously clean to protect the body from contamination. In Niniveh, the capital of ancient Assyria on the eastern bank of the river Tigris, a Cuneiform table was found whose text deals with a King Ashurbanipal (669626 BC) whose physician said The pains in his head, arms and feet are caused by his teeth and must be removed (12, 16). The Greeks considered strong teeth indicative of good health. Diocles of Carystus, an Athenian physician of Aristotles time, stated Every morning you should rub your gums and teeth with your bare ngers and with nely pulverized mint, inside and outside, and remove thus the adherent particles (31). Hippocrates (400 BC) described a patient with rheumatism whose arthritis was cured by the extraction of a tooth (24). The Roman physician Galen (166201 AD) believed that the head was the source of all ills. An extract from his book On hygiene emphasizes this inter-relationship between the oral cavity and other illnesses although he sees oral sepsis as being the result rather than the cause of a variety of ailments.
When the head becomes disordered in nature it produces many excrements from which lesions of the lower organs occur because excrement passes to them. Now most readily their passage is to the mouth ... It is obvious also that uvulitis, tonsillitis and gingivitis and cervical adenitis and dental caries and ulcers and pyorrhea in the mouth are due to the catarrhal ichors descending to them from the head (31).

Giovanni dArcoli stated that, in cases of violent dental pains, early intervention was advisable as such violent pains are followed by syncope or epilepsy, through injury communicated to the heart or brain (2). The importance of oral hygiene in relation to bacteriology was rst detailed by the Dutch scientist Antonie von Leeuwenhoek in 1683. Using a primitive homemade microscope, he described animicules found in scrapings from between the teeth. He related lack of oral hygiene to an increase in the quantity of these organisms (8). In 1768, Thomas Berdmore in A treatise on the disorders and deformities of the teeth and gums described the relationship between the teeth and the entire body as one leading to the most excruciating pains and dangerous inammations and sometimes deep seated abscesses which destroy neighboring parts and affect the whole system by sympathy, or by infecting the blood with corrupted matter (32).

Modern times
In 1818, one of the most famous physicians in America, Benjamin Rush (a signatory to the Declaration of Independence) reported the course of a disease in which a woman who was suffering from rheumatism of long standing had an aching tooth extracted and she recovered in just a few days (32). The evolution of the study of microbiology took major strides in the nineteenth century thanks to the work of Pasteur, Lister and Koch. In 1884, Koch presented a paper on the causation of tuberculosis that included recovery of the organism from the infected patients, identifying it microscopically, obtaining

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A history of oral sepsis as a cause of disease

pure cultures and producing the infection by inoculation of the pure culture (31). These later became known as Kochs postulates. Working in Kochs laboratory at this time was an American dentist W.D. Miller. In 1891 Miller published a classic article entitled The human mouth as a focus of infection (28). In this article he endeavors
to call attention to the various diseases both local and general, which have been found to result from the actions of micro-organisms which have collected in the mouth, and to the various channels through which these micro-organisms or their waste products may obtain entrance to parts of the body adjacent to or remote from the mouth.

sepsis as a cause of disease (18), in which he states because of oral sepsis

... that not only is the constant swallowing of pus a most potent and prevalent cause of gastric trouble, but that the catarrh set up is not simply irritant but actually infective, and may lead in time to other more permanent effects namely atrophy of glands and chronic gastritis and in certain cases even to suppurative gastritis.

He also tried to establish the great importance of a thorough understanding on the part of the physician, no less than of the dentist, of mouth germs as a factor in the production of disease. Diseases he felt were able to be traced to the action of mouth bacteria 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 stulae of dental origin that opened on the neck, shoulder, arm or breast and cites a case report of a 33-year-old woman where
the connection of a chronic stula on the breast just above the nipple was discovered by the discharge, on the day following a visit to a dentist, smelling like the medicament used by the dentist in treating a badly diseased root. A solution of cochineal injected into the root also made an appearance at the opening of the stula a few hours later.

The stula resolved upon extraction of the tooth. Miller stressed that, wherever such germ organisms existed, there was a risk that they could produce a metastic abscess wherever a point of diminished resistance existed. Therefore not only teeth may be suspected as a focus he said but other organs as well such as the tonsils and uterus. Miller presented this paper at the International Congress of Hygiene, in the Bacteriology section presided over by Lord Lister. In the audience that day was William Hunter, at that time the senior assistant physician at the London Fever Hospital. This topic particularly interested Dr. Hunter, as his earlier work on pernicious anemia had drawn his attention to the mouth as a possible source of infection. In 1900, he wrote an article entitled Oral

However, he did not believe that the effects of oral sepsis were conned to gastritis but also diseases such as tonsillitis, glandular swellings, middle-ear suppurations, ulcerative endocarditis, empyemata, meningitis, nephritis and osteomyelitis. He advocated oral antisepsis measures including the application of carbolic acid (a 1 to 20 solution) to diseased teeth or inamed gums, the removal of tooth stumps, the boiling of every tooth plate worn and the avoidance of too much conservative dentistry and the use of contrivances like bridges which cannot be kept aseptic. In 1900, Godlee (14) described how the signs and symptoms of other conditions (such as pleurisy and suspected carcinoma of the stomach) could be attributed to pyorrhea alveolaris and how all the signs and symptoms disappeared after careful removal of all calculus and regular syringing of the pockets with a hydrogen peroxide solution. In 1902, Colyer described the resolution of irregular heartbeat, gastric effects and general debility after the treatment of any oral sepsis present. He also suggested a good maxim for the dentist to work was better no teeth than septic ones (7). Antral disease was put forward as an important sequela of oral sepsis. It was believed that prolonged antral suppuration could lead to extreme mental depression, often ending in a suicidal tendency (38). Also special reference was made to oral asepsis before surgical procedures involving the pelvic viscera with several cases of parotitis and fatal cases of angina ludovica following pelvic operations being attributed to buccal sepsis. Other relationships that were put forward were those between oral sepsis and migraine headaches, laryngeal pain and spasm (which could induce cough, loss of voice and wasting), blindness and deafness all which may be cured on treatment of the oral sepsis (21). As the theory of oral sepsis became more popular, theories were put forward as to which organs were most susceptible to different types of oral sepsis and how the treatment of oral sepsis could lead to recovery from tonsillitis, tuberculosis and diabetes. It was

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also believed that oral sepsis could be transmitted by the licking of envelopes, use of contaminated telephone receivers and men with beards (35). In many cases of malnutrition the sole cause was felt to be a lthy mouth and that no greater good could come to humanity than the full recognition of the dangers from this insidious, prolic, and virulent infection in the human mouth and that the adoption of proper oral hygiene practices would result in immediate and marked improvement to general health, and in notable increase in the average duration of human life (25).

Oral sepsis and septic dentistry

On October 3rd, 1910, William Hunter delivered an address at the opening of McGill University in Montreal. The title of his address was The role of sepsis and antisepsis in medicine, and because he was considered the pre-eminent physician in this eld, his address was reprinted fully in the leading British medical journal of the time, The Lancet. In his address he formally warned his medical colleagues of the danger of ignoring sepsis, particularly oral sepsis. What made the address particularly remarkable was the surprising attack he made on conservative dentistry, or as he called it, septic dentistry:
No one has probably had more reason than I have had to admire the sheer ingenuity and mechanical skill constantly displayed by the dental surgeon. And no one has had more reason to appreciate the ghastly tragedies of oral sepsis which misplaced ingenuity so often carries in its train. Gold llings, gold caps, gold bridges, xed dentures, built in, on, and around diseased teeth which form a veritable mausoleum of gold over a mass of sepsis to which there is no parallel in the whole realm of medicine.

Hunter was particularly erce in his criticism of American dentistry. He blamed the dirty grey, sallow, pale, wax-like complexions, and chronic dyspepsias, intestinal disorders, ill health, anaemias and nervous complaints on high class American work and the inability of the dentist to recognize the septic effects he produces (19). Unfortunately for American dentistry, the high standard of its work and the strong reputation it had garnered in Europe had led to a number of unscrupulous European dentists adding DDS to their title, and indeed, Edward Cameron Kirk, the respected editor of The Dental Cosmos, in reply to Hunters attack suggested that the work Hunter had seen was by an advertising quack and ... a so

called American dentist, who had never seen America and of whose cult London is full (12). Kirk, however, recognized the potential systemic effects of oral sepsis, for in that years description of dentistry in the Encyclopaedia Britannica, he characterized the increasingly apparent relationship between diseases of the teeth and general pathology as laying the basis for a scientic foundation in dentistry (11). In 1911 Frank Billings, Professor of Medicine and head of the focal infection research team at Rush Medical College and Presbyterian Hospital in Chicago, replaced the term oral sepsis with focal infection. In the Lane medical lecture delivered in San Francisco in 1915, he dened a focus of infection as a circumscribed area of tissue infected with pathogenic organisms and said that the term focal infection implied 1) that such a focus or lesion of infection existed, 2) that the infection was bacterial in nature and 3) that as such it was capable of dissemination, resulting in systemic infection of other contiguous or noncontiguous parts. These areas were most commonly located in the head in the form of an alveolar abscess, an infected tonsil, or a chronic sinusitis, although other areas such as a cholecystitis could equally be a cause of focal infection (5). Billings advocated the removal of all foci of infection and the improvement in patient immunity by absolute rest and improvement of the general and individual hygiene. It was his opinion that these measures alone will stop the further progress of the disease, and usually entire recovery will take place (4). A measurement of the clinical benet of removing focal infection was conducted as a retrospective postal survey in 1917. Twenty-three percent of cases reported a cure for their arthritis following removal of infective foci, while another 46% experienced some improvement in symptoms (17). One of Billings research associates in Chicago was Dr. E.C. Rosenow, who later went on to work at the Mayo Clinic in Minnesota. He utilized special methods for culturing material from various foci of infection. He obtained a number of pathogenic bacteria, including streptococci and gonococci, which were injected in animals. He found that strains of these organisms obtained from patients with chronic arthritis, rheumatic fever, or chronic infectious endocarditis, when injected into animals, tended to produce lesions similar to the secondary manifestations noted in the patients from whom the foci had been removed. On the basis of these experimental results, Rosenow introduced the term elective localization for certain strains of pathogenic organisms, with special reference to streptococci, meaning that

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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 a causative factor in miscarriage, pyelitis, mastitis, phlebitis, anemia and toxemia in pregnancy (13), as well as predisposing to gastric cancer (36). Leading members of the medical community such as Charles Mayo of the Mayo Clinic advocated the focal infection theory. He stated that in children the tonsils and mouth probably carry eighty percent of the infective diseases that cause so much trouble in later life (24). Rosenow advocated that
... the prevention of oral sepsis in the future, with a view to lessening the incidence of systemic diseases, should henceforth take precedence in dental practice over the preservation of the teeth almost wholly for mechanical or cosmetic purposes, as has largely been the case in the past (6).

47 did not get any better and 3 became more ill (6). Williams & Burket (39) reviewed a series of papers on focal infection and found that
there is no good scientic evidence to support the theory that removal of these infected teeth would relieve or cure arthritis, rheumatic heart disease, and kidney, eye, sin, or other disorders ... On the other hand, it is well to keep in mind that if a focus of infection has been found in the mouth, every effort should be made to remove the infection as a general hygiene measure.

What followed in dentistry was the avoidance of conservative dentistry in favor of extractions. There developed a philosophy by which many dentists practiced that came to be known as the hundred percenter, whereby all teeth that were endodontically (symptomatic, asymptomatic or successfully treated) or periodontally involved were extracted to avoid a possible focus of infection. The leading spokesperson for this radical approach was the physiologist Martin H. Fisher from Cincinnati. He regarded a tooth with a root lling as a dead organ. To Fisher, extraction was the only possible way out of what he termed the dentists dilemma.

Edmund Kells (a pioneer in the eld of dental radiology) asserted that conservative treatment might be justiable but that the danger of focal infection had to be kept in mind (12). In 1951, the 2nd annual Workshop of the New Jersey section of the American Academy of Dental Medicine considered Focal infection with relation to dental medicine. Submissions were made by many study groups including periodontology, endodontics, oral surgery, internal medicine and pathology. The reports from this group were inconclusive; the periodontal group stated that there is a direct relationship between a periodontal condition and an associated systemic problem, particularly in opthalmology and cardiology, whereas the endodontic group said there was no systemic contraindication for endodontic treatment of teeth, while later stating that endodontics may act as a trigger area where there is a base of lowered resistance (29). An editorial in the Journal of the American Medical Association in 1952 (10) stated that the focal infection theory had fallen out of favor because
many patients with diseases presumably caused by foci of infection have not been relieved of their symptoms by removal of the foci. Many patients with these same systemic diseases have no evident focus of infection, and also foci of infection are, according to statistical studies, as common in apparently healthy persons as those with disease.

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 in which the pulps are involved has been practiced sufciently long to convince even the most rabid hundred percenter that it is irrational and does not meet the demands of either medical or dental requirements, and much less those of the patient.

The editorial called for a return to constructive rather than destructive treatment. The medical community also started to re-evaluate its approach to focal infection. R.C. Cecil, who had been a great proponent of the focal infection theory, published an article in 1938 in which he reported a follow-up study of 156 patients with rheumatoid arthritis who had teeth and/or tonsils removed because of foci of infection. Of the 52 patients that had teeth extracted,

Focal infection has continued to be explored as a possible cause or exacerbating factor of some systemic conditions, but this time it is being evaluated on a scientic basis (9, 27, 30, 37). The concept of focal infection, while shifting in and out of favor as a pathogenic mechanism, has always been recognized as being potentially causal in bacterial endocarditis. Most recently, intense attention has focused on oral sepsis and its relation to the causology of conditions such as osteopenia, diabetes, cardiovascular disease, and pre-term low-birth-weight infants. Apparently, an old concept is seeing new light

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

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