The combination syndrome: A literature review

Sigvard Palmqvist, LDS, Odont Dr,a Gunnar E. Carlsson, LDS, Odont Dr, Dr Odont hc,b and Bengt Owall, LDS, Odont Dr, Dr Med hcc School of Dentistry, University of Copenhagen, Copenhagen, Denmark; and School of Dentistry, Goteborg University, Goteborg, Sweden
Although combination syndrome is recognized by many clinicians, documented observations seem to be rare. The aim of this article was to critically review the literature regarding combination syndrome to evaluate the evidence for this concept. A search of the dental literature with Medline/PubMed through July 2002, focusing on the combination syndrome and related features, was undertaken and combined with a hand search of older references and textbooks on removable prosthodontics. (J Prosthet Dent 2003;90:270-5.)

oss of bone of the anterior edentulous maxilla when opposed by natural mandibular anterior teeth is 1 of several features of the combination syndrome. Although recognized by many clinicians, documented observations seem to be rare. The Glossary of Prosthodontic Terms1 denes combination syndrome as the characteristic features that occur when an edentulous maxilla is opposed by natural mandibular anterior teeth, including loss of bone from the anterior portion of the maxillary ridge, overgrowth of the tuberosities, papillary hyperplasia of the hard palatal mucosa, extrusion of mandibular anterior teeth, and loss of alveolar bone and ridge height beneath the mandibular removable partial denture bases, also called anterior hyperfunction syndrome. Ellsworth Kelly2 was the rst person to use the term combination syndrome. He followed a small group of patients wearing a complete maxillary denture opposed by mandibular anterior teeth and a distal extension distal removable partial denture (RPD). Of the 6 patients followed up for 3 years, all showed a reduction of the anterior bone in the maxilla along with enlarged tuberosities. For 5 patients there was an increased bone level of the tuberosities. Kelly2 blamed the mandibular RPD and the lack of a posterior seal in the maxillary denture for these changes. He discussed excessive bony resorption under the mandibular removable partial denture bases but provided no values. Kelly2 discussed various possibilities to avoid combination syndrome, including extraction of the mandibular teeth, but did not advocate this solution. Instead, he proposed using the roots of anterior mandibular teeth to support an overdenture. He also mentioned the option of using endodontic ima

plants to preserve questionable roots for support in the posterior part of the mandible. A few years later, further characteristics were added to the combination syndrome: loss of vertical dimension of occlusion, occlusal plane discrepancy, anterior spatial repositioning of the mandible, poor adaptation of the prostheses, epulis ssuratum, and periodontal changes.3 However, these changes are not generally associated with combination syndrome. In spite of his emphasis on the negative role of the mandibular RPD, Kelly2 wrote: The early loss of bone from the anterior part of the maxillary jaw is the key to the other changes of the combination syndrome. This view was previously published in The American TextBook of Prosthetic Dentistry4 in 1907 in the following manner: One of the most commonly observed cases of this sort (localized adsorption) is that in which a full upper plate denture is antagonized only by six or eight lower natural teeth, there being no teeth posterior to this point, adsorption of the alveolar process in the maxilla in front occurring as a result of the undue pressure on it. Clinicians have recognized a number of the aforementioned features in some patients, but documented observations are rare. About 25 years after the publication of Kellys2 article, a review of sequelae of treatment with complete dentures argued that there was a lack of evidence for the combination syndrome.5 Today, accepting the principle of evidence-based dentistry, a critical review of the documentation behind the concept of combination syndrome seems warranted. The aim of this article was to evaluate the evidence for this concept.

LITERATURE REVIEW
A search of medical and dental literature through July 2002 was undertaken by use of Medline/PubMed. The focus of the search was on combination syndrome and related features such as alveolar bone loss, bone resorption, maxillary tuberosities, denture stomatitis, and maxillary abnormalities, all combined with removable partial denture variables. Along with the articles found
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Professor emeritus, Department of Prosthetic Dentistry, University of Copenhagen. b Professor emeritus, Department of Prosthetic Dentistry, Goteborg University. c Professor and Chair, Department of Prosthetic Dentistry, University of Copenhagen. 270 THE JOURNAL OF PROSTHETIC DENTISTRY

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in Medline/PubMed, those found by a hand search of older references were also considered. In addition, some common textbooks on removable prosthodontics were scrutinized for additional documentation.

Residual ridge resorption general aspects

After extraction of teeth, a remodeling process of the alveolar bone occurs, including bone resorption and a changed contour.6,7 The loss of bone in the maxilla was reported to be less if an immediate denture technique was used compared with a healing period without denture.8,9 For the mandible, no difference or a smaller difference in resorption rate during this initial stage was found between the immediate technique and a healing period without denture.9,10 After the initial remodeling phase, there is continuous bone resorption under denture bases. It is inevitable and has been called a major oral disease entity.11 The initial prosthetic technique probably has no long-term inuence on residual ridge resorption, which is more pronounced in the mandible than in the maxilla and has been demonstrated to occur for up to 30 years.11-14 Bone resorption under dentures can affect not only the alveolar bone but also, in some situations, the basal bone.11-13 However, great individual differences have been noted, and factors other than the wearing of removable dentures may be involved in the resorption process.15-17 There are clear indications and little doubt that the removable denture plays an important causative role in the bone resorption process. This is supported by studies showing signicant differences in residual alveolar bone between edentulous subjects wearing or not wearing removable dentures.18,19 Subjects not wearing dentures had more remaining bone. In groups of patients who had been wearing complete mandibular dentures for different lengths of time, the continuous bone resorption stopped in the areas distal to the mandibular foramina after the patients had been provided with xed prostheses supported by implants placed anterior to the foramina.20 In another study, a xed implant-supported prosthesis of the same design produced bone apposition in the posterior parts of the mandible, whereas an overdenture supported by 2 implants resulted in a continuous resorption of the same areas.21 Moreover, animal studies have shown that continuous pressure from an experimental denture caused bone resorption when exceeding a threshold value, and that the resorbed bone was not reshaped when pressure was discontinued.22-24

Maxillary ridge resorption in relation to mandibular status

Mandibular natural teeth with or without RPD. Bone resorption in the anterior part of the edentulous maxilla, the main feature of the combination syndrome, has been the subject of many clinical reports and some inSEPTEMBER 2003

vestigations of series of patients. No longitudinal study with the extraction of the anterior maxillary teeth as the starting point and randomly chosen mandibular status exists. Most studies comprise only small groups of patients. However, some cautious conclusions may be drawn by comparing results from available studies of various designs. Most studies have used radiographic cephalometry for measurement of residual ridge height. With this technique, 1 study7 compared bone resorption of the anterior maxilla in patients wearing a complete maxillary denture with different mandibular status: (1) mandibular complete denture; (2) anterior mandibular teeth and a Class I mandibular RPD; and (3) natural mandibular teeth only. No statistically signicant differences were found between these groups. However, the smallest resorbed area of the maxillary residual ridge, calculated from the radiographs for the period between 6 months and 5 years after extraction, was noted for group 3 (natural teeth only). Grouping the subjects with complete dentures together with those with natural teeth including molars, and comparing them with a group having only anterior teeth (with or without an RPD) showed slightly greater bone resorption in the latter group which was signicantly different (P .05). However, there were considerable individual variations in the extent of the changes in all groups. In a 21-year follow-up of the same patients, the individual variations were still very large, and there was no support for systematic development of combination syndrome.13 At the same center, other groups of patients with a maxillary complete denture and various prosthodontic solutions for the partially edentulous mandible were also followed.25,26 The rst group had no posterior teeth and no RPD; the second group had a Class I mandibular RPD; the third group had an RPD retained by a bar splint uniting crowns, primarily on the canines. Over a 5-year period there was a signicant reduction of the measured height of the anterior maxillary bone in the rst 2 groups with similar mean values for both groups. In the bar splint group no signicant reduction in bone height was noted in the anterior maxilla. When evaluating the horizontal dimension and calculating the anterior bone area of the maxillary residual ridge on the radiographs, a reduction was noted in all groups without signicant differences between them. Only small and statistically insignicant changes in the bone height of the edentulous maxilla were found during a 5-year observation period in a patient group where the complete maxillary denture was opposed by a bar-retained mandibular RPD.27 The bone resorption under complete maxillary dentures was also studied during a 5-year period in patients wearing either a conventional complete mandibular denture or an overdenture supported by roots of the mandibular canines.28 Similar values were noted for both groups. An earlier longitudi271

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nal study over 7 years found no signicant difference in maxillary bone resorption in patients wearing a complete maxillary denture opposed by either a complete mandibular denture or natural teeth and a removable partial denture, even if somewhat higher values were noted in the latter group.29 Examination records were reviewed in 150 consecutive denture patients at a dental school with regard to prevalence of symptoms associated with combination syndrome.30 All patients had a maxillary complete denture; however, the mandibular status differed. Maxillary anterior alveolar bone loss was nearly nonexistent in the group with complete mandibular dentures as well as in the group with natural dentition including bilateral molars. In groups with unilateral or bilateral missing molars, different percentages of maxillary anterior bone loss were noted. However, the authors found no significant difference related to whether the patients wore an RPD or not. This might partly be explained by the small number of subjects in these 2 groups. In fact, the highest percentage of maxillary anterior alveolar bone loss (56%) was noted for the group wearing a Class I mandibular RPD. The authors listed 5 changes most consequential to denture wearing and most difcult to correct: maxillary anterior bone loss, mandibular posterior bone loss, maxillary alveolar ridge canting, tuberosity enlargement, and hypermobile maxillary residual ridge. All of these changes were prevalent in less than 7% of the total sample but were found in 24% of the patients with a bilateral distal-extension RPD. It should be noted, however, that this was not an epidemiologic study of a random sample, but ndings in patients at a dental school. Further, all variables presented in the article were dichotomous, and the criteria were not claried to the readers. No epidemiologic study of the combination syndrome was found. Mandibular implant-supported or -retained prostheses. An Australian implant center reported on anterior bone resorption beneath complete maxillary dentures when opposed by implant-supported mandibular prostheses.31,32 The situation with a mandibular overdenture supported by 2 bar-connected implants resembled the situation with natural anterior teeth and an RPD. Maxillary changes similar to the combination syndrome, anterior bone loss in the maxilla, and posterior loss of occlusal contact were observed.31 The situation with a xed implant-supported prosthesis in the mandible32 did not appear to promote a condition similar to combination syndrome. However, loss of posterior occlusal contact was also observed in these patients. The anterior bone loss under a maxillary complete denture has also been studied when the mandibular overdenture was supported by a transmandibular implant with 4 posts penetrating the mandibular crest between the mental foramina.33,34 Some changes consistent with signs associated with combination syndrome
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were noted33 but maxillary bone resorption was smaller compared with that reported by Kelly2 in the situation with remaining anterior teeth and a Class I mandibular RPD. According to the authors, a possible explanation of these improved results could be that implants do not supra-erupt as natural teeth do.34 Using panoramic radiographs, Jacobs et al35 followed up 3 groups of patients, all with a complete maxillary denture. In the mandible, 1 group had a complete denture, another group an implant-retained overdenture, and the third group had a xed implant-supported prosthesis. The most pronounced annual bone resorption in the maxilla was noted in the complete denture group and was statistically signicant compared with the overdenture group. Bone resorption in the xed implantsupported prosthesis group demonstrated values in between the other 2 groups that were not signicantly different from the other groups. The masticatory forces and deformation of the maxillary complete denture during function have been studied in patients with either a complete denture or a xed implant-supported prosthesis in the mandible.36 The results showed a marked improvement in chewing ability after implant treatment, as indicated by changes in measured masticatory forces. However, no signicantly increased levels of loading were measured by the strain gauges placed in the maxillary dentures. The conclusion was that there should be no increased risk of failure or complications associated with loading clinically with the type of xed implant-supported prostheses that were studied. In another study of a group of patients with implantsupported overdentures in the mandible, frequent midline fractures of the opposing maxillary complete denture was noted, indicating an increase in denture deformation during function.37 However, this nding has not been conrmed in more recent studies.38-40 Regarding changes of the edentulous maxilla in complete denture wearers, there are also several studies in which radiographs have not been used but measurements have been performed on casts.41-43 The relevance of these studies concerning bone resorption can be questioned, and they are not included in this review.

Enlargement of the tuberosities

In a study of denture patients treated at a dental school,30 tuberosity elongation was found in 5% of patients with complete dentures in both jaws. In patients with bilaterally missing mandibular molars, tuberosity elongation was found in 22% of those wearing a removable partial denture and in 56% of those with no RPD. The groups were small, and the study was not longitudinal, indicating that no conclusions can be drawn about the development of the noted elongations.
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Papillary hyperplasia of the hard palates mucosa

Epidemiologic studies of mucosal changes in denture wearers mostly report low percentage gures for papillary hyperplasia of the hard palatal mucosa, also called papillomatous stomatitis.44,45 No study was found focusing specically on changes in the maxillary mucosa with respect to the mandibular dentition status.

Extrusion of mandibular anterior teeth

Kelly demonstrated extrusion of the mandibular anterior teeth in all 6 patients with combination syndrome followed up for 3 years by means of prole radiographs.2 The amount of extrusion varied between 1.0 and 1.5 mm. No other reports have been found regarding extrusion of mandibular anterior teeth in combination with a complete maxillary denture and a mandibular RPD.

Bone resorption under mandibular RPD bases

Continuous bone resorption in the mandible posterior to the remaining anterior teeth has been demonstrated in 2 groups of patients wearing different types of Class I mandibular RPDs, whereas no change of the bone level in the posterior region was noted for the group not wearing an RPD.25,26 In patients who received mandibular implant-supported xed prostheses, bone resorption in the posterior part of the mandible practically ceased.20 This result has been conrmed in recent studies, some even reporting bone apposition in the posterior areas when a xed implant-supported prosthesis was used.21,46 Most follow-up studies of removable partial dentures have not included measurement of bone resorption beneath the distal extension bases.47-50 For example, the longitudinal study over 25 years by Bergman et al49 provides no information on this point. However, it may be indirectly concluded that there were considerable changes of the supporting tissues judging from the frequent relining of the RPDs during the rst 10 years.48 Kelly2 provided values for the resorption in the edentulous maxilla but not for the posterior, edentulous parts of the mandible. A study of patients with a complete maxillary denture opposed by a mandibular distal extension RPD retained by an anterior bar revealed more bone resorption in the posterior mandible than in the maxilla.27

DISCUSSION
Dorlands Illustrated Medical Dictionary51 denes syndrome as a set of symptoms which occur together; the sum of signs of any morbid state; a symptom complex. Combination syndrome is not included among hundreds of syndromes listed in the dictionary. From this review of the literature it seems obvious that
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combination syndrome does not meet the criteria to be included in such a list. In a review of the literature, the authors have found no epidemiologic study of combination syndrome. Compared with the main feature, loss of bone from the anterior portion of the edentulous maxilla, ndings such as papillary hyperplasia of the hard palatal mucosa seem to be rare.44,45 Enlarged tuberosities may also have other causes than those described by Kelly2 as part of the combination syndrome. Enlarged tuberosities are often seen together with supraerupted maxillary molars. In situations where mandibular molars have been lost, the opposing maxillary molars may supraerupt together with the alveolar process.52 The supraeruption may create enlarged tuberosities without inuence of a denture. Not surprisingly, no randomized controlled trials (RCTs) on combination syndrome were found. A review of U.S. prosthodontic journals showed that less than 2% of 3631 articles published over a 10-year period could be classied as RCTs.53 A more extensive review up to the end of year 2000 identied 92 RCTs in prosthodontics, but none related to combination syndrome.54 Perhaps somewhat more surprising, is that there seems to be no prospective study of the combination syndrome in spite of the fact that many people have been provided with a complete maxillary denture opposed by anterior mandibular teeth with or without a Class I mandibular RPD. A long-term 21-year study of patients wearing complete maxillary dentures provided no support for a systematic development of the combination syndrome.13 This does not mean that the observations made by Kelly2 were false. In the title of his article, he emphasized the negative role of the mandibular RPD. The same view was expressed by Keltjens et al,55 who found the traditional treatment for an edentulous maxilla opposed by a partially edentulous mandible with a complete denture and a Class I mandibular RPD to be fundamentally inadequate. The authors also suggested use of implants for distal support. Loss of established posterior occlusal contacts has been discussed as an important factor in relation to the combination syndrome.30 However, loss of occlusal contacts can be attributed not only to bone resorption under mandibular distal extension bases but also to wear of the articial denture teeth, as well as to changes in position of the anterior mandibular teeth. It can be speculated that such changes in occlusion facilitate parafunctional activities such as clenching and thereby increase the pressure on the maxillary anterior alveolar bone. This speculative theory ts well with the result that patients who had been provided with Class I mandibular RPDs had development of more signs and symptoms of temporomandibular disorders over a 5-year period compared with a matched group of patients treated with cantilevered xed partial dentures.56 It is also compatible with results from in vivo measurements showing that
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a xed implant-supported prosthesis in the mandible opposing a complete maxillary denture improved the chewing ability but did not increase the levels of loads transferred to the denture base.36 Loss of alveolar bone and residual ridge height beneath the mandibular removable partial denture bases was included in the combination syndrome by Kelly.2 Reviewed articles have shown greater bone loss in the mandible associated with an RPD compared with when no RPD or a xed prostheses supported by anterior implants was provided.20,21,25,26,46 Compared with cantilevered xed partial dentures, conventional Class I mandibular RPDs have been shown to cause more carious lesions, more plaque and gingivitis, as well as more signs and symptoms of temporomandibular disorders.56,57 The poor biologic outcome with Class I mandibular RPDs constitutes a strong indirect support for the shortened dental arch concept,58,59 indicating that missing posterior teeth should not necessarily be replaced. It has been convincingly demonstrated that dentitions consisting of only anterior and premolar teeth can meet oral functional demands in most situations.60-63 Also in patients with dentitions associated with the combination syndrome (edentulous maxilla, bilaterally missing mandibular posterior teeth) it seems reasonable to adopt the shortened dental arch concept. This view is also in agreement with the well-documented excellent long-term results with xed mandibular prostheses supported by implants placed between the mental foramina and opposing maxillary complete dentures.64,65

SUMMARY
Bone resorption of the anterior part of the edentulous maxilla in association with remaining anterior mandibular teeth has been the subject of a limited number of studies of acceptable quality, but the results have not been conclusive. No epidemiologic study of the various features related to combination syndrome has been published. There is no evidence that a mandibular removable partial denture can prevent the development of the events described. On the basis of this review of the literature it may therefore be concluded that the combination syndrome does not meet the criteria to be accepted as a medical syndrome. The single features associated with the combination syndrome exist but to what extent or in which combinations has not been claried.
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