Factors in implant integration failure after bone grafting

Int. J. Oral Maxillofac. Surg. 1996; 25:63~68 Printed in Denmark. All rights reserved

Copyright9 1996 tn~.rnatlonalJournalof

Oral&

Maxill~acialSurgery ISSN 0901-5027

Research;development

Factors in implant integration failure after bone grafting An osteometricand endocrinologicmatchedanalysis

John Eric Blomqvist 1, Per Alberius a, Sten Isaksson 1, Anders Linde a, Bengt-G6ran Hansson 4 1Department of Oral and Maxillofacial Surgery, L~mssjukhuset,Halmstad; 2Department of Plastic Surgery, University of Lund, MAS, Maim6; aDepartment of Oral Biochemistry, Faculty of Odontology, G6teborg University,G6teborg; 4Department of Internal Medicine, L&nssjukhuset, Halmstad, Sweden

J. E. Blomqvist, P. Alberius, S. Isaksson, A. Linde, B.-G. Hansson: Factors in implant integration failure after bone grafting. An osteometric and endocrinologic matched analysis. Int. J. Oral Maxillofac. Surg. 1996; 25." 63~68. 9 Munksgaard, 1996 Abstract. In a retrospective analysis of 49 patients who received bone graft augmentation to the maxillary sinuses in conjunction with implant insertion, 11 patients had a significantly reduced success rate. The aim of the present study was to determine whether bone quality, as assessed by osteometry and selected haematologic and urinary tests, influences the integration of implants, and whether such data can be prognostically useful. Relative bone mass density (BMD%) differed significantly among these patients as compared to age- and sex-matched control patients receiving the same reconstructive treatment (P= 0.01). Other parameters tested did not demonstrate arty significant differences. In addition to local complications, general disorders, such as osteoporosis, must be considered in cases of excessive implant loss.

Accepted for publication21 August 1995

Rehabilitation of edentulous jaws with implants is quite predictable x,2. Loss of implants, due to failure to integrate, may cause therapeutic problems as well as patient anxiety and discomfort. This problem is even more pronounced when dealing with patients who have a severely resorbed maxilla which requires bone grafting. Most studies on the results of simultaneous implant insertion and bone grafting report implant losses near 20~ 4"9"10'12. In a recent retrospective study of 49 patients treated with sinusfloor augmentation using a technique described by LouIr et al. xS, the majority of patients lost 6% of the implants inserted4. In 11 patients, however, a larger percentage (43%) was lost, implying that renewed insertion prior to the manufacturing of a fixed bridge had

(classes V-VI5) who received implants and sinus-floor bone grafting by a one-stage procedure18. The study group lost significantly more fixtures (43%) than the remaining patients (6%) and were selected for further analyses. A control group, matched for sex and age, was obtained from the successfully treated patients, who directly obtained fixed bridges. The mean age was 59 years (range 46-75; Table 1). The osteometric and endocrinologic examinations were undertaken at a mean of 30 months (range 14-58) after the abutment operation at a regular follow-up.A questionnaire was filled out at the same visit (Tables 2a and b). All 22 patients were in good health. Only a few patients were prescribed regular medication; three (two in the experimental group and one in the control group) had antihypertensive medication, and two (one in each group) had taken corticosteroids for shorter periods in the past. None had diabetes mellitus, thyroid dysfunction, or pre-

to be undertaken. To avoid such failures, one must explore the mechanisms influencing bone-implant integration and to identify the characteristics of the recipient bone. The aim of this investigation was to evaluate to what extent bone quality, as assessed by osteometry and endocrinologic parameters, influences integration of implants, and whether such data can be used to predict the success of implant integration and, hence, identify high-risk patients.

Material and methods Patients Eleven patients (Table 1), four men .and seven women, were selected from a recent retrospective study4 of 49 patients with severely atrophied maxillary alveolar processes

Key words: bone graft; bone mineral density;

hormone; implant.

64

Blomqvist et al.

Table 1. Patient sample and distribution of inserted and lost implants Sex Experimental (n= 11) Controls (n=l 1)

Age

Male

Female

Mean

Range

4 4

7 7

59 59

46--75 44-71

vious treatment for malignant disease. No female patient had been operated on for any major gynaecologic disorder. One woman in the experimental group had been prescribed oestrogen substitution for more than 10 years.

Surgery The surgical technique used has been described previously ~s. The operations were performed under general anaesthesia, and included a palatinally pedicled mucoperiosteal flap raised to expose the lateral wall of the maxilla. A window, approximately 10x20 mm, was created to give access to the floor of the antral cavity. The antral mucosa was reflected superioy,,ly, and efforts were made to maintain mucosal integrity. Corticocancellous bone blocks, harvested from the anterior iliac crest, were placed on the sinus floor, with the cortical layer facing superiorly to secure a two-point compact bone anchorage by the inserted implants. Usually, no further fixation was necessary. Cancellous bone chips were used to fill spaces between the sinus floor and the bone graft. Great care was

Implants inserted

Implants lost

Relative loss

Graft Adjacent bone

Graft Adjacent bone

Graft Adjacent bone

39 41

35 30

taken to secure the initial stability of the graft and the implants.

Haematology Selected blood and urine samples (Table 3) were collected from each patient. These were analysed at the Central Chemical Laboratory, the County Hospital in Halmstad, or at the University Hospital in Lund.

Osteometry The bone mineral content on the forearm was measured by applying the method (Fig. 1) of single-photon gamma absorptiometry 6"8,16,17. An americium-241 source and a scintillation detector (DTX-100, Osteometer A/S, Rodovre, Denmark) were moved simultaneously across the forearm, which was placed in a basin with water completely covering the whole forearm. The bone mineral in the pathway of the beam was calculated. From the data printout, the approximate widths of the radius and ulna were estimated. The ulnar length (the distance from the tip of the olecranon to the tip of the ulnar

Table 2a. Contents of questionnaire; general issues Issue

Information

Physical constitution

Height Weight Weight at age 25 years

Dental care

Regularity, previous treatment

Edentulous maxilla

Duration Reason for loss of teeth

Fractures

History

Medication

Special attention to Hypertension Thyroid dysfunction Cortisone, number of periods exceeding 1 month

Diabetes mellitus

Present? What treatment Duration (years)

Smoking habits

Smoker/nonsmoker Age at debut Duration Number of cigarettes/day

Coffee drinking

Cups/day

Intake of dairy products

Amount/day

Physical activity

Profession Leisure activities

Malignancy

Previous? present? Treatment: cytostatics/radiation

18 2

14 2

46% 5%

40% 7%

styloid process) was measured. The scanning area was localized at a distance from the tip of the styloid process, corresponding to onequarter of the ulnar length. At this level, both bones are of similar dimensions, and for further calculations a hypothetical model bone, i.e., a radius or ulna constituting a cylindrical shape and without regard to the existing marrow cavity, was used to express the various parameters of bone mass. Parameters registered were bone mass content (BMC; g) and bone mineral density (BMD; g/cm2). "BMD percentage of age matched" (BMD%) describes the mean value matched for age and sex, and is normally 100%. The Z-score expresses this divergence numerically in SD (standard deviation); a divergence of slightly less than -1.0 SD (Zscore) implies an increased fracture risk of 23 times for a 50-year-old woman. The Tscore, comparing (in SD) each specific value relative to the mean value of a normal 40year-old subject of the same sex, was also re-

Table 2b. Contents of questionnaire; female issues Issue

Information

Menstruation

Age at debut Duration (years)

Contraceptives

Duration (months)

Births

Number of deliveries

Breast-feeding

Duration (months)

Gynaecologic interventions

Hysterectomy Ovarectomy

Oestrogen substitution Duration (years)

Source

~---'--'-'-~J

U 'Soft tissue

Detector

Fig. 1. Principle of single photon gamma absorptiometry.

65

Implant integration failure

Table 6. Comparison of osteometric values

Table 3. Analyses performed Standard

Thyroid

Weight Length S-calcium S-albumin

Bone markers

S-TSH S-T4 (free)

Urine

S-parathormone S-hydroxy-vit-D S-dihydroxy-vit-D S~alkaline phosphatase S-osteocalcin S-procoltagen peptide (type I) S-collagen telopeptide (type I)

U-Calcium/creatinine U-Cortisol

BMD Matched for

BMDpercentage of age matched

Sex, age, length, weight, arm (dominant/nondominant)

Z-score

As above

BMD percentage of reference age

Sex, age, length, weight, arm (dominant/nondominant), 40-year-old healthy woman

T-score

As above

Unit % Divergence from 100% in absolute figures related to SD %

Divergence from 100% in absolute figures related to SD

BMD=bone mineral density. SD=standard deviation.

Table 5. Results (mean, range) of haematotogic and urinary analyses Test S-calcium S-albumin S-alkaline phosphatase S-TSH S-T4 S-procollagen peptide S-collagen telopeptide S-parathormone S-dihydroxy-vit-D S-hydroxy-vit-D S-osteocalcin U-Ca/creatinine U-cortisol

Experimental (n = 11)

Range

Controls (n = 11)

Range

2.48 42 3.01 3.7 14.2 116 3.2 2.6 79 59 3.0 0.5 187

2.20-2.78 40-48 1.32-4.38 0.7-22.5 7.6-18.9 63-172 1.7-7.3 1.2-4.4 46-105 40-81 1.4--4.4 0.4-6.8 66-340

2.49 42 2.67 1.6 15.3 114 3.0 3.1 70 64 3.0 0.8 188

2.34-2.69 39-47 1.95 3.53 0.6-3.5 11.4-17.8 92 139 2.2-3.8 2.1-5.7 40-102 33-110 1.5-5.2 0.2-3.5 113-283

Normal ranges 2.20-2.60 mmol/1 36--48g/1 0.8~1.6/tkat/1 0.1-6.0 mUd 8.0-26.0 pmol/l 50-170/zg/l 1.8-5.0 pg/l 1.0-5.0 pmol/1 36-120 pmol/l 20-100 nmol/l 1.8-6.6/tg/l >0.7 80-350 mmol//day

No significant difference was registered between groups with Student's t-test.

corded. These variables are further presented in Table 4.

tation period. Gynaecologic interventions and present or earlier substitution with oestrogens were also noted.

Questionnaire

The questionnaire (Table 2a) contained questions on oral and general health issues, present medical problems, and medication. Any periods of corticosteroid medication exceeding t month, present or past, were recorded. Any history of malignant disease was noted. Smoking habits were registered, and the physical constitution and condition of the patients were checked. For female patients, some pertinent questions were added (Table 2b), such as start and cessation of menstruation, use of contraceptives, number of births, and length of lac-

BMD% Z-score BMD40 T-score

Experimental Controls (n=ll) (n=ll) 89.2 -0.86 77.5 -2.1

98.6 -0.09 85.8 - 1.3

P 0.01 0.006 0.053 0.048

BMD%=BMD percentage of age matched. Z-score=BMD percentage of age matched expressed in standard deviations (SD). BMD40=BMD percentage of reference age. T-score=BMD percentage of reference age expressed in standard deviations (SD). Statistical evaluation was performed with Student's t-test.

Table 4. Variables used for osteometric registration of bone mass Variable

Test

Results

The experimental and control groups received a total of 145 titanium screw implants (Brhnemark | M a r k II). The distribution o f inserted and lost implants is presented in Table 1. In the experimental group, 46% (18/39) of implants inserted in the sinus inlay graft were lost, as were 40% (14/35) of those inserted in the bone anterior to the maxillary sinuses. In controls, these

figures were 5% (2/41) and 7% (2/30), respectively. All mean haematologic and urinary parameters investigated were within n o r m a l ranges (Table 5). Only a few individual values were abnormal. One w o m a n in the experimental group exhibited an S-TSH of 22.5 m U d (normal range 0.1-6.0 mU/l). Two subnormal samples of S-osteocalcin (1.4 and 1.5 /zg/1) were detected in one patient from each group. The mean ratio (0.5) for UCa/creatinine in the experimental group was slightly less than for controls (0.8). N o significant differences between the groups in any o f the haematologic and urinary parameters were detected (Student's t-test). In the experimental group, significant correlations were found between alkaline phosphatase and procollagen peptide (r=0.847, P=0.001; controls: r=0.054, NS). The results of the osteometric assessment are presented in Table 6 and Figs. 2 and 3. The mean B M D % was 89.2% for the experimental group as compared to 98.6% for controls (P<0.01; Student's t-test). Similarly, the Z-score differed significantly (P<0.006). A linear multiple regression test, in which the dependent variable was the total relative loss of implants (experimental group, mean 43%; controls, m e a n 6%), and the B M D % constituted the independent variable, verified that the number o f lost implants was highly dependent on the B M D % registration (P=0.0275). If further independent variables, i.e., the haematologic or urinary parameters, were added in a linear regression test, no individual parameter seemed to have any influence on the number of lost implants. N o correlation (Pearson's correlation test) was found when investigating whether an in-

66

Blomqvist et al.

creased loss of implants was affected by any single variable. Smoking habits are presented in Table 7. The extent of smoking showed no correlation with BMD%. N o correlation was observed between any parameter analysed and the osteometric variables BMD% or Z-score of the experimental group. This included body mass index (Table 7) and the specific female parameters (Table 8).

4"

n u

e r

/

2

o

Experiment Controls

l

76-80

81-85

86-90

91-95

96-100

BMD%

Fig. 2. Distribution of patients relative to variations in BMD%.

110"

,~ "I

I I

-e

100-

80' [] Experiment 7O

O Controls

i

3

4

5

6

7

8

9

10

11

Patient pairs Fig. 3. Illustration of BMD% for each of 11 patient pairs.

Table 7. Results (mean) from questionnaire

Issue

Unit

Body weight (mean) Increase of body weight after age 25 years Body mass index Physical activity

kg kg Weight/length squared Yes No Office work Varying Walking, lifting Heavy work Periodontitis Caries Trauma Years No Yes Previous smoker Years

Working situation

Loss of maxillary teeth due to Edentulous for Smoking Duration of smoking Cigarettes/day

Discussion

>101

Experimental Controls (n = 11) (n = 11) 70.6 10.2 25 5 5 2 2 3 4 4 5 2 21 3 3 5 19 14

No significant difference was registered between groups using Student's t-test.

75.7 12.1 26 3 7 0 7 2 2 7 4 0 19 4 2 5 22 11

Implant integration failure is a problem familiar to most surgeons involved in reconstructive maxillofacial procedures. A second operation is 9sometimes required or the number of integrated implants is accepted, and then a bridge construction or overdenture is manufactured. When more implants are lost, the question arises of whether the surgical technique used was adequate or whether the quality and quantity of the recipient bone were sufficient or the healing conditions in general were disturbed. All 11 patients with extensive implant loss4 studied were operated on by experienced surgeons, and the technique did not differ from patient to patient. Initial stability was obtained in all patients. No local or general initial healing problem occurred. Consequently, it was thought important to investigate various systemic factors that could point to a specific risk factor. The purpose of this study was to analyse comprehensively the endocrinologic status and the bone quality of these patients. Several factors are known to enhance osteoporosis, such as ovarial dysfunction, low weight, smoking, alcohol intake, and the degree of physical activity 17. Several endocrinologic parameters known to detect and characterize normal bone metabolism were analysed. However, no significant difference was observed between these variables in the experimental group or in controls. One patient in each group will be further assessed for hyperparathyroidism, due to hypercalcaemia and high serum levels of parathormone. Not even procollagen peptide, known to increase in conditions exhibiting bone formation, or collagen telopeptide, believed to reflect bone resorption, contributed any significant data. A positive correlation was detected in the experimental group only for alkaline phos-

Implant integration failure Table 8. Female parameters (mean values) Experimental (n = 7)

Issue

Unit

Start of menstruation Cessation of menstruation Contraceptives

Age Age Yes No Months

Contraceptives Children Breast-feeding

Months

Controls (n = 7)

14 35 3 4 10 3.0 11.4

14 44 3 4 40 2.5 9.2

No significant difference was registered between groups with Student's t-test.

phatase and procollagen, seemingly implying ongoing bone remodelling. The metabolic status was probably static, and divergences are not easily detected on single examinations. All individuals in this age group will, sooner or later, reach a steady-state condition which, in all probability, is intermittent. Consequently, the chance of acquiring positive responses in the performed blood and urine tests, when analysed on a single occasion, appears small. However, serial evaluations are not indicated in this context simply because a preoperative evaluation is the only thing needed, in contrast to assessments in conjunction with treatment for osteoporosis. Interestingly, other somatic parameters, such as weight and body mass index, seemed not to contribute any meaningful information. Tobacco smoking is believed to have an antioestrogenic effect in postmenopausal women 1], and the duration of smoking negatively correlates with B M D in that age-group 13'2~ In this study, smoking habits did n o t significantly negatively influence B M D % or implant failure. Our material contained only a few smokers with a restricted consumption of tobacco, a fact which may explain the observation. The osteometric examination revealed interesting and useful information. Osteometry, which enables quantitative assessment of bone mass density, is used clinically mainly to characterize and evaluate treatment of osteoporosis and to assess the risk of fractures in the individual patient 6,s. A definite advantage of the technique used in this study is that its reproducibility, at repeated measurements, is very high 3. Highly significant differences between the patients with failed implants and sex- and age-matched controls were registered both for the B M D % and Zscore. This was verified by the multiple regression test. Such information may

be quite useful for future patient selection. For evaluation of the risk of implant failure in each patient, an equation of multiple response was calculated: y = 1 3 1 . 8 - 1.2• where y signifies the relative total implant loss (%). This equation has been tested and found quite accurate even in other patients subjected to bone grafting in reconstructive implant surgery. However, the n u m b e r of patients tested, as yet, is limited and further studies are contemplated. Previous studies dealing with generalized skeletal osteopenia and bone loss in the jaw in nongrafted patients have given vague and contradictory data 7A4,15. This new approach to a more accurate assessment of patients in need of reconstructive procedures in implantology requires further scientific evaluation, but seems, at present, to be clinically quite promising.

Acknowledgments. The valuable advice offered by Drs Anders Isaksson and Pavo Hedner, Lund University Hospital, is gratefully acknowledged. We thank Mrs Inga Lill Johansson, Varberg Hospital, for technical assistance with the osteometric tests, and Ms M.-L. Jonson for help with the line drawing.

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Address:

Dr John Eric Blomqvist Department of Oral and Maxillofacial Surgery LLinssjukhuset S-30185 Halmstad Sweden