Indian Journal of Dental Research

: 2010  |  Volume : 21  |  Issue : 3  |  Page : 349--352

Titanium implants: A removal torque study in osteopenic rabbits

Carine M Carvalho, Luiz F Carvalho, Lino J Costa, Marcelo J Sá, Cláudia R Figueiredo, Adílio S Azevedo 
 Clinics and Social Dentistry Department, Federal University of Paraíba, Paraíba, Brazil

Correspondence Address:
Carine M Carvalho
Clinics and Social Dentistry Department, Federal University of Paraíba, Paraíba


Context: Osteoporosis is a skeletal disorder characterized by low bone mass and microarchitectural deterioration of bone tissue. It may affect the craniomaxillofacial complex and result in less bone-implant contact. Aims: The objective of this study was to measure the endosseous integration of titanium implants using the removal torque test in low-mineral density experimental animal models. Materials and Methods: Thirty female New Zealand white rabbits were divided into two groups: control (n=14), sham-operated; and test (n=16), ovariectomized. All animals received 2.2 mm Χ 4.0 mm titanium implants in the right tibia, 120 days after ovariectomy or sham surgery. Animals were killed at 7 and 14 weeks of postimplant insertion, when implants were removed by reverse torque rotation using a digital torque meter. Statistical analysis used was Student«SQ»s t-test. Results and Conclusion: At the 7-week period, the mean torque values for the control and test groups were 11.6 Ncm and 10.4 Ncm, respectively, with no statistical significance. Implant removal torque analysis showed statistically lower values (P<0.05) for the test group at the 14-week period (control=16.7 Ncm and test=9.7 Ncm). The results of this study indicate that hormonal privacy compromise implants biomechanical performance.

How to cite this article:
Carvalho CM, Carvalho LF, Costa LJ, Sá MJ, Figueiredo CR, Azevedo AS. Titanium implants: A removal torque study in osteopenic rabbits.Indian J Dent Res 2010;21:349-352

How to cite this URL:
Carvalho CM, Carvalho LF, Costa LJ, Sá MJ, Figueiredo CR, Azevedo AS. Titanium implants: A removal torque study in osteopenic rabbits. Indian J Dent Res [serial online] 2010 [cited 2020 May 28 ];21:349-352
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Full Text

Osseointegration is a term initially suggested by Branemark [1] and was first defined as a histological concept with direct bone-to-implant contact at the resolution of a microscope. Later, in 1978, Zarb and Albrektsson proposed a new definition, "a process whereby clinically asymptomatic rigid fixation of alloplastic materials is achieved and maintained in bone during functional loading." [2] Due to the improvement of techniques, different shape, diameter, length, materials, coating and surface treatment, the use of osseointegrated implants as oral rehabilitation of partially and completely edentulous patients has become an excellent option. [3] The success of osseointegration depends, in part, on exogenous factors such as implant characteristics, biocompatibility, operator ability and surgical technique. [4] Endogenous factors such as state of the host bone, quantity, quality and its healing capacity must also be considered. [5]

In the last few decades, a number of factors have contributed to an increase in the life expectancy of human being leading to an elderly population and high rates of osteometabolic diseases such as osteoporosis. [6] According to the World Health Organization, osteoporosis is characterized by low bone mass and microarchitectural deterioration of bone tissue, leading to an increase of bone fragility and fracture risk. [7] It is well known that osteoporosis is associated with lower levels of bone forming factors (Osteoprotegerin - OPG; Insulin like growth factor 1 - GF-1; Tumor growth factor β - TGF- β) as well as a decreased capacity of osteoblasts to proliferate in response to systemic or locally released osteotropic factors and angiogenesis. An increase in pro-inflammatory cytokines such as interleukins (IL-1, IL-6) and tumor necrosis factor (TNF-α) is also observed. [8] In view that age, gender and estrogen deficiency are reported to be major risk factors of the disease and that osseointegration depends on a series of vascular and osteogenic events, it seems that implants failure may also be expected. [5] The purpose of this study was to determinate whether osteoporosis influences the implants remove torque values.

 Materials and Methods

The present study was initiated only after approval by the Institutional Animal Care and Use Committee, Federal University of Paraνba-Brazil, and was conducted in accordance with the standards of its Pharmaceutical Technology Laboratory. Two veterinary doctors duly settled in the Council of Veterinary Medicine were present in all surgical procedures performed in the study.

The experimental animals consisted of 30 female New Zealand white rabbits that were skeletally mature. The rabbits were kept in individual 80 cm Χ 35 cm Χ 50 cm stainless steel cages and were fed with a standard laboratory diet and water ad libitum. They were kept in an air-conditioned environment (24±1°C, 50-60% humidity) with a circadian light rhythm of 12 h/d. All animals were randomly divided into control group (n=14), submitted to sham surgery, and experimental group (n=16), submitted to ovariectomy surgery. A higher number of animals were assigned to the experimental group because this group was subjected to more invasive surgical procedures.

The food and water consumption were restricted 4 hr before ovariectomy or sham surgery. Animals were tranquilized with acepromazine 1% (Acepran® ; Univet-Brazil) and anesthetized with a combination of ketamine chlorhydrate 10% (Dopalen® ; Vetbrands-Brazil), at a concentration of 50 mg/kg, and xylazine chlorhydrate 2% (Rompun® ; Bayer-Brazil), at a concentration of 10 mg/kg body weight, administered intramuscularly. The test animals had their ovaries and uterus exposed and completely excised from a dorsal approach. In contrast, the control animals had their ovaries exposed and then returned to their original position. Postoperatively, antibiotic enrofloxacin 10% (Baytril® ; Bayer-Brazil) was administered during a period of 7 days and nonsteroidal antiinflamatory flunixin meglumine (Banamine® ; Schering-Plough-Brazil) was administered during a period of 3 days. A spray of hydrocortisone and oxytetracycline (Terra-Cortril® ; Pfizer-Brazil) was applied twice-a-day for 1 week.

After 120 days of the ovariectomies and sham surgeries, the animals were submitted to a bone mineral density analysis to evaluate the systemic bone mass loss. The distal tibial shaft of the rabbits were scanned three times by dual-energy X-ray absorptiometry using a densitometer (QDR 2000; Hologic, Bedford, MA, USA) at a location of 6 cm above the plantar aspect of the heel. [5]

Then, the animals were submitted to surgery for implant placement in the proximal third of the right tibia. Tranquilization and anesthesia were performed as cited before. The legs were shaved, washed and decontaminated with povidone-iodine 1% (PVP-I) (Riodeine Tσpico® ; Rioquνmica-Brazil) before surgical draping. A 10-mm incision was made on the internal side of the tibia and the bone surface was surgically exposed. Under continuous irrigation with sterile saline, cylindrical, commercially pure titanium screw implants with machined surface, 2.2 mm in diameter and 4.0 mm in length (Titanium Fix® ; A.S. Technology-Sγo Josι dos Campos-Sγo Paulo-Brazil) were inserted in a hole 2.0 mm in diameter drilled at a rotator speed not exceeding 1500 rpm. After implant placement, the soft tissues were replaced and sutured and the animals received the same antibiotic and antiinflamatory that was used previously.

Seven weeks post-operatively, half of the animals from both groups were sacrificed with an excess dose of sodium pentobarbital. The other animals were sacrificed after a 14-week period. Each implant was surgically exposed via sharp dissection. The reverse torque test was performed using a digital torque meter (Model TQ-8800® ; Lutron Electronic Enterprise CO. Ltd., Taiwan) with a force registry range of 0-147.1 Ncm. After adapting a wrench to the implant head, a torque was applied in the reverse direction of implant placement in order to rupture the bone-implant interface, signaled by rotation of the implant. This reading was performed by a single examiner who was blinded to the group tested.


The descriptive analysis resulted in average, median, standard deviation, coefficient of variation, minimum and maximum value. The inferential analysis was performed according to the Student t-test with equal variances, with a statistical significance at 0.05. The Levene test was used to assess the equality of variances.


The mean bone mass density in the control group and experimental group, respectively, was 462 g/cm 2 and 378 g/cm 2 . Densitometric analysis showed that the experimental group presented lower values that were statistically different from those of the control group (P<0.05).

Seven weeks after implant placement, the average removal torque was 11.6±4.5 Ncm and 10.4±4.9 Ncm for the control and test groups, respectively. The mean resistance to torque removal increased from 11.6 Ncm to 16.7 Ncm over the 7- to 14-week intervals in the control group. In the test group, the mean resistance to torque removal decreased from 10.4 Ncm to 9.7 Ncm. Analysis of torque removal measurements revealed a P<0.05 between the control and the test groups at the 14-week evaluation [Table 1].{Table 1}


Dental implants represent a reliable alternative to oral rehabilitation, providing comfort and welfare to edentulous patients. Because the implant becomes permanently incorporated to bone, it is suggested that titanium implants can be used with a certain degree of long-term predictability and success. These data are supported by many clinical studies that report success rates higher than 90%. [6],[9]

However, some factors like poor oral hygiene and biomechanical factors may lead to marginal bone loss. [3] Bone quantity, bone quality and implant characteristics are some of the biomechanical aspects that influence implant osseointegration. [2],[3],[10],[11],[12] About 35% of the implants inserted in type IV are reported to fail after 5 years while in type I, II and III, the bone failure rates were 3% over the same period. [13]

Shorter implants as well as decreased bone mass lead to less contact area between implant and bone and may also cause a reduction in the supporting ability of the implant, [12] characterized by lower removal torque. [14] Osteoporosis is a systemic disease characterized by reduced bone mass and deterioration of the microarchitecture of the bone tissue, diminishing their adaptative ability and affecting maxillary bones, causing erosion, height and thickness reduction of the cortical bone. [7],[15],[16],[17],[18]

Ovariectomy and corticosteroids are two of the methods that can be used to induce osteoporosis in experimental animals, and the removal of the ovaries is well documented in the literature. [5],[11],[12],[19],[20],[21],[22],[23],[24]

Although many studies have used rats as experimental animals, [11],[12],[19],[20],[21],[22],[23],[24] according to the Standards of International Organization for Standardization, the implant insertion in the diaphyseal cortical bone of this small-size animal cannot be recommended for the evaluation of biomaterials. [25] Moreover, there are reports that suggest that rats should not be used to evaluate the effects of ovariectomy in cortical bone because the bone architecture of these animals is not representative of Haversian systems. [25],[26]

The present study opted for the use of rabbits that were easily managed and provided good bone thickness to implant insertion, preventing bone fracture. Also, rabbits do not demand much time for osteopeny induction, as opposed to dogs and sheep. [5],[19] In rabbits, the bone mass reduction can be achieved in a period of 30 days. [5] To certify the establishment of rabbit model with low bone mineral density, this work has taken a period of a 120 days, which is higher than the one reported in the literature. As in other researches, [27],[28],[29] this study had the sample composed of the tibia of adult animals in which the bone growth process has already ceased. However, there are reports that used young animals that were subjected to the influence of growth hormones that affects new bone formation. [30]

The use of histomorphometry and biomechanical tests are reported in researches that intend to evaluate new bone formation around titanium implants. The reverse torque removal method has been used since 1991, when Johansson and Albrektsson showed the existence of a strong positive correlation between the force necessary for removal of implants and the degree of bone-implant contact. [14]

The outcome of the biomechanical test provided data that allowed to verify that until a period of 7 weeks healthy and osteopenic animals achieve similar bone responses, corroborating the findings of other papers. [30]

The post-operative periods recorded by researches that had the purpose of evaluating the influence of osteopeny over new bone formation around implants in osteopenic rabbits are 4 and 12 weeks. [30] The present study also performed a second assessment at 14 weeks postoperatively, which is longer than that achieved by the previous available researches.

When a period of 14 weeks is used to promote bone formation, the healthy animals present better response than the osteopenic ones, with a significant difference between the groups.

It is worth to mention that the biomechanical findings of this study are consistent with the histological data in the literature as a higher torque resistance is related to a greater supporting ability of the implant and a thicker bone tissue. [10],[11],[12],[19],[20],[22]

Within the limits of this study, it is possible to suggest that the difference obtained in the removal torque values between the groups was due to the fact that osteopenic individuals do not present the same new bone formation intensity around titanium implants as the healthy ones. Although it is known that occlusal load serves as a functional stimulus to bone, which allows us to suppose that it can, in some way, positively affect bone formation. However, it was not the objective of the present study to evaluate the endosseous titanium implants in function.

It is suggested that a standardization of the evaluation methods and the completion of a laboratorial study to evaluate implants in function as well as histological researches and clinical long-term studies be performed in order to determine the use of titanium implants in osteoporotic patients.


It can be concluded that the biomechanical performance achieved by titanium implants inserted in healthy animals does not differ from that obtained by osteopenic animals in the postoperative period of 7 weeks. However, in the period of 14 weeks, the implants inserted in healthy animals present a statistically significant greater reverse torque resistance than the ones inserted in osteopenic animals. The estrogen deficiency caused by ovariectomy negatively affects new bone formation around titanium implants.


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