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Basic and Clinical Research

One-Year Clinical Outcome of Dental Implants Placed in Patients With Type 2 Diabetes Mellitus: A Case Series

Turkyilmaz, Ilser DDS, PhD

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doi: 10.1097/ID.0b013e3181e40366
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Abstract

The prevalence of diabetes is high and increasing dramatically.1 It has been predicted that the number of patients with diabetes mellitus worldwide will increase from an estimated 135 million in 1995 to 300 million in 2025.2 Diabetes mellitus is the most prevalent endocrine disease affecting 5% to 10% of the overall population. It is diagnosed when fasting plasma glucose reaches or exceeds 126 mg/dL. Diabetes mellitus occurs in 2 types. Type 1 diabetes mellitus (insulin-dependent diabetes mellitus) is caused by the autoimmune destruction of β cell, which results in partial or complete insulin deficiency. Type 2 diabetes mellitus (non-insulin–dependent diabetes mellitus) is characterized by variable degrees of insulin resistance in peripheral tissue, impaired insulin secretion, and increased glucose production. It arises in response to genetic and environmental factors.3 Type 2 diabetes mellitus represents approximately 90% of the total diabetic patients.1

Poorly controlled diabetes mellitus is associated with systemic adverse sequelae such as increased susceptibility to infection, delayed wound healing, and microvascular complications. Diabetic patients were rejected from dental implant therapy for a long time because of concerns related to healing.1,4 To date, the use of dental implants in diabetic patients is controversial.5 Although it is generally accepted that patients with controlled diabetes mellitus have similar success rates for dental implants compared with healthy people,6,7 several reports have shown contradicting results.8 Therefore, factors influencing successful implant therapy for patients with diabetes mellitus still remain in question, specifically with limited information available on the influence of glycemic control on implant success.9

There are limited and controversial data available in the dental literature regarding the clinical outcome of implant treatment for patients with diabetes mellitus.1,6,9–11 In this clinical report, 1-year clinical results of 23 implants placed in10 patients with type 2 diabetes mellitus were presented.

Patients and Methods

Ten patients with type 2 diabetes mellitus suffering from various degrees of edentulism and requesting implant treatment were retrospectively evaluated for this study. Preoperative planning included a medical history and information such as diabetes duration, type of medication used to control diabetic condition, frequency of glucose monitoring, and any complication related to diabetes (eg, retinopathy, macrovascular complications) was noted. The patients' laboratory test results regarding HbA1c (glycosylated hemoglobin), fasting plasma glucose, cholesterol, blood lipids data were obtained preoperatively, and a consultation with their physicians was done. The inclusion criteria were (1) a diagnosis of type 2 diabetes mellitus, (2) partial or fully edentulism and request for implant therapy, (3) an HbA1c values ≤10% during the perioperative period, and (4) control of periodontal disease, if present, before implant placement. Patients with type 2 diabetes mellitus could be on a modified diet or receiving oral medication, insulin, or combination therapies. An HbA1c value ≤8.0% represents a well-controlled type 2 diabetes while an HbA1c value from 8.1% to 10.0% represents a moderately controlled type 2 diabetes.9

A total of 23 dental implants (Astra Osseospeed, Astra Tech, Molndal, Sweden) were placed in 10 patients with type 2 diabetes in the implant clinic in 2007 and 2008 (Table 1). At the time of implant placement, the mean age of the patients was 58 ± 9 years (range, 45 to 71 years). Each patient signed an informed consent before implant placement. All implants were placed according the manufacturer's instructions. A traditional 2-stage surgical protocol was used for implant placement. The surgical procedure consisted of a local anesthesia with or without intravenous sedation. A crestal incision was made followed by a full-thickness mucoperiosteal flap elevation. After the implant sites were prepared, all implants were placed using a torque controller (Fig. 1). The final insertion torque values recorded during the implant placement in this study were 35, 40, or 45 N·cm. The mucosa was sutured after the implant placement. All patients received postoperative antibiotic treatment (500 mg amoxicillin and clavulanate potassium twice a day for 5 days). Also, a mouth rinse including 0.2% chlorhexidine was prescribed to the patients starting the day after the surgery and continued for 2 weeks. The implants were left to heal 3 months in the mandible and 6 months in the maxilla for osseointegration. At the second surgery, the healing abutments were placed on top the implant body after the cover screws were removed (Fig. 2). Final impressions were made, and the implant-supported definitive dental prostheses were fabricated using traditional dental methods (Fig. 3).

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Table 1:
Overview of Data Related to Patients and to Implants Placed in This Study
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Fig. 1.:
After flap elevation, 3 implants were placed using a surgical guide. High primary stability was achieved during the implant placement.
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Fig. 2.:
Intraoral view of healing abutments and soft tissue before final impression. The soft tissue with pale pink color was healthy.
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Fig. 3.:
Periapical radiograph of implants and screw-retained restoration after 1 year. Almost no marginal bone loss was noted around the implants.

The patients were recalled at 1 week and at 3, 6, and 12 months after the implant placement. Implant success was based on the following criteria suggested by Misch et al.12

Results

No implants were lost at 1 year after the implant placement. All implants were stable. Mean marginal bone loss of 0.3 ± 0.2 mm was observed during the follow-up period, as determined by digital periapical radiographs. Marginal bone changes were measured in a computer using image analysis software, by 1 examiner, using the implant-abutment junction as a reference. No periapical radiolucencies, no bleeding on probing, or pathologic probing depth were recorded at these recalls. All implants were considered successful at the 1-year follow-up.

Discussion

Infection in clean wounds is more likely to occur in diabetic patients compared with patients without diabetes mellitus. Poorly controlled diabetic patients present more difficult management problems.4,7 Postponement of surgical procedures has been recommended until optimum glucose and protein levels are obtained and maintained.13 Bacterial infection and occlusal overload are the most common factors causing implant failures.14,15 Peri-implantitis that may cause implant failure exhibits clinical signs similar to those found around periodontally diseased teeth.16,17 These signs can be considered as bleeding, suppuration, pain, mobility, increased probing depth, radiographic evidence of bone loss, and presence of bacteria.4,7,15 Morris et al,18 found that the survival of implants placed with preoperative antibiotics was 4.5% higher than implants placed without antibiotic coverage at implant placement. It has also been reported that the use of chlorhexidine before and after implant placement provided better outcomes in patients with type 2 diabetes.18 Therefore, postoperative antibiotics and chlorhexidine rinsing were used to reduce complications in the patients described in this report.

It has been reported that uncontrolled diabetes may impair wound healing, which may affect osseointegration of dental implants. The influence of diabetes on the survival of dental implants has been analyzed in animal studies.3,19 Hasegawa et al3 [T1], histologically and histomorphometrically examined bone healing around the implants in the type 2 diabetes rat model. They found that bone volume around implants was consistently smaller for the diabetes group than for the control group in the cortical area. They also observed that bone-implant contact percentage was considerably lower for the diabetes group in both the cortical and marrow areas. Iyama et al,19 found that the bone formation around a hydroxyapatite implant away from the endosteum and periosteum was suppressed in the diabetic model.

As mentioned in the introduction section, the use of dental implants is controversial in patients with type 2 diabetes. There are few reports regarding the clinical outcome of implant treatment for patients with diabetes mellitus.1,6,9,11 Tawil et al,1 placed 255 implants in 45 patients with type 2 diabetes mellitus (mean perioperative HbA1c level of 7.2%) and followed these patients for 1 to 12 years. They reported that the overall survival rate was 97.2% for the diabetic group and 98.8% for the control group. There was no significant difference for age, gender, diabetes duration, smoking, or type of hypoglycemic therapy. Olson et al6 placed 178 implants and reported that the overall survival rate was 88% from prosthesis placement through the 60-month follow-up in 58 patients. Dowell et al9 evaluated 50 implants in 35 patients in whom the HbA1c levels ranged from 4.5% to 13.8%. They reported that all 50 implants placed were osseointegrated at the abutment connection, which was 4 months after the implant placement. Bugea et al11 placed 3 implants in the anterior mandible to support an overdenture in a patient with type 2 diabetes mellitus. One of the implants, which was osseointegrated, was removed 2 months after the implant placement because its position was prosthetically unfavorable. They histologically evaluated the implant after it was removed and found that bone-to-implant contact was 80%, meaning successful osseointegration.

It has been reported that high primary implant stability, which is 32 N·cm or above, is one of the prerequisites to achieve osseointegration.20 It has been considered that the high insertion torque values recorded (35, 40, or 45 N·cm), and 2-stage surgical approach, and conventional loading protocol used in this study might have resulted in an implant success rate of 100%. Although Brånemark et al21 suggested healing periods of 3 to 6 months for the mandible and maxilla, respectively, the length of healing time to achieve osseointegration has not been established for patients with diabetes. Future clinical studies may be helpful to establish appropriated healing times in patients with diabetes.

Conclusion

It has been concluded that because no evidence of diminished clinical success and/or significant complications related to implant treatment were observed for this patient population, dental implant treatment can be offered to patients with well- or moderately controlled type 2 diabetes mellitus. Further studies including a greater number of patients are needed to understand better the relationship between type 2 diabetes mellitus and osseointegration.

Disclosure

The author has no conflict of interest. No special relationship between company and author exists.

References

1.Tawil G, Younan R, Azar P, et al. Conventional and advanced implant treatment in the type II diabetic patient: Surgical protocol and long-term clinical results. Int J Oral Maxillofac Implants. 2008;23:744–752.
2.King H, Aubert RE, Herman WH. Global burden of diabetes, 1995–2025: Prevalence, numerical estimates, and projections. Diabetes Care. 1998;21:1414–1431.
3.Hasegawa H, Ozawa S, Hashimoto K, et al. Type 2 diabetes impairs implant osseointegration capacity in rats. Int J Oral Maxillofac Implants. 2008;23:237–246.
4.Klokkevold PR, Han TJ. How do smoking, diabetes, and periodontitis affect outcomes of implant treatment? Int J Oral Maxillofac Implants. 2007;22(Suppl):173–202.
5.Kotsovilis S, Karoussis IK, Fourmousis I. A comprehensive and critical review of dental implant placement in diabetic animals and patients. Clin Oral Implants Res. 2006;17:587–559.
6.Olson JW, Shernoff AF, Tarlow JL, et al. Dental endosseous implant assessments in a type 2 diabetic population: A prospective study. Int J Oral Maxillofac Implants. 2000;15:811–818.
7.van Steenberghe D, Jacobs R, Desnyder M, et al. The relative impact of local and endogenous patient-related factors on implant failure up to the abutment stage. Clin Oral Implants Res. 2002;13:617–622.
8.Fiorellini JP, Chen PK, Nevins M, et al. A retrospective study of dental implants in diabetic patients. Int J Periodontics Restorative Dent. 2000;20:366–733.
9.Dowell S, Oates TW, Robinson M. Implant success in people with type 2 diabetes mellitus with varying glycemic control: A pilot study. J Am Dent Assoc. 2007;138:355–361.
10.Salvi GE, Carollo-Bittel B, Lang NP. Effects of diabetes mellitus on periodontal and peri-implant conditions: Update on associations and risks. J Clin Periodontol. 2008;35(8 Suppl):398–409.
11.Bugea C, Luongo R, Di Iorio D, et al. Bone contact around osseointegrated implants: Histologic analysis of a dual-acid-etched surface implant in a diabetic patient. Int J Periodontics Restorative Dent. 2008;28:145–151.
12.Misch CE, Perel ML, Wang HL, et al. Implant success, survival, and failure: The International Congress of Oral Implantologists (ICOI) Pisa Consensus Conference. Implant Dent. 2008;17:5–15.
13.McMurry JF. Wound healing with diabetes mellitus. Surg Clin North Am. 1984;64:769–778.
14.Tonetti M, Schmidt J. Pathogenesis of implant failure. Periodontol 2000. 1994;4:127–138.
15.Sbordone L, Barone A, Ramaglia L, et al. Antimicrobial susceptibility of periodontopathic bacteria associated with failing implants J Periodontol. 1995;66:69–74.
16.Schwartz-Arad D, Laviv A, Levin L. Failure causes, timing, and cluster behavior: An 8-year study of dental implants. Implant Dent. 2008;17:200–207.
17.Meffert RM. Periodontitis vs. peri-implantitis: The same disease? The same treatment? Crit Rev Oral Biol Med. 1996;7:278–291.
18.Morris HF, Ochi S, Winkler S. Implant survival in patients with type 2 diabetes: Placement to 36 months. Ann Periodontol. 2000;5:157–165.
19.Iyama S, Takeshita F, Ayukawa Y, et al. A study of the regional distribution of bone formed around hydroxyapatite implants in the tibiae of streptozotocin- induced diabetic rats using multiple fluorescent labeling and confocal laser scanning microscopy. J Periodontol. 1997;68:1169–1175.
20.Turkyilmaz I, McGlumphy EA. Influence of bone density on implant stability parameters and implant success: A retrospective clinical study. BMC Oral Health. 2008;8:32.
21.Brånemark PI, Adell R, Breine U, et al. Intra-osseous anchorage of dental prostheses. I. Experimental studies. Scan J Plast Reconst Surg. 1969;3:81–100.

Abstract Translations

GERMAN / DEUTSCH

AUTOR: Ilser Turkyilmaz, DDS, PhD

Klinische Ergebnisse im Verlauf eines Jahres bei Zahnimplantaten, die Patienten mit einer Erkrankung an Typ 2 Diabetes Mellitus eingepflanzt wurden: Eine Anwendungsbeobachtung

ZUSAMMENFASSUNG: Zielsetzung: Bei Diabetes Mellitus handelt es sich um eine weit verbreitete medizinische Störung. Dies wird oft von systemischen negativen Folgeer scheinungen begleitet, wie beispielsweise eine Veränderung des Wundheilungsverhaltens, das die Knochengewebsintegration von Zahnimplantaten beeinflussen kann. Die Verwendung von Zahnimplantaten bei Patienten mit Diabetes Mellitus bleibt daher umstritten, da von einer veränderten Knochenheilung im Bereich um die Implantate herum berichtet wird. Die vorliegende Studie zielte darauf ab, die klinischen Ergebnisse über einen Verlauf von einem Jahr bei 23 Implantaten vorzustellen, die bei 10 Patienten mit einem gut oder ausreichend eingestellten Typ 2 Diabetes Mellitus eingepflanzt worden waren. (Dies bezieht sich auf Hb1Ac-Werte, die im ersten Abschnitt zu Materialien und Methoden bestimmt worden sind). Materialien und Methoden: Alle Implantate konnten ohne Komplikationen im Unter- oder Oberkiefer eingepflanzt werden. Es wurden für die Patienten drei unterschiedliche Arten von endgültiger Implantatgestützter Prothese, Zement- bzw. Schraubgehaltene feste Zahnprothesen und Deckprothesen, angefertigt. Ergebnisse: Bei der Nachfolgeuntersuchung ein Jahr nach dem Einpflanzen waren alle Implantate intakt. Es wurde ein marginaler Knochengewebsverlust von 0.3 ± 0.2 mm festgestellt. Bei diesen Untersuchungen wurden keine periapikale Röntgenstrahldurchlässigkeit, keine Blutung auf Sondieren oder pathologische Sondierungstiefe verzeichnet. Schlussfolgerung: Dieser klinische Bericht unterstützt die Verwendung von Zahnimplantaten bei Patienten mit einem gut oder ausreichend eingestellten Typ 2 Diabetes Mellitus als zahnmedizinische Behandlungsmöglichkeit. Bei der untersuchten Patientengruppe fand sich keinerlei Hinweis auf einen verminderten klinischen Erfolg oder mit der Implantierungsbehandlung in Verbindung stehende maßgebliche Komplikationen.

SCHLÜSSELWÖRTER: Implantat, Diabetes, Insulin, Prothese

SPANISH / ESPAÑOL

AUTOR: Ilser Turkyilmaz, DDS, PhD

Resultado clínico de un año en implantes dentales colocados en pacientes con diabetes mellitus tipo 2: Una serie de casos

ABSTRACTO: Propósito: La diabetes mellitus es una enfermedad frecuente. A menudo, está acompañada por secuelas sistémicas adversas, como alteraciones en la curación de heridas, que podrían afectar la oseointegración de los implantes dentales. El uso de implantes dentales en pacientes con diabetes mellitus sigue siendo controvertido ya que se ha informado una curación alterada del hueso alrededor de los implantes. El propósito de este estudio fue presentar los resultados clínicos de 1 año de 23 implantes colocados en 10 pacientes con diabetes mellitus tipo 2 controlada bien o moderadamente bien. (Esto se relaciona con los niveles de Hb1Ac, que se define en el primer párrafo de materiales y métodos). Materiales y métodos: Todos los implantes se colocaron sin dificultades en el maxilar o la mandíbula. Tres tipos diferentes de prótesis permanentes soportadas por implantes, prótesis dentales retenidas con cementos o tornillos y sobredentaduras se colocaron en los pacientes. Resultados: En la evaluación de seguimiento de 1 año, no se había perdido ningún implante y se notó una pérdida del hueso marginal de 0.3 ± 0.2 mm. No se registraron radiolucencias periapicales, pérdida de sangre ni profundidad patológica al tocar los lugares. Conclusión: Este informe clínico apoya el uso de implantes dentales en pacientes con diabetes mellitus tipo 2 bien o moderadamente bien controlada como una modalidad de tratamiento dental. No se encontró evidencia de reducción en el éxito clínico ni complicaciones de importancia relacionadas con el tratamiento con implantes en este grupo de pacientes.

PALABRAS CLAVES: implante, diabetes, insulina, prótesis

PORTUGUESE / PORTUGUÊS

AUTOR: Ilser Turkyilmaz, Cirurgião-Dentista, PhD

Resultado clínico após um ano de implantes dentários colocados em pacientes com diabete melito Tipo 2: Série de caso

RESUMO: Objetivo: O diabete melito é um distúrbio médico prevalente. É frequentemente acompanhado de sequelas sistêmicas adversas, tais como alterações de cura de ferida, que podem afetar a osseointegração de implantes dentários. O uso de implantes dentários em pacientes com diabete melito permanece controverso, já que a cura de osso alterado em torno de implantes foi relatada. O objetivo deste estudo foi apresentar resultados clínicos após 1 ano de 23 implantes colocados em 10 pacientes com diabete melito tipo 2 bem ou moderadamente bem controlado. (Iso está relacionado a níveis de Hb1Ac, que foi definido no 1° parágrafo de materiais e métodos). Materiais e Métodos: Todos os implantes foram rotineiramente colocados na mandíbula ou maxila. Três diferentes tipos de próteses definitivas suportadas por implante, próteses dentárias fixas retidas por cimento ou parafuso e sobredentaduras foram entregues aos pacientes. Resultados: Na convocação para acompanhamento após 1 ano, nenhum implante estava perdido e 0.3 ± 0.2 mm de perda de osso marginal foi observada. Nenhuma radiolucência periapical, nenhum sangramento ao fazer sondagem ou profundidade de sondagem patológica foram registrados nessas convocações. Conclusão: Este relatório clínico apoia o uso de implantes dentários em pacientes com diabete melito tipo 2 bem ou moderadamente bem controlado como modalidade de tratamento dentário. Nenhuma evidência de sucesso clínico diminuído ou complicação significativa relacionados a tratamento de implante foi encontrada para essa população de pacientes.

PALAVRAS-CHAVE: implante, diabete, insulina, prótese

RUSSIAN / SYMBOL

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АВТОР: Ilser Turkyilmaz, доктор xирургичeской стоматологии, доктор философии

Клиничeский рeзультат установки зубныx имплантатов пациeнтам с саxарным диабeтом 2-го типа по итогам одного года: исслeдованиe сeрии случаeв

РEЗЮМE.Цeль. Саxарный диабeт являeтся распространeнным заболeваниeм. Он часто сопровождаeтся соматичeскими осложнeниями, такими как нарушeниe процeсса заживлeния ран, которыe могут повлиять на остeоинтeграцию зубныx имплантатов. Использованиe зубныx имплантатов у пациeнтов с саxарным диабeтом остаeтся спорным вопросом в связи с нарушeниeм процeсса заживлeния костной ткани вокруг имплантатов. Цeлью данного исслeдования являeтся прeдставлeниe клиничeскиx рeзультатов постановки 23 имплантатов 10 пациeнтам с компeнсированным (или относитeльно компeнсированным) саxарным диабeтом 2-го типа по итогам одного года. (Показатeлeм компeнсации являeтся уровeнь гликированного гeмоглобина (Hb1Ac), который был опрeдeлeн в 1-ом абзацe раздeла «Матeриалы и мeтоды».) Матeриалы и мeтоды. Всe имплантаты были установлeны бeз осложнeний в нижнeй или вeрxнeй чeлюсти. Пациeнтам были установлeны три разныx типа постоянныx протeзов с опорой на имплантаты, зубныe протeзы с винтовой или цeмeнтной фиксациeй и съeмныe протeзы. Рeзультаты. Послeдующee наблюдeниe в тeчeниe 1 года показало, что всe имплантаты прижились, потeря маргинальной костной ткани составила 0.3 ± 0.2 мм. В xодe послeдующeго наблюдeния пeриапикальной рeнтгeнопрозрачности, кровоточивости при зондировании или патологичeской глубины зондирования выявлeно нe было. Вывод. Данный клиничeский отчeт подкрeпляeт доводы в пользу примeнeния зубныx имплантатов в качeствeмeтода лeчeния пациeнтов с компeнсированным (или относитeльно компeнсированным) саxарным диабeтом 2-го типа. Признаков клиничeской нeэффeктивности или значитeльныx осложнeний в связи с примeнeниeм зубныx имплантатов у данной группы пациeнтов выявлeно нe было.

КЛЮХEВЫE СЛОВА: имплантат, диабeт, инсулин, протeзированиe

TURKISH / TÜRKÇE

YAZAR: Ilser Turkyilmaz, DDS, PhD

Tip 2 diyabetes mellitus hastalarinda yerleştirilen dental implantlarda bir yil sonra alinan klinik sonuc: Bir olgu serisi

ÖZET: Amaç: Diabetes mellitus yaygin bir tibbi bozukluktur. Dental implantlarin osseoentegrasyonunu etkileyebilen yara iyileşmesinde değişiklik gibi sistemik advers sekeller siklikla bu hastaliğa eşlik eder. İmplantlarin etrafindaki kemik iyileşmesinde değişiklik bildirilmiş olduğundan diabetes mellitus hastalarinda dental implant kullanimi tartişmalidir. Bu çalişmanin amaci, iyi bir şekilde veya orta derecede kontrol edilen tip 2 diabetes mellitus hastaliği olan 10 olguda yerleştirilen 23 implantin 1-yil sonraki klinik sonuçlarini sunmaktir. (Diabetes mellitusun kontrolü, gereç, ve yöntemin birinci paragrafinda tanimlanan Hb1Ac düzeyleri ile bağlantilidir). Gereç ve Yöntem: Tüm implantlar, alt çenede ya da maksillada olaysiz bir şekilde yerleştirildi. Olgulara, sement veya vida ile tutturulan sabit dental protezler ve dişüstü protezler gibi üç, değişik tür implant ile desteklenen protezler uygulandi. Bulgular: Bir yil sonraki ziyarette hic,bir implant kaybi olmadiği ve marjinal kemik kaybinin 0.3±0.2 mm olduğu gozlendi. Bu ziyaretlerde periapikal radyolusensi, sondlamada kanama ya da patolojik sondlama derinliği görülmedi. Sonuç: Bu klinik rapor, iyi veya orta derecede kontrol edilen diabetes mellitusu olan hastalarda dental tedavi modalitesi olarak dental implant kullanimini desteklemektedir. Bu hasta popülasyonunda implant tedavisine ilişkin olarak klinik başarida azalma veya önemli ölçüde komplikasyon kaniti bulunmadi.

ANAHTAR KELİMELER: İmplant, diabetes, insülin, protez

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CHINESE / SYMBOL

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Keywords:

implant; diabetes; insulin; prosthesis

© 2010 Lippincott Williams & Wilkins, Inc.