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PAPER
Comparison of surgical duration of canine ovariectomy and ovariohysterectomy in a veterinary teaching hospital K. P. Harris*, V. J. Adams†, P. Fordyce* and J. Ladlow* *Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES †Veterinary Epidemiology, Suffolk IP28 9BF
OBJECTIVE: To prospectively evaluate ovariectomy and ovariohysterectomy via midline coeliotomy when being employed by supervised final year veterinary students for the purpose of routine canine neutering. METHODS: One hundred and eight female dogs of various breeds, presented to a veterinary teaching hospital for neutering, were randomly allocated to one of two surgery groups, ovariectomy or ovariohysterectomy. The specified procedure was performed by a supervised final year veterinary student. If the duration of surgery exceeded 2 hours or if major surgical or anaesthetic complications occurred, the supervising surgeon intervened to complete the procedure. RESULTS: Data analysed included age, weight, time from first incision to start of closure, duration of closure, total surgical time and length of incision. Fifty-four dogs underwent each procedure. There was no significant difference between the two surgery groups for any of the measured variables. CLINICAL SIGNIFICANCE: Ovariectomy is not associated with shorter surgical times or smaller abdominal incisions than ovariohysterectomy when employed by inexperienced surgeons. As no major complications novel to ovariectomy occurred in this cohort of dogs, this study adds support to the existing literature indicating that ovariectomy is an acceptable alternative to ovariohysterectomy for canine neutering.
Journal of Small Animal Practice (2013) 54, 579–583 DOI: 10.1111/jsap.12147 Accepted: 3 September 2013
INTRODUCTION Ovariectomy (OVE) via ventral midline coeliotomy for the purpose of canine neutering remains an infrequently performed technique in contrast to ovariohysterectomy (OHE) in general practice in the UK (Tivers et al. 2005) despite growing support in the literature for OVE (Van Goethem et al. 2006, DeTora & McCarthy 2011, Peeters & Kirpensteijn 2011). This may be because of OHE being the procedure traditionally taught in British veterinary schools, a sparsity of information on OVE via midline coeliotomy in several of the current popular surgical Journal of Small Animal Practice
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Vol 54
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November 2013
•
textbooks (such as Fingland (1997), Danova et al. (2005) and Hedlund (2007)) or anecdotal concern that leaving the uterine body in situ could lead to the future development of cystic endometrial hyperplasia (CEH)–pyometra complex or uterine neoplasia (DeTora & McCarthy 2011). Potential benefits of OVE over OHE were investigated by Peeters & Kirpensteijn (2011). When performed via midline celiotomy, the skin and fascial incisions required were found to be shorter and more cranially located with OVE. This study of 40 dogs failed to detect any significant difference for total surgical time, pain scores and wound scores between the OVE and
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OHE groups, however, it is worthy of note that all surgeries were performed by a single experienced surgeon. It is possible that with an experienced surgeon, skilled suturing negates any difference in wound length on duration of surgery. Given that final year veterinary students take, on average, over twice the time of an experienced surgeon to suture an OHE wound (Burrow et al. 2005, Peeters & Kirpensteijn 2011); the shorter incision length with OVE would be expected to notably shorten total surgical times for final year students and presumably all inexperienced surgeons. Longer total surgical time and anaesthetic duration have been demonstrated to be positively correlated with the incidence of wound infection (Brown et al. 1997), and, in addition, to negatively impact on practice efficiency and economics. The intention of this report was to prospectively compare OVE with OHE when being employed by a cohort of supervised final year clinical veterinary students in the setting of a veterinary teaching hospital. It was hypothesised that OVE would be performed more rapidly than OHE and through a smaller incision.
MATERIALS AND METHODS All bitches presented to the Queen’s Veterinary School Hospital for routine neutering between 2008 and 2011 were eligible for inclusion in the study. A clinical examination of each dog was performed on the day of surgery. Bitches that were palpably pregnant, in oestrus or in pseudopregnancy were excluded from the study, as was any bitch considered unsuitable for anaesthesia or surgery because of ill health or abnormal clinical examination findings. Each case was randomly allocated to undergo either OHE or OVE through blind selection of one of two cards (marked with OHE and OVE, respectively) from an envelope. Both cards were returned to the envelope for randomization of subsequent cases. The final year student allocated to the case was provided with a written explanation of the procedure to be performed (based on the technique described by Stone (2003)) and given time to read it whilst anaesthesia was induced and the ventral abdomen aseptically prepared. The student performed the entire procedure; however, a qualified veterinary surgeon was always scrubbed in to provide direction and assistance (typically retraction of viscera to improve visualization of the ovarian pedicles and pass instruments) where necessary. A non-sterile member of the theatre team was asked to note the time of the first incision, the time of the start of closure and the time of the completion of closure on a data collection form. At the end of the procedure, the operating student was asked to cut a piece of sterile suture material to the same length as the wound. This was then measured against a ruler with millimeter graduations. The student was asked to fill in the patient’s details on the data collection form, including case number, age, weight, length of incision and any intra-operative complications. If the duration of surgery exceeded 2 hours or if major surgical or anaesthetic complications occurred, the supervising surgeon intervened to complete the procedure. Major surgical complications requiring surgeon intervention were pre-agreed to include either severe haemorrhage or inadvertent laceration/ligation of another tissue 580
necessitating release or repair. Dogs were excluded from the study if upon opening the abdomen they were observed to have any gross or palpable abnormalities of the ovaries or uterus, or if they were found to be pregnant. Statistical analysis Variables included in the analysis were age in months, bodyweight in kilograms, time in minutes from first incision to start of closure (TIC), time from start of closure to end of closure (DC), total surgical time (TST=TIC+DC) and length of incision (LI) in centimeters. Incidence of intra-operative complications was also analysed to test a secondary hypothesis that intra-operative complication rates between the two procedures would not be significantly different. Following a Wilk–Shapiro test for normality, two-sample T tests were used to compare age, bodyweight, TIC, DC, TST and LI by surgical procedure. Results are reported as mean and standard deviation (±sd) with P-values, mean differences and 95% confidence intervals given by the Satterthwaite method for unequal variances (Snedecor & Cochran 1989) as in this dataset the assumption of equal variances was violated for all variables. Cross-tabulations and Fishers exact tests were used to compare proportions. The level of significance was set at P2000
48 50 98
27·8 (±7·4) 29·9 (±11·0) 2·1 (−1·7 to 5·8) 197
53 51 104
88·7 (±20·6) 92·0 (±27·6) 3·2 (−6·3 to 12·7) 614
53 50 103
8·7 (±2·6) 9·6 (±3·4) 0·9 (−0·3 to 2·1) 134
*Minimum sample size (SS) required for each treatment group to show statistically significant differences based on the observed differences and variability in the data
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and quantification of incision location along the xiphoid–pubis axis would have ensured that any difference in body size distribution amongst the OVE and OHE groups was accounted for, and confirmed whether OVE incisions were made more cranially as suspected. Limitations of this study include the inability to have the same supervising surgeon throughout, potentially leading to variation in the degree of their involvement and the directions given to the student intra-operatively. Eleven different surgeons supervised the 108 cases included in this study including four Diplomates of the European College of Veterinary Surgeons, four residents and two staff surgeons. It is possible that before this study, some of the supervising surgeons had little or no experience of performing/supervising OVE via midline coeliotomy, yet all had extensive experience performing/supervising OHE. Whilst teaching/ supervising the technical skills required for OVE is much the same as teaching/supervising the technical skills required for OHE (midline coeliotomy, location of the ovaries, placement of secure encircling and transfixing ligatures, etc.), the OVE technique was discussed with each supervising surgeon before their involvement with the study, and they were asked to read the written explanation of both OVE and OHE given to the students. This was intended to limit variation in advice given to the students intra-operatively between different surgeons. Whilst the lectures given to these students regarding routine canine neutering in their penultimate year explained both OHE and OVE via midline coeliotomy, it is possible that any practical teaching the students had received on neutering before their involvement in this study concentrated on OHE (particularly if they were assisting with or performing neutering via midline coeliotomy in British general practices whilst on extra-mural study placements). This, however, was not considered to be a major source of bias as any skills (such as ligature placement, suturing, etc.) perfected on previous OHE surgeries would be directly transferable to an OVE procedure. Any uncertainty, for example regarding where to ligate the uterine horn during OVE, could be easily clarified by the supervising surgeon. The weight variation in the study population was large and it is perhaps illogical to include a 51·5 kg dog in a study assessing inexperienced surgeons. However, imposing a weight range would have severely reduced the number of eligible cases. Conducting a multi-center study can overcome the problem of limited eligible cases; however, it often reduces the number of variables which can be controlled. A further limitation to this study was the omission of body condition scoring (BCS) at the time of surgery. Although a subjective measurement, BCS would provide a more accurate indication of the distribution of obesity amongst the OVE and OHE groups than bodyweight given the great variation in body size amongst the dog breeds represented. Whilst obesity is anecdotally reported to make OHE more difficult (Burrows et al. 2005), to the authors’ knowledge only one study has investigated the effect of BCS on surgical time, relative incision length and relative blood loss in dogs undergoing OHE or OVE via midline coeliotomy (Peeters & Kirpensteijn 2011). These authors reported that the preoperative BCS had no significant influence on any 582
of these variables, potentially because of the absence of a correlation between BCS and the amount of intra-abdominal fat. A subjective scale for grading the amount of fat in the ovarian ligament (Van Nimwegan & Kirpensteijn 2007) was used in a study evaluating laparoscopic ovariectomy and a higher amount of fat was significantly associated with a longer operative time (Dupre et al. 2009). If obesity could be controlled for using BCS and/or the ovarian ligament fat scale then any variation in LI or TST should be more directly attributable to surgical procedure. This may highlight a difference between OHE and OVE that at present is not significant. Although the exact pathophysiology of CEH–pyometra complex is not fully understood, the involvement of progesterone is widely accepted (Smith 2006, Verstegen et al. 2008) and as such, following complete removal of the ovaries by OVE, CEH–pyometra complex should not occur in the remaining uterine body. In support of this, a study by Okkens et al. (1997) identified no occurrence of endometritis in a group of 69 bitches that had undergone OVE 8 to 11 years previously, and a study by Janssens & Janssens (1991) identified no case of pyometra in a group of 72 dogs followed for 6 to 13 years after bilateral flank ovariectomy. There appear to be no published case reports of pyometra following complete ovariectomy in the dog or cat. Malignant uterine neoplasia is extremely rare in bitches with an incidence of approximately 0·003% (Van Goethem et al. 2006). In addition, a hormonal influence on the occurrence of these tumours has been postulated (DeTora & McCarthy 2011) and therefore OVE itself may be protective regardless of the fact that the uterine body remains in situ. Complication rates with canine OHE are dependent on surgeon experience (Johnston 1991) and range from 6·3 to 31·5% in the literature (Dorn & Swist 1977, Burrows et al. 2005), although these figures are difficult to compare because of the variation in author definition of intra-, peri- and post-operative complications. Certain complications of OHE are inherent to the ligation and transection of the uterine body at the level of the cervix. These include granuloma formation at the cervical stump (which can lead to adhesion formation with the bladder, ureters, large intestine, mesentery or small intestine), or accidental ureteric or bladder ligation/transection leading to hydroureter, hydronephrosis, ureterovaginal fistula or vesicovaginal fistula (MacCoy et al. 1988, Pearson 1973, Ewers & Holt 1992, Apparicio et al. 2007). Other complications include intra-abdominal haemorrhage from the transected broad ligament or cervical stump, and vaginal bleeding (Pearson 1973). Although mostly rare, these complications can be associated with severe morbidity or even mortality. It is possible that with a more cranially located coeliotomy incision (previously identified with OVE by Peeters & Kirpensteijn 2011) and by avoiding ligation and transection of the uterine body at the level of the cervix, the incidence of these complications may be lower for OVE than OHE. Because of the infrequency with which the more severe complications appear to occur (no known cases of uterine stump granuloma formation in 377 canine OHE procedures (Berzon 1979) for example), this possible benefit of OVE over OHE must not be overstated.
Journal of Small Animal Practice
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© 2013 British Small Animal Veterinary Association
Comparing ovariectomy and ovariohysterectomy
Although a significant decrease in surgical duration was not apparent in this study, the authors still propose that OVE is an appropriate alternative to OHE for canine neutering in the hands of veterinary students. No major complications novel to OVE occurred in the cohort of 54 dogs. The avoidance of complications such as bladder laceration (as occurred in this study in an OHE dog) and other rare complications such as caudal ureteric ligation (reported to occur more than proximal ureteric ligation because of the intra-peritoneal location of the caudal ureter and its close proximity to the uterine body (DeTora & McCarthy 2011) might be possible with OVE performed through a cranially located incision, however, a much larger scale multi-centre study would be required to conclude this with any certainty. Long-term follow-up of the cases in this study is planned to establish the incidence of ovarian remnant syndrome, urinary incontinence and post-OVE uterine disease in this cohort of dogs. Acknowledgements The authors would like to express their gratitude to the staff and students of the Queen’s Veterinary School Hospital, Cambridge, for their involvement in data collection, in particular Mr. David Sheen. Conflict of interest None of the authors of this article has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. References Apparicio, M., Vicente, W. R. R., Farias, A., et al. (2007) Pyonephrosis following ovariohysterectomy in a bitch. Ars Veterinaria 23, 19-22 Berzon, J. L. (1979) Complications of elective ovariohysterectomies in the dog and cat at a teaching institution: clinical review of 853 cases. Veterinary Surgery 8, 89-91 Brown, D. C., Conzemius, M. G., Schofer, F. et al. (1997) Epidemiological evaluation of postoperative wound infections in dogs and cats. Journal of the American Veterinary Medical Association 210, 1302-1306 Burrow, H., Batchelor, D. & Cripps, P. (2005) Complications observed during and after ovariohysterectomy of 142 bitches at a veterinary teaching hospital. The Veterinary Record 157, 829-833
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Danova, N. A., Schmiedt, C. & Bjorling, D. (2005) The female reproductive system. In: BSAVA Manual of Canine and Feline Abdominal Surgery. Eds J. M. Williams & J. D. Niles. BSAVA, Gloucester, MA, USA. pp 298-306 DeTora, M. & McCarthy, R. J. (2011) Ovariohysterectomy versus ovariectomy for elective sterilization of female dogs and cats: is removal of the uterus necessary? Journal of the American Veterinary Medical Association 239, 1409-1412 Dorn, A. S. & Swist, R. A. (1977) Complications of canine ovariohysterectomy. Journal of the American Animal Hospital Association 13, 720-724 Dupre, G., Fiorbianco, V., Skalicky, M. et al. (2009) Laparoscopic ovariectomy in dogs: comparison between single portal and two-portal access. Veterinary Surgery 38, 818-824 Ewers, R. S. & Holt, P. E. (1992) Urological complications following ovariohysterectomy in a bitch. Journal of Small Animal Practice 33, 236-238 Fingland, R. B. (1997) Uterus. In: Current Techniques in Small Animal Surgery. 4th edn. Ed M. J. Bojrab. Williams and Wilkins, Baltimore, MD, USA. pp 489-502 Hedlund, C. S. (2007) Surgery of the reproductive and genital systems. In: Small Animal Surgery. 3rd edn. Ed T. W. Fossum. Mosby Elsevier, St. Louis, MO, USA. pp 702-774 Janssens, L. A. A. & Janssens, G. H. R. R. (1991) Bilateral flank ovariectomy in the dog - surgical technique and sequelae in 72 animals. Journal of Small Animal Practice 32, 249-252 Johnston, S. D. (1991) Questions and answers on the effects of surgically neutering dogs and cats. Journal of the American Veterinary Medical Association 198, 1206-1214 MacCoy, D. M., Ogilvie, G., Burke, T. et al. (1988). Postovariohysterectomy ureterovaginal fistula in a dog. Journal of the American Animal Hospital Association 24, 469-471 Okkens, A. C., Kooistra, H. S. & Nickel, R. F. (1997) Comparison of long-term effects of ovariectomy versus ovariohysterectomy in bitches. Journal of Reproduction and Fertility Supplement 51, 227-231 Pearson, H. (1973) The complications of ovariohysterectomy in the bitch. Journal of Small Animal Practice 14, 257-266 Peeters, M. E. & Kirpensteijn, J. (2011) Comparison of surgical variables and short-term postoperative complications in healthy dogs undergoing ovariohysterectomy or ovariectomy. Journal of the American Veterinary Medical Association 238, 189-194 Smith, F. O. (2006) Canine pyometra. Theriogenology 66, 610-612 Snedecor, G. W. & Cochran, W. G. (1989) The comparison of two samples. In: Statistical Methods. 8th edn. Iowa State University Press, Iowa City, IA, USA. pp 83-106 Stone, E. A. (2003) Ovary and Uterus. In: Textbook of Small Animal Surgery. 3rd edn. Ed D. Slatter. Saunders, Philadelphia, PA, USA. pp 1947-1502 Tivers, M. S., Travis, T. R. D., Windsor, R. V., et al. (2005) Questionnaire study of canine neutering techniques taught in UK veterinary schools and those used in practice. Journal of Small Animal Practice 46, 430-435 Van Goethem, B., Schaefers-Okkens, A. & Kirpensteijn, J. (2006) Making a rational choice between ovariectomy and ovariohysterectomy in the dog: A discussion of the benefits of either technique. Veterinary Surgery 35, 136-143 Van Nimwegan, S. A. & Kirpensteijn, J. (2007) Comparison of Nd:YAG surgical laser and Remorgida bipolar electrosurgery forceps for canine laparoscopic ovariectomy. Veterinary Surgery 36, 533-540 Verstegen, J., Dhaliwal, G. & Verstegen-Onclin, K. (2008) Mucometra, cystic endometrial hyperplasia, and pyometra in the bitch: advances in treatment and assessment of future reproductive success. Theriogenology 70, 364-374
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PAPER
Comparison of surgical duration of canine ovariectomy and ovariohysterectomy in a veterinary teaching hospital K. P. Harris*, V. J. Adams†, P. Fordyce* and J. Ladlow* *Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES †Veterinary Epidemiology, Suffolk IP28 9BF
OBJECTIVE: To prospectively evaluate ovariectomy and ovariohysterectomy via midline coeliotomy when being employed by supervised final year veterinary students for the purpose of routine canine neutering. METHODS: One hundred and eight female dogs of various breeds, presented to a veterinary teaching hospital for neutering, were randomly allocated to one of two surgery groups, ovariectomy or ovariohysterectomy. The specified procedure was performed by a supervised final year veterinary student. If the duration of surgery exceeded 2 hours or if major surgical or anaesthetic complications occurred, the supervising surgeon intervened to complete the procedure. RESULTS: Data analysed included age, weight, time from first incision to start of closure, duration of closure, total surgical time and length of incision. Fifty-four dogs underwent each procedure. There was no significant difference between the two surgery groups for any of the measured variables. CLINICAL SIGNIFICANCE: Ovariectomy is not associated with shorter surgical times or smaller abdominal incisions than ovariohysterectomy when employed by inexperienced surgeons. As no major complications novel to ovariectomy occurred in this cohort of dogs, this study adds support to the existing literature indicating that ovariectomy is an acceptable alternative to ovariohysterectomy for canine neutering.
Journal of Small Animal Practice (2013) 54, 579–583 DOI: 10.1111/jsap.12147 Accepted: 3 September 2013
INTRODUCTION Ovariectomy (OVE) via ventral midline coeliotomy for the purpose of canine neutering remains an infrequently performed technique in contrast to ovariohysterectomy (OHE) in general practice in the UK (Tivers et al. 2005) despite growing support in the literature for OVE (Van Goethem et al. 2006, DeTora & McCarthy 2011, Peeters & Kirpensteijn 2011). This may be because of OHE being the procedure traditionally taught in British veterinary schools, a sparsity of information on OVE via midline coeliotomy in several of the current popular surgical Journal of Small Animal Practice
•
Vol 54
•
November 2013
•
textbooks (such as Fingland (1997), Danova et al. (2005) and Hedlund (2007)) or anecdotal concern that leaving the uterine body in situ could lead to the future development of cystic endometrial hyperplasia (CEH)–pyometra complex or uterine neoplasia (DeTora & McCarthy 2011). Potential benefits of OVE over OHE were investigated by Peeters & Kirpensteijn (2011). When performed via midline celiotomy, the skin and fascial incisions required were found to be shorter and more cranially located with OVE. This study of 40 dogs failed to detect any significant difference for total surgical time, pain scores and wound scores between the OVE and
© 2013 British Small Animal Veterinary Association
579
K. P. Harris et al.
OHE groups, however, it is worthy of note that all surgeries were performed by a single experienced surgeon. It is possible that with an experienced surgeon, skilled suturing negates any difference in wound length on duration of surgery. Given that final year veterinary students take, on average, over twice the time of an experienced surgeon to suture an OHE wound (Burrow et al. 2005, Peeters & Kirpensteijn 2011); the shorter incision length with OVE would be expected to notably shorten total surgical times for final year students and presumably all inexperienced surgeons. Longer total surgical time and anaesthetic duration have been demonstrated to be positively correlated with the incidence of wound infection (Brown et al. 1997), and, in addition, to negatively impact on practice efficiency and economics. The intention of this report was to prospectively compare OVE with OHE when being employed by a cohort of supervised final year clinical veterinary students in the setting of a veterinary teaching hospital. It was hypothesised that OVE would be performed more rapidly than OHE and through a smaller incision.
MATERIALS AND METHODS All bitches presented to the Queen’s Veterinary School Hospital for routine neutering between 2008 and 2011 were eligible for inclusion in the study. A clinical examination of each dog was performed on the day of surgery. Bitches that were palpably pregnant, in oestrus or in pseudopregnancy were excluded from the study, as was any bitch considered unsuitable for anaesthesia or surgery because of ill health or abnormal clinical examination findings. Each case was randomly allocated to undergo either OHE or OVE through blind selection of one of two cards (marked with OHE and OVE, respectively) from an envelope. Both cards were returned to the envelope for randomization of subsequent cases. The final year student allocated to the case was provided with a written explanation of the procedure to be performed (based on the technique described by Stone (2003)) and given time to read it whilst anaesthesia was induced and the ventral abdomen aseptically prepared. The student performed the entire procedure; however, a qualified veterinary surgeon was always scrubbed in to provide direction and assistance (typically retraction of viscera to improve visualization of the ovarian pedicles and pass instruments) where necessary. A non-sterile member of the theatre team was asked to note the time of the first incision, the time of the start of closure and the time of the completion of closure on a data collection form. At the end of the procedure, the operating student was asked to cut a piece of sterile suture material to the same length as the wound. This was then measured against a ruler with millimeter graduations. The student was asked to fill in the patient’s details on the data collection form, including case number, age, weight, length of incision and any intra-operative complications. If the duration of surgery exceeded 2 hours or if major surgical or anaesthetic complications occurred, the supervising surgeon intervened to complete the procedure. Major surgical complications requiring surgeon intervention were pre-agreed to include either severe haemorrhage or inadvertent laceration/ligation of another tissue 580
necessitating release or repair. Dogs were excluded from the study if upon opening the abdomen they were observed to have any gross or palpable abnormalities of the ovaries or uterus, or if they were found to be pregnant. Statistical analysis Variables included in the analysis were age in months, bodyweight in kilograms, time in minutes from first incision to start of closure (TIC), time from start of closure to end of closure (DC), total surgical time (TST=TIC+DC) and length of incision (LI) in centimeters. Incidence of intra-operative complications was also analysed to test a secondary hypothesis that intra-operative complication rates between the two procedures would not be significantly different. Following a Wilk–Shapiro test for normality, two-sample T tests were used to compare age, bodyweight, TIC, DC, TST and LI by surgical procedure. Results are reported as mean and standard deviation (±sd) with P-values, mean differences and 95% confidence intervals given by the Satterthwaite method for unequal variances (Snedecor & Cochran 1989) as in this dataset the assumption of equal variances was violated for all variables. Cross-tabulations and Fishers exact tests were used to compare proportions. The level of significance was set at P2000
48 50 98
27·8 (±7·4) 29·9 (±11·0) 2·1 (−1·7 to 5·8) 197
53 51 104
88·7 (±20·6) 92·0 (±27·6) 3·2 (−6·3 to 12·7) 614
53 50 103
8·7 (±2·6) 9·6 (±3·4) 0·9 (−0·3 to 2·1) 134
*Minimum sample size (SS) required for each treatment group to show statistically significant differences based on the observed differences and variability in the data
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K. P. Harris et al.
and quantification of incision location along the xiphoid–pubis axis would have ensured that any difference in body size distribution amongst the OVE and OHE groups was accounted for, and confirmed whether OVE incisions were made more cranially as suspected. Limitations of this study include the inability to have the same supervising surgeon throughout, potentially leading to variation in the degree of their involvement and the directions given to the student intra-operatively. Eleven different surgeons supervised the 108 cases included in this study including four Diplomates of the European College of Veterinary Surgeons, four residents and two staff surgeons. It is possible that before this study, some of the supervising surgeons had little or no experience of performing/supervising OVE via midline coeliotomy, yet all had extensive experience performing/supervising OHE. Whilst teaching/ supervising the technical skills required for OVE is much the same as teaching/supervising the technical skills required for OHE (midline coeliotomy, location of the ovaries, placement of secure encircling and transfixing ligatures, etc.), the OVE technique was discussed with each supervising surgeon before their involvement with the study, and they were asked to read the written explanation of both OVE and OHE given to the students. This was intended to limit variation in advice given to the students intra-operatively between different surgeons. Whilst the lectures given to these students regarding routine canine neutering in their penultimate year explained both OHE and OVE via midline coeliotomy, it is possible that any practical teaching the students had received on neutering before their involvement in this study concentrated on OHE (particularly if they were assisting with or performing neutering via midline coeliotomy in British general practices whilst on extra-mural study placements). This, however, was not considered to be a major source of bias as any skills (such as ligature placement, suturing, etc.) perfected on previous OHE surgeries would be directly transferable to an OVE procedure. Any uncertainty, for example regarding where to ligate the uterine horn during OVE, could be easily clarified by the supervising surgeon. The weight variation in the study population was large and it is perhaps illogical to include a 51·5 kg dog in a study assessing inexperienced surgeons. However, imposing a weight range would have severely reduced the number of eligible cases. Conducting a multi-center study can overcome the problem of limited eligible cases; however, it often reduces the number of variables which can be controlled. A further limitation to this study was the omission of body condition scoring (BCS) at the time of surgery. Although a subjective measurement, BCS would provide a more accurate indication of the distribution of obesity amongst the OVE and OHE groups than bodyweight given the great variation in body size amongst the dog breeds represented. Whilst obesity is anecdotally reported to make OHE more difficult (Burrows et al. 2005), to the authors’ knowledge only one study has investigated the effect of BCS on surgical time, relative incision length and relative blood loss in dogs undergoing OHE or OVE via midline coeliotomy (Peeters & Kirpensteijn 2011). These authors reported that the preoperative BCS had no significant influence on any 582
of these variables, potentially because of the absence of a correlation between BCS and the amount of intra-abdominal fat. A subjective scale for grading the amount of fat in the ovarian ligament (Van Nimwegan & Kirpensteijn 2007) was used in a study evaluating laparoscopic ovariectomy and a higher amount of fat was significantly associated with a longer operative time (Dupre et al. 2009). If obesity could be controlled for using BCS and/or the ovarian ligament fat scale then any variation in LI or TST should be more directly attributable to surgical procedure. This may highlight a difference between OHE and OVE that at present is not significant. Although the exact pathophysiology of CEH–pyometra complex is not fully understood, the involvement of progesterone is widely accepted (Smith 2006, Verstegen et al. 2008) and as such, following complete removal of the ovaries by OVE, CEH–pyometra complex should not occur in the remaining uterine body. In support of this, a study by Okkens et al. (1997) identified no occurrence of endometritis in a group of 69 bitches that had undergone OVE 8 to 11 years previously, and a study by Janssens & Janssens (1991) identified no case of pyometra in a group of 72 dogs followed for 6 to 13 years after bilateral flank ovariectomy. There appear to be no published case reports of pyometra following complete ovariectomy in the dog or cat. Malignant uterine neoplasia is extremely rare in bitches with an incidence of approximately 0·003% (Van Goethem et al. 2006). In addition, a hormonal influence on the occurrence of these tumours has been postulated (DeTora & McCarthy 2011) and therefore OVE itself may be protective regardless of the fact that the uterine body remains in situ. Complication rates with canine OHE are dependent on surgeon experience (Johnston 1991) and range from 6·3 to 31·5% in the literature (Dorn & Swist 1977, Burrows et al. 2005), although these figures are difficult to compare because of the variation in author definition of intra-, peri- and post-operative complications. Certain complications of OHE are inherent to the ligation and transection of the uterine body at the level of the cervix. These include granuloma formation at the cervical stump (which can lead to adhesion formation with the bladder, ureters, large intestine, mesentery or small intestine), or accidental ureteric or bladder ligation/transection leading to hydroureter, hydronephrosis, ureterovaginal fistula or vesicovaginal fistula (MacCoy et al. 1988, Pearson 1973, Ewers & Holt 1992, Apparicio et al. 2007). Other complications include intra-abdominal haemorrhage from the transected broad ligament or cervical stump, and vaginal bleeding (Pearson 1973). Although mostly rare, these complications can be associated with severe morbidity or even mortality. It is possible that with a more cranially located coeliotomy incision (previously identified with OVE by Peeters & Kirpensteijn 2011) and by avoiding ligation and transection of the uterine body at the level of the cervix, the incidence of these complications may be lower for OVE than OHE. Because of the infrequency with which the more severe complications appear to occur (no known cases of uterine stump granuloma formation in 377 canine OHE procedures (Berzon 1979) for example), this possible benefit of OVE over OHE must not be overstated.
Journal of Small Animal Practice
•
Vol 54
•
November 2013
•
© 2013 British Small Animal Veterinary Association
Comparing ovariectomy and ovariohysterectomy
Although a significant decrease in surgical duration was not apparent in this study, the authors still propose that OVE is an appropriate alternative to OHE for canine neutering in the hands of veterinary students. No major complications novel to OVE occurred in the cohort of 54 dogs. The avoidance of complications such as bladder laceration (as occurred in this study in an OHE dog) and other rare complications such as caudal ureteric ligation (reported to occur more than proximal ureteric ligation because of the intra-peritoneal location of the caudal ureter and its close proximity to the uterine body (DeTora & McCarthy 2011) might be possible with OVE performed through a cranially located incision, however, a much larger scale multi-centre study would be required to conclude this with any certainty. Long-term follow-up of the cases in this study is planned to establish the incidence of ovarian remnant syndrome, urinary incontinence and post-OVE uterine disease in this cohort of dogs. Acknowledgements The authors would like to express their gratitude to the staff and students of the Queen’s Veterinary School Hospital, Cambridge, for their involvement in data collection, in particular Mr. David Sheen. Conflict of interest None of the authors of this article has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. References Apparicio, M., Vicente, W. R. R., Farias, A., et al. (2007) Pyonephrosis following ovariohysterectomy in a bitch. Ars Veterinaria 23, 19-22 Berzon, J. L. (1979) Complications of elective ovariohysterectomies in the dog and cat at a teaching institution: clinical review of 853 cases. Veterinary Surgery 8, 89-91 Brown, D. C., Conzemius, M. G., Schofer, F. et al. (1997) Epidemiological evaluation of postoperative wound infections in dogs and cats. Journal of the American Veterinary Medical Association 210, 1302-1306 Burrow, H., Batchelor, D. & Cripps, P. (2005) Complications observed during and after ovariohysterectomy of 142 bitches at a veterinary teaching hospital. The Veterinary Record 157, 829-833
Journal of Small Animal Practice
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Vol 54
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November 2013
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Danova, N. A., Schmiedt, C. & Bjorling, D. (2005) The female reproductive system. In: BSAVA Manual of Canine and Feline Abdominal Surgery. Eds J. M. Williams & J. D. Niles. BSAVA, Gloucester, MA, USA. pp 298-306 DeTora, M. & McCarthy, R. J. (2011) Ovariohysterectomy versus ovariectomy for elective sterilization of female dogs and cats: is removal of the uterus necessary? Journal of the American Veterinary Medical Association 239, 1409-1412 Dorn, A. S. & Swist, R. A. (1977) Complications of canine ovariohysterectomy. Journal of the American Animal Hospital Association 13, 720-724 Dupre, G., Fiorbianco, V., Skalicky, M. et al. (2009) Laparoscopic ovariectomy in dogs: comparison between single portal and two-portal access. Veterinary Surgery 38, 818-824 Ewers, R. S. & Holt, P. E. (1992) Urological complications following ovariohysterectomy in a bitch. Journal of Small Animal Practice 33, 236-238 Fingland, R. B. (1997) Uterus. In: Current Techniques in Small Animal Surgery. 4th edn. Ed M. J. Bojrab. Williams and Wilkins, Baltimore, MD, USA. pp 489-502 Hedlund, C. S. (2007) Surgery of the reproductive and genital systems. In: Small Animal Surgery. 3rd edn. Ed T. W. Fossum. Mosby Elsevier, St. Louis, MO, USA. pp 702-774 Janssens, L. A. A. & Janssens, G. H. R. R. (1991) Bilateral flank ovariectomy in the dog - surgical technique and sequelae in 72 animals. Journal of Small Animal Practice 32, 249-252 Johnston, S. D. (1991) Questions and answers on the effects of surgically neutering dogs and cats. Journal of the American Veterinary Medical Association 198, 1206-1214 MacCoy, D. M., Ogilvie, G., Burke, T. et al. (1988). Postovariohysterectomy ureterovaginal fistula in a dog. Journal of the American Animal Hospital Association 24, 469-471 Okkens, A. C., Kooistra, H. S. & Nickel, R. F. (1997) Comparison of long-term effects of ovariectomy versus ovariohysterectomy in bitches. Journal of Reproduction and Fertility Supplement 51, 227-231 Pearson, H. (1973) The complications of ovariohysterectomy in the bitch. Journal of Small Animal Practice 14, 257-266 Peeters, M. E. & Kirpensteijn, J. (2011) Comparison of surgical variables and short-term postoperative complications in healthy dogs undergoing ovariohysterectomy or ovariectomy. Journal of the American Veterinary Medical Association 238, 189-194 Smith, F. O. (2006) Canine pyometra. Theriogenology 66, 610-612 Snedecor, G. W. & Cochran, W. G. (1989) The comparison of two samples. In: Statistical Methods. 8th edn. Iowa State University Press, Iowa City, IA, USA. pp 83-106 Stone, E. A. (2003) Ovary and Uterus. In: Textbook of Small Animal Surgery. 3rd edn. Ed D. Slatter. Saunders, Philadelphia, PA, USA. pp 1947-1502 Tivers, M. S., Travis, T. R. D., Windsor, R. V., et al. (2005) Questionnaire study of canine neutering techniques taught in UK veterinary schools and those used in practice. Journal of Small Animal Practice 46, 430-435 Van Goethem, B., Schaefers-Okkens, A. & Kirpensteijn, J. (2006) Making a rational choice between ovariectomy and ovariohysterectomy in the dog: A discussion of the benefits of either technique. Veterinary Surgery 35, 136-143 Van Nimwegan, S. A. & Kirpensteijn, J. (2007) Comparison of Nd:YAG surgical laser and Remorgida bipolar electrosurgery forceps for canine laparoscopic ovariectomy. Veterinary Surgery 36, 533-540 Verstegen, J., Dhaliwal, G. & Verstegen-Onclin, K. (2008) Mucometra, cystic endometrial hyperplasia, and pyometra in the bitch: advances in treatment and assessment of future reproductive success. Theriogenology 70, 364-374
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