1 2 The ovulation timing service for bitches at the department of clinical 3 sciences of companion animals at Utrecht University: a retrospective study 4 on the period 2003-2010 and a client satisfaction survey 5 6 7 8 9 10 11 12 13 Research Project Veterinary Medicine Utrecht University 14 By Drs. L.J.C. Leijen 15 3155579 16 17 April 2011 18 19 Supervisor: Drs. J. de Gier 20 Department of Clinical Sciences of Companion Animals 21 Faculty of Veterinary Medicine, Utrecht University 22 23 24 25 26 27 28 29 30 31 32 33 34 Table of contents Page 35 36 General introduction 4 38 Part one: Retrospective study on the period: 2003-2010 5 39 Abstract ....................................................................................................................... 5 40 Introduction ................................................................................................................ 5 41 Materials and Methods .............................................................................................. 7 42 1. Animals ......................................................................................................... 7 43 2. Ovulation timing ........................................................................................... 8 44 3. Statistical analysis ........................................................................................ 8 45 Results.......................................................................................................................... 8 46 1. Bitches and their litters................................................................................. 8 47 2. Annual variation in bitches presented for ovulation timing ......................... 9 48 3. Effect of the age of the bitch ......................................................................... 9 49 4. Effect of the parity of the bitch ..................................................................... 10 50 5. Effect of different breeds............................................................................... 11 51 6. Effect of the weight of the bitch .................................................................... 12 52 7. Effect of the fertilization method .................................................................. 13 53 7.1. Natural matings ................................................................................... 13 54 7.2. Artificial insemination ......................................................................... 14 55 Discussion .................................................................................................................... 14 56 1. Bitches and their litters................................................................................. 15 57 2. Annual variation in bitches presented for ovulation timing ......................... 16 58 3. Effect of the age of the bitch ......................................................................... 17 59 4. Effect of the parity of the bitch ..................................................................... 17 60 5. Effect of different breeds............................................................................... 18 61 6. Effect of the weight of the bitch .................................................................... 18 62 7. Effect of the fertilization method .................................................................. 18 63 7.1. Natural matings ................................................................................... 19 64 7.2. Artificial insemination ......................................................................... 20 65 Conclusion ................................................................................................................... 20 66 References ................................................................................................................... 21 67 Appendix ..................................................................................................................... 24 37 2 68 Supplement Table A ......................................................................................... 24 69 70 Part two: Customers satisfaction survey 31 71 Abstract ....................................................................................................................... 31 72 Introduction ................................................................................................................ 31 73 Materials and Methods .............................................................................................. 33 74 1. Participants .................................................................................................. 33 75 2. Questionnaire ............................................................................................... 33 76 3. Statistical analysis ....................................................................................... 33 77 Results.......................................................................................................................... 33 78 1. Main purpose for keeping the dog ................................................................ 34 79 2. Propositions .................................................................................................. 34 80 3. Written information ...................................................................................... 35 81 4. Additional help ............................................................................................. 36 82 5. General evaluation ....................................................................................... 36 83 Discussion .................................................................................................................... 36 84 1. Main purpose for keeping the dog ................................................................ 37 85 2. Propositions .................................................................................................. 38 86 3. Written information ...................................................................................... 39 87 4. Additional help ............................................................................................. 40 88 5. General evaluation ...................................................................................... 40 89 Conclusion ................................................................................................................... 41 90 References ................................................................................................................... 42 91 Appendix ..................................................................................................................... 43 92 Supplement Table A ......................................................................................... 43 93 94 95 96 97 98 99 100 101 3 102 General introduction 103 The department of clinical sciences of companion animals at Utrecht University (UKG) 104 offers an ovulation timing service. This service helps people to find the optimal day for 105 mating in healthy bitches and in bitches with fertility problems and it helps also to manage 106 artificial inseminations. The aim of the ovulation timing service is to improve the pregnancy 107 outcomes. 108 The present study is divided into two parts. In the first part we examined the effect of age, 109 parity, breed, weight and fertilization method on pregnancy rates and litter size. Furthermore, 110 the effect of season on the distribution of presenting dogs for ovulation timing was studied. In 111 the second part the results of a customers satisfaction survey about the ovulation timing 112 service were showed. 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 4 134 Part one: Retrospective study on the period: 2003-2010 135 Abstract 136 The effects of age, parity, breed, weight and fertilization method on pregnancy rates and litter 137 size were studied in 681 bitches of 124 different breeds. Furthermore, the effect of season on 138 the distribution of presenting dogs for ovulation timing was examined. Data collected from 139 the department of clinical sciences of companion animals at Utrecht University during 2003- 140 2010 were analyzed. The number of dogs presented for ovulation timing was reduced 141 between 2003 and 2008 and after 2008 the number was stabilized. Pregnancy rates of dogs 142 presented without fertility problems (85.4%) were higher than pregnancy rates of dogs 143 presented with fertility problems (66.5%). In bitches of one (P = 0.037) and two years old (P 144 = 0.048), which gave birth to their first litter, pregnancy rates were higher than those of 145 bitches of seven years old. Labrador retrievers had a significant (P = 0.01) higher pregnancy 146 rate than Golden retrievers (respectively 90.2% and 74.6%). The mean number of total 147 Doberman pups per litter (8.43± 3.52) was higher than the mean number of German shepherd 148 pups (6.17 ± 3.07, P = 0.04). The median weight of the bitches presented for ovulation timing 149 was 29.4 kg, ranging from 2.0 to 71.1. Pregnancy rates were higher in bitches of 10.0-24.9 kg 150 (87.7%) compared to bitches over 45.0 kg (72.7%, P = 0.02). Weight was also found to effect 151 total litter size. Dogs up to 9.9 kg had smaller litters (4.15 ± 1.39, P = 0.005) than dogs 152 between 10.0-24.9 kg (6.49 ± 2.73). Both those groups had smaller litters (respectively P ≤ 153 0.001 and P ≤ 0.02) than dogs of 25.0-44.9 kg (7.47 ± 2.86) and dogs of more than 45.0 kg 154 (8.40 ± 3.73). A difference (P ≤ 0.001) in pregnancy rate was found between natural matings 155 (85.1%), artificial inseminations with fresh semen (66.7%) and artificial inseminations with 156 frozen-thawed semen (27.8%) and a lower pregnancy rate was observed among bitches that 157 mated without a copulatory tie (71.4%, P = 0.038) compared to matings including a 158 copulatory tie (85.9%). Parity did not have an effect on both pregnancy rates and litter size 159 and season did not affect the number of dogs presented for ovulation timing. 160 161 Introduction 162 The dog is a non-seasonally monoestrous species, typically showing two spontaneous estrus 163 cycles per year (range: 1-4). The estrous cycle of the bitch can be divided into four stages: 164 proestrus, estrus, metestrus and anestrus [1,2]. Proestrus has a duration varying from 3 to 17 165 days [3]. During this period the vulva is swollen and there is serosanguineous discharge from 166 the vulva. Males are attracted to bitches who are not yet receptive to mating [2,4]. During 5 167 estrus the vulva softens but is still enlarged and the color of the vaginal discharge becomes 168 lighter. However, sometimes it can still be serosanguineous. Furthermore, during estrus the 169 bitch will be receptive to the dog for mating and deviates her tail to one side [4]. Estrus lasts 170 for 3-21 days [3]. During diestrus, which has a duration of 45-60 days, the bitch is not 171 receptive anymore, the vulva decreases in size, discharge becomes clear, purulent or 172 hemorrhagic and subsequently stops. Later, mammary development may be noted as a result 173 of increased mammary growth hormone secretion induced by progesterone [2]. Finally, 174 anestrus involves the absence of ovarian activity which is defined as the day that the plasma 175 progesterone concentrations decrease below 6 nmol/L. During this phase bitches are not 176 receptive and the vulva is small [1,2]. 177 178 Logically, dog breeders can only observe the outer clinical symptoms and the dog’s behavior. 179 Unfortunately, duration of proestrus and estrus is variable. For instance, the start of the dog 180 being receptive for mating varies between 5 days before to more than 6 days after the 181 preovulatory LH surge, while optimal fertility can be anticipated if a bitch is bred 2-4 days 182 after ovulation which usually occurs 2-3 days after the LH surge [2,3,5,6]. Therefore, it is 183 difficult for breeders to relate behavior or physical symptoms to the optimal day for mating 184 [3,7]. To better determine the optimal day for mating several diagnostic tools are available, 185 e.g. cytology of vaginal smears, vaginoscopy, and measurement of the plasma progesterone 186 concentration [8]. The department of clinical sciences of companion animals at Utrecht 187 University (UKG) offers an ovulation timing service, which includes these examination 188 methods. The progesterone concentration has been proven to be the most reliable tool 189 because an abrupt increase of the plasma concentration occurs simultaneously with the 190 preovulatory LH surge. The plasma progesterone concentration is measured using an I-125 191 RIA [9]. Progesterone measurement is more convenient than measurement of serum LH 192 concentrations that needs to be done three times daily in order to yield reliable results [9]. 193 Besides helping to improve the pregnancy outcomes, many other reasons may prompt 194 dog owners to make use of the service, such as increasing the efficiency when the male dog 195 of choice is far away, and traveling with the bitch or import of semen have to be timed 196 accurately. Additionally, ovulation timing can be useful if bitches are presented with fertility 197 problems, for instance split heat. 198 199 Other studies [10,11,12,13,14,15] examined the effect of a variety of factors on pregnancy or 200 whelping rates and litter size, for example the influence of age, parity, different breeds and 6 201 insemination method. Okkens et al. found a smaller litter size in West Highland white terriers 202 than in Labrador retrievers [10], which is in agreement with the outcome of Thomassen et al. 203 and Scantlebury, Butterwick and Speakman. They found that smaller dogs breed smaller 204 litters than larger breeds [12,14]. B. Bobic Gavrilovic et al. found that age and parity had a 205 significant effect on litter sizes [11]. It would be interesting to know what the effects of 206 different factors are on pregnancy rates and litter sizes at UKG and to compare the results 207 with other studies. 208 209 The aim of this study is to examine the effect of season on the distribution of presenting dogs 210 for ovulation timing, during the period 2003-2010. Furthermore, the effects of age, parity, 211 breed, weight and fertilization method on pregnancy rates and litter size were examined. 212 213 Materials and Methods 214 1. Animals 215 All bitches, presented for ovulation timing at Utrecht University between January 2003 and 216 August 2010, were included in this study. In total, 681 different bitches were presented for 217 ovulation timing. Some of them were presented only once, others more frequently (up to 6 218 times), making a total of 997 cases. Bitches varied in age between 1 and 9 years old with a 219 mean ± SD age of 3.7 ± 1.6 years. 664 bitches belonged to one of 124 different breeds, 220 recognized by the Fédération Cynologique Internationale (F.C.I.) (suppl. Table A). The 221 remaining 17 dogs were crossbreeds or of breeds not recognized by the F.C.I. 222 Top 10 breeds at UKG Golden Retriever Labrador Retriever German Shepherd Dog Dobermann Drentse Partridge Dog German Boxer Newfoundland Weimaraner, Short-haired French Bulldog Bernese Mountain Dog Total at UKG 223 Number of different dogs presented '03-'10 85 73 37 33 21 19 18 14 14 13 681 Top 10 breeds in Holland Labrador Retriever German Shepherd Dog Golden Retriever Bernese Mountain Dog German Boxer Cavalier King Charles Spaniel Staffordhire Bullterriër Bulldog Border Collie Bouvier des Flandres Total in Holland Dogs in the Netherlands '03-'06 18825 14070 9390 7404 5406 4883 4160 3894 3644 3401 199409 Table 1: Top 10 breeds presented at UKG and Top 10 breeds living in Holland 7 224 The percentages of different breeds presented at UKG are not representative for the entire 225 dog population in the Netherlands during the same period (suppl. Table A.) namely not all 226 breeds found in the Netherlands are presented at UKG and also the percentages of the breeds, 227 which are presented, differ from the percentages of the dogs found in the Netherlands. 228 However, the top three is the same, but in a different order (table 1). 229 230 2. Ovulation timing 231 Ovulation timing was offered in the morning three times each week. A specialized form 232 (“ovulation timing”) in the online software program called Vetware was used by the co- 233 assistant, who was supervised by one of the veterinarians, to record the findings gathered by 234 taking a medical history, physical examination and further medical tests. Blood samples are 235 collected for determination of plasma progesterone concentrations using I-125 236 radioimmunoassay (RIA). After mating, dog owners were encouraged to return with the bitch 237 for a pregnancy diagnosis. Primarily abdominal palpation was used to determine pregnancy. 238 If the outcome was uncertain, abdominal ultrasound, performed by a specialized veterinary 239 radiologist, was advised. Furthermore, owners were asked to return a follow-up form by post 240 containing information on the parturition and litter. Unfortunately, the forms were not always 241 fully completed or returned resulting in missing clinical and follow-up data. 242 243 3. Statistical analysis 244 All relevant information about the cases was retrieved with Vetware. The collected data were 245 organized in Excel, after which the data were exported to SPSS 17.0. SPSS was used for 246 statistical analysis. An F-test was used for comparing differences between years and months 247 in dogs presented for ovulation timing. One-way ANOVA was used to analyze and test the 248 significance of the different factors, which possibly influence pregnancy rates en litter size. 249 Results are presented as percentages and mean ± SD, and were considered to be statistically 250 significant when P ≤ 0.05. 251 252 Results 253 1. Bitches and their litters 254 The descriptive data for bitches, presented for ovulation timing, and their litters are given in 255 table 2. Pregnancy rates of dogs presented without fertility problems (85.4%) were higher 256 than pregnancy rates of dogs presented with fertility problems (66.5%). 257 8 Data UKG 72.8 (687) Dogs presented without a fertility problem (%) (n) 85.4 (503) Pregnancy rates dogs presented without a problem (%) (n) 27.2 (257) Percentage dogs presented with a fertility problem (%) (n) 66.5 (158) Pregnancy rates dogs presented with a fertility problem (%)(n) 258 259 Total number of pups born (n) 2882 Number of pups per litter (range) 7.10 ± 2.98 (1-17) Number of stillborn pups per litter (range) 0.73 ± 1.33 (0-10) Male pups at the time of birth (%) 51.9 Table 2: Descriptive data from UKG for the ovulation timing service during 2003-2010. Data are given as means ± standard deviation (range). 260 261 2. Annual variation in bitches presented 262 for ovulation timing. 263 Between 2003 and 2008 the number of 264 dogs presented for ovulation timing was 265 reduced from 187 to 97 (Fig. 1). This is a Fig 1: Number of dogs offered for ovulation timing to predict the optimal day for mating Number of dogs 200 187 161 266 decrease of 51.9%. Also, the number of 150 267 dogs presented in 2009 (n = 101) was 100 268 reduced compared to 2003. There were 269 no differences found in the distribution 270 between months. 153 122 116 97 101 2008 2009 Year 50 0 2003 2004 2005 2006 2007 271 272 3. Effect of the age of the bitch 273 Most of the bitches are 2 (29.2%, n = 163) or 3 (28.9%, n = 161) years old when first 274 presented for ovulation timing (range from one to seven) at UKG. 275 Pregnancy rates and number of pups per litter for all parities, grouped by age of the 276 bitch, are given in Table 3. Pregnancy rates and number of pups per litter for bitches that 277 gave birth for the first time, grouped by age of the bitch, are given in Table 4. No significant 278 effects of the age of the bitch were found for all parities on pregnancy rates. Nevertheless, 279 there was a difference between bitches that give birth for the first time, namely pregnancy 280 rates of bitches of one (P = 0.037) and two (P = 0.046) years old were higher than those of 281 bitches of seven years old. 282 283 Age was found not to have a significant effect on the total number of pups per litter and pups per litter born alive. 9 284 285 Table 3: Pregnancy rates and number of pups per litter for all parities, grouped by age of the bitch. Age of the bitch Pregnancy rate at the time of given birth, for Percent N all litters (years) Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) Number N (mean ± S.D.) 1 87.5 56 6.86 ± 2.91 35 6.08 ± 3.05 24 2 82.7 150 7.57 ± 3.07 86 6.96 ± 2.86 56 3 83.5 200 7.28 ± 3.05 121 6.93 ± 2.65 81 4 78.7 141 6.91 ± 2.73 70 6.55 ± 2.69 49 5 80.3 117 6.33 ± 2.96 57 5.87 ± 2.83 38 6 77.8 72 7.27 ± 3.05 26 6.48 ± 2.98 21 7 71.9 32 7.88 ± 2.75 8 - - 8 75.0 4 - - - - 286 287 288 289 Table 4: Pregnancy rates and number of pups per litter from bitches that gave birth for the first time, grouped by age. Age of the bitch Pregnancy rate (%) at the time of giving birth to Percent N first litter (years) 290 Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) Number N (mean ± S.D.) 1 87.3 a 55 6.91 ± 2.94 34 6.17 ± 3.08 23 2 83.7 a 135 7.65 ± 3.05 80 7.08 ± 2.76 51 3 78.9 ab 123 6.76 ± 2.89 66 6.28 ± 2.38 43 4 73.1 ab 52 7.27 ± 1.96 22 6.44 ± 2.09 18 5 75.0 ab 20 4.86 ± 2.80 7 5.50 ± 3.11 4 6 33.3 ab 3 - - - - 7 0.0 b 2 - - - - Different superscript letters (a-b) denote significant differences (P ≤ 0.05). 291 292 4. Effect of the parity of the bitch 293 Pregnancy rates and number of pups per litter, grouped by parity of the bitch, are given in 294 Table 5. Parity was found not to have a significant effect on pregnancy rates, total pups per 295 litter and pups per litter born alive. 296 297 298 299 300 10 301 Table 5 Pregnancy rates and number of pups per litter, grouped by parity. Parity of the Pregnancy rate (%) bitch Percent N Number of pups (per Number of pups born alive litter) (per litter) Number (mean N Number (mean ± S.D.) N ± S.D.) 1 80.1 392 7.10 ± 2.92 210 6.53 ± 2.64 140 2 82.4 222 7.34 ± 3.05 124 6.80 ± 2.96 95 3 81.0 100 6.39 ± 3.06 46 5.93 ± 3.13 27 4 82.5 40 7.83 ± 2.73 18 7.45 ± 2.34 11 5 75.0 8 5.50 ± 3.54 2 - - 302 303 5. Effect of different breeds 304 When examining the different breed groups coming to UKG, 26.6% of the dogs are 305 retrievers, flushing dogs and waterdogs (group 8). Almost 25% is from group 2 and 17.8% 306 are sheepdogs and cattle dogs (suppl. Table A and Fig. 2 ). Statistical analyses are only 307 performed with the four breeds most often seen at UKG (Table 1). Number of bitches Fig 2: Number of bitches offered for fertility management at UKG divided in breed groups 181 168 121 61 48 39 3 14 15 14 17 Group 11 308 309 Group10 Breed group Group 9 Group 8 Group 7 Group 6 Group 5 Group 4 Group 3 Group 2 Group 1 200 180 160 140 120 100 80 60 40 20 0 Group 1 Sheepdogs and cattledogs except Swiss cattle dogs Group 2 Pinscher and Schnauzer, molossoid breeds, Swiss mountain and cattle dogs Group 3 Terriers Group 4 Dachshunds Group 5 Spitz and primitive types Group 6 Scenthounds and related breeds Group 7 Pointing dogs Group 8 Retrievers, flushing dogs, water dogs Group 9 Companion and toy dogs Group 10 Sighthounds Group 11 Crossbreed/Unknown 310 11 311 Pregnancy rates and number of pups per litter, grouped by the four breeds most presented at 312 UKG, are given in Table 6. Different breeds were found to have a significant effect on 313 pregnancy rates. Labrador Retrievers had a significant (P = 0.01) higher pregnancy rate than 314 Golden Retrievers (respectively 90.2% and 74.6%). No differences in pregnancy rates were 315 observed with and between the other breeds. There was also found a significant effect of 316 breeds on litter size (P = 0.04). The mean number of total Doberman pups per litter is 8.43 317 and for German shepherd pups the mean is 6.17. The different breeds were not found to 318 influence the number of pups born alive. 319 320 321 Table 6: Pregnancy rates and number of pups per litter, grouped by the four breeds most presented at UKG. Breeds Pregnancy rate (%) Percent N Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) 322 Doberman 89.4 ab German Shepherd 76.5 ab Golden Retriever 74.6 a Labrador Retriever 90.2 b Number N (mean ± S.D.) 47 8.43 ± 3.52 a 23 6.33 ± 3.85 12 34 6.17 ± 3.07 b 18 5.17 ± 3.07 12 7.54 ± 2.74 ab 61 7.24 ± 2.94 41 7.72 ± 2.21 ab 76 7.11 ± 1.99 53 118 112 Different superscript letters (a-b) denote significant differences (P ≤ 0.05). 323 324 6. Effect of the weight of the bitch 325 Weight as well as breed of all bitches presented for ovulation timing was widely diverse. The 326 median weight was 29.4 kg (range from 2.0 to 71.1). To examine whether weight affects 327 pregnancy rate and litter size, the dogs were divided into four weight classes. 328 Pregnancy rate and litter size, grouped by four weight classes, are given in Table 7. 329 Weight was found to have a significant effect on pregnancy rates. The pregnancy rate was 330 highest for dogs in weight class two (87.7%). This percentage was higher (P = 0.02) than the 331 percentage for dogs in weight class four (72.7%). 332 Weight was also found to effect total litter size and number of pups born alive. The 333 total litter size increased significantly in dogs with higher body weight. Dogs between 10.0- 334 24.9 kg (mean = 6.49) had larger litters than dogs up to 9.9 kg (mean = 4.15) (P = 0.005). The 335 number of pups per litter in both group one (P ≤ 0.001) and two (P ≤ 0.02) was significantly 336 smaller than in dogs of 25.0-44.9 kg (mean = 7.47) and in dogs of more than 45.0 kg (mean = 337 8.40). 12 338 Also the number of pups born alive was lower in small dogs. Weight classes 1 (mean 339 = 3.91, P ≤ 0.005) and 2 (mean = 5.92, P = 0.015) had significantly fewer pups born alive 340 than dogs between 25.0 and 44.9 kg (mean = 7.06). 341 342 Table 7 Pregnancy rates and number of pups per litter, grouped by weight. Weight class Pregnancy rate (%) Percent N Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) 343 1: ≤ 9.9 83.3 ab 2: 10.0 - 24.9 87.7 a 3: 25.0 - 44.9 80.0 ab 4: ≥ 45.0 72.7 b 42 187 451 77 4.15 ± 1.39 a 6.49 ± 2.73 b 7.47 ± 2.86 c 8.40 ± 3.73 c Number N (mean ± S.D.) 20 101 242 35 3.91 ± 1.81 a 11 5.92 ± 2.62 ac 74 7.06 ± 2.72 b 161 7.22 ± 3.07 bc 23 Different superscript letters (a-c) denote significant differences (P ≤ 0.05). 344 345 7. Effect of the fertilization method 346 According to the data, natural matings are most common (81.4%, n = 714). 15.3% (n = 134) 347 of the bitches were artificially inseminated (AI) and the remaining 3.3% (n = 29) did not mate 348 at all. Pregnancy rate and litter size, grouped by fertilization method, are given in Table 8. A 349 difference (P ≤ 0.001) in pregnancy rates was found between the three different fertilization 350 methods of which natural mating were the most successful (85.1%), then AI with fresh semen 351 (66.7%) and AI with frozen-thawed semen was the least successful (27.8%). There is no 352 evidence that fertilization method affected the number of pups. 353 354 Table 8: Pregnancy rates and number of pups per litter grouped by fertilization method. Fertilization Pregnancy rate (%) method Percent N Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) Number N (mean ± S.D.) Natural mating 85.1 a 649 7.18 ± 2.92 351 6.59 ± 2.81 241 AI fresh semen 66.7 b 93 6.85 ± 3.36 39 6.50 ± 2.74 24 AI frozen- 27.8 c 18 6.33 ± 3.79 3 - - thawed semen 355 Different superscript letters (a-c) denote significant differences (P ≤ 0.05). 356 357 7.1. Natural matings 358 Pregnancy rate and litter size, grouped by occurrence of the copulatory tie, are given in Table 359 9. 92% of the natural matings included a copulatory tie. A lower percentage of pregnancy 13 360 was observed among bitch that mated without a copulatory tie (P = 0.038). The pregnancy 361 rate for matings including a copulatory tie was 85.9%, compared with 71.4% for matings 362 without a copulatory tie. 363 364 Table 9: Pregnancy rates and number of pups per litter grouped by copulatory tie. Copulatory tie Pregnancy rate (%) Percent N Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) Yes No 365 85.9 a 71.4 b Number N (mean ± S.D.) 446 7.13 ± 2.96 239 6.47 ± 2.83 177 28 7.57 ± 2.88 14 7.33 ± 2.18 9 Different superscript letters (a-b) denote significant differences (P ≤ 0.05). 366 367 7.2. Place of artificial insemination 368 Pregnancy rate and litter size for both places of artificial insemination, are shown in Table 10. 369 In this study, the place of insemination was not found to affect both pregnancy rates and litter 370 size significantly. 371 372 373 Table 10 Pregnancy rates and number of pups per litter in bitches inseminated with fresh or frozen semen, grouped by place of artificial insemination. Place of AI Pregnancy rate (%) Percent N Number of pups (per Number of pups born alive litter) (per litter) Number N (mean ± S.D.) Number N (mean ± S.D.) Cranial vagina 63.3 30 7.08 ± 3.58 12 6.67 ± 2.81 6 Intra-uterine 77.1 35 6.93 ± 3.83 15 6.60 ± 3.24 10 374 375 Discussion 376 The results of the present study show that the number of dogs presented for ovulation timing 377 between 2003 and 2008 decreased significantly and were stable again in 2009. A presentation 378 at UKG showed that the number of dogs was decreased throughout the department of 379 companion dogs. Furthermore, we found that pregnancy rate of dogs without fertility 380 problems was 85.4%. In bitches with fertility problems 66.5% was pregnant after ovulation 381 timing. In bitches that were pregnant for the first time, a lower pregnancy rate was found in 382 bitches of 7 years old compared to bitches of 1 and 2 years old. Thomassen et al. [12] 383 discourage dog owners to breed the bitch when bitches were > 6 years old and had not 14 384 whelped before. Furthermore, breed was found to affect pregnancy rate and litter size. This is 385 in line with the results of Okkens et al [10]. They found that Labrador retrievers and 386 Dobermans have larger litters than West Highland white terriers. Litter size and pregnancy 387 rate are also influenced by weight. Dogs with higher body mass had larger litters which was 388 expected because metabolism costs are relatively smaller in larger breeds [14]. Finally, we 389 found that fertilization method influenced pregnancy rate. Pregnancy rates of natural matings, 390 AI with fresh semen and AI with frozen-thawed semen were 85.1%, 66.7% and 27.8%, 391 respectively. Furthermore, occurrence of a copulatory tie during the natural mating is 392 important because higher pregnancy rates were observed among bitches that mated with a 393 copulatory tie (85.9%) compared to matings without a copulatory tie (71.4%). 394 395 1. Bitches and their litters 396 In the present study was chosen for pregnancy rate while most studies use whelping rate. 397 Because the UKG was not directly involved in the birth process, the amount of information 398 about whelpings was dependent on breeders, who had to complete a follow-up form with 399 information about parturition and litter. Unfortunately only 40.7% of the breeders had 400 returned the follow-up form of which about 65% was fully completed. Pregnancy was 401 established in the clinic by palpation and ultrasonography (if necessary) and then saved to the 402 computer. Consequently, there were many more data available on the number of pregnancies 403 (77.8%) than the number of whelpings. Therefore, pregnancy rates were chosen in this study. 404 Regrettably, not every pregnancy is followed by whelping because resorption or abortion can 405 occur by infectious and non-infectious diseases. Consequently, whelping rate is a bit lower 406 than pregnancy rate which must be taken into account when comparing with other studies. 407 Unfortunately there are no evident rates available about resorption and abortion rates in dogs. 408 At UKG, pregnancy rate of dogs without fertility problems was 85.4%. The expected 409 normal range for whelping rate is between 80-95% according to some studies [11,16]. Both 410 these studies examined the whelping rates retrospectively from Kennel Clubs. It is unclear 411 how many of those breeders made use of an ovulation timing service and how many breeders 412 bred their bitches without any help. When the percentage of abortion of dogs presented at 413 UKG is below 5.4%, the whelping rate falls within the normal range. Unfortunately, this 414 percentage is unknown at UKG. 415 Dogs with fertility problems are dogs that for some reason do not become pregnant. 416 For instance, these include dogs with hypothyroidism or CEH but also dogs that are normally 417 fertile, but where behavior and physical symptoms are not related to the optimal day for 15 418 mating. The definition of infertility used in the present study was that bitches had not become 419 pregnant in the past at least once, regardless of the cause. With medical treatment, 420 measurement of progesterone and managing the entire process concerning the fertility 421 problem, the veterinarians of UKG try to make matings successful. After ovulation timing 422 66.5% of the ‘problem dogs’ were pregnant. So 33.5% of those dogs did not become pregnant 423 even after ovulation timing at UKG. One cause could be infertility of the bitch for example 424 due to problems of the genital tract. Other causes could be the male dog being sterile or the 425 breeder. 426 Percentage of male pups of 51.9% is in agreement with average ratios of B. Bobic 427 Gavrilovic [11] (50.5% for Swedish Kennel Club and 49.6% for Private kennel). According 428 to one study the percentage of male pups is expected to be slightly higher than the percentage 429 of female pups. Namely, in dogs that are genetically carriers of cryptorchidism, an increased 430 percentage of male pups were born (57.6% were male pups if the parents were both carriers 431 of cryptorchidism and 50.0% were male pups if not, P < 0.001) [17]. Studies reported a 432 prevalence of 1-11% [17] and 6.8% [18] of cryptorchidism among dogs. Consequently, a lot 433 of dogs are genetically carriers so the number of males in litters might be greater on 434 population level. 435 436 2. Annual variation in bitches presented for ovulation timing 437 During the period 2003-2008 the number of dogs presented for ovulation timing decreased 438 significantly. In 2009 the number of dogs seemed stable again. The decrease could be related 439 to a number of veterinarians in the field who started to offer ovulation timing service. In the 440 present study it is not investigated if this number had increased. 2008 was the beginning of an 441 economic crisis in the Netherlands. However, the number of dogs presented in 2008 was not 442 significantly decreased compared to the number in 2007. In 2009 the number of dogs even 443 stabilized compared to 2008. Thus, the economic crisis had no significant impact on the 444 number of dogs that was presented for ovulation timing. Furthermore, a presentation at UKG 445 demonstrated that the number of dogs, presented at all disciplines of UKG, showed the same 446 trend as the number of dogs presented for ovulation timing. So, these numbers are stabilized 447 too over the last years. This could be caused by the management taking action against the 448 decreasing number of patients. 449 In the present study there were no significant differences between months. Bouchard 450 et al. [19], studying 67 Colony bitches of 5 different breeds over 4 years during 210 estrous 451 cycles, also found that the occurrences of estrous are the same for each month of the year. By 16 452 contrast, B. Bovic Gavrilovic et al. found that most matings took place during the winter but 453 fewest during summer [11]. In their study they only examined the Drever breed which turned 454 out to be a seasonal breeder. 455 However, it seems that more bitches are bred in August, September, January, 456 February and March. This may be due to management reasons. The matings in August and 457 September may be due to a higher demand for pups for St. Nicholas or Christmas. And the 458 matings during winter give pups in spring and summer. A higher demand in those seasons 459 may be due to dog owners who want to raise and housetrain their dog during the holidays. 460 461 3. Effect of the age of the bitch 462 When analyzing all parities, no association was found between pregnancy rate and age of the 463 bitch in the present study. Other studies [16,20] showed a decrease in conception rate with 464 increasing age. Thomassen et al. [12] reported decreased whelping rates in bitches older than 465 6 years (68.2% compared to younger dogs that have a rate of 77%). The fertilization method 466 in their study was artificial insemination with frozen semen. 467 In the present study there was also no effect found on the number of pups born per 468 litter among all parities, grouped by age. A previous study [11] reported conflicting results. 469 They found the mean number of registered pups per litter was significantly lower in bitches > 470 4 years old. The different results compared to B. Bobic Gavrilovic et al. [11] may be due to a 471 considerably lower number of cases in the our study. Also, some other studies reported a 472 decrease in conception rate and litter size with increasing age [16,20]. 473 In bitches that were pregnant for the first time, a higher pregnancy rate was found in 474 bitches of 1 and 2 years compared to bitches of 7 years old. However, there were only two 475 dogs of 7 years old. So, the outcome is not very reliable because of the small sample size. 476 Though, these findings are in line with the findings of B. Bobic Gavrilovic et al. [11]. 477 Thomassen et al. [12] discourage dog owners to breed the bitch when bitches were > 6 years 478 old and had not whelped before. 479 480 4. Effect of the parity of the bitch 481 In the present study no association was found between parity and litter size. However, 482 Mutembei et al. [20] suggests that parity effects litter size, but not before the fifth parity. In 483 the present study the sample size of the fifth parity was too small. Also, B. Bobic Gavrilovic 484 et al. [11] found that parity effects litter size. In their study the number of pups increased 485 slightly until the third parity and then decreased. 17 486 5. Effect of different breeds 487 In the present study we chose to statistically analyze the four numerically larger breeds to 488 obtain an adequate number of dogs per breed: Golden retrievers, Labrador retrievers, 489 Dobermans and German shepherds. 490 Okkens et al. [10] examined the number of pups per litter for six different breeds, the 491 four breeds mentioned in this study plus Bernese mountain dogs and West Highland white 492 terriers. They found West Highland white terriers had significantly smaller litters than 493 Labrador retrievers (P < 0.001) and Dobermans (P < 0.005). They found no difference 494 between Dobermans and German Shepherds like in this study. A possible explanation is that 495 we had excess to considerably more cases than Okkens et al. 496 497 6. Effect of the weight of the bitch 498 Litter size is positively correlated with weight in the present study. In another study [12], 499 although all dogs were artificially inseminated, it was also found that larger breeds have 500 larger litter sizes than smaller breeds (small 3.9 ± 0.3, n = 50, P ≤ 0.01; medium 5.7 ± 0.3, n = 501 94; large 5.9 ± 0.2, n = 295; giant 6.1 ± 0.5, n = 62). According to Scantlebury, Butterwick 502 and Speakman [14] these results were expected because smaller mothers and their puppies 503 expend more mass-specific energy on their metabolism than larger breeds. Consequently, 504 smaller dogs have fewer resources for milk production for their puppies than larger breeds, 505 although they eat relatively more food, and their offspring are unable to convert as much 506 energy into growth as pups of larger breeds. So, the pups of smaller mothers have to take 507 relatively much more milk to grow. Summarized, because metabolism costs are relatively 508 smaller in larger breeds, larger litters are possible [14]. 509 510 7. Effect of the fertilization method 511 A comparison between results of different fertilization methods obtained with natural matings 512 and AI revealed that pregnancy rates were significantly different. The highest percentage was 513 for natural matings (85.1%), then AI with fresh semen (66.7%) and the lowest percentage for 514 frozen-thawed semen (27.8%). In 29 cases the breeder chose not to breed de bitch anymore. 515 The causes were often medical problems in the bitch or personal reasons of the owner. 516 Pregnancy rates of 85%-95% are shown after well controlled natural mating [21,22] which is 517 in agreement with the results of the present study. Linde-Forsberg and Forsberg [23] found 518 that inseminations with frozen semen resulted in a statistically lower pregnancy rate (51.1% n 519 = 468) than inseminations with fresh semen (62.3%, n = 59), which is in agreement with the 18 520 present study too. However, we found considerably lower pregnancy rates after insemination 521 with frozen semen than Linde-Forsberg and Forsberg [23]. Also Nizanski [15] found that the 522 pregnancy rate was reduced when frozen-thawed semen (60.7%) was used compared to fresh 523 semen (86.7%), both inseminated into the cranial vagina. Decreased pregnancy rates in 524 artificial inseminations are the result of reduced semen quality (especially in frozen-thawed 525 semen) [13,24] and the absence of pressure of the third fraction of the ejaculate through 526 which semen is influenced by the vaginal microenvironment [13]. Another explanation could 527 be that there are not as many and as powerful contractions of the uterus as after a natural 528 mating. In consequence, the semen is transported less rapidly to the distal region of the 529 uterine tubal junction [24]. Nevertheless, when inseminating semen of good quality with an 530 appropriate insemination technique during the fertilization phase, whelping rates can increase 531 to 80-87.5% for frozen-thawed semen [21,25]. Pretzer et al. found pregnancy rates of 89.4% 532 after 161 inseminations with frozen-thawed semen [22]. They used a single, timed TCI 533 procedure on only Greyhound bitches. Therefore, technique or breed may have had an impact 534 on the outcome of their study. 535 Furthermore, Linde-Forsberg and Forsberg [23] found litter size was 30.5% smaller in 536 bitches with frozen-thawed semen. Also other studies reported litters to be 25-30% smaller in 537 bitches that were inseminated with frozen-thawed semen compared to fresh semen [21,26]. 538 This effect also seems to appear in this study but the number of cases is too small for a 539 significant difference. Thus, in general, the results of natural matings are still better than AI, 540 although with good management pregnancy rates may increase. 541 542 7.1. Natural matings 543 In the present study was often unknown how many times a bitch was bred, because usually it 544 was not reported by the owners. Therefore, the influence of the number of matings was not 545 analyzed. One study [11] observed a significant smaller (0.52 pups, P < 0.05) mean litter size 546 at birth when bitches were mated only once compared to multiple mating. The number of 547 days between the first and the last mating did not affect the number of pups. 548 In matings a copulatory tie is important because a significant lower percentage of 549 pregnancies was observed among bitches that mated without a copulatory tie (71.4%, n = 28) 550 compared to matings including one (85.9%, n = 446). 551 552 553 19 554 7.2. Artificial insemination 555 Breeders can have different reasons for choosing Artificial Insemination. Some breeders want 556 AI to prevent the spread of sexual diseases, others use semen from stud dogs who live at a 557 distance or save semen from valuable dogs to use it in later generations [21,23]. 558 In the present study, the site of semen deposition was found not to have a significant 559 effect on pregnancy rates. However, others studies reported it influenced pregnancy/whelping 560 rates. In 2001 Thomassen et al. [25], studying 321 bitches of 70 different breeds inseminated 561 with frozen-thawed semen, found that whelping rates were significantly higher (P < 0.05) 562 after intrauterine insemination (71%) than after insemination into the cranial vagina (29%). In 563 2006 Thomassen et al. [12] artificially inseminated 526 bitches of 99 different breeds with 564 frozen-thawed semen. They observed a significantly higher pregnancy rate after insemination 565 into the uterus (75%) compared to intravaginal insemination (10%; P ≤ 0.05). Similarly, 566 Linde-Forsberg, Ström Holst and Govette [13], studying 327 AIs with frozen-thawed semen, 567 found that whelping rates were 84.4% for intrauterine insemination with the Norwegian 568 catheter and 58.9% for insemination into the cranial vagina (P < 0.001). The superior results 569 of intra-uterine insemination could be caused by sperm loss due to death of sperm in the 570 vagina and semen reflux after artificial insemination. Pregnancy rates could increase by 571 repeating the artificial insemination after 24-48 hours [21]. Unlike in the present study, 572 Linde-Forsberg, Ström Holst and Govette [13] observed the site of semen deposition 573 influenced litter size. They found litter size after intrauterine insemination with frozen semen 574 was 5.4 ± 3.0 and after intravaginal insemination 4.0 ± 2.7 (P< 0.001). The present study had 575 only a small sample size, making the outcome uncertain. 576 577 Conclusion 578 In conclusion, the results of this study suggest that age, fertilization method and the 579 occurrence of a copulatory tie affect pregnancy rates. Breed and weight of the bitch have an 580 effect on both pregnancy rates and litter size. If the veterinarians from the UKG would 581 register more information about the medical history from the bitches and if more breeders 582 would return a completed follow-up form about parturition and litter, there would be much 583 more information available concerning canine reproduction at UKG and many more factors 584 could be examined. 585 586 20 587 588 References 1. JOHNSTON S.D., ROOT KUSTRITZ M.V., OLSON P.N.S. The canine estrous 589 cycle. In: JOHNSTON S.D., ROOT KUSTRITZ M.V., OLSON P.N.S. Canine and 590 feline theriogenology. Philadelphia: Saunders 2001. p. 16-31. 591 592 593 2. CONCANNON P.W. Reproductive cycles of the domestic bitch. Anim Reprod Sci 2010;4231. 594 595 3. WILDT D.E., CHAKRABORTY P.K. Relationship of reproductive behaviour, serum 596 luteinizing hormone and time of ovulation in the bitch. Biol reprod 1978;18:561-570. 597 598 599 4. CONCANNON P.W., HANSEL W. and VISEK W.J. The ovarian cycle of the bitch: plasma estrogen, LH and progesterone. 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OKKENS A.C., TEUNISSEN J.M., OSCH van W., BROM van den W.E., 620 DIELEMAN S.J. and KOOISTRA H.S. Influence of litter size and breed on the 621 duration of gestation in dogs. J Reprod Fertil 2001;57:193-197. 622 623 11. BOBIC GAVRILOVIC B., ANDERSSON K., LINDE FORSBERG C. Reproductive 624 patterns in the domestic dog - A retrospective study of the Drever breed. 625 Theriogenology 2008;70:783-794. 626 627 12. THOMASSEN R., SANSON G., KROGENAES A. et al. Artificial insemination with 628 frozen semen in dogs: A retrospective study of 10 years using a non-surgical 629 approach. Theriogenology 2006;66:1645-1650. 630 631 13. LINDE-FORSBERG C., STRÖM HOLST B., GOVETTE G. Comparison of fertility 632 data from vaginal vs intrauterine insemination of frozen-thawed dog semen: a 633 retrospective study. Theriogenology 1999;52:11-23. 634 635 14. SCANTLEBURY M., BUTTERWICK R., SPEAKMAN J.R. Energetics and litter 636 size variation in domestic dog Canis familiaris breeds of two sizes. 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MUTEMBEI H.M., MUTIGA E.R., TSUMA V.T. An epidemiological survey 659 demonstrating decline in reproductive efficiency with age and non-seasonality of 660 reproductive parameters in German shepherd bitches in Kenya. J S Afr Vet Assoc 661 2002;73:36-37. 662 663 664 21. LINDE-FORSBERG C. Canine artificial insemination: State of the Art. The European Veterinary Society for Small Animal Reproduction 7th Congress 2010:21-25. 665 666 22. PRETZER S.D., LILLICH R.K., ALTHOUSE G.C., Single, transcervical 667 insemination using frozen-thawed semen in the Greyhound: A case series study. 668 Theriogenology 2006;65:1029-1036 669 670 671 23. LINDE-FORSBERG C., FORSBERG M. Results of 527 controlled artificial inseminations of dogs. J Reprod Fertil Suppl. 1993;47:313-323. 672 673 24. ROTA A., MILANI C., ROMAGNOLI S., ZUCCHINI P., MOLLO A. Pregnancy 674 and conception rate after two intravaginal inseminations with dog semen frozen either 675 with 5% glycerol or 5% ethylene glycol. 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Vet Rec 1989;125:399. 683 684 23 Group 1 Sheepdogs Sheepdogs and cattledogs except Swiss Cattle Dogs Australian Kelpie Australian Shepherd Dog Bearded Collie Beauceron Belgian Shepherd Dog, Malinois Belgian Shepherd Dog, Tervueren Berger Picard Border Collie Briard Cão da Serra de Aires Collie Rough Dutch Schapendoes Dutch Shepherd Dog, Rough-haired German Shepherd Dog Gos d'Atura Català Komondor Kuvasz Maremma and Abruzzes Sheepdog Old English Sheepdog Australia Ratio: NL'03-'06 / cases '03-'10 Percent of dogs in Holland Dogs in Holland '03-'06 Percent of different dogs at UKG Number of different dogs '03-'10 Cases '03'10 Country of origin Breed Type Section Appendix Supplement Table A Group number 685 1 1 0,1 186 0,1 0,64 2 12 1 2 7 1 0,3 1,0 0,1 468 983 238 0,2 0,5 0,1 0,80 0,48 0,81 Belgium 1 1 0,1 2675 1,3 9,14 Belgium France Great Britain France 3 2 4 5 2 1 2 5 0,3 0,1 0,3 0,7 1362 42 3644 748 0,7 0,0 1,8 0,4 2,33 0,14 6,22 0,51 Portugal Great Britain The Netherlands 1 11 9 1 11 8 0,1 1,6 1,2 18 1651 1483 0,0 0,8 0,7 0,06 0,51 0,63 The Netherlands 2 2 0,3 180 0,1 0,31 53 2 1 4 37 2 1 2 5,4 0,3 0,1 0,3 14070 143 11 123 7,1 0,1 0,0 0,1 1,30 0,24 0,04 0,21 Italy 1 1 0,1 44 0,0 0,15 Great Britain 3 3 0,4 363 0,2 0,41 U.S.A. Great Britain France Germany Spain Hungary Hungary Saarloos Wolfdog Shetland Sheepdog Tatra Shepherd Dog Welsh Corgi Cardigan Australian Cattle Dog Cattle dogs except Swiss Cattle Dogs Pinscher and Group 2 Schnauzer type Pinschers and Schnauzers, Mollossoid breeds, Swiss Mountain and Cattle Dogs The Netherlands Great Britain Poland Pinscher Smoushond Mastiff type 0,16 0,46 Ratio: NL'03-'06 / cases '03-'10 0,2 0,1 Percent of dogs in Holland 372 134 Dogs in Holland '03-'06 1,2 0,1 Percent of different dogs at UKG 8 1 Number of different dogs '03-'10 Cases '03-'10 Country of origin 8 1 10 6 2 7 6 2 1,0 0,9 0,3 331 1815 156 0,2 0,9 0,1 0,16 1,03 0,27 Great Britain 1 1 0,1 335 0,2 1,14 Australia 4 2 0,3 79 0,0 0,13 4 154 4 121 0,6 17,8 3401 35055 1,7 17,6 2,90 0,99 58 33 4,8 1086 0,5 0,11 2 2 4 5 4 3 2 2 2 3 3 3 0,3 0,3 0,3 0,4 0,4 0,4 184 269 2116 394 659 397 0,1 0,1 1,1 0,2 0,3 0,2 0,31 0,46 3,61 0,45 0,75 0,45 10 1 10 12 36 7 1 7 9 19 1,0 0,1 1,0 1,3 2,8 1983 9 3894 1761 5406 1,0 0,0 2,0 0,9 2,7 0,97 0,03 1,90 0,67 0,97 Bouvier des Flandres Belgium/France Subtotal Schnauzer Molossoid breeds Poland France Breed Type Section Group number Polish Lowland Sheepdog Pyrenean Sheepdog Dobermann Germany German Pinscher Miniature Pinscher Miniature Schnauzer Riesenschnauzer Schnauzer Dutch Smoushond Germany Germany Germany Germany Germany The Netherlands Bordeaux Dog Broholmer Bulldog Bullmastiff German Boxer France Denmark Great Britain Great Britain Germany 25 Mountain type Swiss Mountain and Cattle Dogs Group 3 Terriërs Large and sized TerriërsMedium Small sized Terriërs Anatolian Shepherd Dog Cao da Serra da Estrela Hovawart Landseer Leonberger Newfoundland Saint Bernard Dog, Long-haired 5,71 2,54 0,73 Ratio: NL'03-'06 / cases '03-'10 0,8 0,7 0,9 Percent of dogs in Holland 1671 1488 1712 Dogs in Holland '03-'06 0,1 0,3 1,2 Percent of different dogs at UKG 1 2 8 Number of different dogs '03-'10 Cases '03-'10 1 3 11 Country of origin Italy Germany China Breed Type Section Group number Italian Corso Dog Rottweiler Shar Pei Anatolia (Turkey) 3 3 0,4 85 0,0 0,10 Portugal Germany Germany/Switzerl Germany Canada 2 4 14 18 27 1 3 9 12 18 0,1 0,4 1,3 1,8 2,6 42 525 221 1127 2088 0,0 0,3 0,1 0,6 1,0 0,14 0,60 0,08 0,32 0,40 Switzerland 5 4 0,6 1098 0,6 0,94 Appenzell Cattle Dog Switzerland Bernese Mountain Dog Switzerland Entlebuch Cattle Dog Switzerland Subtotal 1 1 0,1 433 0,2 1,48 16 3 255 13 2 168 1,9 0,3 24,7 7404 308 36360 3,7 0,2 18,2 1,95 0,53 0,74 14 1 8 1 1,2 0,1 1079 1594 0,5 0,8 0,46 5,44 1 1 0,1 164 0,1 0,56 Airedale Terriër Border Terriër Irish Glen of Imaal Terriër Irish Soft Coated Wheaten Terriër Parson Russel Terriër Great Britain Great Britain Ireland Great Britain 20 2 8 1 1,2 0,1 692 982 0,3 0,5 0,30 3,35 Cairn Terriër Jack Russel Terriër Great Britain Australian 2 1 2 1 0,3 0,1 2638 2337 1,3 1,2 4,50 7,98 Ireland 26 Bull type Terriërs American Staffordshire Terriër Bull Terriër, Standard Bull Terriër, miniature Staffordhire Bullterriër Group 5 Nordic Sledge Dogs Spitz and primitive types Nordic Watchdogs and Sheepdogs Asian Spitz and related breeds Primitive types 9 7 1,0 2688 1,3 1,31 Ratio: NL'03-'06 / cases '03-'10 0,63 Percent of dogs in Holland 0,2 Dogs in Holland '03-'06 367 Percent of different dogs at UKG 0,3 Number of different dogs '03-'10 2 Cases '03-'10 2 U.S.A. 1 1 0,1 951 0,5 3,25 Great Britain 7 5 0,7 805 0,4 0,55 Great Britain 1 1 0,1 204 0,1 0,70 Great Britain Subtotal 11 72 10 48 1,5 7,0 4160 18661 2,1 9,4 1,42 1,33 Germany Subtotal 3 3 3 3 0,4 0,4 2767 2767 1,4 1,4 3,15 3,15 Alaskan Malamute U.S.A. 1 1 0,1 269 0,1 0,92 Icelandic Sheepdog Swedish Vallhund Iceland Sweden 2 1 2 1 0,3 0,1 287 62 0,1 0,0 0,49 0,21 Akita Chow Chow Shiba Basenji Mexican Hairless Dog Pharaoh Hound Japan China Japan Central Africa 1 1 5 1 1 1 4 1 0,1 0,1 0,6 0,1 235 530 545 128 0,1 0,3 0,3 0,1 0,80 1,81 0,47 0,44 3 1 16 2 1 14 0,3 0,1 2,1 21 43 2120 0,0 0,0 1,1 0,04 0,15 0,52 Dachshund, Standard, Wirehaired Group 4 Dachshunds Country of origin Breed Type Section Group number Norwich Terriër Great Britain West Highland White Terriër Great Britain Mexico Malta Subtotal 27 Small sized Related breeds Group 7 Continental Pointing dog Continental pointing dog Pointing dogs Spaniel type Griffon type Setter Artesian-Norman Basset Basset Hound Beagle Fawn Brittany Basset Petit Basset Griffon Vendeen Dalmatian Rhodesian Ridgeback German Short-haired Pointing Dog Hungarian Shorthaired Pointing Dog Weimaraner, Shorthaired Drentse Partridge Dog Epagneul Breton Frisian Pointing Dog/Stabyhoun German Long-haired Pointing Dog Large Munsterlander Small Munsterlander Ceský Fousek Irish Red Setter France Great Britain Great Britain France 0,02 Ratio: NL'03-'06 / cases '03-'10 0,0 Percent of dogs in Holland 6 Dogs in Holland '03-'06 0,1 Percent of different dogs at UKG 1 Number of different dogs '03-'10 1 Cases '03-'10 France Country of origin Type Section Scenthounds and related breeds Griffon bleu de Gascogne Breed Medium sized Scenthounds Group number Group 6 1 1 4 1 1 1 4 1 0,1 0,1 0,6 0,1 395 649 1994 560 0,2 0,3 1,0 0,3 1,35 2,22 1,70 1,91 1 4 2 15 1 4 2 15 0,1 0,6 0,3 2,2 339 634 2575 7152 0,2 0,3 1,3 3,6 1,16 0,54 4,40 1,63 Germany 4 2 0,3 877 0,4 1,50 Hungary 5 5 0,7 855 0,4 0,58 Germany 27 14 2,1 909 0,5 0,22 The Netherlands France 31 1 21 1 3,1 0,1 2014 81 1,0 0,0 0,33 0,28 The Netherlands 4 4 0,6 1586 0,8 1,35 Germany Germany Germany Czech Republic Ireland Subtotal 3 1 12 2 2 92 3 1 6 2 2 61 0,4 0,1 0,9 0,3 0,3 9,0 1384 255 909 98 952 9920 0,7 0,1 0,5 0,0 0,5 5,0 1,58 0,87 0,52 0,17 1,63 0,56 France Croatia Southern Africa Subtotal 28 Flushing dogs Water dogs Group 9 Companion and Toy dogs Bichons and Related breeds Poodle Tibetan breeds Bichons Coton de Tuléar Flat Coated Retriever Golden Retriever Labrador Retriever Nova Scotia Duck Tolling Retriever English Cocker Spaniel English Springer Spaniel Field Spaniel Dutch Kooikerhondje Welsh Springer Spaniel Barbet Wetterhoun Great Britain Great Britain Great Britain Maltese Coton de Tuléar Large Poodle Standard Poodle Miniature Poodle Toy Poodle Shih Tzu Tibetan Terriër 0,22 Ratio: NL'03-'06 / cases '03-'10 0,0 Percent of dogs in Holland 63 Dogs in Holland '03-'06 0,1 Percent of different dogs at UKG 1 Number of different dogs '03-'10 1 Country of origin Breed Type Section Retrievers, Flushing dogs and Water dogs U.S.A. Cases '03-'10 Chesapeake Bay Retriever Retrievers Group number Group 8 2 140 127 2 85 73 0,3 12,5 10,7 2845 9390 18825 1,4 4,7 9,4 4,86 0,38 0,88 5 4 0,6 1062 0,5 0,91 12 8 1,2 3338 1,7 1,42 Great Britain Great Britain The Netherlands 1 1 1 1 1 1 0,1 0,1 0,1 1009 59 1960 0,5 0,0 1,0 3,45 0,20 6,69 Great Britain France The Netherlands Subtotal 4 1 1 296 3 1 1 181 0,4 0,1 0,1 26,6 729 16 432 39728 0,4 0,0 0,2 19,9 0,83 0,05 1,48 0,75 Italy 3 3 0,4 980 0,5 1,12 Madagascar France France France France Tibet Tibet 1 5 6 1 2 1 1 1 4 5 1 2 1 1 0,1 0,6 0,7 0,1 0,3 0,1 0,1 339 210 656 552 482 1307 834 0,2 0,1 0,3 0,3 0,2 0,7 0,4 1,16 0,18 0,45 1,89 0,82 4,46 2,85 Canada Great Britain 29 Group 10 Sighthounds Long-haired or Fringed Sighthounds Rough-haired Sighthounds Short-haired Sighthounds Others 8,16 Ratio: NL'03-'06 / cases '03-'10 1,2 Percent of dogs in Holland 2389 Dogs in Holland '03-'06 0,1 Percent of different dogs at UKG 1 Number of different dogs '03-'10 1 Country of origin Breed Type Section Group number English Toy Spaniels Chin and Pekingese Small Molossian type dogs Mexico Cases '03-'10 Chihuahueño Longhaired Chihuahueño Cavalier King Charles Spaniel Great Britain 4 3 0,4 4883 2,4 5,56 Pekingese China 1 1 0,1 57 0,0 0,19 French Bulldog Pug France Great Britain Subtotal 18 2 48 14 2 39 2,1 0,3 5,7 2872 956 16517 1,4 0,5 8,3 0,70 1,63 1,45 Saluki Middle East 14 9 1,3 154 0,1 0,06 Deerhound Irish Wolfhound Great Britain Ireland 1 2 1 2 0,1 0,3 128 390 0,1 0,2 0,44 0,67 Greyhound Whippet Great Britain Great Britain Subtotal The Netherlands 1 1 19 1 1 1 14 1 0,1 0,1 2,1 0,1 245 802 1719 72 0,1 0,4 0,9 0,0 0,84 2,74 0,42 0,25 Germany 4 22 4 12 0,6 1,8 0,0 2,5 ? Markiesje White Shepherd Dog (not F.C.I.) Crossbreeds Other breeds Subtotal Totaal 27 997 17 681 29338 29410 199409 0,0 14,7 14,7 0,00 0,00 5,91 1.46 686 687 30 688 Part two: Customers satisfaction survey 689 690 Abstract 691 The opinion of dog owners concerning the ovulation timing service at the department of 692 clinical sciences of companion animals at Utrecht University (UKG) was examined by an 693 online survey. All clients from the Netherlands (n = 386), who made use of the ovulation 694 timing service between 2003 and 2010, were invited to fill in the questionnaire. The overall 695 response rate was 22.7%, so 95 breeders completed the 22-question survey. The main reason 696 to keep the bitch was companionship for 57% of the respondents, 32.6% work, 5.8% show 697 and 4.7% sport. Propositions were rated on a scale of one to five. Veterinarians were 698 evaluated to be capable for examination (mean = 4.6) and the oral information given by them 699 was understandable (mean = 4.4). Co-assistants handled the dogs in a responsible way (mean 700 = 4.2) and in case of a failure the veterinarian intervened in time (mean = 4.2). Least 701 satisfied, but still sufficient, were people about the waiting time (mean = 3.8) and 702 reasonableness of the costs (mean = 3.6). Dog owners, who had been to UKG for ovulation 703 timing more than 5 times, were less satisfied about the costs than people who used this 704 service infrequently. 60% of the respondents indicated that they would like to receive 705 additional information about topics like important aspects of pregnancy and parturition in 706 bitches. 68.4% of the breeders would like additional veterinary help with topics as genetic 707 screening for hereditary diseases, problems surrounding birth and problems after birth. 708 In general, the ovulation timing service was rated with a median of 8.0 (range 1-10, n = 95) 709 on a scale of 1 to 10. 710 711 Introduction 712 When a company provides a particular service, it is important that clients are satisfied 713 because satisfaction is connected to customer loyalty, which in turn is related to profitability 714 [1,2]. One definition of customer loyalty is behavioral loyalty, which means customers return 715 to purchase services from the same supplier [3]. The department of clinical sciences of 716 companion animals at Utrecht University (UKG) is a veterinary referral clinic that offers a 717 range of services including ovulation timing. To maintain high customer satisfaction, it is 718 necessary to ask opinions from pet owners about various aspects of these services. 719 720 According to a few publications [4,5,6], communication skills are becoming more important 721 in the veterinary practice because good communication improves medical outcomes [4,6] and 722 clients expect their veterinarian to inform and educate them and listen to their concerns [4]. 723 However, client relations are considered to be one of the hardest parts of the veterinary 724 profession [5]. The most common communicating breakdowns in the study of Coe, Adams 725 and Bonnett [4] were because of misinformation about the costs, procedures, diagnosis and 726 prognosis. Furthermore, the second most common consequence of breakdowns in 727 communication was veterinarians who do not always give all the options and did not give 728 owners the opportunity to choose. The third most common result was that veterinarians did 729 not listen to the pet owners concerns. Fortunately, communication skills can be taught as all 730 the other medical skills [6]. 731 732 The aim of the ovulation timing service is to improve pregnancy outcomes. This is achieved 733 by helping people to find the optimal day for mating in healthy bitches and in bitches with 734 fertility problems, and also to manage artificial inseminations. More specifically, the optimal 735 day for mating is determined by longitudinal physical examinations and measurements of the 736 plasma progesterone concentration. Later, pregnancy is determined by palpation, followed by 737 abdominal ultrasonography if necessary. This process is carried out by veterinary students, 738 supervised by a veterinarian, who is specialized in companion animal reproduction. 739 740 Utrecht University is not the only veterinary clinic in the Netherlands that offers an ovulation 741 timing service which ensures there is competition. Furthermore, the number of patients 742 reduced between 2003 and 2008 (Part one: Retrospective study on the period 2003-2010). 743 Therefore, it is important to identify the views of clients so the service can be tailored to their 744 requirements. Finally, the intention is that dog owners will return to UKG, so the number of 745 dogs presented for ovulation timing will increase again. 746 747 The aim of this study is to examine the opinion of dog owners concerning the ovulation 748 timing service at UKG by means of an online questionnaire to maintain high customers 749 satisfaction. 750 751 752 753 32 754 Materials and Methods 755 1. Participants 756 All clients (total of 386) from the Netherlands, who made use of the ovulation timing service 757 between January 2003 and August 2010, were invited to fill in the questionnaire. Only the 758 Dutch clients were invited because the questionnaire was in Dutch, so the clients from abroad 759 (n = 17) did not receive an invitation. 760 761 2. Questionnaire 762 In October, there were sent 419 letters to dog owners. 34 of those letters were sent to 763 K.N.G.F., so they could distribute the invitations to the host families where their breeding 764 bitches live. To encourage people to participate in the survey, there was a prize, namely a 765 ‘free ovulation timing’. To be eligible for the prize, participants had to fill in personal details. 766 The survey was open for about a month, from the end of October 2010 till the end of 767 November 2010. After closing the survey, the winner of the ‘free ovulation timing’ was 768 decided by a random number generator. 769 The questionnaire was put online using an online software program called 770 SurveyMonkey. All dog owners received a letter with a web link and a code that provided 771 them access to the online questionnaire once. There they could give their opinion in the 22- 772 question survey (supplement 1). The questionnaire contained 5 open-ended, 2 yes/no and 6 773 multiple choice questions. There were also 9 propositions were people had to indicate their 774 level of satisfaction on a scale of 1 to 5. 775 776 3. Statistical analysis 777 After the survey was closed the results were imported in Excel. The data were exported to 778 and analyzed with SPSS 17.0. 779 The results of the propositions of the different groups (owners who presented dogs for 780 ovulation timing at UKG ≤ 5 times, owners who presented dogs for ovulation timing at UKG 781 > 5 times) are compared with one-way ANOVA and are presented as percentages and mean. 782 The results were considered to be statistically significant when P ≤ 0.05. 783 784 Results 785 Eventually, the survey was completed 95 times, representing 21.8% (n = 436) of all breeders 786 who came to UKG for ovulation timing service between January 2003 and August 2010. 76 33 787 of the 95 participants (80%) left their personal information for winning the prize and the 788 remaining 19 wanted to be anonymous. The personal data showed that 75 participants were 789 from the Netherlands and only one was from Belgium, due to a recent move. 790 791 1. Main purpose for keeping the dog 792 The main reason for keeping dogs varied by owner (n = 86). Most owners kept their dog for 793 companionship (57%) and 32.6% indicated that the dog was intended primarily for work 794 (table 1a). Of the dogs which are kept for work (n = 28), most were kept as hunting dogs and 795 guide dogs (table 1b). 796 797 Frequency Percent Frequency Percent Companionship 49 57.0 Guide dog 17 60.7 Show 5 5.8 Herding 1 3.6 Sport 4 4.7 Hunting 9 32.1 Work 28 32.6 Police dog 1 3.6 Table 2a: Main purpose for keeping the dog Table 1b: Subgroups of working dogs 798 799 2. Propositions 800 There were 9 propositions where people were asked to indicate to what extent they agreed by 801 a scale of 1 to 5 (table 2). From all propositions, people were most satisfied with the skills of 802 the veterinarians. They thought the vets were capable for examination (mean = 4.6) and the 803 oral information was understandable (mean = 4.4). The participants were also content with 804 the way co-assistants behave. They thought the co-assistants were handling their dogs in a 805 responsible way (mean = 4.2) and when something went wrong or failed, the veterinarian 806 intervened in time (mean = 4.2). Least satisfied, but still sufficient, people were about the 807 waiting time (mean = 3.8) and reasonableness of the costs (mean =3.6). 808 To compare the opinions of people who infrequently visit the UKG for ovulation timing and 809 people who come more frequently, a distinction was made between owners who have been to 810 UKG 5 times or less and owners who have been to UKG more than 5 times during the studied 811 period. It appeared that no differences exist between the results of the propositions, except the 812 costs (P ≤ 0.05). Dog owners, who had been to UKG for ovulation timing more than 5 times, 813 were less satisfied about the costs than people who used this service infrequently. 814 815 34 Often enough time for consultation without Totally Somewhat Neutral Somewhat Totally Mean disagree disagree =3 agree = 4 agree Mark =1 =2 3 (3.3%) 14 14 12 49 (15.2%) (15.2%) (13.0%) (53.3%) 10 18 19 43 (11.0%) (19.8%) (20.9%) (47.3%) appointment (n = 92) Vet accessible fast enough in case of 1 (1.1%) emergency (n = 91) 816 =5 4.0 4.0 Vet is capable for examination 3 1 8 5 77 4.6 (n = 94) (3.2%) (1.1%) (8.5%) (5.3%) (81.9%) Oral information given by the vet is 7 0 7 6 64 understandable (n = 84) (8.3%) (0.0%) (8.3%) (7.1%) (76.2%) Co-assistants examine in a responsible way 3 6 11 22 52 (n = 94) (3.2%) (6.4%) (11.7%) (23.4%) (55.3%) If a co-assistant acts incorrectly, the vet 4 7 11 10 56 intervenes fast enough (n = 88) (4.5%) (8.0%) (12.5%) (11.4) (63.6) Costs are reasonable (n = 84) 8 7 19 25 25 (9.5%) (8.3%) (22.6%) (29.8%) (29.8%) Waiting time for open consultations is 6 6 19 32 28 acceptable (n = 91) (6.6%) (6.6%) (20.9%) (35.2%) (30.8%) The website is a good resource (n = 44) 3 4 14 11 12 (6.8%) (9.1%) (31.8%) (25.0%) (27.3%) 4.4 4.2 4.2 3.6 3.8 3.6 Table 3: To what extent do people agree with these 9 propositions? 817 818 3. Written information 819 40 percent of all participants (n = 95) indicated that they did not need any written information 820 (Table 3). However, 60 percent indicated additional information about one or more topics 821 would be advisable (table 3). Especially information about important aspects of pregnancy 822 and parturition in bitches would be welcomed by many dog owners. 823 Frequency Percent No written information needed 38 40 Important aspects of pregnancy in bitches 36 37.9 What is pregnancy diagnosis about? 16 16.8 Food is important during the period of gestation and lactation 22 23.2 Important aspects of parturition 35 36.8 How to take care of the bitch and puppies after birth? 20 21.1 Other topics 8 8.4 Table 4: About what topics would dog owners want to know more? 35 824 4. Additional help 825 Most dog owners (68.4%) would like additional veterinary help with one or more topics as 826 shown in table 4. Often participants mentioned genetic screening for hereditary diseases 827 (46.3%), management if problems arise surrounding birth (25.3%) and/or after birth (32.6%), 828 in addition to ovulation timing. 31.6% of the owners did not need any additional information 829 from veterinarians apart from ovulation timing. 830 831 832 Frequency Percent No help needed 30 31.6 Selecting material for breeding (for example selecting the right male dog) 8 8.4 Genetic screening for hereditary diseases 44 46.3 Close management if problems surrounding birth 24 25.3 Management if problems with bitch/puppies after birth 31 32.6 Other fields 5 5.3 Table 5: In what other areas, besides ovulation timing, would dog breeders like to obtain additional information? 833 834 5. General evaluation 835 In general, the ovulation timing service was rated with a median of 8.0 (range 1-10, n = 95) 836 on a scale of 1 to 10. Participants supposed to be satisfied when they gave 6-10 and 837 unsatisfied when they gave 1-5. Only a few participants (n = 5, 5.4%) indicated to be 838 unsatisfied. Three of them had filed complaints. Furthermore, two clients filed a complaint 839 and nevertheless indicated to be satisfied in the general evaluation. 840 841 Discussion 842 The results of the present study show that most people kept their dog for companionship or 843 working dog. The high percentages of working dogs are mostly attributable to a high 844 percentage of guide dogs because of a partnership with K.N.G.F. 845 Nine propositions were rated with the highest rate for the competence of the 846 veterinarians of UKG. However, Coe, Adams and Bonnett [4] found that pet owners and 847 veterinarians both feel that it is difficult for pet owners to evaluate the competence of 848 veterinarians accurately. In this survey, the participants also indicated that the oral 849 information given by the veterinarian was understandable. The information given must be 850 adapted to each client according to another study [4]. Furthermore, 90% of the breeders felt 36 851 that co-assistants behaved responsible during examination and that the veterinarian 852 intervened in time. When looking at the number of open access consultations per week, most 853 breeders thought it was often enough. According to the participants the waiting time was 854 acceptable but unpredictable and sometimes too long. For the reasonableness of the costs a 855 3.6 is given by the participants. Some think the prices are too high for the offered service, 856 mainly because other practices charge lower prices. There were no significant differences in 857 opinion seen between people who used ovulation timing service ≤ 5 times and people who 858 used it more frequently during the studied period, except for the costs. These differences 859 could be due to the reason for breeding. 860 60% of the respondents indicated that they would like to receive additional 861 information about topics like important aspects of pregnancy and parturition in bitches. This 862 could be in the form of handouts, pamphlets or information packets [4]. 68.4% of the people 863 would like to see the UKG helping them in other fields than only ovulation timing. Especially 864 genetic screening for hereditary diseases was mentioned often (46.3%). 865 866 In general, the ovulation timing service was rated with a median of 8.0 (range 1-10, n = 95) on a scale of 1 to 10. 867 868 1. Main purpose for keeping the dog 869 More than half of the people indicated that they kept their dog for companionship and a third 870 of the dogs functioned as a working dog. This high percentage of working dogs is mostly 871 attributable to a high percentage of guide dogs because of a partnership with K.N.G.F. (Royal 872 Dutch Guide-dog Foundation). This foundation selects suitable parent dogs to breed puppies 873 meant to enroll the guide dog training program if mentally and physically fit. Those parent 874 dogs stay with a host family, who are taking the dogs to ovulation timing. 19.8% of the 875 participants of this questionnaire were host families while the percentage of guide dogs 876 presented for ovulation timing was only 10.2% of the dogs (n = 560). It is not statistically 877 proven, but it seems that host families are overrepresented in the survey. This might be 878 explained by volunteers making the choice to keep a dog of the K.N.G.F. for this particular 879 purpose because they think it is important to help blind people. Therefore, these people are 880 often very involved in the process. That might be the cause of the relative overrepresentation 881 of those volunteers completing our questionnaire. 882 883 884 37 885 2. Propositions 886 There are no significant differences in opinion seen between people who used ovulation 887 timing service ≤ 5 times and people who used it more frequently during the studied period, 888 except for the costs. Breeders who made use of ovulation timing ≤ 5 times are more satisfied 889 with the costs than breeders who made use of it more than 5 times. It might be that some of 890 the participants, that made use of ovulation timing service ≤ 5 times, bred dogs just for fun. 891 Those people might think good guidance by UKG is more important and profit is less 892 important. Therefore, when the veterinarian costs are somewhat higher, that is not such a 893 problem. On the other hand, among breeders who bred dogs more than five times might be 894 owners who bred their bitches also for profit. For those people it is important that the 895 veterinarian costs are not too high. 896 After rating the various propositions, the participants of the survey had the 897 opportunity to explain their answers. Dog owners were very positive about the veterinarians. 898 Emotional interest and patience of the veterinarians with the dog and dog owner was noted by 899 breeders. In the survey the competence of veterinarians received a high rating (4.6). 900 However, Coe, Adams and Bonnett [4] found that pet owners and veterinarians both feel that 901 it is difficult for pet owners to evaluate the competence of veterinarians accurately. Namely, 902 the way of speaking and the ability of communication can strongly influence the opinion of 903 breeders. In the present survey, the participants also indicated that they understood the oral 904 information given by the veterinarian. Another study [4] reported that each client expected a 905 different level and amount of information and jargon was a possible barrier for transferring 906 information. Therefore, it is important to estimate what level of information is needed to 907 satisfy every breeder. 908 Furthermore, more people were positive about co-assistants than expected. About 909 10% disagree that the co-assistants were responsible during examination so 90% is neutral or 910 positive. People thought the students were emotionally very interested and concerned about 911 the dogs and most owners understood co-assistants were students who were in a learning 912 situation. When participants were negative, it is mainly because there were too much students 913 in the examination room and sometimes every student had to examine the dog. The owners 914 thought that was too stressful for their pet. Another problem was students practicing skills 915 like taking blood samples. Three owners stated that students can try once or twice and when 916 they fail a professional has to take over. This is also reflected in another proposition about the 917 vet intervening when a student acts incorrectly. One of the positive reactions is that the 918 veterinarian gave the student enough space to examine and there was a clear explanation 38 919 about the acts of the vet or student. Three of the participants indicated that examinations 920 without supervision were a negative experience. Sometimes co-assistants were incompetent 921 and then there was nobody to help. This might result in the bitches being more stressed than 922 necessary. According to those owners, co-assistants should have freedom to practice but there 923 must be supervision and the supervisor must intervene in time. 924 When looking at the number of open access consultations per week, most breeders 925 thought it was often enough. Seven of the participants stated the new opening hours (9.30- 926 10.00 am) are better because they have to travel a great distance and two preferred the old 927 opening hours because of the traffic in the morning. Furthermore, two participants mentioned 928 opening hours only on Monday, Wednesday and Friday are not enough because they have to 929 work themselves and they want to come whenever it suits them. According to participants the 930 waiting time was acceptable but there were also some negative experiences. Some people felt 931 waiting time was unpredictable (n = 2) and sometimes it was just too long (n =7). Three 932 people thought consultations by appointment would be a solution and five already made use 933 of appointments. 934 For the reasonableness of the costs a 3.6 is given by the participants. Some think the 935 prices are too high for the offered service, mainly because other practices charge lower 936 prices. Other dog owners feel that they were well supported and that the prices are very 937 reasonable. Other studies [4,7] reported that veterinarians had a feeling of unease about 938 discussing the costs with their clients after experiences when they felt undervalued or guilty. 939 This was not examined in the present study. 940 941 3. Written information 942 The participants who indicated that they need no further information were mainly breeders 943 who bred their bitch more than one time or volunteers of K.N.G.F. Those breeders had 944 experiences so they felt they need no additional information in these areas. Additionally, the 945 K.N.G.F.-volunteers did not feel that they need further information because the foundation 946 ensures that all host families have enough information available. Furthermore, during all 947 parturitions a well trained K.N.G.F. staff member is present to assist. 948 Dog owners who would like to receive some extra information mostly named 949 pregnancy and parturition as topics of interest. Probably this is caused by the inexperience of 950 some who do not know what to expect and who find it hard to discern normal from abnormal. 951 Some of the participants also mentioned other topics they would like to learn more about. It is 952 mentioned several times (n = 3) that people want to know when there is an emergency during 39 953 pregnancy or parturition and intervention is required. Also some information about handling 954 pups, when the bitch does not behave properly or dies, would be appreciated (n = 2). 955 Similarly, in a focus group study of 24 companion animal veterinarians and 32 pet 956 owners [4], they found that owners expected additional written information in the form of 957 handouts, pamphlets or information packets. In the report of Coe, Adams and Bonnett pet 958 owners indicated that they would like information about their pet’s disease, the cost of 959 medical care, possibility of insurance and its coverage, and contact information in case of 960 emergency [4]. On the other hand, other owners felt it was their responsibility to educate 961 themselves and not that of the veterinarian [4]. 962 Coe, Adams and Bonnett [4] found that clients obtain incorrect information from 963 other sources than a veterinarian, for instance internet, other breeders or pet stores. Pet 964 owners had great confidence in those other information sources. One veterinarian stated that 965 once breeders had incorrect information, then they believe that rather than new information 966 given by the veterinarian. Perhaps this problem can be partially solved by providing the 967 correct information from the veterinary practice. 968 969 4. Additional help 970 68.4% of the people would like to see the UKG helping them in other fields than only 971 ovulation timing. Especially genetic screening for hereditary diseases was mentioned often 972 (46.3%), probably because most bitches were pure-bred in our study and many breeds suffer 973 from genetic diseases. Dog owners want to avoid transmission of hereditary diseases by the 974 parent dogs to the puppies. Consequently, they want the parent dogs to be genetically 975 screened. 976 In addition, (inexperienced) breeders often are uncertain when abnormal situations 977 occur during or after birth. They want more support in those situations to support their 978 actions. 979 980 5. General evaluation 981 After a general rating the participants had the possibility to explain their opinion in open 982 boxes, one for positive experiences and one for negative experiences with the ovulation 983 timing service. The dog owners were often positive about the same themes. For example the 984 veterinarians are experts (n = 9) and they treat patients and breeders kindly (n = 10) and with 985 patience (n = 11). The veterinarians also take their time to listen (n = 5) and they explain 40 986 everything in full detail (n = 7). Other reports [4,5] showed that pet owners feel listening and 987 involvement in the pets’ care are very important for a positive experience. 988 The negative box was filled particularly with complaints about excessive waiting 989 periods (n = 7). Three participants think this might be solved with consultation by 990 appointment. Furthermore, five dog owners indicated that they want more openness and 991 explanation about test results (blood tests). Some of the veterinarians already give this 992 information, others do not. There were also tips on supervising co-assistants. One of those 993 was not to discuss failures in presence of the owner because this is uncomfortable for all 994 parties. Two participants indicated that co-assistants have to prepare better so they would not 995 keep repeating the same questions. Finally, some dog owners demand for exploratory 996 facilities to guide them through the process of pregnancy and parturition in bitches. 997 998 Conclusion 999 In conclusion, the results of our study demonstrate that dog owners feel that the veterinarians 1000 at UKG are capable for examination and the oral information given by them was 1001 understandable. Furthermore, co-assistants are responsible in handling the dogs and 1002 veterinarians intervene in time when failures occur. Least satisfied, but still sufficient, people 1003 were about waiting times and the costs. Dog owners, who had been to UKG for ovulation 1004 timing more than 5 times, were less satisfied about the costs than people who used this 1005 service infrequently. This might be due to the reason for breeding the bitch. Furthermore, 1006 breeders indicated that they would like to receive additional information about topics like 1007 important aspects of pregnancy and parturition in bitches. Also additional veterinary help 1008 with topics as genetic screening for hereditary diseases, problems surrounding birth and 1009 problems after birth would be welcome. Finally, the general rating shows that breeders are 1010 satisfied in general. 1011 1012 1013 1014 1015 1016 1017 1018 1019 41 1020 1021 References 1. HALLOWELL R., The relationships of customer satisfaction, customer loyalty and 1022 profitability: an empirical study. International Journal of Service Industry 1023 management 1996;7:27-42. 1024 1025 2. HESKETT J.L., JONES T.O., LOVEMAN G.W., SASSER W.E., JR AND 1026 SCHLESINGER L.A. Putting the service profit chain to work. Harvard Business 1027 Review 1994;105-111 1028 1029 3. YI Y. A critical review of consumer satisfaction. Review of marketing 1990;68-123 1030 1031 4. COE J.B., ADAMS C.L., BONNETT B.N. A focus group study of veterinarians’ and 1032 pet owners’ perceptions of veterinarian-client communication in companion animal 1033 practice. J Am Vet Med Assoc 2008;233:1072-1080 1034 1035 5. SHAW J.R., ADAMS C.L., BONNETT B.N. What can veterinarians learn from 1036 studies of physician-patient communication about veterinarian-client-patient 1037 communication? J Am Vet Med Assoc 2004;224:676-684 1038 1039 6. TINGA C.E., ADAMS C.L., BONNETT B.N., RIBBLE C.S. Survey of veterinary 1040 technical and professional skills in students and recent graduates of a veterinary 1041 college. J Am Vet Med Assoc 2001;219:924-931 1042 1043 7. COE J.B., ADAMS C.L., BONNETT B.N. A focus group study of veterinarians’ and 1044 pet owners’ perceptions of the monetary aspects of veterinary care. J Am Vet Med 1045 Assoc 2007;231:1510-1518 1046 1047 1048 1049 1050 1051 1052 42 1053 Appendix 1054 Supplement 1: Survey 1055 1056 Welcome, 1057 1058 The reproduction unit of the department of clinical sciences of companion animals at Utrecht 1059 University (UKG) strives to achieve the highest possible quality of service, for instance 1060 regarding the ovulation timing service of which you made use in recent years. We value your 1061 opinion to guarantee a high quality. Completing this survey will just take a few minutes of 1062 your time. 1063 1064 Among the participants a free ‘ovulation timing’ will be raffled at the value of €222.501 1065 To be eligible for the prize, please fill in your personal details at the end of the survey. All 1066 answers will remain completely anonymous. 1067 1068 Fill in your personal code. This code can be found in the invitation letter. 1069 … 1070 1071 1072 Question 1 1073 Number … How many litters have you bred in the past with your dogs? 1074 1075 1076 Question 2 With how many different dogs did you make use of the ovulation timing service of UKG? 1077 o 1 dog 1078 o 2 dogs 1079 o 3 dogs 1080 o more than 3 dogs 1081 1082 1083 Question 3 How often did you make use of the ovulation timing service of UKG in total? o 1 time 1084 1 If further examinations are necessary, it will be submitted by the veterinarian. For these examinations the standard prices will be charged. 43 1085 o 2 times 1086 o 3 times 1087 o 4 times 1088 o 5 times 1089 o More than 5 times 1090 1091 Question 4 1092 What is the main purpose of the dogs you are keeping? 1093 o Companionship 1094 o Work 1095 o Show 1096 o Sport 1097 o Other, namely: … 1098 1099 Question 4b 1100 You have indicated in the previous question that you keep your dog(s) mainly for work. Can 1101 you specify the work? 1102 o Hunting 1103 o Police dog 1104 o Herding dog 1105 o Rescue dog 1106 o Tracker dog 1107 o Guide dog 1108 o Other, namely: … 1109 1110 Indicate in the following propositions to what extent you agree. 5. There are often enough open Totally Somewhat disagree disagree ○ ○ ○ ○ Neutral Somewhat Totally Not agree agree applicable ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ consultations for ovulation timing at UKG. 6. The vets are accessible fast enough in case of emergency. 7. The vets are capable for examination 44 8. Co-assistants examine in a ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ responsible way 9. If a co-assistant acts incorrectly, the vet intervenes fast enough 10. Costs for ovulation timing are reasonable 11. Waiting time for open consultations is acceptable 1111 1112 Question 12 1113 Did your bitch have any fertility problems when presented for ovulation timing? 1114 o Yes, namely… 1115 o No 1116 1117 Question 12b (If answered yes to question 6) 1118 Do you think the veterinarian supported you well through these problems? 1119 o Yes 1120 o No because … 1121 1122 Indicate in the following proposition to what extent you agree. 13. Oral information given by the Totally Somewhat disagree disagree ○ ○ Neutral ○ Somewhat Totally Not agree agree applicable ○ ○ ○ vet is understandable 1123 1124 Question14. 1125 What topics would you like to receive further written information to make the ovulation 1126 timing service more complete? (Multiple answers possible) 1127 □ I have no need for written information. 1128 □ Important aspects of gestation in the bitch. 1129 □ How to diagnose pregnancy? 1130 □ What aspects are important to know about food for the bitch during pregnancy and 1131 lactation? 1132 □ Important aspects surrounding birth. 1133 □ How to take care of the bitch and pups after birth? 45 1134 □ Other, namely: …… 1135 1136 Question 15 1137 In what other areas, besides ovulation timing, do you want to be managed by the reproduction 1138 specialists? 1139 □ Selecting breeding material (right female/male pick)) 1140 □ Genetic screening for hereditary diseases 1141 □ Direct supervision if birth problems 1142 □ Support if problems occur with the bitch/puppies after birth 1143 □ Other, namely: …… 1144 1145 Question 16 1146 Are you familiar with the website of the UKG? 1147 o Yes 1148 o No 1149 1150 Indicate in the following proposition to what extent you agree. 17. The website of UKG is a good Totally Somewhat disagree disagree ○ ○ Neutral ○ Somewhat Totally Not agree agree applicable ○ ○ ○ resource 1151 1152 Question 18 1153 What information is missing on the website of UKG? 1154 …… 1155 1156 Question 19 1157 Have you ever filed a complaint regarding the ovulation timing service? 1158 o Yes 1159 o No 1160 o Not applicable, I was not aware of the possibility to file complaints. 1161 1162 Question 20 1163 Overall, how would you rate the entire ovulation timing service of UKG? 46 1 2 3 4 5 6 7 8 9 10 ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ 1164 1165 Question 21 1166 Do you have further positive aspects about the ovulation timing service of UKG? 1167 …… 1168 1169 Question 22 1170 Do you have any comments/improvements for the ovulation timing service of UKG? 1171 …… 1172 1173 To be eligible for the prize, please fill in your personal details. If you prefer to remain 1174 anonymous, this is possible. Please indicate your preference. 1175 o I would like to remain anonymous 1176 o I would like to fill in my personal details 1177 1178 Personal details 1179 First name …… Last name 1180 Address …… House number …… 1181 Postal code …… 1182 Location …… 1183 Telephone …… 1184 Email address …… …… 1185 1186 Thank you kindly for completing this survey! 1187 47