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. 2023 Jan 9;9(2):698–703. doi: 10.1002/vms3.1076

Effect of maternally derived antibodies on two commercial vaccines in changes of serum antibody titres against distemper in puppies

Farzane Shams 1, Hadi Pourtaghi 2,✉
PMCID: PMC10029894  PMID: 36622273

Abstract

Background

Maternally derived antibodies (MDA) have protection against canine distemper virus (CDV) in the first weeks of puppies’ life. However, MDA decreases with age. The most important and effective factor on immunization is timely vaccination. But in recent years, there were some outbreaks of CDV among puppies in Iran and this problem could be related to vaccine failure.

Objectives

The aim of this study is to evaluate the possible effect of MDA titre on vaccines against CDV and the efficacy of two commercial vaccines by using the enzyme‐linked immunosorbent assay (ELISA).

Methods

In this regard, 24 healthy 8‐week old terrier puppies were selected and divided into three identical groups based on a randomized, double‐blind comparative trial. The control group was injected normal saline, and group A was vaccinated by the vaccine namely Biocan L (Bioveta, Czech Republic), and the group B was vaccinated by the other vaccine called Duramune Max 5 + LCI/GP (Fort Dodge Animal Health, USA). The vaccines were used for the puppies between 8 and 16 weeks of age and in every 4 weeks.

Results

The results showed that the response of both vaccines was satisfactory, and no significant difference was observed between them. Moreover, the MDA in the control group reached an unprotective level in all puppies prior to their 14 weeks of age. In the vaccinated groups, after the second vaccine, all puppies in both groups reached protective levels.

Discussion

This is the first study on evaluation of two commercial vaccines in changes of serum antibody titres against distemper in puppies in Iran.

Conclusion

It is recommended that veterinarians during consulting use the ELISA to measure antibody titres to optimize the vaccination schedule and reduce the cost of vaccination failure. This is of paramount importance for puppies.

Keywords: canine distemper, maternally derived antibodies, puppies, vaccine

The results showed that the response of both vaccines was satisfactory, and no significant difference was observed between them. Moreover, the MDA in the control group reached an unprotective level in all puppies prior to their 14 weeks of age. In the vaccinated groups, after the second vaccine, all puppies in both groups reached protective levels.

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1. INTRODUCTION

Canine distemper virus (CDV) is a member of the Paramyxoviridae family, and the Morbillivirus genus (Lanszki et al., 2021) has a global distribution and it causes pathogenicity in domestic and wildlife mammals (Anis et al., 2020). Although puppies with the age of 3 weeks to 6 months are among the most significant victims of this virus, it should be noted that it can infect dogs of all ages (Nova et al., 2018) and it can cause more clinical signs such as diarrhoea, vomiting, anorexia and hyperkeratosis of the nose and footpads (Sheldon et al., 2017). In old dogs, mainly neurological symptoms such as seizures and necrotic encephalitis have been seen (Elias et al., 2019).

Considering the high transmission and pathogenicity of CDV, the prevention will always be a priority to the treatment (Delucchi et al., 2017) and the most important and effective of which is timely vaccination (Shah et al., 2019). Vaccination stimulates both humoral and cellular immunity (Barrett et al., 2020). The antibody titre, as an indicator of immune response, plays a key role in the duration of immunity (Mahon et al., 2017). Besides, the antibody titres can influence the vaccination schedule, and it may decreases by dog's ageing.

Moreover, maternally derived antibody (MDA) has protection against CDV in the first weeks of puppies’ life. It has been found that MDA decreases with age (Wilson et al., 2014). However, MDA decreases with age. The most important and effective factor on immunization is timely vaccination. But in recent years, there were some outbreaks of CDV among puppies in Iran and this problem could be related to vaccine failure. Despite performing the World Small Animal Veterinary Associated (WSAVA) vaccination schedule, more positive cases in Iran were observed which makes it necessary to examine the effectiveness of this vaccination schedule and commercial vaccines. Besides, we have evaluated the most important cause of vaccine failure in the puppies.

2. MATERIALS AND METHODS

2.1. Study design

This study is based on a randomized, double‐blind comparative trial.

2.2. Animals design

In the current study, 24 (12 males and 12 females), healthy, terrier puppies were selected from 2 breeding kennels that they had no clinical signs or positive results in enzyme‐linked immunosorbent assay (ELISA) test for CDV in the last 2 years.

Dames of all puppies had a vaccination schedule against CDV, and the last vaccination was 5 months prior to the delivery. Before entry to the study, all puppies were physically examined by an impartial vet and got cell blood count to make sure that no abnormality and disease could interfere with the results. Then, they received antihelminthic drugs twice. Puppies were weaned at 8 weeks of age. Afterwards, they were randomly divided into three groups and coded by an impartial vet who had unaware of the trial for maintaining the blinding of the study. The team of researchers in this study had no contact with puppies and vaccines until the day of the vaccination. Puppies in these groups were kept in three geographically separate regions. These regions were in three different country sides. Each group was kept in a separate place from other groups. The puppies in each group never met the other groups and even other dogs until the study was finished. So, there was no possibility of transmission of vaccine viruses between these groups. They were housed in wire cages, two in one cage, for each puppy one square meter space was considered. The puppies were fed with commercial dog food that was formulated to grow them. This diet was made in three times a day and at the same time the puppies had freely access to sanitized water.

2.3. Sampling design and vaccines

The puppies have vaccinated in 4 weeks intervals at weeks 8, 12 and 16 of their life.

  • Control group: Injected with normal saline

  • Group A: Vaccinated with Biocan DHPPi + L Bioveta, Czech

  • Group B: Vaccinated with Duramune Max 5 + LCI/GP; Fort Dodge Animal Health, USA

The vaccines were injected subcutaneously in the dorsal region of the shoulder or neck. Blood samples were collected 2 weeks after each vaccination. About 5 ml of blood was collected into a plain tube and allowed to clot. The serum was removed and frozen.

2.4. Laboratory evaluation

All blood samples were analysed in the serology laboratory of veterinary faculty of Islamic Azad University (KIAU) located in Karaj, Iran. The maternal derived and post‐vaccination responses of antibody titre against CDV were evaluated by using an indirect ELISA kit (Distemper IgG Ab ELISA 96, Biopronix). All procedures and stages were carefully followed to satisfy the manufacture's recommendation. Based on the catalogue of the ELISA kit, the cut‐off point was calculated by the multiplication of 0.2 into the mean of 2 wells of OD positive control. The OD that was higher than cut off was considered positive and divided into three groups:

  • Low titres (corresponding to indirect immunofluorescence test [IFI] values of 1/20–1/40). These samples show OD values between: 0.2 × OD positive control and 0.4 × OD positive control.

  • Medium titres (corresponding to IFI values of 1/80–1/160). These samples show OD values between: 0.4 × OD positive control and 0.8 × OD positive control.

  • High titres (corresponding to IFI values ≥1/320). These samples show OD values higher than 0.8 × OD positive control.

2.5. Statistical analysis

SAS 9.2 software was used as a strong statistical tool to analyse the obtained data. We used the Bartlett test to control the variance independence. The ANOVA and Fisher test were also applied to check changes in antibody titre against CDV in the three groups of the subject of this study in four times of sample collection. The mean value of antibodies against the CDV in each group was compared with Duncan's multiple range test. It should be noted that significance levels of 5% and 1% were evaluated for each analysis.

3. RESULTS

At the beginning of the study, the means of the MDA titre in the three groups were not significantly different. However, after the first vaccination, groups A and B showed significantly different antibody levels as compared to the control group, that is P > 0.01.

3.1. Evaluation of changing MDA titre in control group in the passing of time against CDV

The results show that before the study, 87.5% puppies in the control group had the medium antibody level, and other puppies had low antibody level. Besides, ELISA results showed that the mean of titre was 0.870 ± 0.17.

In the 10 weeks of age, half of the puppies had the medium antibody level, and the other had not immune level. Moreover, ELISA data showed that the mean titre was (0.650 ± 0.18) confirming that this decrease is not significantly different from the titre of the beginning.

At the weeks of 14, all puppies reached the low antibody level, and also the ELISA titre was (0.520 ± 0.12). This decrease was not significantly different from the 10‐week age, but it was significantly different from the beginning (P > 0.01).

At the weeks of 18, all puppies were in the low antibody level. ELISA titre was (0.360 ± 0.06). This reduction was not significantly different from the results at weeks of 10 and 14; however, it showed a significantly different outcome as compared to the data from the beginning (P > 0.01) (Figure 1).

FIGURE 1.

FIGURE 1

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The trends of antibody titres against canine distemper virus (CDV) in the control group (unvaccinated group)

3.2. Evaluation of the antibody level against CDV and efficacy of two commercial vaccines

At the week of 8, the mean of MDA titre for the group A was 0.92 ± 0.14, and the group B was 0.95 ± 0.14. There was no a significant difference between these two groups. Besides, the results have shown that all puppies in group A and 87.7% of puppies in group B had medium antibody level, and the rest had low antibody level.

At 10 weeks of age, the mean antibody titre for group A was 1.12 ± 0.15 and for the, group B was 1.18 ± 0.07. There was no a significantly difference between the two groups. Furthermore, the results showed that after got the first dose of vaccine A, 25% of puppies had a decrease antibody level comparing first antibody titre related to MDA at week of 8 of age; however, all puppies still had the medium antibody level. And also, the same decrease occurred in 12.5% of puppies that got vaccine B; however, 50% of the puppies reached the high antibody level.

At the 14 weeks of age, the mean antibody level for the group A and group B was 1.81 ± 0.68 and 1.67 ± 0.31, respectively. There was no a statistically significant difference between the two groups. In addition, after getting the second dose of vaccine A, 12.5% of puppies decreased antibody level comparing antibody titre week 10 of age, although 50% of puppies in group A had high antibody level, on the other hand 62.5% of puppies in group B had high antibody level.

At 18 weeks of age, the mean antibody level for group A and group B was 2.19 ± 0.67 and, 2.21 ± 0.41, respectively. Again like the results in the 14 weeks, there was no a statistically significantly difference between the two groups. Note that after getting the third dose of vaccine A, 12.5% of puppies decreased antibody level comparing antibody titre related week 14 of age, besides 87.5% of the puppies in both groups had high antibody level (Figure 2).

FIGURE 2.

FIGURE 2

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Comparison of the efficacy of the two commercial vaccines against canine distemper virus (CDV) during three doses of vaccination

4. DISCUSSIONS

The vaccine plays a major role in the prevention and control of infectious diseases in humans and animals. For achieving the result of the immunization efficacy in the population, the parameters that should be considered include ages, breeds, habitats, feeding, presence of other animals, the effectiveness of vaccine and disease prevalence (Fischer et al., 2016). If the vaccine is effective and used properly, it can protect against pathogens by providing the right antigen to the immune system (Jensen et al., 2015). Some vaccines with poor efficacy may not be identified until they are used. In Finland, during the epidemic of distemper disease, a large number of dogs were involved with the Dohyvac vaccine and the outcome of vaccination showed significant negative difference as compared to the other vaccines (Rikula et al., 2007). This caused the vaccine to be taken off the market. Therefore, this is the most important reason to evaluate the performance of various vaccines in the world before facing a disaster.

Most puppies are protected by the MDA during the first few weeks of their life. Thus, they are immune to many diseases without needing to get a vaccine (DiGangi et al., 2019). On the other hand, that reduces the severity of vaccines, especially modified live vaccines as it was the important cause of vaccine failure. The previous studies have shown that this maternal titre decreases over time, from 8 to 12 weeks of age, and reaches a level that has the least interaction with the vaccine (Hatke et al., 2020). In the current study, a downward slope of the MDA titre verses time was witnessed. In this study, the golden time for group vaccination against CDV was 14 weeks. However, some studies have shown that due to the low maternal titre, the puppy was ready to be vaccinated at the earlier age than 8 weeks (Wilson et al., 2014). On the other hand, due to the high maternal titre, the puppy still had a protective maternal titre over 12 weeks which has the ability to interfere with the vaccine (Larson et al., 2020).

According to the WSAVA guideline, those puppies that are as young as 8 weeks life can be vaccinated in two ways. The first starts at 8 weeks and then receiving four doses of vaccine every 3–16 weeks or more. The second starts at 8 weeks and get three doses of vaccine every 4–16 weeks or more (Day, 2017). In this study, the second method has been evaluated as the veterinarians mainly follow this schedule in Iran. The results of the first vaccination is in agreement with the study of Bergmann et al. (2021) who worked on six groups of dogs that 17.5% of dogs had decreased the antibody titre after the first vaccination and 33% had no changes in antibody titre (Bergmann et al., 2021). The results of the second vaccination, which assumed that if all puppies have reached a protective titre, the vaccination can be ended, were in the agreement with another study of Bergman et al. (2006). They worked on two groups of puppies that most of them had a response to the second vaccine and they had a protective titre (Bergman et al., 2006). In addition, the results of the third vaccination are in agreement with the study of Ogbu et al. (2017) who investigated on vaccinating dogs against CDV. They showed that the third vaccine had significantly improved the performance of immunization (Ogbu et al., 2017).

The results of comparing the performance of the two vaccines in this study are similar to the study by Ogbu et al. (2017). They compared two vaccines made in Brazil and in the United States. They observed no significant difference in the amount of antibody titre produced (Ogbu et al., 2017).

It should be noted that some factors can affect the vaccine response, such as storage conditions, concurrent disease, feeding, MDA and breed (Anvari et al., 2019). There is still little information about synergy in parasite‐infected hosts and increased vaccination success. However, there is evidence that trypanosomiasis and theileriosis reduce vaccine responses (Yoon et al., 2017). Besides, parasites cause secondary diseases by feeding nutrients of the host cause immune suppression and also increase the risk of stress (Cunha et al., 2020). Additionally, the animals that take drugs such as glucocorticoids and cytotoxic agents or have been hyperthermic at the time of vaccination are not able to respond effectively to the distemper vaccine. They are more likely to be infected with the virulent virus (Inbaraj et al., 2016). Furthermore, other studies showed that some breeds are more susceptible to the distemper disease, such as Doberman and Rottweiler; therefore, they require a different vaccination schedule (da Costa et al., 2019). In the current study, we have tried to decrease the impact of the other effective factors on the vaccine response with the vaccines were stored according to the manufacturer's instructions. Note that all puppies were examined by an impartial veterinarian before starting the study, and their healthy conditions were approved prior to the study. Their health conditions were also monitored during the study and get antihelminthic drugs before the delivery.

5. CONCLUSIONS

The timely vaccination can prevent the prevalence of a deadly infectious disease. It should be noted that various factors affect the response to the vaccine, and among them age is the most critical factor in designing the vaccination schedule. Choosing the right and effective vaccine in the prevalence of CDV can prevent widespread mortality in dogs. It is concluded that both vaccines of the subject of this study have proven desirable immunity. Finally, it is recommended that veterinarians during consulting use the ELISA to measure pre‐vaccination antibody titres, especially in puppies, to optimize the vaccination schedule and reduce the cost of vaccination failure due to interaction with high MDA titres. In the absence of facilities, WSAVA guideline was found as an excellent alternative. It is also better to choose four vaccine schedules for the contaminated areas.

AUTHOR CONTRIBUTIONS

Supervision; conceptualization; investigation and methodology (lead); writing—review and editing (equal): Hadi Pourtaghi. Data curation; writing—original draft (lead); writing—review and editing (equal): Farzaneh Shams.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

ETHICS STATEMENT

All studies were supervised by the Iran national Ethics Committee on the Iran Islamic Azad University, Karaj, Research Ethics Committee (code: IR.IAU.K.REC.1400.16). All experiments were performed in accordance with relevant guidelines and regulations. The study was carried out in compliance with the ARRIVE guidelines.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.1076.

Shams, F. , & Pourtaghi, H. (2023). Effect of maternally derived antibodies on two commercial vaccines in changes of serum antibody titres against distemper in puppies. Veterinary Medicine and Science, 9, 698–703. 10.1002/vms3.1076

DATA AVAILABILITY STATEMENT

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

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