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Alzheimer’s disease (AD) is a multifactorial disease with a still barely understood etiology.
Alzheimer’s disease (AD) is a neurodegenerative disorder involving gray matter (GM) tissue that is now considered to be part of a continuum of clinical and biological phenomena. Although the pathological lesions observed in AD are well characterized, the causes that trigger the onset of the disease are still unknown. After primary infection HSV-1 establishes a long-lasting latent infection in the neurons of the peripheral nervous system (PNS) within the sensory ganglia (trigeminal ganglia). Although the host immune system plays an important role in reactivating of latent HSV-1, the understanding of immunologic control of HSV-1 in humans remains incomplete.
Recent results stemming from the analysis of the potential role of HSV-1 specific humoral immune responses in neurodegeneration that characterize AD have shown that HSV1-specific antibodies (IgG) titers correlate with cortical GM volume (by voxel-based morphometry, VBM) Thus, analyses performed with VBM in AD patients and healthy controls (HC) indicated the presence of significant correlations between the preservation of temporal and orbitofrontal cortices, and higher HSV-1-specific antibody (Ab) titers (Mancuso et al., 2014).
One of the best parameters to perform a qualitative evaluation of Abs is the measurement of avidity: the relative strength with which Abs bind antigens. Based on these previous results we investigated whether the correlation we detected between HSV-1-specific Ab titers and magnetic resonance imaging (MRI) VBM parameters could be observed in aMCI as well; possible associations between HSV-1 specific IgG avidity and preservation of brain areas were also analyzed in a subgroup of AD and MCI patients.
Herpes simplex virus 1 serum IgG titers were measured using commercial enzyme immunoassays (BEIA HSV-1 IgG, Technogenetics, Milano, Italy), according the attached protocol.
Herpes simplex virus 1 specific IgG avidity was measured with a protein-denaturing agent in a subgroup of seropositive subjects (44 AD, 23 aMCI, and 26 HC); the protocol used for evaluation of avidity is the same above-mentioned, with the addition of 6 M urea to the washing solution at the washing step after plasma reaction.
Customer-designed Taqman probes for the 112 and 158 codons were used to determine the genotype of apoliprotein E gene (APOE). Brain MR images were acquired using a 1,5 T scanner (Siemens Magnetom Avanto, Erlangen, Germany). Differences in immunological data (HSV-1 Ab levels and IgG anti- HSV-1 antibodies avidity) among groups where tested using One-way ANOVA with Bonferroni post hoc test after excluding the presence of any significant covariate.
In a randomly selected subgroup of patients (AD, aMCI), RM-ROI data were collected and differences between groups were evaluated by means of Mann Whitney U, Chi-square test and One-way analysis of covariance using the volumetric scaling (V-Scaling) factor obtained with FSL-SIENAX as covariate, in order to take into account the differences in head size among subjects.
All the quantitative variables were described using mean and SD or median and interquartile range (IQR) and an alpha = 0.05 was considered significant. The subgroup of aMCI individuals and AD patients in whom MRI analyses were performed were comparable for age, gender, years of education, and proportion of APOE ε-4 carriers.
No differences were found among the three groups when HSV-1 IgG avidity indexes were analyzed. As expected by the limited range of MMSE score no correlations were detected between MMSE level and HSV-1 IgG titers or avidity indices.
Table 3 shows the results of the VBM on structural MRI data and reveals a well-known pattern of GM atrophy in AD patients compared to MCI patients: patients with AD were significantly more atrophic than aMCI subjects in several brain regions including bilateral hippocampus and parahippocampal gyrus, right middle temporal gyrus (right>left), right fusiform gyrus, and right amygdala.
Correlations between GM values from ROIs of both MCI and AD and HSV-1-specific Ab titers are shown in Figure 1B. Aim of the present study was to further investigate the link between neurodegeneration and HSV-1-humoral immunity by expanding our analyses to aMCI patients.

As expected, and confirming previous data, HSV-1 seroprevalence did not differ when AD or aMCI patients were compared to healthy controls (Mancuso et al., 2014). This means that you will not need to remember your user name and password in the future and you will be able to login with the account you choose to sync, with the click of a button. This page doesn't support Internet Explorer 6, 7 and 8.Please upgrade your browser or activate Google Chrome Frame to improve your experience. Herpes simplex virus 1 (HSV-1) has long been suspected to play a role in the pathogenesis of AD because of its neurotropism, high rate of infection in the general population, and life-long persistence in neuronal cells, particularly in the same brain regions that are usually altered in AD. AD is the most common form of dementia in the elderly, affecting more than 25 million people worldwide, with a prevalence of 5% after 65 years of age, increasing to about 30% in people aged 85 years or older. External stimuli including UV light and stress, can induce reactivation of HSV-1 from latency, an event mostly asymptomatic, or resulting in cold sores. These data suggested a possible protective role for HSV-1-specific humoral immunity in those cerebral regions that are typically affected in AD as well as in HSV-1-associated acute encephalitis. All subjects were consecutively recruited at the Fondazione Don Gnocchi, IRCCS in Milano, Italy. After three washing steps with washing buffer to remove the unbound proteins, 100 μl of horseradish peroxidase conjugate was added to each well and incubated at RT for 30 min.
MR examination was performed in two randomly selected subgroups of AD HSV-1-seropositive patients and aMCI HSV-1 seropositive patients. Demographical, neuropsychological, immunological, and anatomical information of the MRI subsample.
Normalized and modulated GM volumes of every subject were computed in four 10-mm diameter spherical ROIs. We compared aMCI, AD, and HC on demographic data, using the Chi-square test and One-way ANOVA with Bonferroni post hoc test for categorical and continuous variables, respectively. Following our previous work, GM values from ROIs of both MCI and AD were correlated with immunological data by means of Spearman’s correlation coefficient.
Again, a significant difference was found for MMSE values, accordingly with the adopted inclusion criteria (Table 2). No correlations were obtained between age, APOE4 status and the same indices neither in the overall group nor in the groups considered separately.
AD patients also showed decreased GM volume compared to aMCI subjects bilaterally in cerebellum and posterior cingulate cortex. IgG Ab titers, however, were significantly increased in AD compared to HC, reinforcing the borderline value of significance found when a smaller group of individuals was analyzed (Mancuso et al., 2014). The goal of this study was to evaluate HSV-1-specific humoral immune responses in patients with a diagnosis of either AD or amnestic mild cognitive impairment (aMCI), and to verify the possible relation between HSV-1-specific antibody (Ab) titers and cortical damage; results were compared to those obtained in a group of healthy controls (HC).
The amnestic mild cognitive impairment (aMCI) is a syndrome with a high risk of progression to AD, and it could constitute a prodromal stage of this disorder and it represents the borderland condition between normal aging and AD dementia (Petersen, 2004). Serious neurological complications rarely develop and target the same brain regions that are altered in AD (frontal and temporal cortices as well as the hippocampus). Recent results reported an increased HSV-1 IgG Ab avidity index in aMCI patients compared to AD and HC (Kobayashi et al., 2013), suggesting that viral reactivation is a particularly frequent event in the prodromal stage of AD. The measured absorbance is proportional to the concentration of HSV-1 IgG antibodies present.

Such correlation was not observed in aMCI although areas of increased atrophy compared with HC were seen in the bilateral temporal cortex (Figure 1C). In a previous study we found a correlation between cortical atrophy in those areas of the brain that are strongly related to pathology in AD patients and titers of HSV-1-specific Ab, suggesting that HSV-1-humoral immunity could be a protective factor in AD (Mancuso et al., 2014).
An additional significant result obtained in the present study is that HSV-1 IgG titers were significantly increased in aMCI subjects as well. Studies have shown that HSV Type 1 infects tissues such as lung and esophagus and HSV Type 2 infects the genitals and anus. HSV-1 Ab levels were expressed as Ab index (AI), calculated by dividing OD measurement generated from the assay by OD cut-off calibrator. After hippocampal segmentation, volumetric data had been obtained in each subject using a specific FSL function.
After GM segmentation all images underwent spatial smoothing using a Gaussian kernel (FWHM 8 mm). One additional control ROI4 was positioned in dorsolateral prefrontal cortex, an area which is preserved by the HSV-1 and which is affected in moderate to severe AD pathology. No correlations were obtained between the dorsolateral prefrontal cortex (ROI4), an area which is preserved in aMCI and in mild AD, and HSV-1-specific Ab titers either. These results are novel and suggest that this phenomenon occurs already in the early phase of the cognitive impairment decline, before the diagnosis of AD, and that a more robust immune response may be elicited by HSV-1 infection in AD and aMCI subjects.
This antibody does not cross-react with cytomegalovirus, Epstein-Barr virus, or varicella zoster virus and is compatible with formalin fixation; however, prolonged fixation can be detrimental to HSV staining.
HSV-specific Ab avidity and cortical gray matter volumes analyzed by magnetic resonance imaging (MRI) were evaluated as well in a subgroup of these individuals (44 AD, 23 aMCI, and 26 HC).
To identify areas with different GM volume between the two groups direct comparison between AD and MCI patients was performed (two sample t-test). Finally, the statistical linear regression analyses performed between GM values in the ROIs and HSV-1 avidity index did not show any statistically significant differences between aMCI and AD.
Intracranial volume (ICV; obtained by adding up WM volume + GM volume + CSF volume) entered this second level analysis to adjust for potential confounds.
The ROI-volumes were computed after that a threshold of 0.75 was applied to the segmented GM map, in order to increase the certainty of belonging to GM. A subgroup of randomly selected patients underwent advanced MRI acquisition (see MRI acquisitions and analyses for details). Only those areas surviving 0.05 voxel-level FDR corrected threshold have been considered as significant.
Statistical linear regression analyses were performed between GM values in the ROIs and HSV-1 Ab levels and IgG anti-HSV-1 antibodies avidity. Results herein suggest that a strong HSV-1-specific humoral response could be protective toward AD-associated cortical damage.
The study conformed to the ethical principles of the Helsinki Declaration; all patients or their care-givers gave informed consent according to a protocol approved by the local ethics committee of the Don Gnocchi Foundation.

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